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Duur K. Aanen - One of the best experts on this subject based on the ideXlab platform.
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high diversity and low host specificity of termitomyces symbionts cultivated by microtermes spp indicate frequent symbiont exchange
Fungal Ecology, 2020Co-Authors: Lennart J J Van De Peppel, Duur K. AanenAbstract:Abstract Fungus-growing termites (subfamily Macrotermitinae) live in an obligate mutualistic symbiosis with species of the fungal genus Termitomyces (Basidiomycota). Although the species that build large mounds are the most conspicuous, termites of the genus Microtermes construct large underground networks of tunnels connecting many Fungus Gardens. They are also the only entire genus within the Macrotermitinae in which vertical transmission of the fungal symbiont has evolved. To study patterns of genetic diversity in species of the genus Microtermes and their Termitomyces symbionts, we sampled at three different locations in South Africa and sequenced COI for the termites and ITS for the fungi. We discovered high genetic diversity in both termites and fungal symbionts but very low interaction specificity. This implies that frequent horizontal exchange of fungal symbionts occurs between species, despite vertical transmission across generations. We also estimated colony size based on termite haplotype and fungal genotype combinations and found indications that colonies may extend over large areas.
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Oligocene Termite Nests with In Situ Fungus Gardens from the Rukwa Rift Basin, Tanzania, Support a Paleogene African Origin for Insect Agriculture
PloS one, 2016Co-Authors: Eric M. Roberts, Tânia Nobre, Duur K. Aanen, Christopher N. Todd, Hannah L. Hilbert-wolf, Patrick M. O'connor, Leif Tapanila, Cassy Mtelela, Nancy J. StevensAbstract:Based on molecular dating, the origin of insect agriculture is hypothesized to have taken place independently in three clades of Fungus-farming insects: the termites, ants or ambrosia beetles during the Paleogene (66–24 Ma). Yet, definitive fossil evidence of Fungus-growing behavior has been elusive, with no unequivocal records prior to the late Miocene (7–10 Ma). Here we report fossil evidence of insect agriculture in the form of fossil Fungus Gardens, preserved within 25 Ma termite nests from southwestern Tanzania. Using these well-dated fossil Fungus Gardens, we have recalibrated molecular divergence estimates for the origins of termite agriculture to around 31 Ma, lending support to hypotheses suggesting an African Paleogene origin for termite-Fungus symbiosis; perhaps coinciding with rift initiation and changes in the African landscape.
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farming termites determine the genetic population structure of termitomyces fungal symbionts
Molecular Ecology, 2011Co-Authors: Tânia Nobre, Cecilia Fernandes, Judith Korb, Jacobus J. Boomsma, Duur K. AanenAbstract:Symbiotic interactions between macrotermitine termites and their fungal symbionts have a moderate degree of specificity. Consistent with horizontal symbiont transmission, host switching has been frequent over evolutionary time so that single termite species can often be associated with several fungal symbionts. However, even in the few termite lineages that secondarily adopted vertical symbiont transmission, the fungal symbionts are not monophyletic. We addressed this paradox by studying differential transmission of fungal symbionts by alate male and female reproductives, and the genetic population structure of Termitomyces Fungus Gardens across 74 colonies of Macrotermes bellicosus in four west and central African countries. We confirm earlier, more limited, studies showing that the Termitomyces symbionts of M. bellicosus are normally transmitted vertically and clonally by dispersing males. We also document that the symbionts associated with this termite species belong to three main lineages that do not constitute a monophyletic group. The most common lineage occurs over the entire geographical region that we studied, including west, central and southern Africa, where it is also associated with the alternative termite hosts Macrotermes subhyalinus and Macrotermes natalensis. While Termitomyces associated with these alternative hosts are horizontally transmitted and recombine freely, the genetic population structure of the same Termitomyces associated with M. bellicosus is consistent with predominantly clonal reproduction and only occasional recombination. This implies that the genetic population structure of Termitomyces is controlled by the termite host and not by the Termitomyces symbiont.
