Cargando…

The gut microbiome mediates adaptation to scarce food in Coleoptera

Beetles are ubiquitous cave invertebrates worldwide that adapted to scarce subterranean resources when they colonized caves. Here, we investigated the potential role of gut microbiota in the adaptation of beetles to caves from different climatic regions of the Carpathians. The beetles’ microbiota wa...

Descripción completa

Detalles Bibliográficos
Autores principales: Moldovan, Oana Teodora, Carrell, Alyssa A., Bulzu, Paul-Adrian, Levei, Erika, Bucur, Ruxandra, Sitar, Cristian, Faur, Luchiana, Mirea, Ionuț Cornel, Șenilă, Marin, Cadar, Oana, Podar, Mircea
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10644639/
https://www.ncbi.nlm.nih.gov/pubmed/37957741
http://dx.doi.org/10.1186/s40793-023-00537-2
_version_ 1785147272099528704
author Moldovan, Oana Teodora
Carrell, Alyssa A.
Bulzu, Paul-Adrian
Levei, Erika
Bucur, Ruxandra
Sitar, Cristian
Faur, Luchiana
Mirea, Ionuț Cornel
Șenilă, Marin
Cadar, Oana
Podar, Mircea
author_facet Moldovan, Oana Teodora
Carrell, Alyssa A.
Bulzu, Paul-Adrian
Levei, Erika
Bucur, Ruxandra
Sitar, Cristian
Faur, Luchiana
Mirea, Ionuț Cornel
Șenilă, Marin
Cadar, Oana
Podar, Mircea
author_sort Moldovan, Oana Teodora
collection PubMed
description Beetles are ubiquitous cave invertebrates worldwide that adapted to scarce subterranean resources when they colonized caves. Here, we investigated the potential role of gut microbiota in the adaptation of beetles to caves from different climatic regions of the Carpathians. The beetles’ microbiota was host-specific, reflecting phylogenetic and nutritional adaptation. The microbial community structure further resolved conspecific beetles by caves suggesting microbiota-host coevolution and influences by local environmental factors. The detritivore species hosted a variety of bacteria known to decompose and ferment organic matter, suggesting turnover and host cooperative digestion of the sedimentary microbiota and allochthonous-derived nutrients. The cave Carabidae, with strong mandibula, adapted to predation and scavenging of animal and plant remains, had distinct microbiota dominated by symbiotic lineages Spiroplasma or Wolbachia. All beetles had relatively high levels of fermentative Carnobacterium and Vagococcus involved in lipid accumulation and a reduction of metabolic activity, and both features characterize adaptation to caves. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00537-2.
format Online
Article
Text
id pubmed-10644639
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-106446392023-11-13 The gut microbiome mediates adaptation to scarce food in Coleoptera Moldovan, Oana Teodora Carrell, Alyssa A. Bulzu, Paul-Adrian Levei, Erika Bucur, Ruxandra Sitar, Cristian Faur, Luchiana Mirea, Ionuț Cornel Șenilă, Marin Cadar, Oana Podar, Mircea Environ Microbiome Research Beetles are ubiquitous cave invertebrates worldwide that adapted to scarce subterranean resources when they colonized caves. Here, we investigated the potential role of gut microbiota in the adaptation of beetles to caves from different climatic regions of the Carpathians. The beetles’ microbiota was host-specific, reflecting phylogenetic and nutritional adaptation. The microbial community structure further resolved conspecific beetles by caves suggesting microbiota-host coevolution and influences by local environmental factors. The detritivore species hosted a variety of bacteria known to decompose and ferment organic matter, suggesting turnover and host cooperative digestion of the sedimentary microbiota and allochthonous-derived nutrients. The cave Carabidae, with strong mandibula, adapted to predation and scavenging of animal and plant remains, had distinct microbiota dominated by symbiotic lineages Spiroplasma or Wolbachia. All beetles had relatively high levels of fermentative Carnobacterium and Vagococcus involved in lipid accumulation and a reduction of metabolic activity, and both features characterize adaptation to caves. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00537-2. BioMed Central 2023-11-13 /pmc/articles/PMC10644639/ /pubmed/37957741 http://dx.doi.org/10.1186/s40793-023-00537-2 Text en © The Author(s) 2023 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Moldovan, Oana Teodora
Carrell, Alyssa A.
Bulzu, Paul-Adrian
Levei, Erika
Bucur, Ruxandra
Sitar, Cristian
Faur, Luchiana
Mirea, Ionuț Cornel
Șenilă, Marin
Cadar, Oana
Podar, Mircea
The gut microbiome mediates adaptation to scarce food in Coleoptera
title The gut microbiome mediates adaptation to scarce food in Coleoptera
title_full The gut microbiome mediates adaptation to scarce food in Coleoptera
title_fullStr The gut microbiome mediates adaptation to scarce food in Coleoptera
title_full_unstemmed The gut microbiome mediates adaptation to scarce food in Coleoptera
title_short The gut microbiome mediates adaptation to scarce food in Coleoptera
title_sort gut microbiome mediates adaptation to scarce food in coleoptera
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10644639/
https://www.ncbi.nlm.nih.gov/pubmed/37957741
http://dx.doi.org/10.1186/s40793-023-00537-2
work_keys_str_mv AT moldovanoanateodora thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT carrellalyssaa thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT bulzupauladrian thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT leveierika thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT bucurruxandra thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT sitarcristian thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT faurluchiana thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT mireaionutcornel thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT senilamarin thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT cadaroana thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT podarmircea thegutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT moldovanoanateodora gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT carrellalyssaa gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT bulzupauladrian gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT leveierika gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT bucurruxandra gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT sitarcristian gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT faurluchiana gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT mireaionutcornel gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT senilamarin gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT cadaroana gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera
AT podarmircea gutmicrobiomemediatesadaptationtoscarcefoodincoleoptera