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Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America

As an important coastal “blue carbon sink,” mangrove ecosystems contain microbial communities with an as-yet-unknown high species diversity. Exploring the assemblage and structure of sediment microbial communities therein can aid in a better understanding of their ecosystem functioning, such as carb...

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Autores principales: Du, Huan, Pan, Jie, Zhang, Cuijing, Yang, Xilan, Wang, Cheng, Lin, Xiaolan, Li, Jinhui, Liu, Wan, Zhou, Haokui, Yu, Xiaoli, Mo, Shuming, Zhang, Guoqing, Zhao, Guoping, Qu, Wu, Jiang, Chengjian, Tian, Yun, He, Zhili, Liu, Yang, Li, Meng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580968/
https://www.ncbi.nlm.nih.gov/pubmed/37668400
http://dx.doi.org/10.1128/spectrum.01577-23
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author Du, Huan
Pan, Jie
Zhang, Cuijing
Yang, Xilan
Wang, Cheng
Lin, Xiaolan
Li, Jinhui
Liu, Wan
Zhou, Haokui
Yu, Xiaoli
Mo, Shuming
Zhang, Guoqing
Zhao, Guoping
Qu, Wu
Jiang, Chengjian
Tian, Yun
He, Zhili
Liu, Yang
Li, Meng
author_facet Du, Huan
Pan, Jie
Zhang, Cuijing
Yang, Xilan
Wang, Cheng
Lin, Xiaolan
Li, Jinhui
Liu, Wan
Zhou, Haokui
Yu, Xiaoli
Mo, Shuming
Zhang, Guoqing
Zhao, Guoping
Qu, Wu
Jiang, Chengjian
Tian, Yun
He, Zhili
Liu, Yang
Li, Meng
author_sort Du, Huan
collection PubMed
description As an important coastal “blue carbon sink,” mangrove ecosystems contain microbial communities with an as-yet-unknown high species diversity. Exploring the assemblage and structure of sediment microbial communities therein can aid in a better understanding of their ecosystem functioning, such as carbon sequestration and other biogeochemical cycles in mangrove wetlands. However, compared to other biomes, the study of mangrove sediment microbiomes is limited, especially in diverse mangrove ecosystems at a large spatial scale, which may harbor microbial communities with distinct compositions and functioning. Here, we analyzed 380 sediment samples from 13 and 8 representative mangrove ecosystems, respectively, in China and South America and compared their microbial features. Although the microbial community compositions exhibited strong distinctions, the community assemblage in the two locations followed analogous patterns: the assemblages of the entire community, abundant taxa, rare taxa, and generalists were predominantly driven by stochastic processes with significant distance-decay patterns, while the assembly of specialists was more likely related to the behaviors of other organisms in or surrounding the mangrove ecosystems. In addition, co-occurrence and topological network analysis of mangrove sediment microbiomes underlined the dominance of sulfate-reducing prokaryotes in both the regions. Moreover, we found that more than 70% of the keystone and hub taxa were sulfate-reducing prokaryotes, implying their important roles in maintaining the linkage and stability of the mangrove sediment microbial communities. This study fills a gap in the large-scale analysis of microbiome features covering distantly located and diverse mangrove ecosystems. Here, we propose a suggestion to the Mangrove Microbiome Initiative that 16S rRNA sequencing protocols should be standardized with a unified primer to facilitate the global-scale analysis of mangrove microbiomes and further comparisons with the reference data sets from other biomes. IMPORTANCE: Mangrove wetlands are important ecosystems possessing valuable ecological functions for carbon storage, species diversity maintenance, and coastline stabilization. These functions are greatly driven or supported by microorganisms that make essential contributions to biogeochemical cycles in mangrove ecosystems. The mechanisms governing the microbial community assembly, structure, and functions are vital to microbial ecology but remain unclear. Moreover, studying these mechanisms of mangrove microbiomes at a large spatial scale can provide a more comprehensive insight into their universal features and can help untangle microbial interaction patterns and microbiome functions. In this study, we compared the mangrove microbiomes in a large spatial range and found that the assembly patterns and key functional guilds of the Chinese and South American mangrove microbiomes were analogous. The entire communities exhibited significant distance-decay patterns and were strongly governed by stochastic processes, while the assemblage of specialists may be merely associated with the behaviors of the organisms in mangrove ecosystems. Furthermore, our results highlight the dominance of sulfate-reducing prokaryotes in mangrove microbiomes and their key roles in maintaining the stability of community structure and functions.