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Social-insect Fungus farming.
Current Biology, 2006Co-Authors: Duur K. Aanen, Jacobus J. BoomsmaAbstract:Which social insects rear their own food? Growing fungi for food has evolved twice in social insects: once in new-world ants about 50 million years ago; and once in old-world termites between 24 and 34 million years ago [1,2]. The termites domesticated a single fungal lineage — the extant basidiomycete genus Termitomyces — whereas the ants are associated with a larger diversity of fungal lineages (all basidiomycetes). The ants and termites forage for plant material to provision their Fungus Gardens.
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termitomyces sp associated with the termite macrotermes natalensis has a heterothallic mating system and multinucleate cells
Fungal Biology, 2005Co-Authors: Henrik H De Fine Licht, Anders Nyboe Andersen, Duur K. AanenAbstract:Fungi of the genus Termitomyces live in an obligate symbiosis with termites of the subfamily Macrotermitinae. Many species of Termitomyces frequently form fruit bodies, which develop from the Fungus comb within the nest. In this study, we determined the mating system of a species of Termitomyces associated with the South African termite Macrotermes natalensis. Termite nests were excavated and a Termitomyces sp. was isolated into pure culture from the asexual fruit bodies (nodules) growing in the Fungus Gardens. For one strain, single basidiospore cultures were obtained from basidiomes growing from the Fungus comb after incubation without termites. Using nuclear staining, we show that both comb cultures and single spore cultures have multinucleate cells and that the majority of spores has a single nucleus. However, DNA sequencing of the ITS region in the nuclear RNA gene revealed that the comb mycelium had two different ITS types that segregated in the single spore cultures, which consequently had only a single ITS type. These results unambiguously prove that the strain of Termitomyces studied here has a heterothallic mating system, with the Fungus garden of the termite mound being in the heterokaryotic phase. This is the first time the mating system of a Termitomyces species has been studied.
Cameron R Currie - One of the best experts on this subject based on the ideXlab platform.
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Burkholderia from Fungus Gardens of Fungus-growing ants produce antifungals that inhibit the specialized parasite Escovopsis
2021Co-Authors: Charlotte B. Francoeur, Adrián A. Pinto-tomás, Daniel S. May, Margaret W. Thairu, Don Q. Hoang, Olivia Panthofer, Tim S. Bugni, Mônica T. Pupo, Jon Clardy, Cameron R CurrieAbstract:ABSTRACTWithin animal associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the Fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ Fungus Gardens. Fungus Gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus spp. converting plant substrate into energy for the ants. The Fungus garden is host to specialized parasitic fungi in the genus Escovopsis. Here, we examine the potential role of Burkholderia spp. that occur within ant Fungus Gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia spp. and Paraburkholderia spp. from 50% of the 52 colonies sampled, indicating that the family Burkholderiaceae are common Fungus garden inhabitants of a diverse range of Fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of Burkholderiaceae isolates indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed these compounds as responsible for antifungal activity that inhibit Escovopsis but, at low concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the Fungus garden microbiome play an important role in maintaining the health and function of the Fungus-farming ant colony.IMPORTANCEMany organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis spp. The ants take multiple approaches, including weeding their Fungus Gardens to remove Escovopsis spores, as well as harboring Pseudonocardia that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in Fungus Gardens, Burkholderia spp., is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from Fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in Fungus Gardens, adding another possible mechanism within the Fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis.
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Metagenomics Reveals Diet-Specific Specialization of Bacterial Communities in Fungus Gardens of Grass- and Dicot-Cutter Ants.
