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Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications.

ABSTRACT: 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.

SUBMITTER: Somera AF

PROVIDER: S-EPMC4475879 | biostudies-other | 2015 Jul

REPOSITORIES: biostudies-other

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Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications.

Somera Alexandre F AF Lima Adriel M AM Dos Santos-Neto Álvaro J ÁJ Lanças Fernando M FM Bacci Maurício M

Applied and environmental microbiology 20150424 13

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 gard ...[more]

PMID: 25911490

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Project description:BackgroundLeaf-cutter ants use fresh plant material to grow a mutualistic fungus that serves as the ants' primary food source. Within fungus gardens, various plant compounds are metabolized and transformed into nutrients suitable for ant consumption. This symbiotic association produces a large amount of refuse consisting primarily of partly degraded plant material. A leaf-cutter ant colony is thus divided into two spatially and chemically distinct environments that together represent a plant biomass degradation gradient. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies.Methodology/principal findingsUsing microbial membrane lipid analysis and a variety of community metrics, we assessed and compared the microbiota of fungus gardens and refuse dumps from both laboratory-maintained and field-collected colonies. We found that gardens contained a diverse and consistent community of microbes, dominated by Gram-negative bacteria, particularly gamma-Proteobacteria and Bacteroidetes. These findings were consistent across lab and field gardens, as well as host ant taxa. In contrast, dumps were enriched for Gram-positive and anaerobic bacteria. Broad-scale clustering analyses revealed that community relatedness between samples reflected system component (gardens/dumps) rather than colony source (lab/field). At finer scales samples clustered according to colony source.Conclusions/significanceHere we report the first comparative analysis of the microbiota from leaf-cutter ant colonies. Our work reveals the presence of two distinct communities: one in the fungus garden and the other in the refuse dump. Though we find some effect of colony source on community structure, our data indicate the presence of consistently associated microbes within gardens and dumps. Substrate composition and system component appear to be the most important factor in structuring the microbial communities. These results thus suggest that resident communities are shaped by the plant degradation gradient created by ant behavior, specifically their fungiculture and waste management.

Project description:BackgroundAttine ants live in symbiosis with a basidiomycetous fungus that they rear on a substrate of plant material. This indirect herbivory implies that the symbiosis is likely to be nitrogen deprived, so that specific mechanisms may have evolved to enhance protein availability. We therefore hypothesized that fungal proteinase activity may have been under selection for efficiency and that different classes of proteinases might be involved.ResultsWe determined proteinase activity profiles across a wide pH range for fungus gardens of 14 Panamanian species of fungus-growing ants, representing eight genera. We mapped these activity profiles on an independently obtained molecular phylogeny of the symbionts and show that total proteinase activity in lower attine symbionts peaks at ca. pH 6. The higher attine symbionts that have no known free-living relatives had much higher proteinase activities than the lower attine symbionts. Their total in vitro proteinase activity peaked at pH values around 5, which is close to the pH that the ants maintain in their fungus gardens, suggesting that the pH optimum of fungal proteinases may have changed after the irreversible domestication of evolutionary more derived fungal symbionts. This notion is also supported by buffering capacities of fungus gardens at pH 5.2 being remarkably high, and suggests that the fungal symbiont actively helps to maintain garden acidity at this specific level. Metalloproteinases dominated the activity profiles of lower attine gardens and may thus represent the ancestral type of proteinase production, whereas serine proteinase activity dominated the activity profiles of the higher attine gardens reared by Trachymyrmex and Sericomyrmex, suggesting that there may be trade-offs in the production of these enzyme classes. Remarkably, the single symbiont that is shared by species of the crown group of Atta and Acromyrmex leaf-cutting ants mostly showed metalloproteinase activity, suggesting that recurrent changes in enzyme production may have occurred throughout the domestication history of fungus-garden symbionts.ConclusionsProteinase pH optima and buffering capacities of fungal symbionts appear to have evolved remarkable adaptations to living in obligate symbiosis with farming ants. Although the functional roles of serine and metalloproteinases in fungus gardens are unknown, the differential production of these classes of proteolytic enzymes suggest that substrate specificity may be important and that trade-offs may prevent the simultaneous upregulation of both classes of enzymes.

Project description:BackgroundXyloglucan 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.ResultsThe fungal symbiont provides a single xyloglucanase (Xeg1) to its ant farmers by upregulating the expression of this protein in the inflated hyphal tips (gongylidia) that the ants ingest. Similar to other enzymes ingested this way, also Xeg1 is not digested but vectored to the fresh leaf-fragment pulp at the top of fungus gardens via ant fecal fluid. Xeg1 is 4-5 times more active in fecal fluid when ants ingest their normal fungal food, compared to a sucrose control diet, as expected when they cannot produce Xeg1 themselves. We confirm substrate specificity of fungal Xeg1 towards xyloglucan by heterologous expression in yeast and show that xyloglucanase activity is higher in the oldest, bottom layers of fungus gardens and in discarded debris material than in the upper and middle layers of fungus gardens.ConclusionOur results are consistent with Xeg1 playing a role in the initial breakdown of plant cell wall hemicellulose to provide sugars for aggressive hyphal growth before intracellular proteins become available. Xeg1 does not play a major decomposition role in the middle layer of fungus gardens where it is produced by the gongylidia. Overall high xyloglucanase activity in old mycelium that is (about to be) discarded is striking and quite possibly serves defensive purposes by precluding that competing microorganisms can grow. Our results support the hypothesis that the ant-fungus symbiosis prioritizes access to the protein-rich contents of live plant cells and that carbohydrates are not a limiting resource.

Dataset Information

Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications.

Publications

Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications.

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