Abstract
Microscopic fungi occupy a vast number of habitats, are taxonomically diverse, degrade complex substrates, and have stood out for their capacity to biosynthesize a plethora of specialized metabolites. Such molecules are structurally diverse, and many have applications in fundamental and applied sciences, for example, in medicine, material sciences, food chemistry, textile and pharmaceutical industries, and agronomy, among other fields. However, despite the tremendous biotechnological value of fungi, these organisms are understudied, limiting the knowledge to their taxonomy, chemistry, and some putative applications. Notably, some specific habitats remain unexplored in terms of their mycobiota. Based on these considerations, this review describes the known fungal diversity associated with ants/nests, their metabolic potential, and the possible applications of their specialized metabolites in drug discovery programs focused on developing treatments for human diseases. According to this revision, fungal diversity has been studied by applying conventional methodologies such as isolation and morphological identification of soil fungi from mounds and nest chambers, and indirectly from ants’ cuticles and glands. The subfamilies, genera, taxonomical information, and geographical origin of ants from which filamentous fungi and yeast are commonly isolated are also described. Furthermore, some important information is presented concerning the difference between the ant-associated mycobiota and that in the surroundings, discarding the extrapolation of the chemical and biological information known for soil fungi. Altogether, this review evidenced the lack of information regarding the chemical composition of ant-associated fungi, encouraging research focused on exploring the chemistry biosynthesized from ants’ mycobiota, as well as the elucidation of their allelopathic potential inside the nests.
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Introduction
Since ancient times, fungi have been used by humankind as food and through bioprocesses to produce beer and wine (Ghorai et al. 2009). Currently, technological advances have allowed the development of several biotechnological areas, for example, biocontrol, bioremediation, biomass degradation, biofuel, organic acids, enzymes, agrochemical, and pharmaceutical production industries, to name but a few (Berasategui et al. 2016; Meena and Siddhardha 2019; Hyde et al. 2019). The fungi occupy a vast number of habitats, are taxonomically diverse, degrade complex substrates, and have stood out for their capacity to biosynthesize a plethora of specialized metabolites. Moreover, such molecules are structurally diverse, and many have applications in fundamental and applied sciences, for example, in medicine, material sciences, food chemistry, textile and pharmaceutical industries, and agronomy, among other fields (Schueffler and Anke 2014; González-Medina et al. 2016, 2017; Aldholmi et al. 2019). However, despite recent technological advances and the high biotechnological value of fungi, these organisms are understudied, and specific habitats remain unexplored. In this regard, the chemical constituents of a small number of species are known, and consequently, the use of their chemical heritage is limited (Schueffler and Anke 2014; Chassagne et al. 2019; Pham et al. 2019).
Given their biological diversity and cosmopolitan presence, fungi are the second most diverse kingdom on Earth, bringing together among 2.2–3.8 million species. However, so far, just over 200,000 have been described (Hawksworth and Lücking 2017). Macroscopic fungi are recognized due to their fruiting bodies; nevertheless, a considerable part of the biodiversity is composed of those with microscopic reproductive structures. Microscopic fungi are further divided into yeasts and filamentous fungi, and multicellular and unicellular eukaryotic organisms, respectively (De-Wei 2016). Consequently, the study through bioprospecting projects of areas with unknown mycobiota can lead to the description of new species and valuable chemical-biological information about the microorganisms and the specialized molecule produced. Some of these underexplored habitats are the ants’ nests, whose importance from the chemical-pharmaceutical point of view was evidenced by the study of their bacteriobiota, which have led to the discovery of various antifungals, for example, the cyclic depsipeptide dentigerumycin (1), involved in interspecific interactions among ants of the Attini tribe and the mycobiota of their nests (Oh et al. 2009; Pathak et al. 2019; Agarwal et al. 2022). The importance of microbiota associated with the nests and materials of other arthropods such as termites (Bignell et al. 1991; Yan et al. 2011; Chen et al. 2022), bees (Poulsen et al. 2011; Madden et al. 2013; Promnuan et al. 2021), and spiders (Iwai et al. 2009) has also been explored.
Based on these considerations, this review describes the known fungal diversity associated with ants of various species widely distributed globally, their nest, and the metabolic potential of isolated taxa, as well as the possible applications of their specialized metabolites. In a complementary way to some previous works, this compilation provides information concerning the variety of ant species from which fungi have been isolated and chemically studied. Additionally, the mycobiota of the nests is compared with that of the surroundings. However, a similar work highlighting the study of yeast diversity in several ants of the Attini tribe was published (Bizarria et al. 2022). Analysis of the retrieved information shows that literature on fungal diversity associated with nest focuses on the mounds and chambers of a few ant species, mainly the so-called leafcutters, generally distributed in South and North America (Fig. 1). Likewise, the most common ants/nest-associated fungal genera are listed, highlighting the underrepresented ones for their bioactivity. Although the chemical composition of ants/nest-associated fungi remains almost unexplored, compounds with antibacterial, antifungal, antidiabetic, and antiviral activity in vitro isolated from fungi have been described. These data will uncover the potential of the chemical and biological space of unexploited fungal-specialized metabolites. Additionally, they will demonstrate further evidence of their ability to synthesize complex structures applicable in various scientific and industrial fields. Finally, how the known interspecific relationships support the search for antibacterial chemicals from the nest mycobiota is also explained.
Search Strategy
This review began with an independent search for pairwise combinations, using “and” or “ + ” operators, of the English words “fungus,” “mycobiota,” “filamentous fungi,” “yeast,” “molecule,” “compound,” “isolation,” and “natural product” with “ant nest,” “mound,” and “ant.” The search engine Google Scholar and the databases PubMed, ScienceDirect, SciFinder, SciELO, Redalyc.org, JSTOR, Web of Science, and EBSCO were used. In the case of SciELO, the same words were searched for in Spanish and Portuguese. The American Chemical Society, Wiley, Springer, SAGE, Thieme, Royal Society of Chemistry, Canadian Science Publishing, and Taylor & Francis publishers were also consulted directly. Also, tracking additional publications in listed references was also useful. In summary, literature prior to December 2022 on fungal diversity associated with ants, their cuticle, and nests, as well as its chemical composition, were considered for discussion. Then, the publications that did not detail the origin of the mycobiota or the method to determine the fungal species, as well as those that did not provide sufficient evidence for the identification or elucidation of compounds, were excluded; the rest is discussed in this review; laboratory colony-based studies were also considered. The analysis of the mycobiota is restricted to that from healthy terrestrial ants and nests, whose identification of ants and fungi is at least at the genus level. The names of ant and fungal species were verified in the Integrated Taxonomic Information System, as well as AntCat, AntWeb databases, or directly in the report of their discovery (ITIS 2022; Bolton 2023; California Academy of Science 2023).
Discussion
Ants and Their Nests
Ants are a diverse, taxonomically functional group of insects classified in the Formicidae family. These organisms have existed for at least 100 million years and were the first social insects with predatory habits on Earth (Fernández 2003). Ants live in almost all terrestrial environments, underground or in trunks, branches, or subcortical cavities; only Antarctica, Iceland, Greenland, and the central Pacific islands do not have native species (Rojas Fernández 2001). Ants’ abundance is difficult to measure, but they are always in the most copious group of the edaphic macrofauna. The number of species and how they are distributed are unknown. However, their abundance in tropical, low-lying subtropical forests, and hot deserts is well established; temperature is the most critical factor limiting its distribution (Rojas Fernández 2001; Fernández 2003). Currently, more than 12,500 species belonging to 21 subfamilies and 290 genera have been described; nevertheless, it is suggested that the number of species could be up to 30,000, with some awaiting discovery. Among the known taxa, Myrmicinae and Formicinae subfamilies are the most studied (Ríos-Casanova 2014; Boudinot 2015; Bolton 2023).
Ants live in hierarchical communities within which it is possible to distinguish a worker and a reproductive caste. The number of individuals can range from dozens to hundreds of thousands, with specimens ranging from less than a millimeter to 1.5 cm in length (Ríos-Casanova 2014). Considering their diet, ants are highly specialized and generalist and could be classified as omnivorous, mycophagous, granivorous, and predatory (Rojas Fernández 2001). A variety of ant species occasionally feed on fungi, but Attini tribe are remarkably interesting as they grow fungal “gardens” within their nests and feed themselves almost exclusively with mycelium. Species of the Atta, Acromyrmex, and Sericomyrmex genus are called “leafcutters” or “foragers” for their skills to collect fresh plant material as a substrate for the growing fungus, while others, mainly of the Cyphomyrmex, Myrmicocrypta, and Apterostigma genera, collect carcasses, feces, and other materials to feed the fungus.
In contrast, Sericomyrmex and Trachymyrmex have transitional habits (Rojas Fernández 2001; Leal et al. 2011; Sosa-Calvo et al. 2018). It is hypothesized that the development of the metapleural gland played a crucial role in colonization by some ant species in soil (rich in microorganisms). This gland secretes hydroxy and phenylacetic acids that differentially inhibit the growth of microorganisms inside the nests; not surprisingly, species adapted to live in trees have lost this gland (Yek et al. 2012; Vieira et al. 2012; Offenberg and Damgaard 2019; Offenberg et al. 2022).
The impact of ants’ activity on soil health has been moderately addressed and principally considers the modification of physicochemical properties. For example, some studies describe the impact of soil, vegetation, and soil fauna transportation on the construction of underground nests, as well as the modification of chemical properties due to mineralization, organic matter accumulation, and decomposition, among other factors (Wagner et al. 1997; Kristiansen and Amelung 2001; Rojas Fernández 2001; Dostál et al. 2005; Pinto-Tomás et al. 2009; Fernandez et al. 2014; Wang et al. 2017; Zhang et al. 2018).
Associated Mycobiota
Based on the available information and the scope of our current research, this review mainly focuses on fungi isolated from terrestrial ants and their potential as a source of functional secondary metabolites; however, the approaches to study arboreal ants and their associated mycobiota are also summarized in the following paragraph. It is worth mentioning that the chemical composition of ants themselves has already been reported (Mans et al. 2016; Seabrooks and Hu 2017).
Tree ants belong to the Camponotus, Crematogaster, Dolichoderus, Pheidole, Monomorium, Technomyrmex, Allomerus, Cladomyrma, Azteca, and Tretaponera genera, among others. These species have a close relationship with fungi from the Chaetothyriales order, referred to as black yeasts in literature (Weißflog 2001; Ruiz-González et al. 2011; Voglmayr et al. 2011; Nepel et al. 2016; Lucas et al. 2019; Moreno et al. 2019). Interestingly, together with trichomes of some plants, fungal mycelium is part of the walls and galleries of the nest (called carton) or grows in the domatium of a myrmecophyte (Mayer and Voglmayr 2009; Orivel and Leroy 2010; Voglmayr et al. 2011; Nepel et al. 2014; Pringle and Moreau 2017; Baker et al. 2017; Quan et al. 2021). Remarkably, some ants even consume the fungus that develops in the domatium (Blatrix et al. 2012).
Ants with ground-level nests, from which fungi have been isolated, are scarce. Taxonomically (Fig. 2), these individuals are mainly grouped into tribe Attini, which is represented by ants of 7 genera: Apterostigma, Mycocepurus, Myrmicocrypta, Atta, Trachymyrmex, Acromyrmex, and Cyphomyrmex. Other tribes under study with one genus each are Solenopsidini, Tetramoriini, Pheidolini, Formicini, Camponotini, and Tapinomini. The morphology and lifestyle of these species considerably differ depending on their tribe, and the size and structure of their nests. Furthermore, they have a different native distribution, and colonize a great variety of ecosystems. The study of ant-associated mycobiota has been carried out by field sampling of soil from nests in nine countries, although the availability of research on filamentous fungi in North and South America stands out (Fig. 3). However, some research on mycobiota is carried out on colonies maintained in the laboratory under controlled environmental and feeding conditions. In the case of Atta sexdens rubropilosa and Atta cephalotes, for example, such studies have led to a better understanding of the fungal diversity inside the nests, chambers, and the ants themselves (Fisher et al. 1996; Carreiro et al. 1997, 2004; Rodrigues et al. 2005b).