Frontiers in microbiology, 2020Co-Authors: Lily Khadempour, Huan Fan, Nilson S Nagamoto, Miranda A Dam, Monica Tallarico Pupo, Ken Keefover-ring, Camila Carlos-shanley, Cameron R CurrieAbstract:Leaf-cutter ants in the genus Atta are dominant herbivores in the Neotropics. While most species of Atta cut dicots to incorporate into their Fungus Gardens, some species specialize on grasses. Here we examine the bacterial community associated with the Fungus Gardens of grass- and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12 Atta Fungus Gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the Fungus garden bacterial community composition between dicot- and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the Fungus Gardens are significantly different. Specifically, grass-cutter ant Fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant Fungus Gardens metagenomes are enriched in genes involved in membrane transport. Differences between community composition and functional capacity of the bacteria in the two types of Fungus Gardens reflect differences in the substrates that the ants incorporated. These results show that different substrate inputs matter for Fungus garden bacteria and shed light on the potential role of bacteria in mediating the ants' transition to the use of a novel substrate.
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Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System.
mBio, 2020Co-Authors: Charlotte B. Francoeur, Lily Khadempour, Ken Keefover-ring, Adrián A. Pinto-tomás, Rolando D. Moreira-soto, Kirsten Gotting, Adam J. Book, Cameron R CurrieAbstract:ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized Fungus Gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within Fungus Gardens. In this study, we investigated the ability of symbiotic bacteria present within Fungus Gardens of leaf-cutter ants to degrade PSCs. We cultured Fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of Fungus Gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in Fungus Gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant Fungus Gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant Gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the Fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.
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Bacteria contribute to plant secondary compound degradation in a generalist herbivore system
2019Co-Authors: Charlotte B. Francoeur, Lily Khadempour, Ken Keefover-ring, Adrián A. Pinto-tomás, Rolando D. Moreira-soto, Kirsten Gotting, Adam J. Book, Cameron R CurrieAbstract:Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized Fungus Gardens that act as external digestive systems, degrading the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within Fungus Gardens. Here, we investigate the ability of symbiotic bacteria present within Fungus Gardens of leaf-cutter ants to degrade PSCs. We cultured Fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome p450s and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we show that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using GC-MS, we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that sub-colonies of Fungus Gardens reduced α-pinene and linalool over a 36-hour period, while L. gongylophorus strains alone only reduced linalool. Overall, our results reveal that the bacterial community in Fungus Gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system.
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metagenomics reveals diet specific specialization in Fungus Gardens of grass and dicot cutter ants
bioRxiv, 2018Co-Authors: Lily Khadempour, Huan Fan, Ken Keefoverring, Camila Carlos, Nilson S Nagamoto, Miranda A Dam, Monica Tallarico Pupo, Cameron R CurrieAbstract:Leaf-cutter ants are dominant herbivores in the Neotropics. While most leaf-cutter ant species cut dicots to incorporate into their Fungus Gardens, some species specialize on grasses. Here we examine the bacterial community associated with the Fungus Gardens of grass- and dicot-cutter ants to elucidate the potential role of bacteria in leaf-cutter ant substrate specialization. We sequenced the metagenomes of 12 Atta Fungus Gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show that community composition was significantly different between dicot- and grass-cutter ants, with grass-cutter ant Fungus Gardens having significantly lower diversity and a significantly higher abundance of Pantoea, the most abundant genus overall. Reflecting this difference in community composition, the bacterial functional profiles between the Fungus Gardens are significantly different. Specifically, grass-cutter ant Fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant Fungus Gardens metagenomes are enriched in genes involved in membrane transport. Our results suggest that bacteria in leaf-cutter ant Fungus Gardens aid in nutrient supplementation, a function especially relevant for the Fungus Gardens of ants that forage grass, a plant source relatively lower in nutrient value.
Jacobus J. Boomsma - One of the best experts on this subject based on the ideXlab platform.
