Ocurrence of the antibiotic producing bacterium<i>Burkholderia</i>sp. in colonies of the leaf-cutting ant<i>Atta sexdens rubropilosa</i>

Santos, AdÃ£o Valmir; Dillon, Rod J.; Dillon, Vivian M.; Reynolds, Stuart E.; Samuels, Richard Ian

doi:10.1016/j.femsle.2004.09.005

Cited by 133 publications

(122 citation statements)

References 25 publications

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“…Another study, employing the culture-independent analysis of membrane-lipid markers, has supported the hypothesis that a distinct community of predominantly Gram-negative bacteria resides in fungus gardens , and the presence of symbiotic nitrogen-fixing bacteria in the genera Pantoea and Klebsiella has also been shown (Pinto-Tomas et al, 2009). Together with culture-dependent investigations recovering microbial groups with a broad array of metabolic activities (Bacci et al, 1995;Santos et al, 2004), these experiments have led to the suggestion that fungus gardens represent specialized fungusbacteria consortia selected for by the ants, and that the bacteria have essential roles, including plant biomass degradation, nutrient biosynthesis, and competitive or antibiotic-mediated exclusion of pathogens (Mueller et al, 2005;Haeder et al, 2009;Pinto-Tomas et al, 2009;Suen et al, 2010).…”

Section: Introductionmentioning

confidence: 84%

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens

et al. 2012

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Herbivores gain access to nutrients stored in plant biomass largely by harnessing the metabolic activities of microbes. Leaf-cutter ants of the genus Atta are a hallmark example; these dominant neotropical herbivores cultivate symbiotic fungus gardens on large quantities of fresh plant forage. As the external digestive system of the ants, fungus gardens facilitate the production and sustenance of millions of workers. Using metagenomic and metaproteomic techniques, we characterize the bacterial diversity and physiological potential of fungus gardens from two species of Atta. Our analysis of over 1.2 Gbp of community metagenomic sequence and three 16S pyrotag libraries reveals that in addition to harboring the dominant fungal crop, these ecosystems contain abundant populations of Enterobacteriaceae, including the genera Enterobacter, Pantoea, Klebsiella, Citrobacter and Escherichia. We show that these bacterial communities possess genes associated with lignocellulose degradation and diverse biosynthetic pathways, suggesting that they play a role in nutrient cycling by converting the nitrogen-poor forage of the ants into B-vitamins, amino acids and other cellular components. Our metaproteomic analysis confirms that bacterial glycosyl hydrolases and proteins with putative biosynthetic functions are produced in both fieldcollected and laboratory-reared colonies. These results are consistent with the hypothesis that fungus gardens are specialized fungus-bacteria communities that convert plant material into energy for their ant hosts. Together with recent investigations into the microbial symbionts of vertebrates, our work underscores the importance of microbial communities in the ecology and evolution of herbivorous metazoans.

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Section: Introductionmentioning

confidence: 84%

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens

et al. 2012

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“…The mutualism is obligatory for both the symbiotic fungus and the ants (Mueller et al, 2005), as the fungus is dependent on the ants for substrate provisioning and control of competing and pathogenic microbes (Currie et al, 1999;Hart et al, 2002;Valmir Santos et al, 2004), whereas the ants are dependent on the fungus as their main food component (Weber, 1966;Littledyke and Cherrett, 1976;Quinlan and Cherrett, 1979).…”

Section: Introductionmentioning

confidence: 99%

Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)

et al. 2010

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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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“…In addition to the characterization of microbial antifungal compounds (11)(12)(13) involved in mediating the interactions between the different partners, it has become evident that both a large number of pathogens (2-5) pose a threat to the ants' fungus garden and a large diversity of microbial symbionts can be found within the ants' nests. These symbionts fulfill diverse functions, including defense against pathogens or promotion of the growth of the garden fungus (e.g., by nitrogen fixation) (10)(11)(12)(13)(15)(16)(17). Because some bacterial symbionts of leaf-cutting ants can be also detrimental to the growth of the mutualistic fungus L. gongylophorus, the onesided view of leaf-cutting ants and Actinomyces symbionts as mutualistic partners of the leaf-cutting ants should be challenged (18).…”

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confidence: 99%

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

Schoenian

Spiteller

Ghaste

et al. 2011

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

169

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Leaf-cutting ants cultivate the fungus Leucoagaricus gongylophorus, which serves as a major food source. This symbiosis is threatened by microbial pathogens that can severely infect L. gongylophorus. Microbial symbionts of leaf-cutting ants, mainly Pseudonocardia and Streptomyces, support the ants in defending their fungus gardens against infections by supplying antimicrobial and antifungal compounds. The ecological role of microorganisms in the nests of leaf-cutting ants can only be addressed in detail if their secondary metabolites are known. Here, we use an approach for the rapid identification of established bioactive compounds from microorganisms in ecological contexts by combining phylogenetic data, database searches, and liquid chromatography electrospray ionisation high resolution mass spectrometry (LC-ESI-HR-MS) screening. Antimycins A 1 -A 4 , valinomycins, and actinomycins were identified in this manner from Streptomyces symbionts of leaf-cutting ants. Matrix-assisted laser desorption ionization (MALDI) imaging revealed the distribution of valinomycin directly on the integument of Acromyrmex echinatior workers. Valinomycins and actinomycins were also directly identified in samples from the waste of A. echinatior and A. niger leaf-cutting ants, suggesting that the compounds exert their antimicrobial and antifungal potential in the nests of leaf-cutting ants. Strong synergistic effects of the secondary metabolites produced by ant-associated Streptomyces were observed in the agar diffusion assay against Escovopsis weberi. Actinomycins strongly inhibit soil bacteria as well as other Streptomyces and Pseudonocardia symbionts. The antifungal antimycins are not only active against pathogenic fungi but also the garden fungus L. gongylophorus itself. In conclusion, secondary metabolites of microbial symbionts of leaf-cutting ants contribute to shaping the microbial communities within the nests of leaf-cutting ants.

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Ocurrence of the antibiotic producing bacteriumBurkholderiasp. in colonies of the leaf-cutting antAtta sexdens rubropilosa

Cited by 133 publications

References 25 publications

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens

Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

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