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Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)

BACKGROUND: Host associated gut microbiota are important in understanding the coevolution of host-microbe, and how they may help wildlife populations to adapt to rapid environmental changes. Mammalian gut microbiota composition and diversity may be affected by a variety of factors including geograph...

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Autores principales: Neha, Sufia Akter, Salazar-Bravo, Jorge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9979494/
https://www.ncbi.nlm.nih.gov/pubmed/36858951
http://dx.doi.org/10.1186/s12866-023-02778-0
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author Neha, Sufia Akter
Salazar-Bravo, Jorge
author_facet Neha, Sufia Akter
Salazar-Bravo, Jorge
author_sort Neha, Sufia Akter
collection PubMed
description BACKGROUND: Host associated gut microbiota are important in understanding the coevolution of host-microbe, and how they may help wildlife populations to adapt to rapid environmental changes. Mammalian gut microbiota composition and diversity may be affected by a variety of factors including geographic variation, seasonal variation in diet, habitat disturbance, environmental conditions, age, and sex. However, there have been few studies that examined how ecological and environmental factors influence gut microbiota composition in animals' natural environments. In this study, we explore how host habitat, geographical location and environmental factors affect the fecal microbiota of Cynomys ludovicianus at a small spatial scale. We collected fecal samples from five geographically distinct locations in the Texas Panhandle classified as urban and rural areas and analyzed them using high throughput 16S rRNA gene amplicon sequencing. RESULTS: The results showed that microbiota of these fecal samples was largely dominated by the phylum Bacteroidetes. Fecal microbiome diversity and composition differed significantly across sampling sites and habitats. Prairie dogs inhabiting urban areas showed reduced fecal diversity due to more homogenous environment and, likely, anthropogenic disturbance. Urban prairie dog colonies displayed greater phylogenetic variation among replicates than those in rural habitats. Differentially abundant analysis revealed that bacterial species pathogenic to humans and animals were highly abundant in urban areas which indicates that host health and fitness might be negatively affected. Random forest models identified Alistipes shahii as the important species driving the changes in fecal microbiome composition. Despite the effects of habitat and geographic location of host, we found a strong correlation with environmental factors and that- average maximum temperature was the best predictor of prairie dog fecal microbial diversity. CONCLUSIONS: Our findings suggest that reduction in alpha diversity in conjunction with greater dispersion in beta diversity could be indicative of declining host health in urban areas; this information may, in turn, help determine future conservation efforts. Moreover, several bacterial species pathogenic to humans and other animals were enriched in prairie dog colonies near urban areas, which may in turn adversely affect host phenotype and fitness. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02778-0.
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spelling pubmed-99794942023-03-03 Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus) Neha, Sufia Akter Salazar-Bravo, Jorge BMC Microbiol Research BACKGROUND: Host associated gut microbiota are important in understanding the coevolution of host-microbe, and how they may help wildlife populations to adapt to rapid environmental changes. Mammalian gut microbiota composition and diversity may be affected by a variety of factors including geographic variation, seasonal variation in diet, habitat disturbance, environmental conditions, age, and sex. However, there have been few studies that examined how ecological and environmental factors influence gut microbiota composition in animals' natural environments. In this study, we explore how host habitat, geographical location and environmental factors affect the fecal microbiota of Cynomys ludovicianus at a small spatial scale. We collected fecal samples from five geographically distinct locations in the Texas Panhandle classified as urban and rural areas and analyzed them using high throughput 16S rRNA gene amplicon sequencing. RESULTS: The results showed that microbiota of these fecal samples was largely dominated by the phylum Bacteroidetes. Fecal microbiome diversity and composition differed significantly across sampling sites and habitats. Prairie dogs inhabiting urban areas showed reduced fecal diversity due to more homogenous environment and, likely, anthropogenic disturbance. Urban prairie dog colonies displayed greater phylogenetic variation among replicates than those in rural habitats. Differentially abundant analysis revealed that bacterial species pathogenic to humans and animals were highly abundant in urban areas which indicates that host health and fitness might be negatively affected. Random forest models identified Alistipes shahii as the important species driving the changes in fecal microbiome composition. Despite the effects of habitat and geographic location of host, we found a strong correlation with environmental factors and that- average maximum temperature was the best predictor of prairie dog fecal microbial diversity. CONCLUSIONS: Our findings suggest that reduction in alpha diversity in conjunction with greater dispersion in beta diversity could be indicative of declining host health in urban areas; this information may, in turn, help determine future conservation efforts. Moreover, several bacterial species pathogenic to humans and other animals were enriched in prairie dog colonies near urban areas, which may in turn adversely affect host phenotype and fitness. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02778-0. BioMed Central 2023-03-02 /pmc/articles/PMC9979494/ /pubmed/36858951 http://dx.doi.org/10.1186/s12866-023-02778-0 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
Neha, Sufia Akter
Salazar-Bravo, Jorge
Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title_full Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title_fullStr Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title_full_unstemmed Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title_short Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)
title_sort fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (cynomys ludovicianus)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9979494/
https://www.ncbi.nlm.nih.gov/pubmed/36858951
http://dx.doi.org/10.1186/s12866-023-02778-0
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