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Ant mediated redistribution of a xyloglucanase enzyme in Fungus Gardens of Acromyrmex echinatior
BMC microbiology, 2016Co-Authors: Pepijn W. Kooij, Jacobus J. Boomsma, Jeroen Pullens, Morten SchiøttAbstract:Background Xyloglucan is an important component in plant cell walls that herbivores cannot digest without microbial symbionts. Leaf-cutting ants are major insect herbivores in the Neo-Tropics that rely on Fungus-garden enzymes for degrading plant cell walls. However, many of these ants discard much of their harvested plant material after partial degradation, which has led to the hypothesis that the fungal symbionts are primarily producing cell wall degrading enzymes to gain access to intracellular nutrients rather than for obtaining sugars from recalcitrant cell wall polymers, such as (hemi-)cellulose.
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Unique sequences 454 dataset
2016Co-Authors: Joanito Liberti, Rachelle M M Adams, Panagiotis Sapountzis, Lars H. Hansen, Søren J. Sørensen, Jacobus J. BoomsmaAbstract:Following 454 sequencing of the 16s rRNA gene of bacterial communities of 33 samples of attine ants, Megalomyrmex ants and Fungus Gardens, 4882 unique bacterial sequences were identified. The zip file contains a table showing the distribution of sequencing reads for all unique sequences across the 33 samples, the taxonomic classification of these sequences based on the Greengenes reference set (May 2013 release), and a fasta file with all the 4882 unique sequences
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97% OTUs 454 dataset
2016Co-Authors: Joanito Liberti, Rachelle M M Adams, Panagiotis Sapountzis, Lars H. Hansen, Søren J. Sørensen, Jacobus J. BoomsmaAbstract:Following 454 sequencing of the 16s rRNA gene of bacterial communities of 33 samples of attine ants, Megalomyrmex ants and Fungus Gardens, 923 bacterial OTUs (operational taxonomic units at 97% identity) were identified. The zip file contains an OTU table showing the distribution of sequencing reads for all OTUs across the 33 samples, a taxonomy file with the classification of the OTUs based on the Greengenes reference set (May 2013 release), a fasta file with all 923 representative sequences for these OTUs, and a mapping file containing the barcode sequence for each of the 33 samples that were multiplex sequenced
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97% OTUs MiSeq diet experiment dataset
2016Co-Authors: Joanito Liberti, Rachelle M M Adams, Panagiotis Sapountzis, Lars H. Hansen, Søren J. Sørensen, Jacobus J. BoomsmaAbstract:Following MiSeq sequencing of the 16s rRNA gene of bacterial communities of 36 samples of attine ants, Megalomyrmex ants and Fungus Gardens collected after a diet manipulation experiment, 852 bacterial OTUs (operational taxonomic units at 97% identity) were identified. The zip file contains an OTU table showing the distribution of sequencing reads for all OTUs across the 36 samples, a fasta file with all 852 representative sequences for these OTUs and two taxonomy files linking the taxonomic classification of the OTUs based on the Greengenes reference set (May 2013 release) to the OTU IDs found in the OTU table and the sequence identifiers found in the fasta file
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The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides
BMC genomics, 2013Co-Authors: Morten Nedergaard Grell, Jacobus J. Boomsma, Tore Linde, Sanne Nygaard, Kåre Lehmann Nielsen, Lene LangeAbstract:The Fungus Gardens of leaf-cutting ants are natural biomass conversion systems that turn fresh plant forage into fungal biomass to feed the farming ants. However, the decomposition potential of the symbiont Leucocoprinus gongylophorus for processing polysaccharides has remained controversial. We therefore used quantifiable DeepSAGE technology to obtain mRNA expression patterns of genes coding for secreted enzymes from top, middle, and bottom sections of a laboratory Fungus-garden of Acromyrmex echinatior leaf-cutting ants. A broad spectrum of biomass-conversion-relevant enzyme genes was found to be expressed in situ: cellulases (GH3, GH5, GH6, GH7, AA9 [formerly GH61]), hemicellulases (GH5, GH10, CE1, GH12, GH74), pectinolytic enzymes (CE8, GH28, GH43, PL1, PL3, PL4), glucoamylase (GH15), α-galactosidase (GH27), and various cutinases, esterases, and lipases. In general, expression of these genes reached maximal values in the bottom section of the garden, particularly for an AA9 lytic