The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides

Grell, Morten Nedergaard; Linde, T. C. de K. van der; Nygaard, Sanne; Nielsen, Kåre Lehmann; Boomsma, Jacobus J.; Lange, Lene

doi:10.1186/1471-2164-14-928

Cited by 43 publications

(58 citation statements)

References 46 publications

(110 reference statements)

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“…The present transcriptome analysis supports the hypothesis that carbohydrate-active enzymes important for plant material degradation are upregulated in gongylidia and adds the contig03063 GH12 xyloglucanase xeg1 (UniProt accession code U6NF03) to the list of significantly upregulated extracellular gongylidia enzymes (Supplementary Table 3). Expression of this xyloglucanase peaks in the bottom of gardens 55 where many more cellulolytic enzymes are overexpressed 26,53,55 , but the overexpression in gongylidia suggests that xyloglucanase may also be transferred to the top of fungus gardens via faecal droplets.…”

Section: Discussionmentioning

confidence: 99%

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

2014

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Centuries of artificial selection have dramatically improved the yield of human agriculture; however, strong directional selection also occurs in natural symbiotic interactions. Fungusgrowing attine ants cultivate basidiomycete fungi for food. One cultivar lineage has evolved inflated hyphal tips (gongylidia) that grow in bundles called staphylae, to specifically feed the ants. Here we show extensive regulation and molecular signals of adaptive evolution in gene trancripts associated with gongylidia biosynthesis, morphogenesis and enzymatic plant cell wall degradation in the leaf-cutting ant cultivar Leucoagaricus gongylophorus. Comparative analysis of staphylae growth morphology and transcriptome-wide expressional and nucleotide divergence indicate that gongylidia provide leaf-cutting ants with essential amino acids and plant-degrading enzymes, and that they may have done so for 20-25 million years without much evolutionary change. These molecular traits and signatures of selection imply that staphylae are highly advanced coevolutionary organs that play pivotal roles in the mutualism between leaf-cutting ants and their fungal cultivars.

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Section: Discussionmentioning

confidence: 99%

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

2014

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“…Interestingly, proteomic, transcriptomic, and draft genome sequencing have identified some of these missing enzymes to be present and highly expressed in the ant-cultivated fungus Leucoagaricus gongylophorus (Fig. 3 and SI Appendix, Table S10) (2,3). Taken together, these losses are consistent with previous findings that the specialized mycoparasite Escovopsis breaks down fungal but not plant material (7) and suggest that E. weberi has lost the ability to feed on lignocellulosic plant material, an ability retained by other microbial members of fungus-growing ant gardens (46).…”

Section: Specialization and Gene Lossmentioning

confidence: 99%

“…Members of some of these families, indicated in orange, are known to be highly expressed in E. weberi's host fungus (2,3). Additional details are in SI Appendix, Table S10.…”

Section: Further Genomic Signatures Of Exploitation Of a Fungalmentioning

confidence: 99%

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Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture

Man

Stajich

Kubicek

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite’s genome.

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“…L. gongylophorus also secretes enzymes that act synergistically with ant enzymes to degrade plant matter, generating soluble compounds that are subsequently ingested by the ants (10-13). These enzymes attack plant polysaccharides, including starch, hemicellulose, pectin, and, to a lesser extent, cellulose (10,(14)(15)(16)(17)(18)(19)(20)(21)(22)(23). In addition, other microbes living in the fungus garden might mediate ant nutrition on plant polysaccharides (24-27).…”

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confidence: 99%

Leaf-Cutter Ant Fungus Gardens Are Biphasic Mixed Microbial Bioreactors That Convert Plant Biomass to Polyols with Biotechnological Applications

Somera

Lima

Santos-Neto

et al. 2015

Appl Environ Microbiol

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b Leaf-cutter ants use plant matter to culture the obligate mutualistic basidiomycete Leucoagaricus gongylophorus. This fungus mediates ant nutrition on plant resources. Furthermore, other microbes living in the fungus garden might also contribute to plant digestion. The fungus garden comprises a young sector with recently incorporated leaf fragments and an old sector with partially digested plant matter. Here, we show that the young and old sectors of the grass-cutter Atta bisphaerica fungus garden operate as a biphasic solid-state mixed fermenting system. An initial plant digestion phase occurred in the young sector in the fungus garden periphery, with prevailing hemicellulose and starch degradation into arabinose, mannose, xylose, and glucose. These products support fast microbial growth but were mostly converted into four polyols. Three polyols, mannitol, arabitol, and inositol, were secreted by L. gongylophorus, and a fourth polyol, sorbitol, was likely secreted by another, unidentified, microbe. A second plant digestion phase occurred in the old sector, located in the fungus garden core, comprising stocks of microbial biomass growing slowly on monosaccharides and polyols. This biphasic operation was efficient in mediating symbiotic nutrition on plant matter: the microbes, accounting for 4% of the fungus garden biomass, converted plant matter biomass into monosaccharides and polyols, which were completely consumed by the resident ants and microbes. However, when consumption was inhibited through laboratory manipulation, most of the plant polysaccharides were degraded, products rapidly accumulated, and yields could be preferentially switched between polyols and monosaccharides. This feature might be useful in biotechnology. In the nests of leaf-cutter ants of the genera Atta and Acromyrmex, gardens of the obligate mutualistic basidiomycete fungus Leucoagaricus gongylophorus (1, 2) are cultivated on fresh vegetal materials (3-5). Although few leaf-cutter species prefer monocots, most leaf-cutter ants collect plant materials from both monocots and dicots (6). The ants collect and transport these plants to their nests and then fractionate and extensively clean the leaf fragments (7,8). Subsequently, the ants deposit a drop of fecal fluid onto the leaf fragment surface and inoculate the leaf fragment with L. gongylophorus hyphae. The plant-digesting enzymes in the fecal fluid facilitate fungal development (9). This fungus produces swollen hyphal tips, called gongylidia, that cluster together to form macroscopic structures known as staphylae, which are food sources for the ants (3-5). L. gongylophorus also secretes enzymes that act synergistically with ant enzymes to degrade plant matter, generating soluble compounds that are subsequently ingested by the ants (10-13). These enzymes attack plant polysaccharides, including starch, hemicellulose, pectin, and, to a lesser extent, cellulose (10,(14)(15)(16)(17)(18)(19)(20)(21)(22)(23). In addition, other microbes living in the fungus garden might mediate ant nutrition...

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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

Cited by 43 publications

References 46 publications

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture

Leaf-Cutter Ant Fungus Gardens Are Biphasic Mixed Microbial Bioreactors That Convert Plant Biomass to Polyols with Biotechnological Applications

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