Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers

Abstract Background Ligilactobacillus salivarius has been frequently isolated from the gut microbiota of humans and domesticated animals and has been studied as a candidate probiotic. Badger (Meles meles) is known as a “generalist” species that consumes complex foods and exhibits tolerance and resis...

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Main Authors: Yu Wang, Xiaomeng Xu, Huan Chen, Fang Yang, Bo Xu, Kun Wang, Qianwen Liu, Guixin Liang, Ruiqi Zhang, Xin’an Jiao, Yunzeng Zhang
Format: Article
Language:English
Published: BMC 2023-09-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09623-8
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author Yu Wang
Xiaomeng Xu
Huan Chen
Fang Yang
Bo Xu
Kun Wang
Qianwen Liu
Guixin Liang
Ruiqi Zhang
Xin’an Jiao
Yunzeng Zhang
author_facet Yu Wang
Xiaomeng Xu
Huan Chen
Fang Yang
Bo Xu
Kun Wang
Qianwen Liu
Guixin Liang
Ruiqi Zhang
Xin’an Jiao
Yunzeng Zhang
author_sort Yu Wang
collection DOAJ
description Abstract Background Ligilactobacillus salivarius has been frequently isolated from the gut microbiota of humans and domesticated animals and has been studied as a candidate probiotic. Badger (Meles meles) is known as a “generalist” species that consumes complex foods and exhibits tolerance and resistance to certain pathogens, which can be partly attributed to the beneficial microbes such as L. salivarius in the gut microbiota. However, our understanding of the beneficial traits and genomic features of badger-originated L. salivarius remains elusive. Results In this study, nine L. salivarius strains were isolated from wild badgers' feces, one of which exhibited good probiotic properties. Complete genomes of the nine L. salivarius strains were generated, and comparative genomic analysis was performed with the publicly available complete genomes of L. salivarius obtained from humans and domesticated animals. The strains originating from badgers harbored a larger genome, a higher number of protein-coding sequences, and functionally annotated genes than those originating from humans and chickens. The pan-genome phylogenetic tree demonstrated that the strains originating from badgers formed a separate clade, and totally 412 gene families (12.6% of the total gene families in the pan-genome) were identified as genes gained by the last common ancestor of the badger group. The badger group harbored significantly more gene families responsible for the degradation of complex carbohydrate substrates and production of polysaccharides than strains from other hosts; many of these were acquired by gene gain events. Conclusions A candidate probiotic and nine L. salivarius complete genomes were obtained from the badgers’ gut microbiome, and several beneficial genes were identified to be specifically present in the badger-originated strains that were gained in the evolution. Our study provides novel insights into the adaptation of L. salivarius to the intestinal habitat of wild badgers and provides valuable strain and genome resources for the development of L. salivarius as a probiotic.
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spelling doaj.art-030e6ba1e5d1499aab09f742ea4afa192023-11-26T12:25:47ZengBMCBMC Genomics1471-21642023-09-0124111610.1186/s12864-023-09623-8Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgersYu Wang0Xiaomeng Xu1Huan Chen2Fang Yang3Bo Xu4Kun Wang5Qianwen Liu6Guixin Liang7Ruiqi Zhang8Xin’an Jiao9Yunzeng Zhang10Jiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityJiangsu Co‐Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou UniversityAbstract Background Ligilactobacillus salivarius has been frequently isolated from the gut microbiota of humans and domesticated animals and has been studied as a candidate probiotic. Badger (Meles meles) is known as a “generalist” species that consumes complex foods and exhibits tolerance and resistance to certain pathogens, which can be partly attributed to the beneficial microbes such as L. salivarius in the gut microbiota. However, our understanding of the beneficial traits and genomic features of badger-originated L. salivarius remains elusive. Results In this study, nine L. salivarius strains were isolated from wild badgers' feces, one of which exhibited good probiotic properties. Complete genomes of the nine L. salivarius strains were generated, and comparative genomic analysis was performed with the publicly available complete genomes of L. salivarius obtained from humans and domesticated animals. The strains originating from badgers harbored a larger genome, a higher number of protein-coding sequences, and functionally annotated genes than those originating from humans and chickens. The pan-genome phylogenetic tree demonstrated that the strains originating from badgers formed a separate clade, and totally 412 gene families (12.6% of the total gene families in the pan-genome) were identified as genes gained by the last common ancestor of the badger group. The badger group harbored significantly more gene families responsible for the degradation of complex carbohydrate substrates and production of polysaccharides than strains from other hosts; many of these were acquired by gene gain events. Conclusions A candidate probiotic and nine L. salivarius complete genomes were obtained from the badgers’ gut microbiome, and several beneficial genes were identified to be specifically present in the badger-originated strains that were gained in the evolution. Our study provides novel insights into the adaptation of L. salivarius to the intestinal habitat of wild badgers and provides valuable strain and genome resources for the development of L. salivarius as a probiotic.https://doi.org/10.1186/s12864-023-09623-8Ligilactobacillus salivariusBadgerHost adaptationBeneficial effectsComplete genome
spellingShingle Yu Wang
Xiaomeng Xu
Huan Chen
Fang Yang
Bo Xu
Kun Wang
Qianwen Liu
Guixin Liang
Ruiqi Zhang
Xin’an Jiao
Yunzeng Zhang
Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
BMC Genomics
Ligilactobacillus salivarius
Badger
Host adaptation
Beneficial effects
Complete genome
title Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
title_full Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
title_fullStr Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
title_full_unstemmed Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
title_short Assessment of beneficial effects and identification of host adaptation-associated genes of Ligilactobacillus salivarius isolated from badgers
title_sort assessment of beneficial effects and identification of host adaptation associated genes of ligilactobacillus salivarius isolated from badgers
topic Ligilactobacillus salivarius
Badger
Host adaptation
Beneficial effects
Complete genome
url https://doi.org/10.1186/s12864-023-09623-8
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