polysaccharide monooxygenase and for a GH5 (endocellulase), a GH7 (reducing end-acting cellobiohydrolase), and a GH10 (xylanase), all containing a carbohydrate binding module that specifically binds cellulose (CBM1). Although we did not directly quantify enzyme abundance, the profile of expressed cellulase genes indicates that both hydrolytic and oxidative degradation is taking place. The fungal symbiont of Acromyrmex leaf-cutting ants can degrade a large range of plant polymers, but the conversion of cellulose, hemicellulose, and part of the pectin occurs primarily towards the end of the decomposition process, i.e. in the bottom section of the Fungus garden. These conversions are likely to provide nutrients for the Fungus itself rather than for the ants, whose colony growth and reproductive success are limited by proteins obtained from ingesting fungal gongylidia. These specialized hyphal tips are hardly produced in the bottom section of Fungus Gardens, consistent with the ants discarding old fungal biomass from this part of the garden. The transcripts that we found suggest that actively growing mycelium in the bottom of Gardens helps to maintain an optimal water balance to avoid hyphal disintegration, so the ants can ultimately discard healthy rather than decaying and diseased garden material, and to buffer negative effects of varying availability and quality of substrate across the seasons.
Henrik H De Fine Licht - One of the best experts on this subject based on the ideXlab platform.
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A Brazilian Population of the Asexual Fungus-Growing Ant Mycocepurus smithii (Formicidae, Myrmicinae, Attini) Cultivates Fungal Symbionts with Gongylidia-Like Structures
2016Co-Authors: Virginia E. Masiulionis, Henrik H De Fine Licht, Christian Rabeling, Ted Schultz, Maurı́cio Bacci, Cintia Santos M. Bezerra, O C. PagnoccaAbstract:Attine ants cultivate fungi as their most important food source and in turn the Fungus is nourished, protected against harmful microorganisms, and dispersed by the ants. This symbiosis evolved approximately 50–60 million years ago in the late Paleocene or early Eocene, and since its origin attine ants have acquired a variety of fungal mutualists in the Leucocoprineae and the distantly related Pterulaceae. The most specialized symbiotic interaction is referred to as ‘‘higher agriculture’ ’ and includes leafcutter ant agriculture in which the ants cultivate the single species Leucoagaricus gongylophorus. Higher agriculture fungal cultivars are characterized by specialized hyphal tip swellings, so-called gongylidia, which are considered a unique, derived morphological adaptation of higher attine fungi thought to be absent in lower attine fungi. Rare reports of gongylidia-like structures in Fungus Gardens of lower attines exist, but it was never tested whether these represent rare switches of lower attines to L. gonglyphorus cultivars or whether lower attine cultivars occasionally produce gongylidia. Here we describe the occurrence of gongylidia-like structures in Fungus Gardens of the asexual lower attine ant Mycocepurus smithii. To test whether M. smithii cultivates leafcutter ant fungi or whether lower attine cultivars produce gongylidia, we identified the M. smithii Fungus utilizing molecular and morphological methods. Results shows that the gongylidia-like structures of M. smithii Gardens are morphologically similar to gongylidia of higher attine Fungus Gardens and can only be distinguished by their slightly smaller size. A molecular phylogenetic analysis of th
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Rapid shifts in Atta cephalotes Fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)
Insectes Sociaux, 2011Co-Authors: P. W. Kooij, J. J. Boomsma, M. Schiøtt, Henrik H De Fine LichtAbstract:Fungus Gardens of the basidiomycete Leucocoprinus gongylophorus sustain large colonies of leaf-cutting ants by degrading the plant material collected by the ants. Recent studies have shown that enzyme activity in these Gardens is primarily targeted toward starch, proteins and the pectin matrix associated with cell walls, rather than toward structural cell wall components such as cellulose and hemicelluloses. Substrate constituents are also known to be sequentially degraded in different sections of the Fungus garden. To test the plasticity in the extracellular expression of Fungus-garden enzymes, we measured the changes in enzyme activity after a controlled shift in fungal substrate offered to six laboratory colonies