Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

Worsley, Sarah F., Innocent, Tabitha M., Holmes, Neil A., Al-Bassam, Mahmoud M., Schiøtt, Morten, Wilkinson, Barrie, Murrell, J. Colin, Boomsma, Jacobus J., Yu, Douglas W. and Hutchings, Matthew I. (2021) Competition-based screening helps to secure the evolutionary stability of a defensive microbiome. BMC Biology, 19 (1). ISSN 1741-7007

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Abstract

Background: The cuticular microbiomes of Acromyrmex leaf-cutting ants pose a conundrum in microbiome biology because they are freely colonisable, and yet the prevalence of the vertically transmitted bacteria Pseudonocardia, which contributes to the control of Escovopsis fungus garden disease, is never compromised by the secondary acquisition of other bacterial strains. Game theory suggests that competition-based screening can allow the selective recruitment of antibiotic-producing bacteria from the environment, by providing abundant resources to foment interference competition between bacterial species and by using Pseudonocardia to bias the outcome of competition in favour of antibiotic producers. Results: Here, we use RNA-stable isotope probing (RNA-SIP) to confirm that Acromyrmex ants can maintain a range of microbial symbionts on their cuticle by supplying public resources. We then used RNA sequencing, bioassays, and competition experiments to show that vertically transmitted Pseudonocardia strains produce antibacterials that differentially reduce the growth rates of other microbes, ultimately biassing the bacterial competition to allow the selective establishment of secondary antibiotic-producing strains while excluding non-antibiotic-producing strains that would parasitise the symbiosis. Conclusions: Our findings are consistent with the hypothesis that competition-based screening is a plausible mechanism for maintaining the integrity of the co-adapted mutualism between the leaf-cutting ant farming symbiosis and its defensive microbiome. Our results have broader implications for explaining the stability of other complex symbioses involving horizontal acquisition.

Item Type: Article
Additional Information: Funding Information: This work was supported by a NERC PhD studentship to SFW (NERC Doctoral Training Programme grant NE/L002582/1); NERC grants NE/J01074X/1 to MIH and DWY; NE/M015033/1 and NE/M014657/1 to MIH, JCM, DWY, and BW; European Research Council Advanced grant 323085 to JJB; and Marie Curie Individual European Fellowship grant 627949 to TI. DWY was also supported by the Key Research Program of Frontier Sciences, Chinese Academy of Sciences (QYZDY-SSW-SMC024), and the Strategic Priority Research Program, Chinese Academy of Sciences (XDA20050202, XDB31000000). Funding Information: We thank the Smithsonian Tropical Research Institute for the logistical help and facilities for all work in Gamboa, Panama, and the Autoridad Nacional del Ambiente y el Mar for permission to sample and export ants to Copenhagen. We thank Simon Moxon for the advice on RNA sequencing analysis, Paul Disdle for his assistentance with the IRMS analysis, and Elaine Patrick and Sylvia Matthiesen for the lab and logistics support. Publisher Copyright: © 2021, The Author(s).
Uncontrolled Keywords: actinobacteria,antibiotics,attini,defensive microbiome,game theory,horizontal acquisition,interference competition,leaf-cutting ants,mutualism,partner,pseudonocardia,symbiosis,biotechnology,structural biology,ecology, evolution, behavior and systematics,physiology,biochemistry, genetics and molecular biology(all),agricultural and biological sciences(all),plant science,developmental biology,cell biology ,/dk/atira/pure/subjectarea/asjc/1300/1305
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > School of Chemistry
Faculty of Science > School of Environmental Sciences
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Depositing User: LivePure Connector
Date Deposited: 21 Sep 2021 01:36
Last Modified: 14 Oct 2021 01:10
URI: https://ueaeprints.uea.ac.uk/id/eprint/81466
DOI: 10.1186/s12915-021-01142-w

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