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spelling pubmed-105809682023-10-18 Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America Du, Huan Pan, Jie Zhang, Cuijing Yang, Xilan Wang, Cheng Lin, Xiaolan Li, Jinhui Liu, Wan Zhou, Haokui Yu, Xiaoli Mo, Shuming Zhang, Guoqing Zhao, Guoping Qu, Wu Jiang, Chengjian Tian, Yun He, Zhili Liu, Yang Li, Meng Microbiol Spectr Research Article As an important coastal “blue carbon sink,” mangrove ecosystems contain microbial communities with an as-yet-unknown high species diversity. Exploring the assemblage and structure of sediment microbial communities therein can aid in a better understanding of their ecosystem functioning, such as carbon sequestration and other biogeochemical cycles in mangrove wetlands. However, compared to other biomes, the study of mangrove sediment microbiomes is limited, especially in diverse mangrove ecosystems at a large spatial scale, which may harbor microbial communities with distinct compositions and functioning. Here, we analyzed 380 sediment samples from 13 and 8 representative mangrove ecosystems, respectively, in China and South America and compared their microbial features. Although the microbial community compositions exhibited strong distinctions, the community assemblage in the two locations followed analogous patterns: the assemblages of the entire community, abundant taxa, rare taxa, and generalists were predominantly driven by stochastic processes with significant distance-decay patterns, while the assembly of specialists was more likely related to the behaviors of other organisms in or surrounding the mangrove ecosystems. In addition, co-occurrence and topological network analysis of mangrove sediment microbiomes underlined the dominance of sulfate-reducing prokaryotes in both the regions. Moreover, we found that more than 70% of the keystone and hub taxa were sulfate-reducing prokaryotes, implying their important roles in maintaining the linkage and stability of the mangrove sediment microbial communities. This study fills a gap in the large-scale analysis of microbiome features covering distantly located and diverse mangrove ecosystems. Here, we propose a suggestion to the Mangrove Microbiome Initiative that 16S rRNA sequencing protocols should be standardized with a unified primer to facilitate the global-scale analysis of mangrove microbiomes and further comparisons with the reference data sets from other biomes. IMPORTANCE: Mangrove wetlands are important ecosystems possessing valuable ecological functions for carbon storage, species diversity maintenance, and coastline stabilization. These functions are greatly driven or supported by microorganisms that make essential contributions to biogeochemical cycles in mangrove ecosystems. The mechanisms governing the microbial community assembly, structure, and functions are vital to microbial ecology but remain unclear. Moreover, studying these mechanisms of mangrove microbiomes at a large spatial scale can provide a more comprehensive insight into their universal features and can help untangle microbial interaction patterns and microbiome functions. In this study, we compared the mangrove microbiomes in a large spatial range and found that the assembly patterns and key functional guilds of the Chinese and South American mangrove microbiomes were analogous. The entire communities exhibited significant distance-decay patterns and were strongly governed by stochastic processes, while the assemblage of specialists may be merely associated with the behaviors of the organisms in mangrove ecosystems. Furthermore, our results highlight the dominance of sulfate-reducing prokaryotes in mangrove microbiomes and their key roles in maintaining the stability of community structure and functions. American Society for Microbiology 2023-09-05 /pmc/articles/PMC10580968/ /pubmed/37668400 http://dx.doi.org/10.1128/spectrum.01577-23 Text en Copyright © 2023 Du 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
Du, Huan
Pan, Jie
Zhang, Cuijing
Yang, Xilan
Wang, Cheng
Lin, Xiaolan
Li, Jinhui
Liu, Wan
Zhou, Haokui
Yu, Xiaoli
Mo, Shuming
Zhang, Guoqing
Zhao, Guoping
Qu, Wu
Jiang, Chengjian
Tian, Yun
He, Zhili
Liu, Yang
Li, Meng
Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title_full Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title_fullStr Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title_full_unstemmed Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title_short Analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of China and South America
title_sort analogous assembly mechanisms and functional guilds govern prokaryotic communities in mangrove ecosystems of china and south america
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580968/
https://www.ncbi.nlm.nih.gov/pubmed/37668400
http://dx.doi.org/10.1128/spectrum.01577-23
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