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Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean

Despite being the world’s third largest ocean, the Indian Ocean is one of the least studied and understood with respect to microbial diversity as well as biogeochemical and ecological functions. In this study, we investigated the microbial community and its metabolic potential for nitrogen (N) acqui...

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Autores principales: Wang, Yayu, Liao, Shuilin, Gai, Yingbao, Liu, Guilin, Jin, Tao, Liu, Huan, Gram, Lone, Strube, Mikael Lenz, Fan, Guangyi, Sahu, Sunil Kumar, Liu, Shanshan, Gan, Shuheng, Xie, Zhangxian, Kong, Lingfen, Zhang, Pengfan, Liu, Xin, Wang, Da-Zhi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7935530/
https://www.ncbi.nlm.nih.gov/pubmed/33679623
http://dx.doi.org/10.3389/fmicb.2021.518865
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author Wang, Yayu
Liao, Shuilin
Gai, Yingbao
Liu, Guilin
Jin, Tao
Liu, Huan
Gram, Lone
Strube, Mikael Lenz
Fan, Guangyi
Sahu, Sunil Kumar
Liu, Shanshan
Gan, Shuheng
Xie, Zhangxian
Kong, Lingfen
Zhang, Pengfan
Liu, Xin
Wang, Da-Zhi
author_facet Wang, Yayu
Liao, Shuilin
Gai, Yingbao
Liu, Guilin
Jin, Tao
Liu, Huan
Gram, Lone
Strube, Mikael Lenz
Fan, Guangyi
Sahu, Sunil Kumar
Liu, Shanshan
Gan, Shuheng
Xie, Zhangxian
Kong, Lingfen
Zhang, Pengfan
Liu, Xin
Wang, Da-Zhi
author_sort Wang, Yayu
collection PubMed
description Despite being the world’s third largest ocean, the Indian Ocean is one of the least studied and understood with respect to microbial diversity as well as biogeochemical and ecological functions. In this study, we investigated the microbial community and its metabolic potential for nitrogen (N) acquisition in the oligotrophic surface waters of the Indian Ocean using a metagenomic approach. Proteobacteria and Cyanobacteria dominated the microbial community with an average 37.85 and 23.56% of relative abundance, respectively, followed by Bacteroidetes (3.73%), Actinobacteria (1.69%), Firmicutes (0.76%), Verrucomicrobia (0.36%), and Planctomycetes (0.31%). Overall, only 24.3% of functional genes were common among all sampling stations indicating a high level of gene diversity. However, the presence of 82.6% common KEGG Orthology (KOs) in all samples showed high functional redundancy across the Indian Ocean. Temperature, phosphate, silicate and pH were important environmental factors regulating the microbial distribution in the Indian Ocean. The cyanobacterial genus Prochlorococcus was abundant with an average 17.4% of relative abundance in the surface waters, and while 54 Prochlorococcus genomes were detected, 53 were grouped mainly within HLII clade. In total, 179 of 234 Prochlorococcus sequences extracted from the global ocean dataset were clustered into HL clades and exhibited less divergence, but 55 sequences of LL clades presented more divergence exhibiting different branch length. The genes encoding enzymes related to ammonia metabolism, such as urease, glutamate dehydrogenase, ammonia transporter, and nitrilase presented higher abundances than the genes involved in inorganic N assimilation in both microbial community and metagenomic Prochlorococcus population. Furthermore, genes associated with dissimilatory nitrate reduction, denitrification, nitrogen fixation, nitrification and anammox were absent in metagenome Prochlorococcus population, i.e., nitrogenase and nitrate reductase. Notably, the de novo biosynthesis pathways of six different amino acids were incomplete in the metagenomic Prochlorococcus population and Prochlorococcus genomes, suggesting compensatory uptake of these amino acids from the environment. These results reveal the features of the taxonomic and functional structure of the Indian Ocean microbiome and their adaptive strategies to ambient N deficiency in the oligotrophic ocean.