Fungi associated with wild mature nests have been characterized by sampling mound’s soil, taken from the surface to a certain depth (3–40 cm)—often discarding detritus (Brill et al. 1996; Duff et al. 2016; Maksimova et al. 2016)—as well as the walls and contents of chambers (waste, garden, and breeding), by means of a reasonable excavation aside the entrances (Fisher et al. 1996; Ba et al. 2000; Rodrigues et al. 2014). Likewise, fungi away from the nest (1–10 m) are also considered in studies for comparative purposes (Arcuri et al. 2014; Rodrigues et al. 2014; Duff et al. 2016; Maksimova et al. 2016). Conversely, nest mycobiota do not always consider a description of fungi on or inside the ants (Arcuri et al. 2014; Maksimova et al. 2016).
Ant-associated fungi from soil of nest and fragments of the fungal garden are commonly isolated by conventional techniques based on sample dilution in sterile water and direct seeding in Petri dishes containing, yeast-malt extract agar (Fisher et al. 1996), potato dextrose agar (Rodrigues et al. 2008), glucose-peptone-yeast agar (Maksimova et al. 2016), and medium for aquatic yeasts (Carreiro et al. 1997). Antibiotics such as chloramphenicol (Arcuri et al. 2014; Rodrigues et al. 2014), amoxicillin (Jiménez-Arreola et al. 2020), oxytetracycline (Fisher et al. 1996), and levomycetin (Maksimova et al. 2016) are frequently added to the medium to prevent bacterial growth. It is worth mentioning that in addition to molecular methods some of the filamentous fungi reported in this compilation were identified using classic microbiological methods, which is limited in the identification of fungal taxonomic groups without properly defined morphological keys of their colonies or spores in the bibliography (Fisher et al. 1996; Rodrigues et al. 2008). Conversely, yeast identification is usually performed by genetic means (Carreiro et al. 1997; Rodrigues et al. 2009; Pagnocca et al. 2010; Arcuri et al. 2014).
Studies on fungal microbiome frequently examine anthills of Acromyrmex and Atta ants from Canada, the USA, and some Central and South American countries, mainly Brazil. Additional research has also been carried out in Nigeria and Russia; however, there is a lack of knowledge of the mycobiota found in this niche in Europe, Asia, and Oceania (Fig. 3). Research focused on studying non-mutualistic ant-associated fungi from Brazil led to the identification of species from Acremonium, Escovopsis, Fusarium, Mucor, Escovopsioides, Metarhizium, and Mariannaea genera; all isolates related to A. sexdens rubropilosa. Moreover, Trichoderma species have also been isolated from ants of the Acromyrmex genus (Rodrigues et al. 2005b; Augustin et al. 2013; Montoya et al. 2016; Armando et al. 2017). Species from the Leucocoprinus genus have received particular attention since they are cultivated by mycophagous ants (Lugo et al. 2013; Luiso et al. 2020). Yeast species from Candida, Trichosporon, Debaryomyces, Geotrichum, Hannaella, Cryptococcus, and others have also been described in association with Atta, Myrmicocrypta, and Solenopsis ants in Brazil and the USA (Ba et al. 2000; Pagnocca et al. 2010; Arcuri et al. 2014). A review on the diversity of yeasts associated with fungus-growing ants found that the orders Saccharomycetales, Tremellales, and Trichosporonales are the most common (Bizarria et al. 2022).
Based on comparative studies, it is known that, in general, the mycobiota differs by ant species and even between the interior and exterior of the nests, tending to isolate more rare taxa in ant colonies. Not surprisingly, fungal microbiota differs even between nests of the same ant species; such variations are mainly due to topographic gradients, temporality of the ecosystem, and plant substrate for leafcutter ants (Kaspari et al. 2010; Rodrigues et al. 2011; Reis et al. 2015; Pereira et al. 2016; Russell et al. 2017; Delgado-Baquerizo et al. 2019; Parmentier et al. 2020; Lindström et al. 2021; Siedlecki et al. 2021). These differences also extend to nematodes. For example, it has been proposed that within the nests, a unique microenvironment is created, in which microbes adapt and diverge from the microbiome of the surrounding soil, phenomena mainly due to temperature stability and the continuous processes of organic material decomposition (Laakso et al. 1998; Lindström et al. 2018, 2019). Specifically, in the nests of Aphaenogaster rudis, the richness of phytopathogenic fungi was lower, compared to that of the nearby soil (Tarsa et al. 2018). In nests of the arboreal ant Lasius fuliginosus and Azteca trigona, it was also observed that the fungal community is different from that of the surrounding land over time (Lucas et al. 2017; Brinker et al. 2019). Moreover, some patterns have been noted in several ant species, for example, fungi isolated from Pogonomyrmex occidentalis nest in wood-decaying differ from the mycobiota in dead pines or the dominant vegetation around the nest (Carlson and Whitford 1991; Lupala et al. 2019). Another example involves mycorrhizal fungi, which are more copious in the mounds of harvesting ants (Pogonomyrmex spp.) than in the surroundings. Moreover, it has been projected that the foraging activity of Messor spp. influences soil fertility in nests, increasing microbial biomass and its activity (Snyder et al. 2002; Ginzburg et al. 2008). Additionally, it was found that the Trichoderma genus and mycorrhizal fungi are more abundant in plant material rejected by Atta spp. than that deposited in the mound (Van Bael et al. 2009; Rocha et al. 2017).
The diversity of fungi isolated from ants and their nests is summarized in Fig. 4, regardless of whether a comparison was made among the surrounding soil, or the colony was captive or wild (Ba et al. 2000; Arcuri et al. 2014; Rodrigues et al. 2014; Duff et al. 2016; Maksimova et al. 2016; Montoya et al. 2016). The mycobiota at the genus level isolated from ant nests in the field, compared to that of the colony surroundings, as raised in some investigation, is summarized in Fig. 5 (Rodrigues et al. 2014; Duff et al. 2016; Montoya et al. 2016).
Ant Cuticles
Fungi isolated from ants’ cuticles and their interior are scarce with only six reports found in the literature (Fig. 4), all of them are attributable to ants, and just a few reports dealing with fungi isolated from the nest. Fungi isolated from ants are described in this subtopic. Conversely, actinobacteria living in symbiosis with ants are the most studied microorganisms. In this review, fungi carried by ants were considered part of the nest mycobiota, considering they are distributed by these arthropods from outside and between nest spaces, either from their cuticle or, for example, from their gut through feces. Hyaline filamentous fungi were isolated in Brazil from Atta laevigata workers. The most abundant fungal isolates were Alternaria arborescens, Bipolaris sorokiniana, Bipolaris eleusines, Bipolaris zeae, Curvularia trifolii, and Paraphaeosphaeria michotii, species mainly associated with plants (Guedes et al. 2012). A search for fungi in young queen ants of Atta capigura and A. leviagata concluded that the genera Cladophialophora, Cladosporium, Exophiala, Ochroconis, Phaeococcomyces, Phialophora, and Penidiella are the most common filamentous fungi (mainly dematiaceous), whereas Aureobasidium, Candida, and Cryptococcus are the most represented yeasts (Pagnocca et al. 2008; Miranda Duarte 2013; Duarte et al. 2014). Interestingly, ants play a role as dispersers of mycobiota in nature. In fact, it has been proven that they are vectors of pathogenic species to humans. For example, it was reported that in several hospital areas in Greece, Brazil, France, and Iran, ants carry some opportunistic fungi such as Penicillium sp., Acremonium sp., and Mucor sp. All represent the known causal agents of mycoses (Aquino et al. 2013).
Remarkably, although entomopathogenic fungi are usually isolated from insect bodies, the prevalence of Cordyceps sp. in healthy ants is low, as demonstrated by Hughes in 2004, according to a study in which the cuticle of four different species of foraging ants from a tropical forest in Panama was examined (Hughes et al. 2004). Interestingly, dead ant specimens are a better source of entomopathogenic fungi and have led to the isolation of Aspergillus parasiticus, Aspergillus ochraceus, Beauveria bassiana, Metarhizum anisopliae, Pandora formicae, Ophiocordyceps sp., and Kneallhazia solenopsae species, all of them from dead females of Atta mexicana, workers of Atta bisphaerica, specimens of Formica sp., Camponotus sp., and Solenopsis sp. (Sokolova and Fuxa 2008; Ribeiro et al. 2012; Kobmoo et al. 2015; Małagocka et al. 2017). Furthermore, Aspergillus nomius was isolated from A. sexdens rubropilosa, and it was suggested that its pathogenicity comes from the mycotoxins it produces, such as aflatoxins B1 (2) and G1 (3) (Da Silva-Junior et al. 2017). On that subject, it has been demonstrated that certain entomopathogenic fungi could perform well in ants’ biocontrol (Ortiz and Orduz 2001; López Arismendy and Orduz Peralta 2002; Ribeiro et al. 2012).
Among the fungal species internally colonizing ants, the most common species include some entomopathogenic species in Acromyrmex octopinosus, intracellular parasites of Microsporidia genus and yeast in Formica excelsa, Debaryomyces polymorphus in the infrabuccal pocket of Camponotus vicinus (Van Borm et al. 2002; Mankowski and Morrell 2004; Johansson et al. 2013), and endoparasitic fungi inhabiting ant species (Aegeritella sp., Laboulbenia sp., Ricki sp., Hormiscium sp., Myrmicinosporidium sp.) of the Holarctic biogeographic region (Espadaler and Santamaria 2012).
Anthills
The interiors of anthills are a series of complex, interlaced tunnels with various chambers to provide some larger areas inside the nest. These chambers have a variety of uses including storage areas for food, nurseries for ant larvae and their caretakers, and even areas for ants to simply rest. According to the literature, several filamentous fungi and yeasts have been isolated from anthills, the former being the most studied. To date, due to the number of species grouped together, Trichoderma spp. stand out among the filamentous ones, while Candida and Cryptoccocus are the most reported among yeasts. The association of this fungal diversity with some ant species is described below, although it is important to consider that most of the available information contemplate ant species of the Attini tribe (Fig. 4). So far, 360 species of fungi associated with ants and their nests have been isolated, 229 are filamentous, and 131 yeast-like, classified into 120 and 53 genera, respectively. This information was generated from the study of 34 species of ants, belonging to 13 genera, mainly Acromyrmex and Atta. The apparent diversity of filamentous fungi in Fig. 4 owes to the fact that most of these studies have focused on such microorganisms. Moreover, it can be noted that in terms of the number of fungal species, those found only in the nests are more copious than those found in the surrounding soil, for both filamentous and yeast-like species (Fig. 5). It cannot be overlooked that the fungal diversity associated with nests is the result of modifying that originally found in the soil, and that the differences observed are in fact, the effect of the establishment of ant’s colonies. In general, the diversity of fungi associated with nests is outstanding, although the genus varies from ant species, time, and geographical location.
From the nest mounds of F. aquilonia ants in Novosibirsk, Russia, yeast species belonging to the Debaryomycetaceae family (Debaryomyces hansensii and Schwanniomyces vanrijiae) have been isolated. Notably, fungi isolated from the mounds differed from those species colonizing the surroundings (Trichosporon moniliforme and Cystofilobasidium capitatum) (Maksimova et al. 2016).
Similar differences in the distribution of filamentous fungi were found for Formica ulkei in Alberta and Nova Scotia, Canada. In this case, Aspergillus navahoensis, Aspergillus pseudodeflectus, Aspergillus spp., Paecilomyces sp., and Penicillium sp. were the most copious fungi in the mounds. In contrast, Cladosporium cladosporioides, Geomyces pannorum, Acremonium sp., Fusarium sp., Penicillium sp., and Phoma strains were the dominant species in the surroundings. Temperature and water availability in mounds are hypothesized to differentiate the ant/nest-associated fungi from species colonizing nearby soil (Duff et al. 2016). It should be noted that nest sediments and neighboring anthills are a great source of entomopathogenic fungi, especially M. anisopliae and B. bassiana (Hughes et al. 2004; Angelone and Bidochka 2018), highlighting the ecological role of those fungal species in preventing anthill from other insects.
