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Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle

BACKGROUND: Microbiome assembly in early life may have a long-term impact on host health. Larval nursery is a crucial period that determines the success in culture of Litopenaeus vannamei, the most productive shrimp species in world aquaculture industry. However, the succession patterns and assembly...

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Autores principales: Wang, Yanting, Wang, Kai, Huang, Lei, Dong, Pengsheng, Wang, Sipeng, Chen, Heping, Lu, Zheng, Hou, Dandi, Zhang, Demin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7334860/
https://www.ncbi.nlm.nih.gov/pubmed/32620132
http://dx.doi.org/10.1186/s40168-020-00879-w
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author Wang, Yanting
Wang, Kai
Huang, Lei
Dong, Pengsheng
Wang, Sipeng
Chen, Heping
Lu, Zheng
Hou, Dandi
Zhang, Demin
author_facet Wang, Yanting
Wang, Kai
Huang, Lei
Dong, Pengsheng
Wang, Sipeng
Chen, Heping
Lu, Zheng
Hou, Dandi
Zhang, Demin
author_sort Wang, Yanting
collection PubMed
description BACKGROUND: Microbiome assembly in early life may have a long-term impact on host health. Larval nursery is a crucial period that determines the success in culture of Litopenaeus vannamei, the most productive shrimp species in world aquaculture industry. However, the succession patterns and assembly mechanisms of larval shrimp bacterial community still lack characterization at a fine temporal scale. Here, using a high-frequency sampling strategy and 16S rRNA gene amplicon sequencing, we investigated dynamics of larval shrimp bacterial community and its relationship with bacterioplankton in the rearing water across the whole developmental cycle in a realistic aquaculture practice. RESULTS: Alpha-diversity of larval shrimp bacteria showed a U-shaped pattern across the developmental cycle with the stages zoea and mysis as the valley. Correspondingly, the compositions of dominant bacterial taxa at the stages nauplius and early postlarvae were more complex than other stages. Remarkably, Rhodobacteraceae maintained the overwhelming dominance after the mouth opening of larvae (zoea I~early postlarvae). The taxonomic and phylogenetic compositions of larval bacterial community both showed stage-dependent patterns with higher rate of taxonomic turnover, suggesting that taxonomic turnover was mainly driven by temporal switching among closely related taxa (such as Rhodobacteraceae taxa). The assembly of larval bacteria was overall governed by neutral processes (dispersal among individuals and ecological drift) at all the stages, but bacterioplankton also had certain contribution during three sub-stages of zoea, when larval and water bacterial communities were most associated. Furthermore, the positive host selection for Rhodobacteraceae taxa from the rearing water during the zoea stage and its persistent dominance and large predicted contribution to metabolic potentials of organic matters at post-mouth opening stages suggest a crucial role of this family in larval microbiome and thus a potential source of probiotic candidates for shrimp larval nursery. CONCLUSIONS: Our results reveal pronounced succession patterns and dynamic assembly processes of larval shrimp bacterial communities during the developmental cycle, highlighting the importance of the mouth opening stage from the perspective of microbial ecology. We also suggest the possibility and potential timing in microbial management of the rearing water for achieving the beneficial larval microbiota in the nursery practice.
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spelling pubmed-73348602020-07-06 Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle Wang, Yanting Wang, Kai Huang, Lei Dong, Pengsheng Wang, Sipeng Chen, Heping Lu, Zheng Hou, Dandi Zhang, Demin Microbiome Research BACKGROUND: Microbiome assembly in early life may have a long-term impact on host health. Larval nursery is a crucial period that determines the success in culture of Litopenaeus vannamei, the most productive shrimp species in world aquaculture industry. However, the succession patterns and assembly mechanisms of larval shrimp bacterial community still lack characterization at a fine temporal scale. Here, using a high-frequency sampling strategy and 16S rRNA gene amplicon sequencing, we investigated dynamics of larval shrimp bacterial community and its relationship with bacterioplankton in the rearing water across the whole developmental cycle in a realistic aquaculture practice. RESULTS: Alpha-diversity of larval shrimp bacteria showed a U-shaped pattern across the developmental cycle with the stages zoea and mysis as the valley. Correspondingly, the compositions of dominant bacterial taxa at the stages nauplius and early postlarvae were more complex than other stages. Remarkably, Rhodobacteraceae maintained the overwhelming dominance after the mouth opening of larvae (zoea I~early postlarvae). The taxonomic and phylogenetic compositions of larval bacterial community both showed stage-dependent patterns with higher rate of taxonomic turnover, suggesting that taxonomic turnover was mainly driven by temporal switching among closely related taxa (such as Rhodobacteraceae taxa). The assembly of larval bacteria was overall governed by neutral processes (dispersal among individuals and ecological drift) at all the stages, but bacterioplankton also had certain contribution during three sub-stages of zoea, when larval and water bacterial communities were most associated. Furthermore, the positive host selection for Rhodobacteraceae taxa from the rearing water during the zoea stage and its persistent dominance and large predicted contribution to metabolic potentials of organic matters at post-mouth opening stages suggest a crucial role of this family in larval microbiome and thus a potential source of probiotic candidates for shrimp larval nursery. CONCLUSIONS: Our results reveal pronounced succession patterns and dynamic assembly processes of larval shrimp bacterial communities during the developmental cycle, highlighting the importance of the mouth opening stage from the perspective of microbial ecology. We also suggest the possibility and potential timing in microbial management of the rearing water for achieving the beneficial larval microbiota in the nursery practice. BioMed Central 2020-07-03 /pmc/articles/PMC7334860/ /pubmed/32620132 http://dx.doi.org/10.1186/s40168-020-00879-w Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Wang, Yanting
Wang, Kai
Huang, Lei
Dong, Pengsheng
Wang, Sipeng
Chen, Heping
Lu, Zheng
Hou, Dandi
Zhang, Demin
Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title_full Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title_fullStr Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title_full_unstemmed Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title_short Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle
title_sort fine-scale succession patterns and assembly mechanisms of bacterial community of litopenaeus vannamei larvae across the developmental cycle
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7334860/
https://www.ncbi.nlm.nih.gov/pubmed/32620132
http://dx.doi.org/10.1186/s40168-020-00879-w
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