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Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress

Exploring the ecological mechanism of microbial community assembly in soil and the earthworm gut in a vanadium polluted environment could help us understand the effects of vanadium stress on microbial diversity maintenance and function, as well as the mechanism of microbial mitigation of vanadium st...

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Autores principales: Xia, Rong, Shi, Yu, Wang, Xinwei, Wu, Yunling, Sun, Mingming, Hu, Feng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725585/
https://www.ncbi.nlm.nih.gov/pubmed/35089099
http://dx.doi.org/10.1128/mSystems.01253-21
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author Xia, Rong
Shi, Yu
Wang, Xinwei
Wu, Yunling
Sun, Mingming
Hu, Feng
author_facet Xia, Rong
Shi, Yu
Wang, Xinwei
Wu, Yunling
Sun, Mingming
Hu, Feng
author_sort Xia, Rong
collection PubMed
description Exploring the ecological mechanism of microbial community assembly in soil and the earthworm gut in a vanadium polluted environment could help us understand the effects of vanadium stress on microbial diversity maintenance and function, as well as the mechanism of microbial mitigation of vanadium stress. Combining metagenomic sequencing and abundance distribution models, we explored the assembly of earthworm intestinal bacteria and native soil bacteria after 21 days of earthworm exposure to a gradient level of vanadate (0 to 300 mg kg(−1)) in soil. Stochastic processes dominated the assembly of both genes and taxa in earthworm gut and soil. Both the composition of taxa and functional genes in earthworm gut varied highly with the vanadium concentration, while in soil, only the taxa changed significantly, whereas the functional genes were relatively stable. The functional redundancy in soil, but not in the earthworm gut, was confirmed by a Mantel test and analysis of similarities (ANOSIM) test. In addition, vanadium detoxifying gene (VDG)-carrying taxa were more diverse but less abundant in soil than in the worm gut; and VDGs were more abundant in soil than in the worm gut. Their wider niche breadth indicated that VDG-carrying taxa were generalists in soil, in contrast to their role in the worm gut. These results suggested that earthworm intestinal and soil microbes adopted different strategies to counteract vanadium stress. The results provide new insights into the effects of soil vanadium stress on the assembly of earthworm gut and soil microbiota from both bacterial taxa and genetic function perspectives. IMPORTANCE Metagenomic sequencing revealed the variation of functional genes in the microbial community in soil and earthworm gut with increasing vanadium concentrations, which provided a new insight to explore the effect of vanadium stress on microbial community assembly from the perspective of functional genes. Our results reinforced the view that functional genes and taxa do not appear to have a simple corresponding relationship. Taxa are more sensitive compared with functional genes, suggesting the existence of bacterial functional redundancy in soil, but not in the earthworm gut. These observations indicate different assembly patterns of earthworm intestinal and soil bacteria under vanadium stress. Thus, it is important and necessary to include genetic functions to comprehensively understand microbial community assembly.
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spelling pubmed-87255852022-01-06 Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress Xia, Rong Shi, Yu Wang, Xinwei Wu, Yunling Sun, Mingming Hu, Feng mSystems Research Article Exploring the ecological mechanism of microbial community assembly in soil and the earthworm gut in a vanadium polluted environment could help us understand the effects of vanadium stress on microbial diversity maintenance and function, as well as the mechanism of microbial mitigation of vanadium stress. Combining metagenomic sequencing and abundance distribution models, we explored the assembly of earthworm intestinal bacteria and native soil bacteria after 21 days of earthworm exposure to a gradient level of vanadate (0 to 300 mg kg(−1)) in soil. Stochastic processes dominated the assembly of both genes and taxa in earthworm gut and soil. Both the composition of taxa and functional genes in earthworm gut varied highly with the vanadium concentration, while in soil, only the taxa changed significantly, whereas the functional genes were relatively stable. The functional redundancy in soil, but not in the earthworm gut, was confirmed by a Mantel test and analysis of similarities (ANOSIM) test. In addition, vanadium detoxifying gene (VDG)-carrying taxa were more diverse but less abundant in soil than in the worm gut; and VDGs were more abundant in soil than in the worm gut. Their wider niche breadth indicated that VDG-carrying taxa were generalists in soil, in contrast to their role in the worm gut. These results suggested that earthworm intestinal and soil microbes adopted different strategies to counteract vanadium stress. The results provide new insights into the effects of soil vanadium stress on the assembly of earthworm gut and soil microbiota from both bacterial taxa and genetic function perspectives. IMPORTANCE Metagenomic sequencing revealed the variation of functional genes in the microbial community in soil and earthworm gut with increasing vanadium concentrations, which provided a new insight to explore the effect of vanadium stress on microbial community assembly from the perspective of functional genes. Our results reinforced the view that functional genes and taxa do not appear to have a simple corresponding relationship. Taxa are more sensitive compared with functional genes, suggesting the existence of bacterial functional redundancy in soil, but not in the earthworm gut. These observations indicate different assembly patterns of earthworm intestinal and soil bacteria under vanadium stress. Thus, it is important and necessary to include genetic functions to comprehensively understand microbial community assembly. American Society for Microbiology 2022-01-04 /pmc/articles/PMC8725585/ /pubmed/35089099 http://dx.doi.org/10.1128/mSystems.01253-21 Text en Copyright © 2022 Xia et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Xia, Rong
Shi, Yu
Wang, Xinwei
Wu, Yunling
Sun, Mingming
Hu, Feng
Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title_full Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title_fullStr Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title_full_unstemmed Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title_short Metagenomic Sequencing Reveals that the Assembly of Functional Genes and Taxa Varied Highly and Lacked Redundancy in the Earthworm Gut Compared with Soil under Vanadium Stress
title_sort metagenomic sequencing reveals that the assembly of functional genes and taxa varied highly and lacked redundancy in the earthworm gut compared with soil under vanadium stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725585/
https://www.ncbi.nlm.nih.gov/pubmed/35089099
http://dx.doi.org/10.1128/mSystems.01253-21
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