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Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling

BACKGROUND: As genetic entities infecting and replicating only in bacteria, bacteriophages can regulate the community structure and functions of their host bacteria. The ecological roles of bacteriophages in aquatic and forest environments have been widely explored, but those in agroecosystems remai...

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Autores principales: Wang, Yajiao, Liu, Yu, Wu, Yuxing, Wu, Nan, Liu, Wenwen, Wang, Xifeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8985318/
https://www.ncbi.nlm.nih.gov/pubmed/35387674
http://dx.doi.org/10.1186/s40793-022-00410-8
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author Wang, Yajiao
Liu, Yu
Wu, Yuxing
Wu, Nan
Liu, Wenwen
Wang, Xifeng
author_facet Wang, Yajiao
Liu, Yu
Wu, Yuxing
Wu, Nan
Liu, Wenwen
Wang, Xifeng
author_sort Wang, Yajiao
collection PubMed
description BACKGROUND: As genetic entities infecting and replicating only in bacteria, bacteriophages can regulate the community structure and functions of their host bacteria. The ecological roles of bacteriophages in aquatic and forest environments have been widely explored, but those in agroecosystems remains limited. Here, we used metagenomic sequencing to analyze the diversity and interactions of bacteriophages and their host bacteria in soils from three typical rice agroecosystems in China: double cropping in Guangzhou, southern China, rice–wheat rotation cropping in Nanjing, eastern China and early maturing single cropping in Jiamusi, northeastern China. Enterobacter phage-NJ was isolated and its functions on soil nitrogen cycling and effect on soil bacterial community structure were verified in pot inoculation experiments and 16S rRNA gene sequencing. RESULTS: Soil bacterial and viral diversity and predicted functions varied among the three agroecosystems. Genes detected in communities from the three agroecosystems were associated with typical functions: soil bacteria in Jiamusi were significantly enriched in genes related to carbohydrate metabolism, in Nanjing with xenobiotics biodegradation and metabolism, and in Guangzhou with virulence factors and scarce in secondary metabolite biosynthesis, which might lead to a significant occurrence of rice bacterial diseases. The virus community structure varies significantly among the three ecosystems, only 13.39% of the total viral species were shared by the three rice agroecosystems, 59.56% of the viral species were specific to one agroecosystem. Notably, over-represented auxiliary carbohydrate-active enzyme (CAZyme) genes were identified in the viruses, which might assist host bacteria in metabolizing carbon, and 67.43% of these genes were present in Jiamusi. In bacteriophage isolation and inoculation experiments, Enterobacter bacteriophage-NJ reduced the nitrogen fixation capacity of soil by lysing N-fixing host bacteria and changed the soil bacterial diversity and community structure. CONCLUSION: Our results showed that diversity and function predicted of paddy soil bacteria and viruses varied in the three agroecosystems. Soil bacteriophages can affect nutrient cycling by boosting host metabolism through the carried auxiliary metabolic genes (AMGs) and lysing the host bacteria that are involved in biogeochemical cycles. These findings form a basis for better understanding bacterial and bacteriophage diversity in different rice agroecosystems, laying a solid foundation for further studies of soil microbial communities that support ecofriendly production of healthy rice. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00410-8.
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spelling pubmed-89853182022-04-07 Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling Wang, Yajiao Liu, Yu Wu, Yuxing Wu, Nan Liu, Wenwen Wang, Xifeng Environ Microbiome Research Article BACKGROUND: As genetic entities infecting and replicating only in bacteria, bacteriophages can regulate the community structure and functions of their host bacteria. The ecological roles of bacteriophages in aquatic and forest environments have been widely explored, but those in agroecosystems remains limited. Here, we used metagenomic sequencing to analyze the diversity and interactions of bacteriophages and their host bacteria in soils from three typical rice agroecosystems in China: double cropping in Guangzhou, southern China, rice–wheat rotation cropping in Nanjing, eastern China and early maturing single cropping in Jiamusi, northeastern China. Enterobacter phage-NJ was isolated and its functions on soil nitrogen cycling and effect on soil bacterial community structure were verified in pot inoculation experiments and 16S rRNA gene sequencing. RESULTS: Soil bacterial and viral diversity and predicted functions varied among the three agroecosystems. Genes detected in communities from the three agroecosystems were associated with typical functions: soil bacteria in Jiamusi were significantly enriched in genes related to carbohydrate metabolism, in Nanjing with xenobiotics biodegradation and metabolism, and in Guangzhou with virulence factors and scarce in secondary metabolite biosynthesis, which might lead to a significant occurrence of rice bacterial diseases. The virus community structure varies significantly among the three ecosystems, only 13.39% of the total viral species were shared by the three rice agroecosystems, 59.56% of the viral species were specific to one agroecosystem. Notably, over-represented auxiliary carbohydrate-active enzyme (CAZyme) genes were identified in the viruses, which might assist host bacteria in metabolizing carbon, and 67.43% of these genes were present in Jiamusi. In bacteriophage isolation and inoculation experiments, Enterobacter bacteriophage-NJ reduced the nitrogen fixation capacity of soil by lysing N-fixing host bacteria and changed the soil bacterial diversity and community structure. CONCLUSION: Our results showed that diversity and function predicted of paddy soil bacteria and viruses varied in the three agroecosystems. Soil bacteriophages can affect nutrient cycling by boosting host metabolism through the carried auxiliary metabolic genes (AMGs) and lysing the host bacteria that are involved in biogeochemical cycles. These findings form a basis for better understanding bacterial and bacteriophage diversity in different rice agroecosystems, laying a solid foundation for further studies of soil microbial communities that support ecofriendly production of healthy rice. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00410-8. BioMed Central 2022-04-06 /pmc/articles/PMC8985318/ /pubmed/35387674 http://dx.doi.org/10.1186/s40793-022-00410-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wang, Yajiao
Liu, Yu
Wu, Yuxing
Wu, Nan
Liu, Wenwen
Wang, Xifeng
Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title_full Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title_fullStr Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title_full_unstemmed Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title_short Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
title_sort heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8985318/
https://www.ncbi.nlm.nih.gov/pubmed/35387674
http://dx.doi.org/10.1186/s40793-022-00410-8
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