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A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus.

ABSTRACT: Attine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria. One hypothesis suggests that bacteria from the genus Pseudonocardia are the sole, co-evolved mutualists of attine ants and are transmitted vertically by the queens. A recent study identified a Pseudonocardia-produced antifungal, named dentigerumycin, associated with the lower attine Apterostigma dentigerum consistent with the idea that co-evolved Pseudonocardia make novel antibiotics. An alternative possibility is that attine ants sample actinomycete bacteria from the soil, selecting and maintaining those species that make useful antibiotics. Consistent with this idea, a Streptomyces species associated with the higher attine Acromyrmex octospinosus was recently shown to produce the well-known antifungal candicidin. Candicidin production is widespread in environmental isolates of Streptomyces, so this could either be an environmental contaminant or evidence of recruitment of useful actinomycetes from the environment. It should be noted that the two possibilities for actinomycete acquisition are not necessarily mutually exclusive.In order to test these possibilities we isolated bacteria from a geographically distinct population of A. octospinosus and identified a candicidin-producing Streptomyces species, which suggests that they are common mutualists of attine ants, most probably recruited from the environment. We also identified a Pseudonocardia species in the same ant colony that produces an unusual polyene antifungal, providing evidence for co-evolution of Pseudonocardia with A. octospinosus.Our results show that a combination of co-evolution and environmental sampling results in the diversity of actinomycete symbionts and antibiotics associated with attine ants.

SUBMITTER: Barke J

PROVIDER: S-EPMC2942817 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus.

Barke Jörg J Seipke Ryan F RF Grüschow Sabine S Heavens Darren D Drou Nizar N Bibb Mervyn J MJ Goss Rebecca J M RJ Yu Douglas W DW Hutchings Matthew I MI

BMC biology 20100826

<h4>Background</h4>Attine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria. One hypothesis suggests that bacteria from the genus Pseudonocardia are the sole, co-evolved mutualists of attine ants and are transmitted vertically by the queens. A recent study identified a Pseudonocardia-produced antifungal, named dentigerumycin, associated with the lower attine Apte ...[more]

PMID: 20796277

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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.

Project description:Evolutionary adaptations for maintaining beneficial microbes are hallmarks of mutualistic evolution. Fungus-farming "attine" ant species have complex cuticular modifications and specialized glands that house and nourish antibiotic-producing Actinobacteria symbionts, which in turn protect their hosts' fungus gardens from pathogens. Here we reconstruct ant-Actinobacteria evolutionary history across the full range of variation within subtribe Attina by combining dated phylogenomic and ultramorphological analyses. Ancestral-state analyses indicate the ant-Actinobacteria symbiosis arose early in attine-ant evolution, a conclusion consistent with direct observations of Actinobacteria on fossil ants in Oligo-Miocene amber. qPCR indicates that the dominant ant-associated Actinobacteria belong to the genus Pseudonocardia Tracing the evolutionary trajectories of Pseudonocardia-maintaining mechanisms across attine ants reveals a continuum of adaptations. In Myrmicocrypta species, which retain many ancestral morphological and behavioral traits, Pseudonocardia occur in specific locations on the legs and antennae, unassociated with any specialized structures. In contrast, specialized cuticular structures, including crypts and tubercles, evolved at least three times in derived attine-ant lineages. Conspicuous caste differences in Pseudonocardia-maintaining structures, in which specialized structures are present in worker ants and queens but reduced or lost in males, are consistent with vertical Pseudonocardia transmission. Although the majority of attine ants are associated with Pseudonocardia, there have been multiple losses of bacterial symbionts and bacteria-maintaining structures in different lineages over evolutionary time. The early origin of ant-Pseudonocardia mutualism and the multiple evolutionary convergences on strikingly similar anatomical adaptations for maintaining bacterial symbionts indicate that Pseudonocardia have played a critical role in the evolution of ant fungiculture.

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A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus.

Publications

A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus.

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