Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes

Culture enrichment was developed to discover the uncharted microbial species in the environmental microbiota. Yet this strategy has not been widely used to study microbes of deep-sea environments. Here, we report the cultivation and metagenomic analysis of oceanic sediment microbiota collected from...

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Autores principales: Huan Wang, Meng Wang, Shen Fan, Jie Lu, Yi Lan, Menggong Li, Jiangyan Li, Rulong Liu, Jin Sun, Jiasong Fang, Pei-Yuan Qian, Yu-Zhong Zhang, Weipeng Zhang
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:375ece2ef66a457cbfb13ec4c93956812021-11-10T05:48:55ZCulture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes2296-774510.3389/fmars.2021.754332https://doaj.org/article/375ece2ef66a457cbfb13ec4c93956812021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmars.2021.754332/fullhttps://doaj.org/toc/2296-7745Culture enrichment was developed to discover the uncharted microbial species in the environmental microbiota. Yet this strategy has not been widely used to study microbes of deep-sea environments. Here, we report the cultivation and metagenomic analysis of oceanic sediment microbiota collected from 6,477 m deep in the Mariana Trench. The sediment samples were cultured anaerobically in the laboratory for 4 months, before being subjected to full-length 16S rRNA gene sequencing using the PacBio technique and metagenome sequencing using both the Illumina and Oxford Nanopore techniques. The 16S rRNA gene analyses revealed 437 operational taxonomic units specific to the cultured microbes, despite the lower diversity of the cultured microbiota in comparison with the original. Metagenome analyses revealed the prevalence of functions related to respiration, energy production, and stress response in the cultured microbes, suggesting these functions may contribute to microbial proliferation under laboratory conditions. Binning of the assembled metagenome contigs of the cultured microbiota generated four nearly complete genomes affiliated to yet unclassified species under the genera Alcanivorax, Idiomarina, Sulfitobacter, and Erythrobacter. Excepting Alcanivorax, the other three genera were almost undetectable in the original samples and largely enriched in the cultured samples. The four genomes possessed a variety of genes for carbohydrate utilization and nitrite reduction, pointing to an ability to respire diverse carbon sources using nitrite as the final electron acceptor. Taken together, the findings suggest that a combination of culture enrichment and long-read sequencing is an ideal way to mine novel microbial species in the hadal environment, particularly species that are rare in their native environmental niches, and thus expand our understanding of the hadal microbial diversity and function.Huan WangHuan WangHuan WangMeng WangMeng WangMeng WangShen FanShen FanShen FanJie LuJie LuJie LuYi LanYi LanMenggong LiJiangyan LiRulong LiuJin SunJiasong FangPei-Yuan QianPei-Yuan QianYu-Zhong ZhangYu-Zhong ZhangYu-Zhong ZhangWeipeng ZhangWeipeng ZhangFrontiers Media S.A.articlemarine microbiotahadal sedimentculture-enriched metagenomicsOxford Nanopore sequencinggenome binningScienceQGeneral. Including nature conservation, geographical distributionQH1-199.5ENFrontiers in Marine Science, Vol 8 (2021)
institution DOAJ
collection DOAJ
language EN
topic marine microbiota
hadal sediment
culture-enriched metagenomics
Oxford Nanopore sequencing
genome binning
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
spellingShingle marine microbiota
hadal sediment
culture-enriched metagenomics
Oxford Nanopore sequencing
genome binning
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
Huan Wang
Huan Wang
Huan Wang
Meng Wang
Meng Wang
Meng Wang
Shen Fan
Shen Fan
Shen Fan
Jie Lu
Jie Lu
Jie Lu
Yi Lan
Yi Lan
Menggong Li
Jiangyan Li
Rulong Liu
Jin Sun
Jiasong Fang
Pei-Yuan Qian
Pei-Yuan Qian
Yu-Zhong Zhang
Yu-Zhong Zhang
Yu-Zhong Zhang
Weipeng Zhang
Weipeng Zhang
Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
description Culture enrichment was developed to discover the uncharted microbial species in the environmental microbiota. Yet this strategy has not been widely used to study microbes of deep-sea environments. Here, we report the cultivation and metagenomic analysis of oceanic sediment microbiota collected from 6,477 m deep in the Mariana Trench. The sediment samples were cultured anaerobically in the laboratory for 4 months, before being subjected to full-length 16S rRNA gene sequencing using the PacBio technique and metagenome sequencing using both the Illumina and Oxford Nanopore techniques. The 16S rRNA gene analyses revealed 437 operational taxonomic units specific to the cultured microbes, despite the lower diversity of the cultured microbiota in comparison with the original. Metagenome analyses revealed the prevalence of functions related to respiration, energy production, and stress response in the cultured microbes, suggesting these functions may contribute to microbial proliferation under laboratory conditions. Binning of the assembled metagenome contigs of the cultured microbiota generated four nearly complete genomes affiliated to yet unclassified species under the genera Alcanivorax, Idiomarina, Sulfitobacter, and Erythrobacter. Excepting Alcanivorax, the other three genera were almost undetectable in the original samples and largely enriched in the cultured samples. The four genomes possessed a variety of genes for carbohydrate utilization and nitrite reduction, pointing to an ability to respire diverse carbon sources using nitrite as the final electron acceptor. Taken together, the findings suggest that a combination of culture enrichment and long-read sequencing is an ideal way to mine novel microbial species in the hadal environment, particularly species that are rare in their native environmental niches, and thus expand our understanding of the hadal microbial diversity and function.
format article
author Huan Wang
Huan Wang
Huan Wang
Meng Wang
Meng Wang
Meng Wang
Shen Fan
Shen Fan
Shen Fan
Jie Lu
Jie Lu
Jie Lu
Yi Lan
Yi Lan
Menggong Li
Jiangyan Li
Rulong Liu
Jin Sun
Jiasong Fang
Pei-Yuan Qian
Pei-Yuan Qian
Yu-Zhong Zhang
Yu-Zhong Zhang
Yu-Zhong Zhang
Weipeng Zhang
Weipeng Zhang
author_facet Huan Wang
Huan Wang
Huan Wang
Meng Wang
Meng Wang
Meng Wang
Shen Fan
Shen Fan
Shen Fan
Jie Lu
Jie Lu
Jie Lu
Yi Lan
Yi Lan
Menggong Li
Jiangyan Li
Rulong Liu
Jin Sun
Jiasong Fang
Pei-Yuan Qian
Pei-Yuan Qian
Yu-Zhong Zhang
Yu-Zhong Zhang
Yu-Zhong Zhang
Weipeng Zhang
Weipeng Zhang
author_sort Huan Wang
title Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
title_short Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
title_full Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
title_fullStr Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
title_full_unstemmed Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes
title_sort culture enrichment combined with long-read sequencing facilitates genomic understanding of hadal sediment microbes
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/375ece2ef66a457cbfb13ec4c9395681
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