From nest interiors, especially fungal gardens, and waste deposits of A. sexdens and Myrmicocrypta sp., yeasts of Candida, Rhodotorula, and Trichosporon genus prevail, with Candida dubliniensis, Candida oleophilia, Cryptococcus haglerorum, Trichosporon chiarellii, and Hanseniaspora uvarum being the most common species (Carreiro et al. 1997; Middelhoven et al. 2003; Pagnocca et al. 2010). In addition, Candida parapsilosis and Candida lipolytica were identified in the brood chambers of Solenopsis invicta or “ant fire” (Ba et al. 2000). Concerning filamentous fungi within ants’ nests, Leucoagaricus gongylophorus stands out as a symbiont of foraging ants; in-depth aspects such as its distribution among ant species or their lineage are not included in this review. However, according to the available information, this fungus and its parasite (Escovopsis sp.) are widely distributed throughout various ant species, and considered to have co-evolved together with ants (Seifert et al. 1995; Currie et al. 2003; Lugo et al. 2013; Mueller et al. 2017; Bich et al. 2020). It should be added that only certain species of Escovopsis are considered opportunistic parasites and a pair of members have been reclassified into new genera, Sympodiorosea and Luteomyces (Montoya et al. 2021). In addition, E. nivea has also been identified as an antagonist of fungal gardens (Pietrobon et al. 2022). Up to today, the chemical composition of L. gongylophorus remains largely unknown, but given its importance as food for ant colonies, its study may be of interest from a nutraceutical point of view. It has also been suggested that certain fungi collaborate with L. gongylophorus on degrading plant material (Rodrigues et al. 2005b). Moreover, inhibition of the symbiotic fungus is a proposed target for ant control (Della Lucia et al. 2014; Araújo et al. 2022).
Several species of Trichoderma genus are commonly found in the chambers-nest garden of Atta and Acromyrmex genus, for example, A. sexdens rubropilosa, A. lobicornis, and A. lundii (Montoya et al. 2016; Armando et al. 2017). From Acromyrmex, Trichoderma lentiforme, Trichoderma inhamatum, Trichoderma virens, Trichoderma koningiopsis, and Trichoderma aff. Neotropical, among others, have been identified (Armando et al. 2017). Trichoderma spp. have been proposed to be a pathogen of Trachymyrmex septentrionalis fungal gardens (Kyle et al. 2023). In addition, several new species of Trichoderma, including T. attinorum, T. texanum, and T. longifialidicum spp. Nov., have been discovered (Montoya et al. 2016).
Interestingly, it was found that the foraging ant Atta colombica does not prefer plants with a high abundance of endophytes; the 30–43% increase in the time required to cut, transport, and clean this type of tissue was shown to be an undesirable cost. Furthermore, since this preference is independent of endophyte diversity, it is suggested that the techniques used by ants are general. Further, it was found that the colonization by the symbiont fungus showed the same performance in plant tissues with a high and low abundance of endophytes (Bittleston et al. 2011; Van Bael et al. 2012).
The mycobiota diversity isolated from fungal gardens may reflect the endophytic and epiphytic mycobiota of the plant material collected by ants, which vary over time, as detailed in a report on A. cephalotes from which Aspergillus niger, Epicoccum nigrum, Fusarium culmorum, Fusarium solani, Phomopsis glandicola, Phomopsis illicit, and Phomopsis quercella, among other species, have been identified (Fisher et al. 1996). In addition to the fungal composition in healthy nests of A. sexdens rubropilosa, there has been an interest on knowing the fungi that mainly establish in the fungal garden of intoxicated or abandoned colonies, noting that the parasite Escovopsis spp. cannot only establish in these weakened nests (Rodrigues et al. 2005a, b; Carlos et al. 2011).
Today, the fungal strains isolated from ants or their nest are all within the Ascomycota, Basidiomycota, Mucoromycota, and Zoopagomycota phyla. Among them, the most represented subphylums are Pezizimycotina with 82 plus genera, Saccharomycotina (19), Agaricomycotina (35), Ustilaginomycotina (6), Mucoromycotina (5), and finally Mortierellomycotina and Zoopagomycotina with one genus each (Fig. 6). This data highlights the broad fungal diversity carried by ants and that enclosed in their nests, and at the same time, projects this ecological niche as a rich source for rare cultivable fungi.
Chemical Compounds
Chemical information available on ant-associated fungi demonstrates the ability of these microorganisms to synthesize complex structures with unknown ecological roles. Notwithstanding, specialized metabolites produced by fungi are incredibly valuable in drug discovery programs aiming to find new molecules to treat human infectious and chronic diseases (O’Brien and Wright 2011). Currently, only 27 specialized metabolites reported in the literature have been isolated from ant/nests-associated fungi, including triterpenoids, indolterpenoids, and linear and polyaromatic polyketides. This chemical information has been partially described in some compilations focused on the chemical ecology of microbial and insect interactions (Beemelmanns et al. 2016; Van Arnam et al. 2018; Worsley et al. 2018; Batey et al. 2020; Menegatti et al. 2021). A brief description of the source and biological activity of all isolated molecules is presented in the following lines.
Sulfated triterpenoids A-108835 (4) and A-108836 (5) were obtained from Fusarium compactum cultivated in tomato and oat medium. This fungal strain was isolated from nest-mound soil harvested in Rantan (Nigeria, Africa). The major compound A-108835 (4) is substituted with an acetyloxy group, whereas the minor triterpene sulfate A-108836 (5) differs from A-108835 in the arrangement of the heteroannular diene with 7,8:9,11 position of rings B and C instead of the 8,9:14,15 positions of the C and D rings (Brill et al. 1996). Also, in A-108836 (5), the hydroxy group at C-11 is missing and a methoxy group at C-12 replaced the acetyloxy subtituent at C-12 in A-108835 (4). The initial report on the structure of compound 4 referred to this molecule as a diastereomer with the sodium 3-sulfate of 4,4,24-trimethylcholesta-8,14,24(28)-trien-2α,3β,11α,12β-tetrol-12-acetate, a compound isolated from the plant pathogen Fusarium graminearum. In vitro assays demonstrated that compound 4 inhibited the proteolytic activity of rhinovirus 3C protease (IC50 48 μg/ml), a molecular target to treat the common cold. However, it does not show antibacterial and antifungal activity against human pathogens (Brill et al. 1996). It was found that these triterpene sulfates and some semi-synthetic derivatives can inhibit HIV-1 integrase enzyme with IC50 values ranging from 4.8 to 15 μM, essential in HIV-1 virus replication. A charged group, e.g., a sulfate or carboxy, is required for the antiviral activity demonstrated in a viral spread assay. Unfortunately, these molecules show a very small therapeutic window (Singh et al. 2003).
Chemical investigation of the parasitic fungus Escovopsis weberi obtained from the nest of Acromyrmex echinatior dereplicated a series of shearinine-type indoletriterpenes, including shearinine L (6), M (7), D (8), E (9), and A (10), which were subsequently isolated from its axenic culture in soy flour media. In addition, emodin (11) and cycloarthropsone (12) were also obtained (Dhodary et al. 2018). 10 is a part of a family of indole alkaloids isolated from sclerotioid ascostromata of Eupenicillium shearii, reported as antifeedants of Helicoverpa zea larvae plague in topical application trials (Magnus and Mansley 1999). More recently, the related structure 6 also showed insecticidal effect by decreasing A. octospinosus foraging of substrate impregnated with it, adding a negative allelopathic effect of the parasite Escovopsis to the nests (Dhodary et al. 2018). The insecticidal activity of the indole alkaloids has been linked to the ABC ring system, 1,3,9,9a-tetrahydroindeno[2,1-c]pyran, present in other families of compounds with the same effect (Belofsky et al. 1995). Compounds 8 and 9 were isolated from the seafloor fungus Penicillium janthinellum; these molecules have been described in vitro as inducers of apoptosis in human leukemia HL-60 cells. Compound 9 also prevented epidermal growth factor-induced malignant transformation of JB6 P + Cl 41 cell line in agar with an IC50 of 13 µM (Smetanina et al. 2007). Product 8 was previously dereplicated from Escovopsis sp. by comparison of spectrometric data with databases, together with shearinines F and J. Furthermore, it was determined that aromatic compounds 11 and 12 inhibit the growth of Leucoagaricus gongylophorus (symbiotic fungus) in agar diffusion tests (Dhodary et al. 2018), acting as fungicides against the symbiont fungus, promoting foraging ant control. Moreover, it was previously described that certain coumarins related to 11 inhibit Leucoagaricus sp. in vitro, especially those possessing the 2H-chromen-2-one unit (Godoy et al. 2005).
Molecular network analysis guided the isolation and characterization of several specialized metabolites, including the 22,23-dehydroshearinine A (13), and the sulfur-containing diketopiperazines melinacidin IV (14), melinacidin III (15), chetracin B (16), and chetracin C (17) from the extracts of Escovopsis sp. Compounds 14 and 8 are synthesized in excess during fungal garden infection and inhibit the growth of Pseudonocardia sp. (Heine et al. 2018). Additionally, the linear polyketide conocandin B (18) and its derivative, conocandin C (19), were isolated from this fungus. Interestingly, 18 also inhibited the growth of Pseudonocardia sp., when evaluated in vitro, whereas 19 did not show the same activity (Bae et al. 2021) (Fig. 7).
Bionectria sp. was isolated from the fungal garden of Apterostigma dentigerum in Costa Rica. Its fermentation in potato dextrose agar (PDA) revealed the production of bionectriol A (20), a glycosylated polyketide, which did not show antifungal activity when tested in coculture trials against Escovopsis sp. and Candida albicans (Freinkman et al. 2009). Structurally related compounds were isolated from Bionectria chroleuca, of which TMC-151E, TMC-151F, and bionectriol C moderately inhibited Candida sp. biofilm formation (CI50 815.3, 23.5, and 42.3 μM, respectively) (Wang et al. 2014).
From the fungus Talaromyces sp. IQ-313, isolated from the mound of an anthill located at Huasteca Hidalguense, Hidalgo, Mexico, a series of asymmetric dimeric phenalenones: duclauxin (21), talaromycesone B (22), xenoclauxin (23), and bacillisporin G (24) were found when the fungus was cultivated in oat cereal. Biological evaluation of such compounds as inhibitors of a full-length protein tyrosine phosphatase 1B (hPTP1B1-400), a therapeutic target for developing antidiabetic and anticancer drugs (Jiménez-Arreola et al. 2020), evidenced the potential of these molecules as prototypes for developing hypoglycemic drugs. Other oxyphenalenones were isolated from fungi such as Penicillium duclauxii, Gilmaniella humicola, and Neonectria sp., and have been evaluated mostly as inhibitors of the growth of cancer cell lines (Elsebai et al. 2014).
As for the symbiont fungus, it has been ruled out that its volatile compounds play an ecological role. However, some compounds act as signalers in their interaction with pathogens and maximize their growth in the garden (Folgarait et al. 2011; Bueno de Oliveira 2020; Sousa et al. 2020). Characterization of volatile compounds in culture assays of Escovopsis sp. and L. gongylophorus has allowed their tentative identification by solid-phase microextraction and gas chromatography-mass spectrometry analysis (Masiulionis and Pagnocca 2020).
From Lepiota sp., a fungus isolated from the nest of Cyphomyrmex costatus ant produces lepiochlorin (25) when cultivated in a medium composed of mineral salts and sucrose supplemented with vitamins (Weber 1957; Nair and Hervey 1979). Moreover, Tyridiomyces formicatum, a fungal species obtained from Cyphomyrmex minutus, synthesizes a variety of diketopiperazines, for example, (3S,8aS)-3-isobutylhexahydropyrrolo[1,2-α]pyrazine-1,4-dione (26), (3S,8aS)-3-benzylhexahydropyrrolo[1,2-α]pyrazine-1,4-dione (27), and (3S,8aR)-3-benzylhexahydropyrrolo[1,2-α]pyrazine-1,4-dione (28), when cultivated in potato dextrose broth supplemented with tryptone; their evaluation as inhibitors of Candida sp. growth showed that these molecules had a weak effect compared to the positive control nystatin (Wang et al. 1999). It is worth mentioning that some compounds with antibiotic activity have been isolated from Leucoagaricus species although they are not listed as ants’ symbionts (Ilnuma et al. 1983; Huff et al. 1994).
The limited number of specialized metabolites isolated from ant/nest-associated fungi considerably focuses on the chemical composition of the parasitic fungus Escovopsis sp. and the symbiotic taxa Leucoagaricus sp. These data show the lack of research, not only regarding the mycobiote of the enormous diversity of ant species available, but also the chemical composition of their fungi and how this could favor the discovery of new functional chemical entities with potential applications in human or veterinary medicine, agriculture, and research, to mention a few areas (Scherlach et al. 2013; Meena and Siddhardha 2019). However, the importance of understanding the role that these secondary metabolites of microbial origin play in these biological systems should not go unnoticed (Frey Klett et al. 2011; O’Brien and Wright 2011; Moreau 2020).
