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Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments

BACKGROUND: Mangrove wetlands are coastal ecosystems with important ecological features and provide habitats for diverse microorganisms with key roles in nutrient and biogeochemical cycling. However, the overall metabolic potentials and ecological roles of microbial community in mangrove sediment ar...

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Autores principales: Zhang, Zhi-Feng, Liu, Li-Rui, Pan, Yue-Ping, Pan, Jie, Li, Meng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10464287/
https://www.ncbi.nlm.nih.gov/pubmed/37612768
http://dx.doi.org/10.1186/s40168-023-01630-x
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author Zhang, Zhi-Feng
Liu, Li-Rui
Pan, Yue-Ping
Pan, Jie
Li, Meng
author_facet Zhang, Zhi-Feng
Liu, Li-Rui
Pan, Yue-Ping
Pan, Jie
Li, Meng
author_sort Zhang, Zhi-Feng
collection PubMed
description BACKGROUND: Mangrove wetlands are coastal ecosystems with important ecological features and provide habitats for diverse microorganisms with key roles in nutrient and biogeochemical cycling. However, the overall metabolic potentials and ecological roles of microbial community in mangrove sediment are remained unanswered. In current study, the microbial and metabolic profiles of prokaryotic and fungal communities in mangrove sediments were investigated using metagenomic analysis based on PacBio single-molecule real time (SMRT) and Illumina sequencing techniques. RESULTS: Comparing to Illumina short reads, the incorporation of PacBio long reads significantly contributed to more contiguous assemblies, yielded more than doubled high-quality metagenome-assembled genomes (MAGs), and improved the novelty of the MAGs. Further metabolic reconstruction for recovered MAGs showed that prokaryotes potentially played an essential role in carbon cycling in mangrove sediment, displaying versatile metabolic potential for degrading organic carbons, fermentation, autotrophy, and carbon fixation. Mangrove fungi also functioned as a player in carbon cycling, potentially involved in the degradation of various carbohydrate and peptide substrates. Notably, a new candidate bacterial phylum named as Candidatus Cosmopoliota with a ubiquitous distribution is proposed. Genomic analysis revealed that this new phylum is capable of utilizing various types of organic substrates, anaerobic fermentation, and carbon fixation with the Wood-Ljungdahl (WL) pathway and the reverse tricarboxylic acid (rTCA) cycle. CONCLUSIONS: The study not only highlights the advantages of HiSeq-PacBio Hybrid assembly for a more complete profiling of environmental microbiomes but also expands our understanding of the microbial diversity and potential roles of distinct microbial groups in biogeochemical cycling in mangrove sediment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01630-x.
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spelling pubmed-104642872023-08-30 Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments Zhang, Zhi-Feng Liu, Li-Rui Pan, Yue-Ping Pan, Jie Li, Meng Microbiome Research BACKGROUND: Mangrove wetlands are coastal ecosystems with important ecological features and provide habitats for diverse microorganisms with key roles in nutrient and biogeochemical cycling. However, the overall metabolic potentials and ecological roles of microbial community in mangrove sediment are remained unanswered. In current study, the microbial and metabolic profiles of prokaryotic and fungal communities in mangrove sediments were investigated using metagenomic analysis based on PacBio single-molecule real time (SMRT) and Illumina sequencing techniques. RESULTS: Comparing to Illumina short reads, the incorporation of PacBio long reads significantly contributed to more contiguous assemblies, yielded more than doubled high-quality metagenome-assembled genomes (MAGs), and improved the novelty of the MAGs. Further metabolic reconstruction for recovered MAGs showed that prokaryotes potentially played an essential role in carbon cycling in mangrove sediment, displaying versatile metabolic potential for degrading organic carbons, fermentation, autotrophy, and carbon fixation. Mangrove fungi also functioned as a player in carbon cycling, potentially involved in the degradation of various carbohydrate and peptide substrates. Notably, a new candidate bacterial phylum named as Candidatus Cosmopoliota with a ubiquitous distribution is proposed. Genomic analysis revealed that this new phylum is capable of utilizing various types of organic substrates, anaerobic fermentation, and carbon fixation with the Wood-Ljungdahl (WL) pathway and the reverse tricarboxylic acid (rTCA) cycle. CONCLUSIONS: The study not only highlights the advantages of HiSeq-PacBio Hybrid assembly for a more complete profiling of environmental microbiomes but also expands our understanding of the microbial diversity and potential roles of distinct microbial groups in biogeochemical cycling in mangrove sediment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01630-x. BioMed Central 2023-08-23 /pmc/articles/PMC10464287/ /pubmed/37612768 http://dx.doi.org/10.1186/s40168-023-01630-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Zhang, Zhi-Feng
Liu, Li-Rui
Pan, Yue-Ping
Pan, Jie
Li, Meng
Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title_full Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title_fullStr Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title_full_unstemmed Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title_short Long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
title_sort long-read assembled metagenomic approaches improve our understanding on metabolic potentials of microbial community in mangrove sediments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10464287/
https://www.ncbi.nlm.nih.gov/pubmed/37612768
http://dx.doi.org/10.1186/s40168-023-01630-x
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