of Atta cephalotes . An ant diet consisting exclusively of grains of parboiled rice rapidly increased the activity of endo-proteinases and some of the pectinases attacking the backbone structure of pectin molecules, relative to a pure diet of bramble leaves, and this happened predominantly in the most recently established top sections of Fungus Gardens. However, Fungus-garden amylase activity did not significantly increase despite the substantial increase in starch availability from the rice diet, relative to the leaf diet controls. Enzyme activity in the older, bottom sections of Fungus Gardens decreased, indicating a faster processing of the rice substrate compared to the leaf diet. These results suggest that leaf-cutting ant Fungus Gardens can rapidly adjust enzyme activity to provide a better match with substrate availability and that excess starch that is not protected by cell walls may be digested by the ants rather than by the Fungus-garden symbiont.
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the dynamics of plant cell wall polysaccharide decomposition in leaf cutting ant Fungus Gardens
PLOS ONE, 2011Co-Authors: Isabel Moller, Henrik H De Fine Licht, Jesper Harholt, William G T Willats, Jacobus J. BoomsmaAbstract:The degradation of live plant biomass in Fungus Gardens of leaf-cutting ants is poorly characterised but fundamental for understanding the mutual advantages and efficiency of this obligate nutritional symbiosis. Controversies about the extent to which the garden-symbiont Leucocoprinus gongylophorus degrades cellulose have hampered our understanding of the selection forces that induced large scale herbivory and of the ensuing ecological footprint of these ants. Here we use a recently established technique, based on polysaccharide microarrays probed with antibodies and carbohydrate binding modules, to map the occurrence of cell wall polymers in consecutive sections of the Fungus garden of the leaf-cutting ant Acromyrmex echinatior. We show that pectin, xyloglucan and some xylan epitopes are degraded, whereas more highly substituted xylan and cellulose epitopes remain as residuals in the waste material that the ants remove from their Fungus garden. These results demonstrate that biomass entering leaf-cutting ant Fungus Gardens is only partially utilized and explain why disproportionally large amounts of plant material are needed to sustain colony growth. They also explain why substantial communities of microbial and invertebrate symbionts have evolved associations with the dump material from leaf-cutting ant nests, to exploit decomposition niches that the ant garden-Fungus does not utilize. Our approach thus provides detailed insight into the nutritional benefits and shortcomings associated with Fungus-farming in ants.
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Evolutionary transitions in enzyme activity of ant Fungus Gardens.
Evolution; international journal of organic evolution, 2010Co-Authors: Henrik H De Fine Licht, Morten Schiøtt, Ulrich G. Mueller, Jacobus J. BoomsmaAbstract:Fungus-growing (attine) ants and their fungal symbionts passed through several evolutionary transitions during their 50 million year old evolutionary history. The basal attine lineages often shifted between two main cultivar clades, whereas the derived higher-attine lineages maintained an association with a monophyletic clade of specialized symbionts. In conjunction with the transition to specialized symbionts, the ants advanced in colony size and social complexity. Here we provide a comparative study of the functional specialization in extracellular enzyme activities in Fungus Gardens across the attine phylogeny. We show that, relative to sister clades, Gardens of higher-attine ants have enhanced activity of protein-digesting enzymes, whereas Gardens of leaf-cutting ants also have increased activity of starch-digesting enzymes. However, the enzyme activities of lower-attine Fungus Gardens are targeted primarily toward partial degradation of plant cell walls, reflecting a plesiomorphic state of nondomesticated fungi. The enzyme profiles of the higher-attine and leaf-cutting Gardens appear particularly suited to digest fresh plant materials and to access nutrients from live cells without major breakdown of cell walls. The adaptive significance of the lower-attine symbiont shifts remains unclear. One of these shifts was obligate, but digestive advantages remained ambiguous, whereas the other remained facultative despite providing greater digestive efficiency.