Nest Interspecific Relationships
Studies on the ecological interaction of fungi inhabiting ants or their nests have proposed that species of the Attini tribe, mainly those cultivating Leucoagaricus gongylophorus, establish a mutualistic symbiotic relationship, which is complemented with Streptomyces, Pseudonocardia, and Burkholderia actinobacteria (Currie et al. 1999, 2006; Currie 2001; Santos et al. 2004; Poulsen et al. 2009; Barke et al. 2010; Seipke et al. 2011; Sit et al. 2015; Dângelo et al. 2016; Goldstein and Klassen 2020; Nascimento et al. 2022). Specialized necrotrophic parasitic fungi such as some species of Escovopsis sp. can lead to colony death, especially when invading the fungal gardens of susceptible nests; however, certain actinobacteria are known to prevent the growth of this parasite by producing antifungal compounds (Reynolds and Currie 2004; Sen et al. 2009; Schoenian et al. 2011; Jiménez-Gómez et al. 2021). For example, Trachymyrmex cf. zeteki carries actinobacteria in its cuticle and mixes them with unhealthy parts in an infraoral pouch to clear infections; other species of the Attini group carry them in complex cuticular modifications (Little et al. 2006; Li et al. 2018) (Fig. 7). The putative symbiotic nature of the ant-actinobacteria relationship remains under discussion; nevertheless, the recruitment of effective actinobacteria against Escovopsis sp. by ants has been described (Mueller et al. 2008). A similar relationship has been described for Allomerus decemarticulatus and Allomerus octoarticulatus ants that inhabit plant cavities constructed with fungi of the order Chaetothyriales, carrying bacteria of Streptomyces and Amycolatopsis genera capable of inhibiting the growth of fungi contaminating their nests, for example, Annulophypoxylon spp. and Chaunopycnis spp. (Seipke et al. 2012). In addition, it has been proposed that black yeasts (Phialophora genus) are an additional component of the ant-actinobacteria relationship, since some isolated species of ants can inhibit the development of actinobacteria and impact their effect on Escovopsis sp. (Little and Currie 2007, 2008). The opportunistic microorganisms of the nests can also be bacteria. Amycolatopsis bacterium was isolated from the fungal garden of Trachymyrmex smithi; from this microorganism, nocamycin V (29), a heterotricyclic compound capable of inhibiting the growth of Pseudonocardia sp. strains under laboratory conditions, was obtained from its extract (Hansen et al. 2022).
Some of the compounds that have been reported as inhibitors of fungi Ecovopsis sp. and its derivatives are summarized below. Several dentigerumycins have been found since the discovery of dentigerumycin (1) from a strain of Pseudonocardia associated with the nest of Apterostigma dentigerum. Compound 1 was one of the first molecules identified as a mediator of ant-actinobacteria mutualism by in vitro growth inhibition assays of Escovopsis sp. (IC50 2.8 µM), but it does not affect the symbiotic fungus (Oh et al. 2009). Another molecule, candicidin C (30), was dereplicated as the major component of the bioactive fractions of Streptomyces sp., isolated of Acromyrmex octospinosus. This molecule is capable of inhibiting the development of E. weberi and Escovosis aspergilloides but not L. gongylophorus (Haeder et al. 2009). Subsequent investigations with Pseudonocardia associated with Attini ants led to the finding of other compounds. GE37468 (31) is a known thiopeptide isolated from bacteria related with the cuticle of T. septentrionalis ant, which antagonize other bacteria of the same genus in the nest (Chang et al. 2020). Other important molecules are dentigerumycin F (32) and anttimicin (33); the former was found in the actinobacteria extract when it was cocultured with the Escovopsis supernatant, while the latter, known as a siderophore compound, inhibited the development of the parasite in its iron-depleted form (IC50 12.5 µg/ml) (Bae et al. 2021; Fukuda et al. 2021). Dereplication of compounds from antimicrobial extracts of Pseudonocardia sp., Streptomyces sp., and Escovopsis sp. by spectrometric analysis and the identification of multiple biosynthetic pathways of antibiotics have been recurrent (Barke et al. 2010; Seipke et al. 2011), as well as by direct analysis of the ant exoskeleton (Boya et al. 2017; Gemperline et al. 2017).
All these compounds that share chemical and biological features, for example, are made up of highly modified amino acids, the cyclic depsipeptide, or polyene cores, and inhibit the growth of Escovopsis sp. in vitro. Nevertheless, in competition evaluations Pseudonocardia strains also inhibit the growth of the entomopathogenic fungi M. anisopliae (Bruner-Montero et al. 2021). Given the lack of specificity, it is speculated that such molecules also model the ant/nest-associated mycobiota, which would also be expected as an effect of the metapleural glands in some ants and its defensins in general (Schoenian et al. 2011; Yek and Mueller 2011; Vander Meer 2012; Sakolrak et al. 2018). Compound 33 is also synthesized in response to entomopathogenic fungi (Gómez-Díaz et al. 2022), as evidenced by the behavior of ants inside the nests during sanitization of fungal gardens by some species (Goes et al. 2022). In this context, fungi in the nest are expected to have developed adaptation mechanisms based on evolutionary competition, for example, through resistance mechanisms or allelochemical interactions mediated by specialized metabolites. Analogous to the bioprospecting of antifungals, antibacterial, and antiparasitic from ant-associated actinobacteria (Desireé et al. 2013; Holmes et al. 2016; Efimenko et al. 2020; Ortega et al. 2021; Wu et al. 2022), it is proposed that the nest mycobiota constitutes a rich source of antibacterial molecules, especially useful in the search for treatments for species resistant to conventional drugs (OMS 2020).
Perspectives and Future Directions
The information available on fungal diversity associated with ants and their nests is limited; in this review, it can be noted how most of the research is related to Attini ants and given their economic importance it is not expected for such interest to diminish. Likewise, we anticipate that the description of chemicals from micromycetes will not depart from the study of their role in interactions within Attini nests, in the same way that the subject favored the discovery of a variety of metabolites of bacterial origin (Ramadhar et al. 2014; Artavia-León et al. 2018; Chevrette et al. 2019; Van Moll et al. 2021; Selim et al. 2021). Regarding the rest of ant species, certain bioprospecting studies have allowed to unveil the chemical composition of their mycobiota, although exclusively from filamentous fungi and using conventional techniques in organic chemistry. Perhaps this mycobiota, both filamentous and yeast-like, goes unnoticed, likely due to the belief of its similarity with species isolated from soil; however, according with the information presented, it is proposed to abandon this point of view, as ants modify not only the physicochemical characteristics of the soil in which they settle, but also its microbiota. Accordingly, the way in which this difference can be exploited is promising, as well as the micromycetes associated with arboreal and warrior ants. We believe that studies on the variation of the mycobiota in anthills will continue to offer interesting information, even more with the facilities of massive sequencing techniques, and the development of analytical methods to study their chemical composition.
Conclusions
Based on the literature revision, the biological diversity of fungi inhabiting ant nests has not been extensively studied. Pioneering research has focused on analyzing soil samples from mounds and nest chambers, and indirectly from ant cuticles. As a result, only a few hundred of ant-associated filamentous fungi and yeasts have been described, being Trichoderma, Penicillium, and Fusarium the most reported genera within the Pezizomycotina subphylum and Candida and Cryptococcus in the Saccharomycotina clade. The majority of chemical entities have been isolated from 14 ant species, mainly of the Acromyrmex and Atta genera found in the American continent, perhaps because of their economic importance as pests. Since this information was obtained almost exclusively through classical methods in microbiology, the application of modern massive sequencing techniques would help to fill this gap due to many ant species and their cosmopolitan nature. Also, the diversity of the secondary metabolites produced by these microorganisms and their potential application are promising fields. In the background, compounds with in vitro antibacterial, antifungal, antidiabetic, and antiviral activity have been mentioned, as well as interspecific relationships that place the anthills’ mycobiota as a source of chemical entities whose bioactivity should be pondered through bioprospecting studies, leading to discover molecules with applications in human or veterinary medicine, agriculture, and research, to mention a few. Finally, the ecological role of fungi in nests is just beginning to take place in relationships that have been investigated for a few years.
Data Availability
The data used and/or analyzed during this review are provided as supporting information files.
References
Agarwal S, Sharma G, Verma K, Latha N, Mathur V (2022) Pharmacological potential of ants and their symbionts – a review. Entomol Exp Appl 170:1032–1048. https://doi.org/10.1111/eea.13236
Aldholmi M, Marchand P, Ourliac-Garnier I, Le Pape P, Ganesan A (2019) A decade of antifungal leads from natural products: 2010–2019. Pharmaceuticals 12:182. https://doi.org/10.3390/ph12040182
Angelone S, Bidochka MJ (2018) Diversity and abundance of entomopathogenic fungi at ant colonies. J Invertebr Pathol 156:73–76. https://doi.org/10.1016/j.jip.2018.07.009
Aquino RSS, Silveira SS, Pessoa WFB, Rodrigues A, Andrioli JL, Delabie JHC, Fontana R (2013) Filamentous fungi vectored by ants (Hymenoptera: Formicidae) in a public hospital in north-eastern Brazil. J Hosp Infect 83:200–204. https://doi.org/10.1016/j.jhin.2012.11.022
Araújo S, Seibert J, Ruani A, Alcántara-de la Cruz R, Cruz A, Pereira A, Zandonai D, Forim M, Silva MF, Bueno O, Fernandes J (2022) The symbiotic fungus Leucoagaricus gongylophorus (Möller) Singer (Agaricales, Agaricaceae) as a target organism to control leaf-cutting ants. Insects 13:359. https://doi.org/10.3390/insects13040359
Arcuri SL, Pagnocca FC, Da Paixão Melo WG, Nagamoto NS, Komura DL, Rodrigues A (2014) Yeasts found on an ephemeral reproductive caste of the leaf-cutting ant Atta sexdens rubropilosa. Antonie Van Leeuwenhoek 106:475–487. https://doi.org/10.1007/s10482-014-0216-2
Armando NG, Marfetán JA, Folgarait PJ (2017) Trichoderma species associated with Acromyrmex ant nests from Argentina and first report of Trichoderma lentiforme for the country. Darwiniana 5:72–82. https://doi.org/10.14522/darwiniana.2017.51.724
