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Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments

BACKGROUND: Nitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Despite the well-known studies on diazotrophs in surficial sediments,...

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Autores principales: Luo, Zhiwen, Zhong, Qiuping, Han, Xingguo, Hu, Ruiwen, Liu, Xingyu, Xu, Wenjun, Wu, Yongjie, Huang, Weiming, Zhou, Zhengyuan, Zhuang, Wei, Yan, Qingyun, He, Zhili, Wang, Cheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549172/
https://www.ncbi.nlm.nih.gov/pubmed/34702367
http://dx.doi.org/10.1186/s40168-021-01164-0
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author Luo, Zhiwen
Zhong, Qiuping
Han, Xingguo
Hu, Ruiwen
Liu, Xingyu
Xu, Wenjun
Wu, Yongjie
Huang, Weiming
Zhou, Zhengyuan
Zhuang, Wei
Yan, Qingyun
He, Zhili
Wang, Cheng
author_facet Luo, Zhiwen
Zhong, Qiuping
Han, Xingguo
Hu, Ruiwen
Liu, Xingyu
Xu, Wenjun
Wu, Yongjie
Huang, Weiming
Zhou, Zhengyuan
Zhuang, Wei
Yan, Qingyun
He, Zhili
Wang, Cheng
author_sort Luo, Zhiwen
collection PubMed
description BACKGROUND: Nitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Despite the well-known studies on diazotrophs in surficial sediments, the diversity, structure, and ecological functions of diazotrophic communities along environmental gradients of mangrove sediment across different depths are largely unknown. Here, we investigated how biological nitrogen fixation varied with the depth of mangrove sediments from the perspectives of both NFR and diazotrophic communities. RESULTS: Through acetylene reduction assay, nifH gene amplicon and metagenomic sequencing, we found that the NFR increased but the diversity of diazotrophic communities decreased with the depth of mangrove sediments. The structure of diazotrophic communities at different depths was largely driven by salinity and exhibited a clear divergence at the partitioning depth of 50 cm. Among diazotrophic genera correlated with NFR, Agrobacterium and Azotobacter were specifically enriched at 50–100 cm sediments, while Anaeromyxobacter, Rubrivivax, Methylocystis, Dickeya, and Methylomonas were more abundant at 0–50 cm. Consistent with the higher NFR, metagenomic analysis demonstrated the elevated abundance of nitrogen fixation genes (nifH/D/K) in deep sediments, where nitrification genes (amoA/B/C) and denitrification genes (nirK and norB) became less abundant. Three metagenome-assembled genomes (MAGs) of diazotrophs from deep mangrove sediments indicated their facultatively anaerobic and mixotrophic lifestyles as they contained genes for low-oxygen-dependent metabolism, hydrogenotrophic respiration, carbon fixation, and pyruvate fermentation. CONCLUSIONS: This study demonstrates the depth-dependent variability of biological nitrogen fixation in terms of NFR and diazotrophic communities, which to a certain extent relieves the degree of nitrogen limitation in deep mangrove sediments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01164-0.
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spelling pubmed-85491722021-10-27 Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments Luo, Zhiwen Zhong, Qiuping Han, Xingguo Hu, Ruiwen Liu, Xingyu Xu, Wenjun Wu, Yongjie Huang, Weiming Zhou, Zhengyuan Zhuang, Wei Yan, Qingyun He, Zhili Wang, Cheng Microbiome Research BACKGROUND: Nitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Despite the well-known studies on diazotrophs in surficial sediments, the diversity, structure, and ecological functions of diazotrophic communities along environmental gradients of mangrove sediment across different depths are largely unknown. Here, we investigated how biological nitrogen fixation varied with the depth of mangrove sediments from the perspectives of both NFR and diazotrophic communities. RESULTS: Through acetylene reduction assay, nifH gene amplicon and metagenomic sequencing, we found that the NFR increased but the diversity of diazotrophic communities decreased with the depth of mangrove sediments. The structure of diazotrophic communities at different depths was largely driven by salinity and exhibited a clear divergence at the partitioning depth of 50 cm. Among diazotrophic genera correlated with NFR, Agrobacterium and Azotobacter were specifically enriched at 50–100 cm sediments, while Anaeromyxobacter, Rubrivivax, Methylocystis, Dickeya, and Methylomonas were more abundant at 0–50 cm. Consistent with the higher NFR, metagenomic analysis demonstrated the elevated abundance of nitrogen fixation genes (nifH/D/K) in deep sediments, where nitrification genes (amoA/B/C) and denitrification genes (nirK and norB) became less abundant. Three metagenome-assembled genomes (MAGs) of diazotrophs from deep mangrove sediments indicated their facultatively anaerobic and mixotrophic lifestyles as they contained genes for low-oxygen-dependent metabolism, hydrogenotrophic respiration, carbon fixation, and pyruvate fermentation. CONCLUSIONS: This study demonstrates the depth-dependent variability of biological nitrogen fixation in terms of NFR and diazotrophic communities, which to a certain extent relieves the degree of nitrogen limitation in deep mangrove sediments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01164-0. BioMed Central 2021-10-27 /pmc/articles/PMC8549172/ /pubmed/34702367 http://dx.doi.org/10.1186/s40168-021-01164-0 Text en © The Author(s) 2021 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
Luo, Zhiwen
Zhong, Qiuping
Han, Xingguo
Hu, Ruiwen
Liu, Xingyu
Xu, Wenjun
Wu, Yongjie
Huang, Weiming
Zhou, Zhengyuan
Zhuang, Wei
Yan, Qingyun
He, Zhili
Wang, Cheng
Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title_full Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title_fullStr Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title_full_unstemmed Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title_short Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
title_sort depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549172/
https://www.ncbi.nlm.nih.gov/pubmed/34702367
http://dx.doi.org/10.1186/s40168-021-01164-0
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