Gut microbiota drives structural variation of exogenous probiotics to enhance colonization

Probiotics encounter colonization resistance from native gut microbiomes, affecting their effectiveness. Genetic engineering of probiotics lacks universal applicability, as gut microbiotas are highly individualized. Here, we employed probiotic Lactiplantibacillus plantarum HNU082 (Lp082) to test whe...

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Main Authors: Shuaiming Jiang, Shi Huang, Zeng Zhang, Wenyao Ma, Zhe Han, Yuan Song, Dongxue Huo, Weipeng Cui, Jiachao Zhang
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2025.2503371
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author Shuaiming Jiang
Shi Huang
Zeng Zhang
Wenyao Ma
Zhe Han
Yuan Song
Dongxue Huo
Weipeng Cui
Jiachao Zhang
author_facet Shuaiming Jiang
Shi Huang
Zeng Zhang
Wenyao Ma
Zhe Han
Yuan Song
Dongxue Huo
Weipeng Cui
Jiachao Zhang
author_sort Shuaiming Jiang
collection DOAJ
description Probiotics encounter colonization resistance from native gut microbiomes, affecting their effectiveness. Genetic engineering of probiotics lacks universal applicability, as gut microbiotas are highly individualized. Here, we employed probiotic Lactiplantibacillus plantarum HNU082 (Lp082) to test whether Lp082 gut-adapted mutants can resolve colonization resistance in a new gut environment. Relying on culture-based methods and metagenomics, two distinct evolutionary clades of Lp082 in mice gut were observed, where one clade, which acquired more mutations, exhibited a longer survival time. However, these Lp082 isolates carrying many single nucleotide variants (SNVs) still exhibited phenotypic inconsistencies, with 13 strains of enhanced acid resistance. Thus, nanopore sequencing was proposed to identify structural variations (SVs). Among them, 12 strains had the Cro/C1-type HTH DNA-binding domain insertion, which enhanced growth and reproduction under bile salt stress, thereby increasing colonization time and quantity in the gut. The gut domestication process can drive probiotics to undergo many SNVs and SVs, thereby enhancing their colonization ability, which provides new insights into the colonization mechanisms and offers an ecology-based strategy.
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institution Kabale University
issn 1949-0976
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language English
publishDate 2025-12-01
publisher Taylor & Francis Group
record_format Article
series Gut Microbes
spelling doaj-art-3bacb5adbf8f4f4e837bd1f1bc0f42592025-08-20T03:53:21ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2503371Gut microbiota drives structural variation of exogenous probiotics to enhance colonizationShuaiming Jiang0Shi Huang1Zeng Zhang2Wenyao Ma3Zhe Han4Yuan Song5Dongxue Huo6Weipeng Cui7Jiachao Zhang8School of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaFaculty of Dentistry, The University of Hong Kong, Hong Kong, SAR, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaSchool of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou, ChinaProbiotics encounter colonization resistance from native gut microbiomes, affecting their effectiveness. Genetic engineering of probiotics lacks universal applicability, as gut microbiotas are highly individualized. Here, we employed probiotic Lactiplantibacillus plantarum HNU082 (Lp082) to test whether Lp082 gut-adapted mutants can resolve colonization resistance in a new gut environment. Relying on culture-based methods and metagenomics, two distinct evolutionary clades of Lp082 in mice gut were observed, where one clade, which acquired more mutations, exhibited a longer survival time. However, these Lp082 isolates carrying many single nucleotide variants (SNVs) still exhibited phenotypic inconsistencies, with 13 strains of enhanced acid resistance. Thus, nanopore sequencing was proposed to identify structural variations (SVs). Among them, 12 strains had the Cro/C1-type HTH DNA-binding domain insertion, which enhanced growth and reproduction under bile salt stress, thereby increasing colonization time and quantity in the gut. The gut domestication process can drive probiotics to undergo many SNVs and SVs, thereby enhancing their colonization ability, which provides new insights into the colonization mechanisms and offers an ecology-based strategy.https://www.tandfonline.com/doi/10.1080/19490976.2025.2503371Gut-adapted strainsprobiotic bacteriaLactiplantibacillus plantarum HNU082divergent evolutionstructural variationscolonization
spellingShingle Shuaiming Jiang
Shi Huang
Zeng Zhang
Wenyao Ma
Zhe Han
Yuan Song
Dongxue Huo
Weipeng Cui
Jiachao Zhang
Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
Gut Microbes
Gut-adapted strains
probiotic bacteria
Lactiplantibacillus plantarum HNU082
divergent evolution
structural variations
colonization
title Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
title_full Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
title_fullStr Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
title_full_unstemmed Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
title_short Gut microbiota drives structural variation of exogenous probiotics to enhance colonization
title_sort gut microbiota drives structural variation of exogenous probiotics to enhance colonization
topic Gut-adapted strains
probiotic bacteria
Lactiplantibacillus plantarum HNU082
divergent evolution
structural variations
colonization
url https://www.tandfonline.com/doi/10.1080/19490976.2025.2503371
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