Artavia-León A, Pacheco-Leiva M, Moya-Román C, Rodríguez-Hernández N, Pinto-Tomás AA (2018) Ant microbial symbionts are a new model for drug discovery. Drug Discov Today Dis Models 28:27–33. https://doi.org/10.1016/j.ddmod.2019.08.011
Augustin JO, Groenewald JZ, Nascimento RJ, Mizubuti ESG, Barreto RW, Elliot SL, Evans HC (2013) Yet more “weeds” in the garden: fungal novelties from nests of leaf-cutting ants. PLoS ONE 8:e82265. https://doi.org/10.1371/journal.pone.0082265
Ba AS, Phillips SA, Anderson JT (2000) Yeasts in mound soil of the red imported fire ant. Mycol Res 104:969–973. https://doi.org/10.1017/S0953756299002385
Bae M, Mevers E, Pishchany G, Whaley SG, Rock CO, Andes DR, Currie CR, Pupo MT, Clardy J (2021) Chemical exchanges between multilateral symbionts. Org Lett 23:1648–1652. https://doi.org/10.1021/acs.orglett.1c00068
Baker CCM, Martins DJ, Pelaez JN, Billen JPJ, Pringle A, Frederickson ME, Pierce NE (2017) Distinctive fungal communities in an obligate African ant-plant mutualism. P R Soc B 284:20162501. https://doi.org/10.1098/rspb.2016.2501
Barke J, Seipke RF, Grüschow S, Heavens D, Drou N, Bibb MJ, Goss RJ, Yu DW, Hutchings MI (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8:109. https://doi.org/10.1186/1741-7007-8-109
Batey SFD, Greco C, Hutchings MI, Wilkinson B (2020) Chemical warfare between fungus-growing ants and their pathogens. Curr Opin Chem Biol 59:172–181. https://doi.org/10.1016/j.cbpa.2020.08.001
Beemelmanns C, Guo H, Rischer M, Poulsen M (2016) Natural products from microbes associated with insects. Beilstein J Org Chem 12:314–327. https://doi.org/10.3762/bjoc.12.34
Belofsky GN, Gloer JB, Wicklow DT, Dowd PF (1995) Antiinsectan alkaloids: shearinines A-C and a new paxilline derivative from the ascostromata of Eupenicillium shearii. Tetrahedron 51:3959–3968. https://doi.org/10.1016/0040-4020(95)00138-X
Berasategui A, Shukla S, Salem H, Kaltenpoth M (2016) Potential applications of insect symbionts in biotechnology. Appl Microbiol Biotechnol 100:1567–1577. https://doi.org/10.1007/s00253-015-7186-9
Bich GÁ, Randon DN, Castrillo ML, Villalba LL, Zapata PD (2020) Aislamiento y caracterización morfológica y molecular de cepas de Escovopsis aisladas de nidos de hormigas cortadoras de hojas de Argentina. Rev Mex Biodivers 91:912581. https://doi.org/10.22201/ib.20078706e.2020.91.2581
Bignell DE, Anderson JM, Chosse R (1991) Isolation of facultatively aerobic actinomycetes from the gut, parent soil and mound materials of the termites Procubitermes aburiensis and Cubitermes severus. FEMS Microbiol Lett 85:151–160. https://doi.org/10.1111/j.1574-6968.1991.tb04707.x-i1
Bittleston LS, Brockmann F, Wcislo W, van Bael SA (2011) Endophytic fungi reduce leaf-cutting ant damage to seedlings. Biol Lett 7:30–32. https://doi.org/10.1098/rsbl.2010.0456
Bizarria R, Pagnocca FC, Rodrigues A (2022) Yeasts in the attine ant–fungus mutualism: diversity, functional roles, and putative biotechnological applications. Yeast 39:25–39. https://doi.org/10.1002/yea.3667
Blatrix R, Djiéto-Lordon C, Mondolot L, la Fisca P, Voglmayr H, Mckey D (2012) Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant-plant interactions. P R Soc B 279:3940–3947. https://doi.org/10.1098/rspb.2012.1403
Bolton B (2023) An online catalog of the ants of the world. https://antcat.org. Accessed 30 Apr 2023
Boudinot BE (2015) Contributions to the knowledge of formicidae (Hymenoptera, Aculeata): a new diagnosis of the family, the first global male-based key to subfamilies, and a treatment of early branching lineages. Eur J Taxon 2015:1–62. https://doi.org/10.5852/ejt.2015.120
Boya CA, Fernández-Marín H, Mejiá LC, Spadafora C, Dorrestein PC, Gutiérrez M (2017) Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants. Sci Rep 7:5604. https://doi.org/10.1038/s41598-017-05515-6
Brill GM, Kati WM, Montgomery D, Karwowski JP, Humphrey PE, Jackson M, Clement JJ, Kadam S, Chen RH, McAlpine JB (1996) Novel triterpene sulfates from Fusarium compactum using a rhinovirus 3C protease inhibitor screen. J Antibiot 49:541–546. https://doi.org/10.7164/antibiotics.49.541
Brinker P, Weig A, Rambold G, Feldhaar H, Tragust S (2019) Microbial community composition of nest-carton and adjoining soil of the ant Lasius fuliginosus and the role of host secretions in structuring microbial communities. Fungal Ecol 38:44–53. https://doi.org/10.1016/j.funeco.2018.08.007
Bruner-Montero G, Wood M, Horn HA, Gemperline E, Li L, Currie CR (2021) Symbiont-mediated protection of Acromyrmex leaf-cutter ants from the entomopathogenic eungus Metarhizium anisopliae. mBio 12:e01885–21. https://doi.org/10.1128/mBio.01885-21
Bueno de Oliveira K (2020) Metabólitos do fungo mutualista das formigas atíneas como mediadores da interação com o parasita Escovopsis. Universidade Estadual Paulista
California Academy of Science (2023) AntWeb. https://www.antweb.org/. Accessed 1 May 2023
Carlos AA, Rodrigues A, Forti LC, Passador MM, Sierra JF (2011) Filamentous fungi found in Atta sexdens rubropilosa colonies after treatment with different toxic bait formulations. J Appl Entomol 135:326–331. https://doi.org/10.1111/j.1439-0418.2010.01551.x
Carlson SR, Whitford WG (1991) Ant mound influence on vegetation and soils in a semiarid mountain ecosystem. Am Midl Nat 126:125. https://doi.org/10.2307/2426157
Carreiro SC, Pagnocca FC, Bacci M, Lachance MA, Bueno OC, Hebling MJA, Ruivo CCC, Rosa CA (2004) Sympodiomyces attinorum sp. nov., a yeast species associated with nests of the leaf-cutting ant Atta sexdens. Int J Syst Evol Microbiol 54:1891–1894. https://doi.org/10.1099/ijs.0.63200-0
Carreiro SC, Pagnocca FC, Bueno OC, Bacci M, Hebling MJA, Da Silva OA (1997) Yeasts associated with nests of the leaf-cutting ant Atta sexdens rubropilosa Forel, 1908. Antonie Van Leeuwenhoek 71:243–248. https://doi.org/10.1023/A:1000182108648
Chang PT, Rao K, Longo LO, Lawton ES, Scherer G, Van Arnam EB (2020) Thiopeptide defense by an ant’s bacterial symbiont. J Nat Prod 83:725–729. https://doi.org/10.1021/acs.jnatprod.9b00897
Chassagne F, Cabanac G, Hubert G, David B, Marti G (2019) The landscape of natural product diversity and their pharmacological relevance from a focus on the Dictionary of Natural Products ®. Phytochem Rev 18:601–622. https://doi.org/10.1007/s11101-019-09606-2
Chen S, Cheng D, Liu Z, Hassan B, Xu Y (2022) Community structure and antifungal activity of actinobacteria in a fungus-growing termite. Ecol Entomol. https://doi.org/10.1111/een.13219
Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE, Barns KJ, Book AJ, Cagnazzo J, Carlos C, Flanigan W, Grubbs KJ, Horn HA, Hoffmann FM, Klassen JL, Knack JJ, Lewin GR, McDonald BR, Muller L, Melo WGP, Pinto-Tomás AA, Schmitz A, Wendt-Pienkowski E, Wildman S, Zhao M, Zhang F, Bugni TS, Andes DR, Pupo MT, Currie CR (2019) The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 10:516. https://doi.org/10.1038/s41467-019-08438-0
Currie CR (2001) A Community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380. https://doi.org/10.1146/annurev.micro.55.1.357
Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83. https://doi.org/10.1126/science.1119744
Currie CR, Scottt JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704. https://doi.org/10.1038/19519
Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung GH, Spatafora JW, Straus NA (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299:386–388. https://doi.org/10.1126/science.1078155
Da Silva-Junior EA, Paludo CR, Valadares L, Lopes NP, Do Nascimento FS, Pupo MT (2017) Aflatoxins produced by Aspergillus nomius ASR3, a pathogen isolated from the leaf-cutter ant Atta sexdens rubropilosa. Rev Bras Farmacogn 27:529–532. https://doi.org/10.1016/j.bjp.2017.05.001
Dângelo RAC, de Souza DJ, Mendes TD, Couceiro J da C, Lucia TMC Della (2016) Actinomycetes inhibit filamentous fungi from the cuticle of Acromyrmex leafcutter ants. J Basic Microbiol 56:229–237. https://doi.org/10.1002/jobm.201500593
Delgado-Baquerizo M, Eldridge DJ, Hamonts K, Singh BK (2019) Ant colonies promote the diversity of soil microbial communities. ISME J 13:1114–1118. https://doi.org/10.1038/s41396-018-0335-2
Della Lucia TM, Gandra LC, Guedes RN (2014) Managing leaf-cutting ants: peculiarities, trends and challenges. Pest Manag Sci 70:14–23. https://doi.org/10.1002/ps.3660
Desireé M, Medina D, Morales GG, Daniel F, Castillo H, María Y, Fuente O, Flores Olivas A (2013) Actinomicetos antagónicos contra hongos fitopatógenos de importancia agrícola. Rev Mex De Cienc Agric 4:1187–1196
De-Wei L (2016) Introduction: advances and predicament. In: De-Wei L (ed) Biology of microfungi. Springer International Publishing, Cham, pp 1–6
Dhodary B, Schilg M, Wirth R, Spiteller D (2018) Secondary metabolites from Escovopsis weberi and their role in attacking the garden fungus of leaf-cutting ants. Chem Eur J 24:4445–4452. https://doi.org/10.1002/chem.201706071
Dostál P, Březnová M, Kozlíčková V, Herben T, Kovář P (2005) Ant-induced soil modification and its effect on plant below-ground biomass. Pedobiologia 49:127–137. https://doi.org/10.1016/j.pedobi.2004.09.004
Duarte APM, Attili-Angelis D, Baron NC, Forti LC, Pagnocca FC (2014) Leaf-cutting ants: an unexpected microenvironment holding human opportunistic black fungi. Antonie Van Leeuwenhoek 106:465–473. https://doi.org/10.1007/s10482-014-0215-3
Duff LB, Urichuk TM, Hodgins LN, Young JR, Untereiner WA (2016) Diversity of fungi from the mound nests of Formica ulkei and adjacent non-nest soils. Can J Microbiol 62:562–571. https://doi.org/10.1139/cjm-2015-0628
Efimenko TA, Glukhova AA, Demiankova MV, Boykova YV, Malkina ND, Sumarukova IG, Vasilieva BF, Rogozhin EA, Ivanov IA, Krassilnikov VA, Efremenkova OV (2020) Antimicrobial activity of microorganisms isolated from ant nests of Lasius niger. Life 10:91. https://doi.org/10.3390/life10060091
Elsebai MF, Saleem M, Tejesvi Mv, Kajula M, Mattila S, Mehiri M, Turpeinen A, Pirttilä AM (2014) Fungal phenalenones: chemistry, biology, biosynthesis and phylogeny. Nat Prod Rep 31:628–645
Espadaler X, Santamaria S (2012) Ecto- and endoparasitic fungi on ants from the Holarctic Region. Psyche 2012:168478. https://doi.org/10.1155/2012/168478
Fernandez A, Farji-Brener AG, Satti P (2014) Moisture enhances the positive effect of leaf-cutting ant refuse dumps on soil biota activity. Austral Ecol 39:198–203. https://doi.org/10.1111/aec.12059
Fernández F (2003) Breve introducción a la biología social de las hormigas. In Fernández F (ed) Introducción a las hormigas de la región Neotropical, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, pp 89–96
Fisher PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leaf-cutting ant Atta cephalotes: a preliminary study. Mycol Res 100:541–546. https://doi.org/10.1016/S0953-7562(96)80006-2
Folgarait PJ, Marfetán JA, Cafaro MJ (2011) Growth and conidiation response of Escovopsis weberi (Ascomycota: Hypocreales) against the fungal cultivar of Acromyrmex lundii (Hymenoptera: Formicidae). Environ Entomol 40:342–349. https://doi.org/10.1603/EN10111