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spelling pubmed-79355302021-03-06 Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean Wang, Yayu Liao, Shuilin Gai, Yingbao Liu, Guilin Jin, Tao Liu, Huan Gram, Lone Strube, Mikael Lenz Fan, Guangyi Sahu, Sunil Kumar Liu, Shanshan Gan, Shuheng Xie, Zhangxian Kong, Lingfen Zhang, Pengfan Liu, Xin Wang, Da-Zhi Front Microbiol Microbiology Despite being the world’s third largest ocean, the Indian Ocean is one of the least studied and understood with respect to microbial diversity as well as biogeochemical and ecological functions. In this study, we investigated the microbial community and its metabolic potential for nitrogen (N) acquisition in the oligotrophic surface waters of the Indian Ocean using a metagenomic approach. Proteobacteria and Cyanobacteria dominated the microbial community with an average 37.85 and 23.56% of relative abundance, respectively, followed by Bacteroidetes (3.73%), Actinobacteria (1.69%), Firmicutes (0.76%), Verrucomicrobia (0.36%), and Planctomycetes (0.31%). Overall, only 24.3% of functional genes were common among all sampling stations indicating a high level of gene diversity. However, the presence of 82.6% common KEGG Orthology (KOs) in all samples showed high functional redundancy across the Indian Ocean. Temperature, phosphate, silicate and pH were important environmental factors regulating the microbial distribution in the Indian Ocean. The cyanobacterial genus Prochlorococcus was abundant with an average 17.4% of relative abundance in the surface waters, and while 54 Prochlorococcus genomes were detected, 53 were grouped mainly within HLII clade. In total, 179 of 234 Prochlorococcus sequences extracted from the global ocean dataset were clustered into HL clades and exhibited less divergence, but 55 sequences of LL clades presented more divergence exhibiting different branch length. The genes encoding enzymes related to ammonia metabolism, such as urease, glutamate dehydrogenase, ammonia transporter, and nitrilase presented higher abundances than the genes involved in inorganic N assimilation in both microbial community and metagenomic Prochlorococcus population. Furthermore, genes associated with dissimilatory nitrate reduction, denitrification, nitrogen fixation, nitrification and anammox were absent in metagenome Prochlorococcus population, i.e., nitrogenase and nitrate reductase. Notably, the de novo biosynthesis pathways of six different amino acids were incomplete in the metagenomic Prochlorococcus population and Prochlorococcus genomes, suggesting compensatory uptake of these amino acids from the environment. These results reveal the features of the taxonomic and functional structure of the Indian Ocean microbiome and their adaptive strategies to ambient N deficiency in the oligotrophic ocean. Frontiers Media S.A. 2021-02-18 /pmc/articles/PMC7935530/ /pubmed/33679623 http://dx.doi.org/10.3389/fmicb.2021.518865 Text en Copyright © 2021 Wang, Liao, Gai, Liu, Jin, Liu, Gram, Strube, Fan, Sahu, Liu, Gan, Xie, Kong, Zhang, Liu and Wang. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wang, Yayu
Liao, Shuilin
Gai, Yingbao
Liu, Guilin
Jin, Tao
Liu, Huan
Gram, Lone
Strube, Mikael Lenz
Fan, Guangyi
Sahu, Sunil Kumar
Liu, Shanshan
Gan, Shuheng
Xie, Zhangxian
Kong, Lingfen
Zhang, Pengfan
Liu, Xin
Wang, Da-Zhi
Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title_full Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title_fullStr Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title_full_unstemmed Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title_short Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean
title_sort metagenomic analysis reveals microbial community structure and metabolic potential for nitrogen acquisition in the oligotrophic surface water of the indian ocean
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7935530/
https://www.ncbi.nlm.nih.gov/pubmed/33679623
http://dx.doi.org/10.3389/fmicb.2021.518865
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