Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>

ABSTRACT Symbiotic microorganisms can have a profound impact on the host physiology and behavior, and novel relationships between symbionts and their hosts are continually discovered. A colony of social ants consists of various castes that exhibit distinct lifestyles and is, thus, a unique model for...

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Autores principales:	Akiko Koto, Masaru Konishi Nobu, Ryo Miyazaki
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	ant gut microbiota social insect Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5175a41ecb794d8187d01017d44bd85f
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spelling	oai:doaj.org-article:5175a41ecb794d8187d01017d44bd85f2021-11-15T15:57:03ZDeep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>10.1128/mBio.00408-202150-7511https://doaj.org/article/5175a41ecb794d8187d01017d44bd85f2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00408-20https://doaj.org/toc/2150-7511ABSTRACT Symbiotic microorganisms can have a profound impact on the host physiology and behavior, and novel relationships between symbionts and their hosts are continually discovered. A colony of social ants consists of various castes that exhibit distinct lifestyles and is, thus, a unique model for investigating how symbionts may be involved in host eusociality. Yet our knowledge of social ant-symbiont dynamics has remained rudimentary. Through 16S rRNA gene deep sequencing of the carpenter ant Camponotus japonicus symbiont community across various castes, we here report caste-dependent diversity of commensal gut microbiota and lineage divergence of “Candidatus Blochmannia,” an obligate endosymbiont. While most prevalent gut-associated bacterial populations are found across all castes (Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes, and Cyanobacteria), we also discovered uncultured populations that are found only in males (belonging to Corynebacteriales, Alkanindiges, and Burkholderia). Most of those populations are not detected in laboratory-maintained queens and workers, suggesting that they are facultative gut symbionts introduced via environmental acquisition. Further inspection of “Ca. Blochmannia” endosymbionts reveals that two populations are dominant in all individuals across all castes but that males preferentially contain two different sublineages that are diversified from others. Clearly, each caste has distinct symbiont communities, suggesting an overlooked biological aspect of host-symbiont interaction in social insects. IMPORTANCE Social animals, such as primates and some insects, have been shown to exchange symbiotic microbes among individuals through sharing diet or habitats, resulting in increased consistency of microbiota among social partners. The ant is a representative of social insects exhibiting various castes within a colony; queens, males, and nonreproductive females (so-called workers) show distinct morphologies, physiologies, and behaviors but tightly interact with each other in the nest. However, how this social context affects their gut microbiota has remained unclear. In this study, we deeply sequenced the gut symbiont community across various castes of the carpenter ant Camponotus japonicus. We report caste-dependent diversity of commensal gut microbial community and lineage divergence of the mutualistic endosymbiont “Candidatus Blochmannia.” This report sheds light on the hidden diversity in microbial populations and community structure associated with guts of males in social ants.Akiko KotoMasaru Konishi NobuRyo MiyazakiAmerican Society for Microbiologyarticleantgut microbiotasocial insectMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	ant gut microbiota social insect Microbiology QR1-502
spellingShingle	ant gut microbiota social insect Microbiology QR1-502 Akiko Koto Masaru Konishi Nobu Ryo Miyazaki Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
description	ABSTRACT Symbiotic microorganisms can have a profound impact on the host physiology and behavior, and novel relationships between symbionts and their hosts are continually discovered. A colony of social ants consists of various castes that exhibit distinct lifestyles and is, thus, a unique model for investigating how symbionts may be involved in host eusociality. Yet our knowledge of social ant-symbiont dynamics has remained rudimentary. Through 16S rRNA gene deep sequencing of the carpenter ant Camponotus japonicus symbiont community across various castes, we here report caste-dependent diversity of commensal gut microbiota and lineage divergence of “Candidatus Blochmannia,” an obligate endosymbiont. While most prevalent gut-associated bacterial populations are found across all castes (Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes, and Cyanobacteria), we also discovered uncultured populations that are found only in males (belonging to Corynebacteriales, Alkanindiges, and Burkholderia). Most of those populations are not detected in laboratory-maintained queens and workers, suggesting that they are facultative gut symbionts introduced via environmental acquisition. Further inspection of “Ca. Blochmannia” endosymbionts reveals that two populations are dominant in all individuals across all castes but that males preferentially contain two different sublineages that are diversified from others. Clearly, each caste has distinct symbiont communities, suggesting an overlooked biological aspect of host-symbiont interaction in social insects. IMPORTANCE Social animals, such as primates and some insects, have been shown to exchange symbiotic microbes among individuals through sharing diet or habitats, resulting in increased consistency of microbiota among social partners. The ant is a representative of social insects exhibiting various castes within a colony; queens, males, and nonreproductive females (so-called workers) show distinct morphologies, physiologies, and behaviors but tightly interact with each other in the nest. However, how this social context affects their gut microbiota has remained unclear. In this study, we deeply sequenced the gut symbiont community across various castes of the carpenter ant Camponotus japonicus. We report caste-dependent diversity of commensal gut microbial community and lineage divergence of the mutualistic endosymbiont “Candidatus Blochmannia.” This report sheds light on the hidden diversity in microbial populations and community structure associated with guts of males in social ants.
format	article
author	Akiko Koto Masaru Konishi Nobu Ryo Miyazaki
author_facet	Akiko Koto Masaru Konishi Nobu Ryo Miyazaki
author_sort	Akiko Koto
title	Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
title_short	Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
title_full	Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
title_fullStr	Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
title_full_unstemmed	Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>
title_sort	deep sequencing uncovers caste-associated diversity of symbionts in the social ant <named-content content-type="genus-species">camponotus japonicus</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5175a41ecb794d8187d01017d44bd85f
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Deep Sequencing Uncovers Caste-Associated Diversity of Symbionts in the Social Ant <named-content content-type="genus-species">Camponotus japonicus</named-content>

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