Freinkman E, Oh DC, Scott JJ, Currie CR, Clardy J (2009) Bionectriol A, a polyketide glycoside from the fungus Bionectria sp. associated with the fungus-growing ant Apterostigma dentigerum. Tetrahedron Lett 50:6834–6837. https://doi.org/10.1016/j.tetlet.2009.09.120
Frey Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol R 75:583–609. https://doi.org/10.1128/mmbr.00020-11
Fukuda TTH, Helfrich EJN, Mevers E, Melo WGP, van Arnam EB, Andes DR, Currie CR, Pupo MT, Clardy J (2021) Specialized metabolites reveal evolutionary history and geographic dispersion of a multilateral symbiosis. ACS Cent Sci 7:292–299. https://doi.org/10.1021/acscentsci.0c00978
Gemperline E, Horn HA, Delaney K, Currie CR, Li L (2017) Imaging with mass spectrometry of bacteria on the exoskeleton of fungus-growing ants. ACS Chem Biol 12:1980–1985. https://doi.org/10.1021/acschembio.7b00038
Ghorai S, Banik SP, Verma D, Chowdhury S, Mukherjee S, Khowala S (2009) Fungal biotechnology in food and feed processing. Food Res Int 42:577–587. https://doi.org/10.1016/j.foodres.2009.02.019
Ginzburg O, Whitford WG, Steinberger Y (2008) Effects of harvester ant (Messor spp.) activity on soil properties and microbial communities in a Negev Desert ecosystem. Biol Fertil Soils 45:165–173. https://doi.org/10.1007/s00374-008-0309-z
Glöckner FO, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A, Bruns G, Yarza P, Peplies J, Westram R, Ludwig W (2017) 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol 261:169–176
Godoy MFP, Victor SR, Bellini AM, Guerreiro G, Rocha WC, Bueno OC, Hebling MJA, Bacci M, Fátima M, Da Silva GF, Vieira PC, Fernandes JB, Pagnocca FC (2005) Inhibition of the symbiotic fungus of leaf-cutting ants by coumarins. J Bras Chem Soc 16:669–672. https://doi.org/10.1590/S0103-50532005000400031
Goes AC, Kooij PW, Culot L, Bueno OC, Rodrigues A (2022) Distinct and enhanced hygienic responses of a leaf-cutting ant toward repeated fungi exposures. Ecol Evol 12:e9112. https://doi.org/10.1002/ece3.9112
Goldstein SL, Klassen JL (2020) Pseudonocardia symbionts of fungus-growing ants and the evolution of defensive secondary metabolism. Front Microbiol 11:621041. https://doi.org/10.3389/fmicb.2020.621041
Gómez-Díaz JS, Niño-Castro A, Valencia-Giraldo SM, Cotazo-Calambas KM (2022) Hygienic behavior and antimicrobial peptide expression of the leaf-cutting ant Atta cephalotes (Hymenoptera, Formicidae) to Metharhizium anisopliae. J Hymenopt Res 91:335–356. https://doi.org/10.3897/JHR.91.82381
González-Medina M, Owen JR, El-Elimat T, Pearce CJ, Oberlies NH, Figueroa M, Medina-Franco JL (2017) Scaffold diversity of fungal metabolites. Front Pharmacol 8:180. https://doi.org/10.3389/fphar.2017.00180
González-Medina M, Prieto-Martínez FD, Naveja JJ, Méndez-Lucio O, El-Elimat T, Pearce CJ, Oberlies NH, Figueroa M, Medina-Franco JL (2016) Chemoinformatic expedition of the chemical space of fungal products. Future Med Chem 8:1399–1412. https://doi.org/10.4155/fmc-2016-0079
Guedes FLA, Attili-Angelis D, Pagnocca FC (2012) Selective isolation of dematiaceous fungi from the workers of Atta laevigata (Formicidae: Attini). Folia Microbiol 57:21–26. https://doi.org/10.1007/s12223-011-0081-6
Haeder S, Wirth R, Herz H, Spiteller D (2009) Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Natl Acad Sci USA 106:4742–4746. https://doi.org/10.1073/pnas.0812082106
Hansen KA, Kim RR, Lawton ES, Tran J, Lewis SK, Deol AS, Van Arnam EB (2022) Bacterial associates of a desert specialist fungus-growing ant antagonize competitors with a nocamycin analog. ACS Chem Biol 17:1824–1830. https://doi.org/10.1021/acschembio.2c00187
Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr 5:79–95. https://doi.org/10.1128/microbiolspec.FUNK-0052-2016
Heine D, Holmes NA, Worsley SF, Santos ACA, Innocent TM, Scherlach K, Patrick EH, Yu DW, Murrell JC, Vieria PC, Boomsma JJ, Hertweck C, Hutchings MI, Wilkinson B (2018) Chemical warfare between leafcutter ant symbionts and a co-evolved pathogen. Nat Commun 9:2208. https://doi.org/10.1038/s41467-018-04520-1
Holmes NA, Innocent TM, Heine D, Al Bassam M, Worsley SF, Trottmann F, Patrick EH, Yu DW, Murrell JC, Schiøtt M, Wilkinson B, Boomsma JJ, Hutchings MI (2016) Genome analysis of two Pseudonocardia phylotypes associated with Acromyrmex leafcutter ants reveals their biosynthetic potential. Front Microbiol 7:2073. https://doi.org/10.3389/fmicb.2016.02073
Huff T, Kuball HG, Anke T (1994) 7-Chloro-4,6–dimethoxy-1 (3H)-isobenzofurane and basidalin: antibiotic secondary metabolites from Leucoagaricus carneifolia Gillet (Basidiomycetes). Z Naturforsch C J Biosci 49:407–410. https://doi.org/10.1515/znc-1994-7-803
Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ (2004) Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertebr Pathol 85:46–53. https://doi.org/10.1016/j.jip.2003.12.005
Hyde KD, Xu J, Rapior S, Jeewon R, Lumyong S, Niego AGT, Abeywickrama PD, Aluthmuhandiram JVS, Brahamanage RS, Brooks S, Chaiyasen A, Chethana KWT, Chomnunti P, Chepkirui C, Chuankid B, de Silva NI, Doilom M, Faulds C, Gentekaki E, Gopalan V, Kakumyan P, Harishchandra D, Hemachandran H, Hongsanan S, Karunarathna A, Karunarathna SC, Khan S, Kumla J, Jayawardena RS, Liu JK, Liu N, Luangharn T, Macabeo APG, Marasinghe DS, Meeks D, Mortimer PE, Mueller P, Nadir S, Nataraja KN, Nontachaiyapoom S, O’Brien M, Penkhrue W, Phukhamsakda C, Ramanan US, Rathnayaka AR, Sadaba RB, Sandargo B, Samarakoon BC, Tennakoon DS, Siva R, Sriprom W, Suryanarayanan TS, Sujarit K, Suwannarach N, Suwunwong T, Thongbai B, Thongklang N, Wei D, Wijesinghe SN, Winiski J, Yan J, Yasanthika E, Stadler M (2019) The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Divers 97:1–136. https://doi.org/10.1007/s13225-019-00430-9
Ilnuma H, Nakamura H, Naganawi H, Masuda T, Takano S, Takeuchi T, Umezawa H, IItaka Y, Obayashi A, (1983) Basidalin, a new antibiotic from basidiomycetes. J Antibiot 36:448–450. https://doi.org/10.7164/antibiotics.36.448
ITIS (2022) Integrated Taxonomic Information System. https://www.itis.gov/. Accessed 26 Sep 2022
Iwai K, Iwamoto S, Aisaka K, Suzuki M (2009) Isolation of novel actinomycetes from spider materials. Actinomycetologica 23:8–15. https://doi.org/10.3209/saj.SAJ230103
Jiménez-Arreola BS, Aguilar-Ramírez E, Cano-Sánchez P, Morales-Jiménez J, González-Andrade M, Medina-Franco JL, Rivera-Chávez J (2020) Dimeric phenalenones from Talaromyces sp. (IQ-313) inhibit hPTP1B1-400: insights into mechanistic kinetics from in vitro and in silico studies. Bioorg Chem 101:103893. https://doi.org/10.1016/j.bioorg.2020.103893
Jiménez-Gómez I, Barcoto MO, Montoya QV, Goes AC, Monteiro LSVE, Bueno OC, Rodrigues A (2021) Host susceptibility modulates escovopsis pathogenic potential in the fungiculture of higher Attine ants. Front Microbiol 12:673444. https://doi.org/10.3389/fmicb.2021.673444
Johansson H, Dhaygude K, Lindström S, Helanterä H, Sundström L, Trontti K (2013) A metatranscriptomic approach to the identification of microbiota associated with the ant Formica exsecta. PLoS ONE 8:e0079777. https://doi.org/10.1371/journal.pone.0079777
Kaspari M, Stevenson BS, Shik J, Kerekes JF (2010) Scaling community structure: how bacteria, fungi, and ant taxocenes differentiate along a tropical forest floor. Ecology 91:2221–2226. https://doi.org/10.1890/09-2089.1
Kobmoo N, Mongkolsamrit S, Wutikhun T, Tasanathai K, Khonsanit A, Thanakitpipattana D, Luangsa-Ard JJ (2015) New species of Ophiocordyceps unilateralis, an ubiquitous pathogen of ants from Thailand. Fungal Biol 119:44–52. https://doi.org/10.1016/j.funbio.2014.10.008
Kristiansen SM, Amelung W (2001) Abandoned anthills of Formica polyctena and soil heterogeneity in a temperate deciduous forest: morphology and organic matter composition. Eur J Soil Sci 52:355–363. https://doi.org/10.1046/j.1365-2389.2001.00390.x
Kyle KE, Puckett SP, Mauricio Caraballo-Rodríguez A, Rivera-Chávez J, Samples RM, Earp CE, Raja HA, Pearce CJ, Ernst M, van der Hooft JJ, Adams ME, Oberlies NH, Dorrestein PC, Klassen JL, Balunas MJ (2023) Trachymyrmex septentrionalis ants promote fungus garden hygiene using Trichoderma-derived metabolite cues. bioRxiv 2022.11.12. https://doi.org/10.1101/2022.11.12.516288
Laakso J, Setälä H, Setala H (1998) Composition and trophic structure of detrital food web in ant nest mounds of Formica aquilonia and in the surrounding forest soil. Oikos 81:266. https://doi.org/10.2307/3547047
Leal IR, Silva PSD, Oliveira PS (2011) Natural history and ecological correlates of fungus-growing ants (Formicidae: Attini) in the neotropical cerrado savanna. Ann Entomol Soc Am 104:901–908. https://doi.org/10.1603/AN11067
Li H, Sosa-Calvo J, Horn HA, Pupo MT, Clardy J, Rabeling C, Schultz TR, Currie CR (2018) Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. Proc Natl Acad Sci USA 115:10720–10725. https://doi.org/10.1073/pnas.1809332115
Lindström S, Rowe O, Timonen S, Sundström L, Johansson H (2018) Trends in bacterial and fungal communities in ant nests observed with terminal-restriction fragment length polymorphism (T-RFLP) and next generation sequencing (NGS) techniques-validity and compatibility in ecological studies. PeerJ. https://doi.org/10.7717/peerj.5289
Lindström S, Timonen S, Sundström L (2021) The bacterial and fungal community composition in time and space in the nest mounds of the ant Formica exsecta (Hymenoptera: Formicidae). Microbiologyopen 10:e1201. https://doi.org/10.1002/mbo3.1201
Lindström S, Timonen S, Sundström L, Johansson H (2019) Ants reign over a distinct microbiome in forest soil. Soil Biol Biochem 139:107529. https://doi.org/10.1016/j.soilbio.2019.107529
Little AEF, Currie CR (2008) Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216–1222. https://doi.org/10.1890/07-0815.1
Little AEF, Currie CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biol Lett 3:501–504. https://doi.org/10.1098/rsbl.2007.0253
Little AEF, Murakami T, Mueller UG, Currie CR (2006) Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens. Biol Lett 2:12–16. https://doi.org/10.1098/rsbl.2005.0371
López Arismendy E, Orduz Peralta S (2002) Metarhizium anisopliae y Trichoderma viride controlan colonias de Atta cephalotes en campo mejor que un insecticida químico. Rev Colomb Biotecnol 4:71–78
Lucas J, Bill B, Stevenson B, Kaspari M (2017) The microbiome of the ant-built home: the microbial communities of a tropical arboreal ant and its nest. Ecosphere 8:e1639. https://doi.org/10.1002/ecs2.1639
Lucas JM, Madden AA, Penick CA, Epps MJ, Marting PR, Stevens JL, Fergus DJ, Dunn RR, Meineke EK (2019) Azteca ants maintain unique microbiomes across functionally distinct nest chambers. Proc R Soc B Biol Sci 286:20191026. https://doi.org/10.1098/rspb.2019.1026
Lugo AM, Crespo ME, Cafao M, Jofré L (2013) Hongos asociados con dos poblaciones de Acromyrmex lobicornis (Formicidae) de San Luis, Argentina. Bol Soc Argent Bot 48:5–15
