Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen

Abstract Microbial colonization plays a direct role in host health. Understanding the ecology of the resident microbial community for a given host species is thus an important step for detecting population vulnerabilities like disease. However, the idea of integrating microbiome research into conser...

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Main Authors: Sage D. Rohrer, Gustavo Jiménez-Uzcátegui, Patricia G. Parker, Lon M. Chubiz
Format: Article
Language:English
Published: Nature Portfolio 2023-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-31826-y
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author Sage D. Rohrer
Gustavo Jiménez-Uzcátegui
Patricia G. Parker
Lon M. Chubiz
author_facet Sage D. Rohrer
Gustavo Jiménez-Uzcátegui
Patricia G. Parker
Lon M. Chubiz
author_sort Sage D. Rohrer
collection DOAJ
description Abstract Microbial colonization plays a direct role in host health. Understanding the ecology of the resident microbial community for a given host species is thus an important step for detecting population vulnerabilities like disease. However, the idea of integrating microbiome research into conservation is still relatively new, and wild birds have received less attention in this field than mammals or domesticated animals. Here we examine the composition and function of the gut microbiome of the endangered Galapagos penguin (Spheniscus mendiculus) with the goals of characterizing the normal microbial community and resistome, identifying likely pathogens, and testing hypotheses of structuring forces for this community based on demographics, location, and infection status. We collected fecal samples from wild penguins in 2018 and performed 16S rRNA gene sequencing and whole genome sequencing (WGS) on extracted DNA. 16S sequencing revealed that the bacterial phyla Fusobacteria, Epsilonbacteraeota, Firmicutes, and Proteobacteria dominate the community. Functional pathways were computed from WGS data, showing genetic functional potential primarily focused on metabolism—amino acid metabolism, carbohydrate metabolism, and energy metabolism are the most well-represented functional groups. WGS samples were each screened for antimicrobial resistance, characterizing a resistome made up of nine antibiotic resistance genes. Samples were screened for potential enteric pathogens using virulence factors as indicators; Clostridium perfringens was revealed as a likely pathogen. Overall, three factors appear to be shaping the alpha and beta diversity of the microbial community: penguin developmental stage, sampling location, and C. perfringens. We found that juvenile penguins have significantly lower alpha diversity than adults based on three metrics, as well as significantly different beta diversity. Location effects are minimal, but one site has significantly lower Shannon diversity than the other primary sites. Finally, when samples were grouped by C. perfringens virulence factors, we found dramatic changes in beta diversity based on operational taxonomic units, protein families, and functional pathways. This study provides a baseline microbiome for an endangered species, implicates both penguin age and the presence of a potential bacterial pathogen as primary factors associated with microbial community variance, and reveals widespread antibiotic resistance genes across the population.
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spelling doaj.art-f6251afbc5814ee2849a6fae6f31ea022023-04-03T05:26:08ZengNature PortfolioScientific Reports2045-23222023-04-0113111310.1038/s41598-023-31826-yComposition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogenSage D. Rohrer0Gustavo Jiménez-Uzcátegui1Patricia G. Parker2Lon M. Chubiz3Department of Biology and Whitney R. Harris World Ecology Center, University of Missouri-St. Louis, One University Blvd.Charles Darwin Research Station, Charles Darwin FoundationDepartment of Biology and Whitney R. Harris World Ecology Center, University of Missouri-St. Louis, One University Blvd.Department of Biology and Whitney R. Harris World Ecology Center, University of Missouri-St. Louis, One University Blvd.Abstract Microbial colonization plays a direct role in host health. Understanding the ecology of the resident microbial community for a given host species is thus an important step for detecting population vulnerabilities like disease. However, the idea of integrating microbiome research into conservation is still relatively new, and wild birds have received less attention in this field than mammals or domesticated animals. Here we examine the composition and function of the gut microbiome of the endangered Galapagos penguin (Spheniscus mendiculus) with the goals of characterizing the normal microbial community and resistome, identifying likely pathogens, and testing hypotheses of structuring forces for this community based on demographics, location, and infection status. We collected fecal samples from wild penguins in 2018 and performed 16S rRNA gene sequencing and whole genome sequencing (WGS) on extracted DNA. 16S sequencing revealed that the bacterial phyla Fusobacteria, Epsilonbacteraeota, Firmicutes, and Proteobacteria dominate the community. Functional pathways were computed from WGS data, showing genetic functional potential primarily focused on metabolism—amino acid metabolism, carbohydrate metabolism, and energy metabolism are the most well-represented functional groups. WGS samples were each screened for antimicrobial resistance, characterizing a resistome made up of nine antibiotic resistance genes. Samples were screened for potential enteric pathogens using virulence factors as indicators; Clostridium perfringens was revealed as a likely pathogen. Overall, three factors appear to be shaping the alpha and beta diversity of the microbial community: penguin developmental stage, sampling location, and C. perfringens. We found that juvenile penguins have significantly lower alpha diversity than adults based on three metrics, as well as significantly different beta diversity. Location effects are minimal, but one site has significantly lower Shannon diversity than the other primary sites. Finally, when samples were grouped by C. perfringens virulence factors, we found dramatic changes in beta diversity based on operational taxonomic units, protein families, and functional pathways. This study provides a baseline microbiome for an endangered species, implicates both penguin age and the presence of a potential bacterial pathogen as primary factors associated with microbial community variance, and reveals widespread antibiotic resistance genes across the population.https://doi.org/10.1038/s41598-023-31826-y
spellingShingle Sage D. Rohrer
Gustavo Jiménez-Uzcátegui
Patricia G. Parker
Lon M. Chubiz
Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
Scientific Reports
title Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
title_full Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
title_fullStr Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
title_full_unstemmed Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
title_short Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen
title_sort composition and function of the galapagos penguin gut microbiome vary with age location and a putative bacterial pathogen
url https://doi.org/10.1038/s41598-023-31826-y
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