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Distinctive microbial community and genome structure in coastal seawater from a human-made port and nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean

Pollution in human-made fishing ports caused by petroleum from boats, dead fish, toxic chemicals, and effluent poses a challenge to the organisms in seawater. To decipher the impact of pollution on the microbiome, we collected surface water from a fishing port and a nearby offshore island in norther...

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Published in:PloS one 2023-06, Vol.18 (6), p.e0284022-e0284022
Main Authors: Shih, Chi-Yu, Chen, Shiow-Yi, Hsu, Chun-Ru, Chin, Ching-Hsiang, Chiu, Wei-Chih, Chang, Mei-Hung, Kang, Lee-Kuo, Yang, Cing-Han, Pai, Tun-Wen, Hu, Chin-Hwa, Hsu, Pang-Hung, Tzou, Wen-Shyong
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container_title PloS one
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creator Shih, Chi-Yu
Chen, Shiow-Yi
Hsu, Chun-Ru
Chin, Ching-Hsiang
Chiu, Wei-Chih
Chang, Mei-Hung
Kang, Lee-Kuo
Yang, Cing-Han
Pai, Tun-Wen
Hu, Chin-Hwa
Hsu, Pang-Hung
Tzou, Wen-Shyong
description Pollution in human-made fishing ports caused by petroleum from boats, dead fish, toxic chemicals, and effluent poses a challenge to the organisms in seawater. To decipher the impact of pollution on the microbiome, we collected surface water from a fishing port and a nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean. By employing 16S rRNA gene amplicon sequencing and whole-genome shotgun sequencing, we discovered that Rhodobacteraceae, Vibrionaceae, and Oceanospirillaceae emerged as the dominant species in the fishing port, where we found many genes harboring the functions of antibiotic resistance (ansamycin, nitroimidazole, and aminocoumarin), metal tolerance (copper, chromium, iron and multimetal), virulence factors (chemotaxis, flagella, T3SS1), carbohydrate metabolism (biofilm formation and remodeling of bacterial cell walls), nitrogen metabolism (denitrification, N2 fixation, and ammonium assimilation), and ABC transporters (phosphate, lipopolysaccharide, and branched-chain amino acids). The dominant bacteria at the nearby offshore island (Alteromonadaceae, Cryomorphaceae, Flavobacteriaceae, Litoricolaceae, and Rhodobacteraceae) were partly similar to those in the South China Sea and the East China Sea. Furthermore, we inferred that the microbial community network of the cooccurrence of dominant bacteria on the offshore island was connected to dominant bacteria in the fishing port by mutual exclusion. By examining the assembled microbial genomes collected from the coastal seawater of the fishing port, we revealed four genomic islands containing large gene-containing sequences, including phage integrase, DNA invertase, restriction enzyme, DNA gyrase inhibitor, and antitoxin HigA-1. In this study, we provided clues for the possibility of genomic islands as the units of horizontal transfer and as the tools of microbes for facilitating adaptation in a human-made port environment.
doi_str_mv 10.1371/journal.pone.0284022
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To decipher the impact of pollution on the microbiome, we collected surface water from a fishing port and a nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean. By employing 16S rRNA gene amplicon sequencing and whole-genome shotgun sequencing, we discovered that Rhodobacteraceae, Vibrionaceae, and Oceanospirillaceae emerged as the dominant species in the fishing port, where we found many genes harboring the functions of antibiotic resistance (ansamycin, nitroimidazole, and aminocoumarin), metal tolerance (copper, chromium, iron and multimetal), virulence factors (chemotaxis, flagella, T3SS1), carbohydrate metabolism (biofilm formation and remodeling of bacterial cell walls), nitrogen metabolism (denitrification, N2 fixation, and ammonium assimilation), and ABC transporters (phosphate, lipopolysaccharide, and branched-chain amino acids). The dominant bacteria at the nearby offshore island (Alteromonadaceae, Cryomorphaceae, Flavobacteriaceae, Litoricolaceae, and Rhodobacteraceae) were partly similar to those in the South China Sea and the East China Sea. Furthermore, we inferred that the microbial community network of the cooccurrence of dominant bacteria on the offshore island was connected to dominant bacteria in the fishing port by mutual exclusion. By examining the assembled microbial genomes collected from the coastal seawater of the fishing port, we revealed four genomic islands containing large gene-containing sequences, including phage integrase, DNA invertase, restriction enzyme, DNA gyrase inhibitor, and antitoxin HigA-1. In this study, we provided clues for the possibility of genomic islands as the units of horizontal transfer and as the tools of microbes for facilitating adaptation in a human-made port environment.