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Worker-dependent gut symbiosis in an ant

The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbion...

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Autores principales: Shimoji, Hiroyuki, Itoh, Hideomi, Matsuura, Yu, Yamashita, Rio, Hori, Tomoyuki, Hojo, Masaru K., Kikuchi, Yoshitomo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723695/
https://www.ncbi.nlm.nih.gov/pubmed/37938661
http://dx.doi.org/10.1038/s43705-021-00061-9
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author Shimoji, Hiroyuki
Itoh, Hideomi
Matsuura, Yu
Yamashita, Rio
Hori, Tomoyuki
Hojo, Masaru K.
Kikuchi, Yoshitomo
author_facet Shimoji, Hiroyuki
Itoh, Hideomi
Matsuura, Yu
Yamashita, Rio
Hori, Tomoyuki
Hojo, Masaru K.
Kikuchi, Yoshitomo
author_sort Shimoji, Hiroyuki
collection PubMed
description The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbionts are generally considered to be maintained in an insect colony in two alternative ways: shared among all colony members or inherited only by a specific caste. Especially in ants, the reproductive caste plays a crucial role in transmission of the symbionts shared among colony members over generations. Here, we report an exceptional case, the worker-dependent microbiota in an ant, Diacamma cf. indicum from Japan. By collecting almost all the individuals from 22 colonies in the field, we revealed that microbiota of workers is characterized by a single dominant bacterium localized at the hindgut. The bacterium belonging to an unclassified member within the phylum Firmicutes, which is scarce or mostly absent in the reproductive castes. Furthermore, we show that the gut symbiont is acquired at the adult stage. Collectively, our findings strongly suggest that the specific symbiont is maintained by only workers, demonstrating a novel pattern of ant-associated bacterial symbiosis, and thus further our understanding of host-microbe interactions in the light of sociobiology.
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spelling pubmed-97236952023-01-04 Worker-dependent gut symbiosis in an ant Shimoji, Hiroyuki Itoh, Hideomi Matsuura, Yu Yamashita, Rio Hori, Tomoyuki Hojo, Masaru K. Kikuchi, Yoshitomo ISME Commun Article The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbionts are generally considered to be maintained in an insect colony in two alternative ways: shared among all colony members or inherited only by a specific caste. Especially in ants, the reproductive caste plays a crucial role in transmission of the symbionts shared among colony members over generations. Here, we report an exceptional case, the worker-dependent microbiota in an ant, Diacamma cf. indicum from Japan. By collecting almost all the individuals from 22 colonies in the field, we revealed that microbiota of workers is characterized by a single dominant bacterium localized at the hindgut. The bacterium belonging to an unclassified member within the phylum Firmicutes, which is scarce or mostly absent in the reproductive castes. Furthermore, we show that the gut symbiont is acquired at the adult stage. Collectively, our findings strongly suggest that the specific symbiont is maintained by only workers, demonstrating a novel pattern of ant-associated bacterial symbiosis, and thus further our understanding of host-microbe interactions in the light of sociobiology. Nature Publishing Group UK 2021-10-28 /pmc/articles/PMC9723695/ /pubmed/37938661 http://dx.doi.org/10.1038/s43705-021-00061-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Shimoji, Hiroyuki
Itoh, Hideomi
Matsuura, Yu
Yamashita, Rio
Hori, Tomoyuki
Hojo, Masaru K.
Kikuchi, Yoshitomo
Worker-dependent gut symbiosis in an ant
title Worker-dependent gut symbiosis in an ant
title_full Worker-dependent gut symbiosis in an ant
title_fullStr Worker-dependent gut symbiosis in an ant
title_full_unstemmed Worker-dependent gut symbiosis in an ant
title_short Worker-dependent gut symbiosis in an ant
title_sort worker-dependent gut symbiosis in an ant
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723695/
https://www.ncbi.nlm.nih.gov/pubmed/37938661
http://dx.doi.org/10.1038/s43705-021-00061-9
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