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Towards a molecular understanding of symbiont function: Identification of a fungal gene for the degradation of xylan in the Fungus Gardens of leaf-cutting ants
BMC microbiology, 2008Co-Authors: Morten Schiøtt, Henrik H De Fine Licht, Lene Lange, Jacobus J. BoomsmaAbstract:Background Leaf-cutting ants live in symbiosis with a Fungus that they rear for food by providing it with live plant material. Until recently the Fungus' main inferred function was to make otherwise inaccessible cell wall degradation products available to the ants, but new studies have shed doubt on this idea. To provide evidence for the cell wall degrading capacity of the attine ant symbiont, we designed PCR primers from conserved regions of known xylanase genes, to be used in PCR with genomic DNA from the symbiont as template. We also measured xylanase, cellulase and proteinase activities in the Fungus Gardens in order to investigate the dynamics of degradation activities.
Andre Rodrigues - One of the best experts on this subject based on the ideXlab platform.
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More pieces to a huge puzzle: Two new Escovopsis species from Fungus Gardens of attine ants
Pensoft Publishers, 2019Co-Authors: Quimi Vidaurre Montoya, Maria Jesus Sutta Martiarena, Danilo augusto Polezel, Sérgio Kakazu, Andre RodriguesAbstract:Escovopsis (Ascomycota: Hypocreales, Hypocreaceae) is the only known parasite of the mutualistic fungi cultivated by Fungus-growing ants (Formicidae: Myrmicinae: Attini: Attina, the “attines”). Despite its ecological role, the taxonomy and systematics of Escovopsis have been poorly addressed. Here, based on morphological and phylogenetic analyses with three molecular markers (internal transcribed spacer, large subunit ribosomal RNA and the translation elongation factor 1-alpha), we describe Escovopsis clavatus and E. multiformis as new species isolated from Fungus Gardens of Apterostigma ant species. Our analysis shows that E. clavatus and E. multiformis belong to the most derived Escovopsis clade, whose main character is the presence of conidiophores with vesicles. Nevertheless, the most outstanding feature of both new species is the presence of a swollen region in the central hypha of the conidiophore named swollen cell, which is absent in all previously described Escovopsis species. The less derived Escovopsis clades lack vesicles and their phylogenetic position within the Hypocreaceae still remains unclear. Considering the high genetic diversity in Escovopsis, the description of these new species adds barely two pieces to a huge taxonomic puzzle; however, this discovery is an important piece for building the systematics of this group of fungi
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Escovopsioides as a fungal antagonist of the Fungus cultivated by leafcutter ants
BMC microbiology, 2018Co-Authors: Julio Osti, Andre RodriguesAbstract:Background Fungus Gardens of Fungus-growing (attine) ants harbor complex microbiomes in addition to the mutualistic Fungus they cultivate for food. Fungi in the genus Escovopsioides were recently described as members of this microbiome but their role in the ant-Fungus symbiosis is poorly known. In this study, we assessed the phylogenetic diversity of 21 Escovopsioides isolates obtained from Fungus Gardens of leafcutter ants (genera Atta and Acromyrmex) and non-leafcutter ants (genera Trachymyrmex and Apterostigma) sampled from several regions in Brazil.
