Cited by 25Probiotics and Fermented FoodsEvolution and Genetic DynamicsGut microbiota and health

Native microbiome dominates over host factors in shaping the probiotic genetic evolution in the gut

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Jiang, Shuaiming, Zhang, Chengcheng, Han, Zhe, Ma, Wenyao, Wang, Shunhe, Huo, Dongxue, Cui, Weipeng, Zhai, Qixiao +2 more·2023·npj Biofilms and Microbiomes

Abstract

Probiotics often acquire potentially adaptive mutations in vivo, gaining new functional traits through gut selection. While both the host and microbiome can contribute to probiotics’ genetic evolution, separating the microbiome and the host’s contribution to such selective pressures remains challenging. Here, we introduced germ-free (GF) and specific pathogen-free (SPF) mouse models to track how probiotic strains, i.e., Lactiplantibacillus plantarum HNU082 (Lp082) and Bifidobacterium animalis subsp. lactis V9 (BV9), genetically evolved under selection pressures derived from host factors alone and both host and microbial ecological factors. Notably, compared to the genome of a probiotic strain before consumption, the host only elicited <15 probiotic mutations in probiotic genomes that emerged in the luminal environment of GF mice, while a total of 840 mutations in Lp082 mutants and 21,579 mutations in BV9 were found in SPF mice, <0.25% of those derived from both factors that were never captured by other experimental evolution studies, indicating that keen microbial competitions exhibited the predominant evolutionary force in shaping probiotic genetic composition (>99.75%). For a given probiotic, functional genes occurring in potentially adaptive mutations induced by hosts (GF mice) were all shared with those found in mutants of SPF mice. Collectively, the native microbiome consistently drove a more rapid and divergent genetic evolution of probiotic strains in seven days of colonization than host factors did. Our study further laid a theoretical foundation for genetically engineering probiotics for better gut adaptation through in vitro artificial gut ecosystems without the selection pressures derived from host factors.

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  • Two probiotics (Lp082 and Bifidobacterium animalis subsp. lactis V9) can both undergo adaptive mutations in the mouse gut and have also been observed to exhibit a trend toward divergent evolution.

    “Our previous research has shown that two probiotics (Lp082 and Bifidobacterium animalis subsp. lactis V9) can both undergo adaptive mutations in the mouse gut and have also been observed to exhibit a trend toward divergent evolution.38”

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Authors
Jiang, S., Zhang, C., Han, Z., Ma, W., Wang, S., Huo, D., Cui, W., Zhai, Q., Huang, S., & Zhang, J.
Affiliations
  • Hainan University (CN)
  • Jiangnan University (CN)
  • University of Hong Kong (HK)
Corresponding author
  • Zhai, Qixiao
  • Huang, Shi
  • Zhang, Jiachao
Venue
npj Biofilms and Microbiomes
Published
2023-10-14
Volume
9
Issue
1
Pages
80-80
ISSN
2055-5008 (ISSN-L)
OpenAlex
W4387640510
Cited by
25
References
40
Citations by year
2026: 12 · 2025: 11 · 2024: 2
FWCI
3.59
Type
journal article
Language
en
Open access
Locations
  • npj Biofilms and Microbiomes (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Natural Science Foundation of China (32222066)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
gut microbiota, host factors, adaptive mutation, Lactobacillus plantarum, Bifidobacterium animalis subsp. lactis, germ-free mice, specific pathogen-free mice, microbial competition, intestinal adaptation
MeSH terms
Gastrointestinal Microbiome, Animals, Probiotics, Mice, Microbiota

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