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Structure of an ant-myrmecophile-microbe community

View ORCID ProfileElena K. Perry, View ORCID ProfileStefanos Siozios, View ORCID ProfileGregory D. D. Hurst, View ORCID ProfileJoseph Parker
doi: https://doi.org/10.1101/2021.10.04.462948
Elena K. Perry
1Division of Biology and Biological Engineering, California Institute of Technology, 1200 E California Boulevard, Pasadena, CA 91125, United States of America
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Stefanos Siozios
2Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Ic2 Liverpool Science Park, 146 Brownlow Hill, Liverpool, L3 5RF, United Kingdom
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Gregory D. D. Hurst
2Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Ic2 Liverpool Science Park, 146 Brownlow Hill, Liverpool, L3 5RF, United Kingdom
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Joseph Parker
1Division of Biology and Biological Engineering, California Institute of Technology, 1200 E California Boulevard, Pasadena, CA 91125, United States of America
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  • For correspondence: joep@caltech.edu
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Abstract

Superorganismal ant colonies play host to a menagerie of symbiotic arthropods, termed myrmecophiles, which exhibit varying degrees of social integration into colony life. Such systems permit examination of how animal community interactions influence microbial assemblages. Here, we present an ecologically and phylogenetically comprehensive characterization of an ant-myrmecophile-microbe community in Southern California. Using 16S rRNA profiling, we find that microbiotas of the velvety tree ant (Liometopum occidentale) and its cohort of myrmecophiles are distinguished by species-specific characteristics but nevertheless bear signatures of their behavioral interactions. We found that the host ant microbiome was diverse at all taxonomic levels; that of a myrmecophilous cricket was moderately diverse, while microbiotas of three myrmecophilous rove beetles (Staphylinidae), which have convergently evolved symbiosis with Liometopum, were dominated by intracellular endosymbionts. Yet, despite these compositional differences, similarities between ant and myrmecophile microbiotas correlated with the nature and intimacy of their behavioral relationships. Physical interactions such as grooming and trophallaxis likely facilitate cross-species extracellular microbial sharing. Further, phylogenetic comparisons of microbiotas from myrmecophile rove beetles and outgroups revealed a lack of co-cladogenesis of beetles and intracellular endosymbionts, and limited evidence for convergence among the myrmecophiles’ intracellular microbiotas. Comparative genomic analyses of the dominant Rickettsia endosymbiont of the most highly socially integrated myrmecophile imply possible functions unrelated to nutrient-provisioning in the host beetle’s specialized lifestyle. Our findings indicate that myrmecophile microbiotas evolve largely independently of the constraints of deep evolutionary history, and that the transition to life inside colonies, including social interactions with hosts, plays a significant role in structuring bacterial assemblages of these symbiotic insects.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 05, 2021.
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Structure of an ant-myrmecophile-microbe community
Elena K. Perry, Stefanos Siozios, Gregory D. D. Hurst, Joseph Parker
bioRxiv 2021.10.04.462948; doi: https://doi.org/10.1101/2021.10.04.462948
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Structure of an ant-myrmecophile-microbe community
Elena K. Perry, Stefanos Siozios, Gregory D. D. Hurst, Joseph Parker
bioRxiv 2021.10.04.462948; doi: https://doi.org/10.1101/2021.10.04.462948

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