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Additional file 1: of Escovopsioides as a fungal antagonist of the Fungus cultivated by leafcutter ants
2018Co-Authors: Julio Osti, Andre RodriguesAbstract:Table S1. Sequences used in the phylogenetic analyses and their associated metadata. Figure S1. Fungus Gardens of Atta sexdens rubropilosa after 10 days of treatment with fungal spores. Fungus Gardens were sampled from a mature colony and left in Petri dishes without any ants. (A) Garden not sprayed with spores (control); (B) Garden overgrown by Escovopsioides nivea LESF 603; (C) Healthy garden after treatment with spores of Escovopsioides sp. LESF 602 and (D) Garden overgrown by Escovopsis sp. LESF 19. Figure S2. Criteria used to designate health conditions of Fungus garden in the bioassays using Fungus Gardens of Atta sexdens rubropilosa. (A) healthy garden; (B) garden in process of deterioration and (C) dead garden after 10 days of experiment. (DOCX 1760 kb
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Escovopsioides as a fungal antagonist of the Fungus cultivated by leafcutter ants
BMC, 2018Co-Authors: Julio Osti, Andre RodriguesAbstract:Abstract Background Fungus Gardens of Fungus-growing (attine) ants harbor complex microbiomes in addition to the mutualistic Fungus they cultivate for food. Fungi in the genus Escovopsioides were recently described as members of this microbiome but their role in the ant-Fungus symbiosis is poorly known. In this study, we assessed the phylogenetic diversity of 21 Escovopsioides isolates obtained from Fungus Gardens of leafcutter ants (genera Atta and Acromyrmex) and non-leafcutter ants (genera Trachymyrmex and Apterostigma) sampled from several regions in Brazil. Results Regardless of the sample locality or ant genera, phylogenetic analysis showed low genetic diversity among the 20 Escovopsisoides isolates examined, which prompted the identification as Escovopsioides nivea (the only described species in the genus). In contrast, one Escovopsioides isolate obtained from a Fungus garden of Apterostigma megacephala was considered a new phylogenetic species. Dual-culture plate assays showed that Escovopsioides isolates inhibited the mycelium growth of Leucoagaricus gongylophorus, the mutualistic Fungus cultivated by somes species of leafcutter ants. In addition, Escovopsioides growth experiments in Fungus Gardens with and without ant workers showed this Fungus is detrimental to the ant-Fungus symbiosis. Conclusions Here, we provide clues for the antagonism of Escovopsioides towards the mutualistic Fungus of leafcutter ants
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Pathogenic nature of Syncephalastrum in Atta sexdens rubropilosa Fungus Gardens.
Pest management science, 2016Co-Authors: Mariana O. Barcoto, Felipe Pedrosa, Odair Correa Bueno, Andre RodriguesAbstract:BACKGROUND Leaf-cutter ants are considered to be a major herbivore and agricultural pest in the Neotropics. They are often controlled by environmentally persistent insecticides. Biological control using pathogenic fungi is regarded as an alternative for the management of these insects. Here, we assess whether the filamentous Fungus Syncephalastrum sp. is a pathogenic microorganism responsible for a characteristic disease in Fungus Gardens. We also characterise the damage caused by this Fungus by evaluating physiological and behavioural responses of Atta sexdens rubropilosa subcolonies infected with Syncephalastrum sp. RESULTS: Syncephalastrum sp. fulfils Koch's postulates characterising it as a pathogenic microorganism. Ant workers recognise the infection and remove contaminated fragments from the Fungus garden. Syncephalastrum sp. infection causes an interruption of foraging activity, an increase in ant mortality, subcolony deterioration and an increase in the amount of waste generated, all resulting in subcolony death. Syncephalastrum sp. also inhibits the ant fungal cultivar in vitro. The pathogenic effect of Syncephalastrum sp. does not depend on host morbidity or stress (e.g. worker mortality caused by an entomopathogenic Fungus). CONCLUSION Syncephalastrum sp. treatment resulted in progressive damage in subcolonies. The interactions among Syncephalastrum sp., Fungus garden and ants offer new opportunities in integrated pest management of leaf-cutter ants. © 2016 Society of Chemical Industry
