Cargando…

Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas

BACKGROUND: In contrast with macroorganisms, that show well-documented biogeographical patterns in distribution associated with local adaptation of physiology, behavior and life history, strong biogeographical patterns have not been found for microorganisms, raising questions about what determines t...

Descripción completa

Detalles Bibliográficos
Autores principales: van Veelen, H. Pieter J., Ibáñez-Álamo, Juan Diego, Horrocks, Nicholas P. C., Hegemann, Arne, Ndithia, Henry K., Shobrak, Mohammed, Tieleman, B. Irene
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9921332/
https://www.ncbi.nlm.nih.gov/pubmed/36765278
http://dx.doi.org/10.1186/s12866-023-02768-2
_version_ 1784887286556524544
author van Veelen, H. Pieter J.
Ibáñez-Álamo, Juan Diego
Horrocks, Nicholas P. C.
Hegemann, Arne
Ndithia, Henry K.
Shobrak, Mohammed
Tieleman, B. Irene
author_facet van Veelen, H. Pieter J.
Ibáñez-Álamo, Juan Diego
Horrocks, Nicholas P. C.
Hegemann, Arne
Ndithia, Henry K.
Shobrak, Mohammed
Tieleman, B. Irene
author_sort van Veelen, H. Pieter J.
collection PubMed
description BACKGROUND: In contrast with macroorganisms, that show well-documented biogeographical patterns in distribution associated with local adaptation of physiology, behavior and life history, strong biogeographical patterns have not been found for microorganisms, raising questions about what determines their biogeography. Thus far, large-scale biogeographical studies have focused on free-living microbes, paying little attention to host-associated microbes, which play essential roles in physiology, behavior and life history of their hosts. Investigating cloacal gut microbiota of closely-related, ecologically similar free-living songbird species (Alaudidae, larks) inhabiting desert, temperate and tropical regions, we explored influences of geographical location and host species on α-diversity, co-occurrence of amplicon sequence variants (ASVs) and genera, differentially abundant and dominant bacterial taxa, and community composition. We also investigated how geographical distance explained differences in gut microbial community composition among larks. RESULTS: Geographic location did not explain variation in richness and Shannon diversity of cloacal microbiota in larks. Out of 3798 ASVs and 799 bacterial genera identified, 17 ASVs (< 0.5%) and 43 genera (5%) were shared by larks from all locations. Desert larks held fewer unique ASVs (25%) than temperate zone (31%) and tropical larks (34%). Five out of 33 detected bacterial phyla dominated lark cloacal gut microbiomes. In tropical larks three bacterial classes were overrepresented. Highlighting the distinctiveness of desert lark microbiota, the relative abundances of 52 ASVs differed among locations, which classified within three dominant and 11 low-abundance phyla. Clear and significant phylogenetic clustering in cloacal microbiota community composition (unweighted UniFrac) showed segregation with geography and host species, where microbiota of desert larks were distinct from those of tropical and temperate regions. Geographic distance was nonlinearly associated with pairwise unweighted UniFrac distances. CONCLUSIONS: We conclude that host-associated microbiota are geographically structured in a group of widespread but closely-related bird species, following large-scale macro-ecological patterns and contrasting with previous findings for free-living microbes. Future work should further explore if and to what extent geographic variation in host-associated microbiota can be explained as result of co-evolution between gut microbes and host adaptive traits, and if and how acquisition from the environmental pool of bacteria contributes to explaining host-associated communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02768-2.
format Online
Article
Text
id pubmed-9921332
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-99213322023-02-12 Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas van Veelen, H. Pieter J. Ibáñez-Álamo, Juan Diego Horrocks, Nicholas P. C. Hegemann, Arne Ndithia, Henry K. Shobrak, Mohammed Tieleman, B. Irene BMC Microbiol Research BACKGROUND: In contrast with macroorganisms, that show well-documented biogeographical patterns in distribution associated with local adaptation of physiology, behavior and life history, strong biogeographical patterns have not been found for microorganisms, raising questions about what determines their biogeography. Thus far, large-scale biogeographical studies have focused on free-living microbes, paying little attention to host-associated microbes, which play essential roles in physiology, behavior and life history of their hosts. Investigating cloacal gut microbiota of closely-related, ecologically similar free-living songbird species (Alaudidae, larks) inhabiting desert, temperate and tropical regions, we explored influences of geographical location and host species on α-diversity, co-occurrence of amplicon sequence variants (ASVs) and genera, differentially abundant and dominant bacterial taxa, and community composition. We also investigated how geographical distance explained differences in gut microbial community composition among larks. RESULTS: Geographic location did not explain variation in richness and Shannon diversity of cloacal microbiota in larks. Out of 3798 ASVs and 799 bacterial genera identified, 17 ASVs (< 0.5%) and 43 genera (5%) were shared by larks from all locations. Desert larks held fewer unique ASVs (25%) than temperate zone (31%) and tropical larks (34%). Five out of 33 detected bacterial phyla dominated lark cloacal gut microbiomes. In tropical larks three bacterial classes were overrepresented. Highlighting the distinctiveness of desert lark microbiota, the relative abundances of 52 ASVs differed among locations, which classified within three dominant and 11 low-abundance phyla. Clear and significant phylogenetic clustering in cloacal microbiota community composition (unweighted UniFrac) showed segregation with geography and host species, where microbiota of desert larks were distinct from those of tropical and temperate regions. Geographic distance was nonlinearly associated with pairwise unweighted UniFrac distances. CONCLUSIONS: We conclude that host-associated microbiota are geographically structured in a group of widespread but closely-related bird species, following large-scale macro-ecological patterns and contrasting with previous findings for free-living microbes. Future work should further explore if and to what extent geographic variation in host-associated microbiota can be explained as result of co-evolution between gut microbes and host adaptive traits, and if and how acquisition from the environmental pool of bacteria contributes to explaining host-associated communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02768-2. BioMed Central 2023-02-11 /pmc/articles/PMC9921332/ /pubmed/36765278 http://dx.doi.org/10.1186/s12866-023-02768-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
van Veelen, H. Pieter J.
Ibáñez-Álamo, Juan Diego
Horrocks, Nicholas P. C.
Hegemann, Arne
Ndithia, Henry K.
Shobrak, Mohammed
Tieleman, B. Irene
Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title_full Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title_fullStr Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title_full_unstemmed Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title_short Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
title_sort cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9921332/
https://www.ncbi.nlm.nih.gov/pubmed/36765278
http://dx.doi.org/10.1186/s12866-023-02768-2
work_keys_str_mv AT vanveelenhpieterj cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT ibanezalamojuandiego cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT horrocksnicholaspc cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT hegemannarne cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT ndithiahenryk cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT shobrakmohammed cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas
AT tielemanbirene cloacalmicrobiotaarebiogeographicallystructuredinlarksfromdeserttropicalandtemperateareas