Luiso J, Kellner K, Matthews AE, Mueller UG, Seal JN (2020) High diversity and multiple invasions to North America by fungi grown by the northern-most Trachymyrmex and Mycetomoellerius ant species. Fungal Ecol 44:100878. https://doi.org/10.1016/j.funeco.2019.100878
Lupala AS, Oh SY, Park MS, Kim T, Yoo JS, Seelan JSS, Lim YW (2019) Co-occurrence patterns of wood-decaying fungi and ants in dead pines of South Korea. J Asia Pac Entomol 22:1154–1160. https://doi.org/10.1016/j.aspen.2019.10.009
Madden AA, Grassetti A, Soriano JAN, Starks PT (2013) Actinomycetes with antimicrobial activity isolated from paper wasp (Hymenoptera: Vespidae: Polistinae) nests. Environ Entomol 42:703–710. https://doi.org/10.1603/EN12159
Magnus P, Mansley TE (1999) Synthesis of the ABCD-rings of the insecticidal indole alkaloid nodulisporic acid. Tetrahedron Lett 40:6909–6912. https://doi.org/10.1016/S0040-4039(99)01355-6
Maksimova IA, Glushakova AM, Kachalkin AV, Chernov IY, Panteleeva SN, Reznikova ZI (2016) Yeast communities of Formica aquilonia colonies. Microbiology 85:124–129. https://doi.org/10.1134/S0026261716010045
Małagocka J, Jensen AB, Eilenberg J (2017) Pandora formicae, a specialist ant pathogenic fungus: new insights into biology and taxonomy. J Invertebr Pathol 143:108–114. https://doi.org/10.1016/j.jip.2016.12.007
Mankowski ME, Morrell JJ (2004) Yeasts associated with the infrabuccal pocket and colonies of the carpenter ant Camponotus vicinus. Mycologia 96:226–231. https://doi.org/10.1080/15572536.2005.11832972
Mans DR, Sairras S, Ganga D, Kartopawiro J (2016) Exploring the global animal biodiversity in the search for new drugs - insects. J Transl Sci 3:371–386. https://doi.org/10.15761/JTS.1000164
Masiulionis VE, Pagnocca FC (2020) In vitro study of volatile organic compounds produced by the mutualistic fungus of leaf-cutter ants and the antagonist Escovopsis. Fungal Ecol 48:100986. https://doi.org/10.1016/j.funeco.2020.100986
Mayer VE, Voglmayr H (2009) Mycelial carton galleries of Azteca brevis (Formicidae) as a multi-species network. Proc R Soc B Biol Sci 276:3265–3273. https://doi.org/10.1098/rspb.2009.0768
Meena H, Siddhardha B (2019) Global scenario of fungal white biotechnology: past, present, and future. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi. Springer International Publishing, Cham, pp 537–571
Menegatti C, Fukuda TTH, Pupo MT (2021) Chemical ecology in insect-microbe interactions in the neotropics. Planta Med 87:38–48. https://doi.org/10.1055/a-1229-9435
Middelhoven WJ, Fonseca A, Carreiro SC, Pagnocca FC, Bueno OC (2003) Cryptococcus haglerorum, sp. nov., an anamorphic basidiomycetous yeast isolated from nests of the leaf-cutting ant Atta sexdens. Antonie Van Leeuwenhoek 83:167–174. https://doi.org/10.1023/A:1023384830802
Miranda Duarte AP (2013) Fungos negros derivados de Atta spp.: diversidad e fatores de virulencia. Dissertation, Universidad Estatal Paulista Júlio de Mesquita Filho
Montoya QV, Martiarena MJS, Bizarria R, Gerardo NM, Rodrigues A (2021) Fungi inhabiting attine ant colonies: reassessment of the genus Escovopsis and description of Luteomyces and Sympodiorosea gens. nov. IMA Fungus 12:23. https://doi.org/10.1186/s43008-021-00078-8
Montoya QV, Meirelles LA, Chaverri P, Rodrigues A (2016) Unraveling Trichoderma species in the attine ant environment: description of three new taxa. Antonie Van Leeuwenhoek 109:633–651. https://doi.org/10.1007/s10482-016-0666-9
Moreau CS (2020) Symbioses among ants and microbes. Curr Opin Insect Sci 39:1–5. https://doi.org/10.1016/j.cois.2020.01.002
Moreno LF, Mayer V, Voglmayr H, Blatrix R, Benjamin Stielow J, Teixeira MM, Vicente VA, de Hoog S (2019) Genomic analysis of ant domatia-associated melanized fungi (Chaetothyriales, Ascomycota). Mycol Prog 18:541–552. https://doi.org/10.1007/s11557-018-01467-x
Mueller UG, Dash D, Rabeling C, Rodrigues A (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62:2894–2912. https://doi.org/10.1111/j.1558-5646.2008.00501.x
Mueller UG, Ishak HD, Bruschi SM, Smith CC, Herman JJ, Solomon SE, Mikheyev AS, Rabeling C, Scott JJ, Cooper M, Rodrigues A, Ortiz A, Brandão CRF, Lattke JE, Pagnocca FC, Rehner SA, Schultz TR, Vasconcelos HL, Adams RMM, Bollazzi M, Clark RM, Himler AG, LaPolla JS, Leal IR, Johnson RA, Roces F, Sosa-Calvo J, Wirth R, Bacci M (2017) Biogeography of mutualistic fungi cultivated by leafcutter ants. Mol Ecol 26:6921–6937. https://doi.org/10.1111/mec.14431
Nair MSR, Hervey A (1979) Structure of lepiochlorin, an antibiotic metabolite of a fungus cultivated by ants. Phytochemistry 18:326–327. https://doi.org/10.1016/0031-9422(79)80085-0
Nascimento MO, Teles Tenório AC, Sarmento RA, de Melo R, CC, della Lucia TMC, Dias Amaral K, Souza DJ, (2022) Soil actinobacteria inhibit antagonistic fungi of leafcutter ant colonies. J Basic Microbiol 62:63–73. https://doi.org/10.1002/jobm.202100476
Nepel M, Voglmayr H, Blatrix R, Longino JT, Fiedler K, Schönenberger J, Mayer VE (2016) Ant-cultivated Chaetothyriales in hollow stems of myrmecophytic Cecropia sp. trees – diversity and patterns. Fungal Ecol 23:131–140. https://doi.org/10.1016/j.funeco.2016.07.007
Nepel M, Voglmayr H, Schönenberger J, Mayer VE (2014) High diversity and low specificity of Chaetothyrialean fungi in carton galleries in a neotropical ant-plant association. PLoS ONE 9:e0112756. https://doi.org/10.1371/journal.pone.0112756
O’Brien J, Wright GD (2011) An ecological perspective of microbial secondary metabolism. Curr Opin Biotechnol 22:552–558. https://doi.org/10.1016/j.copbio.2011.03.010
Offenberg J, Damgaard C (2019) Ants suppressing plant pathogens: a review. Oikos 128:1691–1703. https://doi.org/10.1111/oik.06744
Offenberg J, Jensen IC, Hansen RR (2022) Combatting plant diseases with ant chemicals: a review and meta-analysis. J Appl Ecol 59:25–38. https://doi.org/10.1111/1365-2664.14017
Oh DC, Poulsen M, Currie CR, Clardy J (2009) Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 5:391–393. https://doi.org/10.1038/nchembio.159
OMS (2020) Resistencia a los antimicrobianos. https://www.who.int/es/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed 12 May 2023
Orivel J, Leroy C (2010) The diversity and ecology of ant gardens (Hymenoptera: Formicidae; Spermatophyta: Angiospermae). Myrmecol News 14:73–85
Ortega HE, Lourenzon VB, Chevrette MG, Ferreira LLG, Alvarenga RFR, Melo WGP, Venâncio T, Currie CR, Andricopulo AD, Bugni TS, Pupo MT (2021) Antileishmanial macrolides from ant-associated Streptomyces sp. ISID311. Bioorg Med Chem 32:116016. https://doi.org/10.1016/j.bmc.2021.116016
Ortiz A, Orduz S (2001) In vitro evaluation of Trichoderma and Gliocladium antagonism against the symbiotic fungus of the leaf-cutting ant Atta cephalotes. Mycopathologia 150:53–60. https://doi.org/10.1023/A:1010843413085
Pagnocca FC, Legaspe MFC, Rodrigues A, Ruivo CCC, Nagamoto NS, Bacci M, Forti LC (2010) Yeasts isolated from a fungus-growing ant nest, including the description of Trichosporon chiarellii sp. nov., an anamorphic basidiomycetous yeast. Int J Syst Evol Microbiol 60:1454–1459. https://doi.org/10.1099/ijs.0.015727-0
Pagnocca FC, Rodrigues A, Nagamoto NS, Bacci M (2008) Yeasts and filamentous fungi carried by the gynes of leaf-cutting ants. Antonie Van Leeuwenhoek 94:517–526. https://doi.org/10.1007/s10482-008-9268-5
Parmentier T, De Laender F, Bonte D (2020) The topology and drivers of ant–symbiont networks across Europe. Biol Rev 95:1664–1688. https://doi.org/10.1111/brv.12634
Pathak A, Kett S, Marvasi M (2019) Resisting antimicrobial resistance: lessons from fungus farming ants. Trends Ecol Evol 34:974–976. https://doi.org/10.1016/j.tree.2019.08.007
Pereira JS, Costa RR, Nagamoto NS, Forti LC, Pagnocca FC, Rodrigues A (2016) Comparative analysis of fungal communities in colonies of two leaf-cutting ant species with different substratum preferences. Fungal Ecol 21:68–75. https://doi.org/10.1016/j.funeco.2016.03.004
Pham JV, Yilma MA, Feliz A, Majid MT, Maffetone N, Walker JR, Kim E, Cho HJ, Reynolds JM, Song MC, Park SR, Yoon YJ (2019) A review of the microbial production of bioactive natural products and biologics. Front Microbiol 10:1404. https://doi.org/10.3389/fmicb.2019.01404
Pietrobon T de C, Kooij PW, Montoya QV, Rodrigues A (2022) Escovopsioides nivea is a non-specific antagonistic symbiont of ant-fungal crops. Fungal Ecol 56:101140. https://doi.org/10.1016/j.funeco.2022.101140
Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST, Wallace Cleland W, Weimer PJ, Currie CR (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123. https://doi.org/10.1126/science.1173036
Poulsen M, Cafaro MJ, Erhardt DP, Little AEF, Gerardo NM, Tebbets B, Klein BS, Currie CR (2009) Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Environ Microbiol Rep 2:534–540. https://doi.org/10.1111/j.1758-2229.2009.00098.x
Poulsen M, Oh DC, Clardy J, Currie CR (2011) Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS ONE 6:e16763. https://doi.org/10.1371/journal.pone.0016763
Pringle EG, Moreau CS (2017) Community analysis of microbial sharing and specialization in a Costa Rican ant – plant – hemipteran symbiosis. P R Soc B 284. https://doi.org/10.1098/rspb.2016.2770
Promnuan Y, Promsai S, Pathom-Aree W, Meelai S (2021) Apis andreniformis associated actinomycetes show antimicrobial activity against black rot pathogen (Xanthomonas campestris pv. campestris). PeerJ 9. https://doi.org/10.7717/peerj.12097
Quan Y, Ahmed SA, Menezes da Silva N, Al-Hatmi AMS, Mayer VE, Deng S, Kang Y, Sybren de Hoog G, Shi D (2021) Novel black yeast-like species in Chaetothyriales with ant-associated life styles. Fungal Biol 125:276–284. https://doi.org/10.1016/j.funbio.2020.11.006
Ramadhar TR, Beemelmanns C, Currie CR, Clardy J (2014) Bacterial symbionts in agricultural systems provide a strategic source for antibiotic discovery. J Antibiot 67:53–58. https://doi.org/10.1038/ja.2013.77
Reis BM dos S, Silva A, Alvarez MR, de Oliveira TB, Rodrigues A (2015) Fungal communities in gardens of the leafcutter ant Atta cephalotes in forest and cabruca agrosystems of southern Bahia State (Brazil). Fungal Biol 119:1170–1178. https://doi.org/10.1016/j.funbio.2015.09.001
Reynolds HT, Currie CR (2004) Pathogenicity of Escovopsis weberi: the parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96:955–959. https://doi.org/10.1080/15572536.2005.11832895
Ribeiro MMR, Amaral KD, Seide VE, Souza BMR, Della Lucia TMC, Kasuya MCM, De Souza DJ (2012) Diversity of fungi associated with Atta bisphaerica (Hymenoptera: Formicidae): the activity of Aspergillus ochraceus and Beauveria bassiana. Psyche 2012:389806. https://doi.org/10.1155/2012/389806
Ríos-Casanova L (2014) Biodiversity of ants in Mexico. Rev Mex Biodivers 85:392–398. https://doi.org/10.7550/rmb.32519
Rocha SL, Evans HC, Jorge VL, Cardoso LAO, Pereira FST, Rocha FB, Barreto RW, Hart AG, Elliot SL (2017) Recognition of endophytic Trichoderma species by leaf-cutting ants and their potential in a trojan-horse management strategy. R Soc Open Sci 4. https://doi.org/10.1098/rsos.160628
Rodrigues A, Bacci M, Mueller UG, Ortiz A, Pagnocca FC (2008) Microfungal “weeds” in the leafcutter ant symbiosis. Microb Ecol 56:604–614. https://doi.org/10.1007/s00248-008-9380-0
Rodrigues A, Cable RN, Mueller UG, Bacci M, Pagnocca FC (2009) Antagonistic interactions between garden yeasts and microfungal garden pathogens of leaf-cutting ants. Antonie Van Leeuwenhoek 96:331–342. https://doi.org/10.1007/s10482-009-9350-7
Rodrigues A, Mueller UG, Ishak HD, Bacci M, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78:244–255. https://doi.org/10.1111/j.1574-6941.2011.01152.x
Rodrigues A, Pagnocca F, Bueno O, Pfenning LH, Bacci M (2005a) Assessment of microfungi in fungus gardens free of the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology 46:329–334
Rodrigues A, Pagnocca FC, Bacci M, Hebling MJA, Bueno OC, Pfenning LH (2005b) Variability of non-mutualistic filamentous fungi associated with Atta sexdens rubropilosa nests. Folia Microbiol 50:421. https://doi.org/10.1007/BF02931424
Rodrigues A, Passarini MRZ, Ferro M, Nagamoto NS, Forti LC, Bacci M, Sette LD, Pagnocca FC (2014) Fungal communities in the garden chamber soils of leaf-cutting ants. J Basic Microbiol 54:1186–1196. https://doi.org/10.1002/jobm.201200458
Rojas Fernández P (2001) Las hormigas del suelo en México: Diversidad, distribución e importancia (Hymenoptera: Formicidae). Acta Zool Mex 189–238. https://doi.org/10.21829/azm.2001.8401851
Ruiz-González MX, Malé PJG, Leroy C, Dejean A, Gryta H, Jargeat P, Quilichini A, Orivel J (2011) Specific, non-nutritional association between an ascomycete fungus and Allomerus plant-ants. Biol Lett 7:475–479. https://doi.org/10.1098/rsbl.2010.0920
Russell JA, Sanders JG, Moreau CS (2017) Hotspots for symbiosis: function, evolution, and specificity of ant-microbe associations from trunk to tips of the ant phylogeny (Hymenoptera: Formicidae). Myrmecol News 24:43–69
Sakolrak B, Blatrix R, Sangwanit U, Arnamnart N, Noisripoom W, Thanakitpipattana D, Buatois B, Hossaert-McKey M, Kobmoo N (2018) Ant-produced chemicals are not responsible for the specificity of their Ophiocordyceps fungal pathogens. Fungal Ecol 32:80–86. https://doi.org/10.1016/j.funeco.2017.11.005
Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI (2004) Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 239:319–323. https://doi.org/10.1016/j.femsle.2004.09.005
Scherlach K, Graupner K, Hertweck C (2013) Molecular bacteria-fungi interactions: effects on environment, food, and medicine. Annu Rev Microbiol 67:375–397. https://doi.org/10.1146/annurev-micro-092412-155702
Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D (2011) Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci USA 108:1955–1960. https://doi.org/10.1073/pnas.1008441108
Schueffler A, Anke T (2014) Fungal natural products in research and development. Nat Prod Rep 31:1425–1448. https://doi.org/10.1039/c4np00060a
Seabrooks L, Hu L (2017) Insects: an underrepresented resource for the discovery of biologically active natural products. Acta Pharm Sin B 7:409–426. https://doi.org/10.1016/j.apsb.2017.05.001
Seifert KA, Samson RA, Chapela IH (1995) Escovopsis aspergilloides, a rediscovered hyphomycete from leaf-cutting ant nests. Mycologia 87:407–413. https://doi.org/10.1080/00275514.1995.12026546
Seipke RF, Barke J, Brearley C, Hill L, Yu DW, Goss RJM, Hutchings MI (2011) A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS ONE 6:4–11. https://doi.org/10.1371/journal.pone.0022028
Seipke RF, Barke J, Ruiz-Gonzalez MX, Orivel J, Yu DW, Hutchings MI (2012) Fungus-growing Allomerus ants are associated with antibiotic-producing actinobacteria. Antonie Van Leeuwenhoek 101:443–447. https://doi.org/10.1007/s10482-011-9621-y
Selim MSM, Abdelhamid SA, Mohamed SS (2021) Secondary metabolites and biodiversity of actinomycetes. J Genet Eng Biotechnol 19:72. https://doi.org/10.1186/s43141-021-00156-9
Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, Mueller UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci USA 106:17805–17810. https://doi.org/10.1073/pnas.0904827106
Siedlecki I, Gorczak M, Okrasińska A, Wrzosek M (2021) Chance or necessity—the fungi co−occurring with Formica polyctena ants. Insects 12:204. https://doi.org/10.3390/insects12030204
Singh SB, Ondeyka JG, Schleift WA, Felock P, Hazuda DJ (2003) Chemistry and structure-activity relationship of HIV-1 integrase inhibitor integracide B and related natural products. J Nat Prod 66:1338–1344. https://doi.org/10.1021/np030211s
Sit CS, Ruzzini AC, van Arnam EB, Ramadhar TR, Currie CR, Clardy J, Sit CS, Ruzzini AC, van Arnam EB, Ramadhar TR, Currie CR (2015) Variable genetic architectures produce virtually identical molecules in bacterial symbionts of fungus-growing ants. Proc Natl Acad Sci USA 112:E6717. https://doi.org/10.1073/pnas.1521903112
Smetanina OF, Kalinovsky AI, Khudyakova YV, Pivkin MV, Dmitrenok PS, Fedorov SN, Ji H, Kwak J-Y, Kuznetsova TA (2007) Indole alkaloids produced by a marine fungus isolate of Penicillium janthinellum Biourge. J Nat Prod 70:906–909. https://doi.org/10.1021/np060396d
Snyder SR, Crist TO, Friese CF (2002) Variability in soil chemistry and arbuscular mycorrhizal fungi in harvester ant nests: the influence of topography, grazing and region. Biol Fertil Soils 35:406–413. https://doi.org/10.1007/s00374-002-0487-z
Sokolova YY, Fuxa JR (2008) Biology and life-cycle of the microsporidium Kneallhazia solenopsae Knell Allan Hazard 1977 gen. n., comb. n., from the fire ant Solenopsis invicta. Parasitology 135:903–929. https://doi.org/10.1017/S003118200800440X
Sosa-Calvo J, Schultz TR, JeŠovnik A, Dahan RA, Rabeling C (2018) Evolution, systematics, and natural history of a new genus of cryptobiotic fungus-growing ants. Syst Entomol 43:549–567. https://doi.org/10.1111/syen.12289
Sousa KKA, Catalani GC, Gianeti TMR, Camargo RS, Caldato N, Ramos VM, Forti LC (2020) A volatile semiochemical released by the fungus garden of leaf-cutting ants. Fla Entomol 103:1. https://doi.org/10.1653/024.103.0401
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Tarsa C, McMillan A, Warren RJ (2018) Plant pathogenic fungi decrease in soil inhabited by seed-dispersing ants. Insect Soc 65:315–321. https://doi.org/10.1007/s00040-018-0618-7
Van Arnam EB, Currie CR, Clardy J (2018) Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 47:1638–1651. https://doi.org/10.1039/c7cs00340d
Van Bael SA, Fernández-Marín H, Valencia MC, Rojas EI, Wcislo WT, Herre EA (2009) Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. P R Soc B 276:2419–2426. https://doi.org/10.1098/rspb.2009.0196
Van Bael SA, Seid MA, Wcislo WT (2012) Endophytic fungi increase the processing rate of leaves by leaf-cutting ants (Atta). Ecol Entomol 37:318–321. https://doi.org/10.1111/j.1365-2311.2012.01364.x
Van Borm S, Billen J, Boomsma JJ (2002) The diversity of microorganisms associated with Acromyrmex leafcutter ants. BMC Evol Biol 2:9. https://doi.org/10.1186/1471-2148-2-9
Van Moll L, De Smet J, Cos P, Van Campenhout L (2021) Microbial symbionts of insects as a source of new antimicrobials: a review. Crit Rev Microbiol 47:562–579. https://doi.org/10.1080/1040841X.2021.1907302
Vander Meer R (2012) Ant interactions with soil organisms and associated semiochemicals. J Chem Ecol 38:728–745. https://doi.org/10.1007/s10886-012-0140-8
Vieira AS, Morgan ED, Drijfhout FP, Camargo-Mathias MI (2012) Chemical composition of metapleural gland secretions of fungus-growing and non-fungus-growing ants. J Chem Ecol 38:1289–1297. https://doi.org/10.1007/s10886-012-0185-8
Voglmayr H, Mayer V, Maschwitz U, Moog J, Djieto-Lordon C, Blatrix R (2011) The diversity of ant-associated black yeasts: insights into a newly discovered world of symbiotic interactions. Fungal Biol 115:1077–1091. https://doi.org/10.1016/j.funbio.2010.11.006
Wagner D, Brown MJF, Gordon DM (1997) Harvester ant nests, soil biota and soil chemistry. Oecologia 112:232–236. https://doi.org/10.1007/s004420050305
Wang B, You J, King JB, Cai S, Park E, Powell DR, Cichewicz RH (2014) Polyketide glycosides from Bionectria ochroleuca inhibit Candida albicans biofilm formation. J Nat Prod 77:2273–2279. https://doi.org/10.1021/np500531j
Wang C, Wang G, Wu P, Rafique R, Zi H, Li X, Luo Y (2017) Effects of ant mounds on the plant and soil microbial community in an alpine meadow of Qinghai-Tibet plateau. Land Degrad Dev 28:1538–1548. https://doi.org/10.1002/ldr.2681
Wang Y, Mueller UG, Clardy J (1999) Antifungal diketopiperazines from symbiotic fungus of fungus-growing ant Cyphomyrmex minutus. J Chem Ecol 25:935–941. https://doi.org/10.1023/A:1020861221126
Weber NA (1957) Fungus-growing ants and their fungi: Cyphomyrmex costatus. Ecology 38:480. https://doi.org/10.2307/1929893
Weißflog A (2001) Freinestbau von Ameisen (Hymenoptera: Formicidae) in der Kronenregion feuchttropischer Wälder Südostasiens : Bestandsaufnahme und Phänologie, Ethoökologie und funktionelle Analyse des Nestbaus. Dissertation, Johann Wolfgang Goethe-Universität
Worsley S, Innocent T, Heine D, Murrell C, Yu D, Wilkinson B, Hutchings M, Boomsma J, Holmes N (2018) Symbiotic partnerships and their chemical interactions in the leafcutter ants (Hymenoptera: Formicidae). Myrmecol News 27:59–47
Wu Y, Liu Y, Yu J, Xu Y, Chen S (2022) Observation of the antimicrobial activities of two actinomycetes in the harvester ant Messor orientalis. Insects 13:691. https://doi.org/10.3390/insects13080691
Yan S, Li S, Wu W, Zhao F, Bao L, Ding R, Gao H, Wen H-A, Song F, Liu H-W (2011) Terpenoid and phenolic metabolites from the fungus Xylaria sp. associated with termite nests. Chem Biodivers 8:1689–1700. https://doi.org/10.1002/cbdv.201100026
Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev 86:774–791. https://doi.org/10.1111/j.1469-185X.2010.00170.x
Yek SH, Nash DR, Jensen AB, Boomsma JJ (2012) Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants. P R Soc B 279:4215–4222. https://doi.org/10.1098/rspb.2012.1458
Zhang Z, Wei Z, Wang JJ, Xiao R, Meng Y, Wu H, Lyu X (2018) Ants alter molecular characteristics of soil organic carbon determined by pyrolysis-chromatography/mass spectrometry. Appl Soil Ecol 130:91–97. https://doi.org/10.1016/j.apsoil.2018.05.020
Acknowledgements
ASAC thanks CONACyT for the scholarship (885837) for postgraduate studies.
Funding
This work was funded by the Dirección General de Asuntos del Personal Académico (DGAPA), Universidad Nacional Autónoma de México (UNAM) through the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT: IA207422 and IA203220.) It also received partial support from Consejo Nacional de Ciencia y Tecnología, México (CONACyT: CF-2019-263977).
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Aguilar-Colorado, Á.S., Rivera-Chávez, J. Ants/Nest-Associated Fungi and Their Specialized Metabolites: Taxonomy, Chemistry, and Bioactivity. Rev. Bras. Farmacogn. 33, 901–923 (2023). https://doi.org/10.1007/s43450-023-00417-3
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DOI: https://doi.org/10.1007/s43450-023-00417-3