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0284022</identifier><identifier>PMID: 37294811</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acids ; Ammonium ; Analysis ; Annotations ; Antibiotic resistance ; Antibiotics ; Antitoxins ; Bacteria ; Biofilms ; Biological products ; Biology and Life Sciences ; Boats ; Branched chain amino acids ; Carbohydrate metabolism ; Carbohydrates ; Cell walls ; Chain branching ; Chemotaxis ; Chromium ; Coastal structures ; Composition ; Contamination ; Denitrification ; Deoxyribonucleic acid ; DNA ; DNA topoisomerase ; Dominant species ; Drug resistance ; Drug resistance in microorganisms ; Earth Sciences ; Ecology and Environmental Sciences ; Environmental impact ; Fishing ; Flagella ; Gene sequencing ; Genes ; Genomes ; Genomic islands ; Genomic structural variations ; Genomics ; Health aspects ; Horizontal transfer ; Integrase ; Invertase ; Islands ; Lipopolysaccharides ; Marine pollution ; Medicine and Health Sciences ; Metabolism ; Methods ; Microbiomes ; Microbiota ; Microorganisms ; Nitrogen fixation ; Nitrogen metabolism ; Nitrogenation ; Nitroimidazole ; Nucleotide sequence ; Oceans ; Pathogens ; Pollution ; Ports ; Prevention ; Research and analysis methods ; Rhodobacteraceae ; RNA ; rRNA 16S ; Sea-water ; Seawater ; Surface water ; Taxonomy ; Virulence factors</subject><ispartof>PloS one, 2023-06, Vol.18 (6), p.e0284022-e0284022</ispartof><rights>Copyright: © 2023 Shih et al. 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Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shih, Chi-Yu</au><au>Chen, Shiow-Yi</au><au>Hsu, Chun-Ru</au><au>Chin, Ching-Hsiang</au><au>Chiu, Wei-Chih</au><au>Chang, Mei-Hung</au><au>Kang, Lee-Kuo</au><au>Yang, Cing-Han</au><au>Pai, Tun-Wen</au><au>Hu, Chin-Hwa</au><au>Hsu, Pang-Hung</au><au>Tzou, Wen-Shyong</au><au>Yu, Eizadora Torres</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Distinctive microbial community and genome structure in coastal seawater from a human-made port and nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-06-09</date><risdate>2023</risdate><volume>18</volume><issue>6</issue><spage>e0284022</spage><epage>e0284022</epage><pages>e0284022-e0284022</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Pollution in human-made fishing ports caused by petroleum from boats, dead fish, toxic chemicals, and effluent poses a challenge to the organisms in seawater. To decipher the impact of pollution on the microbiome, we collected surface water from a fishing port and a nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean. By employing 16S rRNA gene amplicon sequencing and whole-genome shotgun sequencing, we discovered that Rhodobacteraceae, Vibrionaceae, and Oceanospirillaceae emerged as the dominant species in the fishing port, where we found many genes harboring the functions of antibiotic resistance (ansamycin, nitroimidazole, and aminocoumarin), metal tolerance (copper, chromium, iron and multimetal), virulence factors (chemotaxis, flagella, T3SS1), carbohydrate metabolism (biofilm formation and remodeling of bacterial cell walls), nitrogen metabolism (denitrification, N2 fixation, and ammonium assimilation), and ABC transporters (phosphate, lipopolysaccharide, and branched-chain amino acids). The dominant bacteria at the nearby offshore island (Alteromonadaceae, Cryomorphaceae, Flavobacteriaceae, Litoricolaceae, and Rhodobacteraceae) were partly similar to those in the South China Sea and the East China Sea. Furthermore, we inferred that the microbial community network of the cooccurrence of dominant bacteria on the offshore island was connected to dominant bacteria in the fishing port by mutual exclusion. By examining the assembled microbial genomes collected from the coastal seawater of the fishing port, we revealed four genomic islands containing large gene-containing sequences, including phage integrase, DNA invertase, restriction enzyme, DNA gyrase inhibitor, and antitoxin HigA-1. In this study, we provided clues for the possibility of genomic islands as the units of horizontal transfer and as the tools of microbes for facilitating adaptation in a human-made port environment.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37294811</pmid><doi>10.1371/journal.pone.0284022</doi><tpages>e0284022</tpages><orcidid>https://orcid.org/0000-0001-6873-6434</orcidid><orcidid>https://orcid.org/0000-0002-6726-1390</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2023-06, Vol.18 (6), p.e0284022-e0284022
issn 1932-6203
1932-6203
language eng
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source Access via ProQuest (Open Access); PubMed Central
subjects Amino acids
Ammonium
Analysis
Annotations
Antibiotic resistance
Antibiotics
Antitoxins
Bacteria
Biofilms
Biological products
Biology and Life Sciences
Boats
Branched chain amino acids
Carbohydrate metabolism
Carbohydrates
Cell walls
Chain branching
Chemotaxis
Chromium
Coastal structures
Composition
Contamination
Denitrification
Deoxyribonucleic acid
DNA
DNA topoisomerase
Dominant species
Drug resistance
Drug resistance in microorganisms
Earth Sciences
Ecology and Environmental Sciences
Environmental impact
Fishing
Flagella
Gene sequencing
Genes
Genomes
Genomic islands
Genomic structural variations
Genomics
Health aspects
Horizontal transfer
Integrase
Invertase
Islands
Lipopolysaccharides
Marine pollution
Medicine and Health Sciences
Metabolism
Methods
Microbiomes
Microbiota
Microorganisms
Nitrogen fixation
Nitrogen metabolism
Nitrogenation
Nitroimidazole
Nucleotide sequence
Oceans
Pathogens
Pollution
Ports
Prevention
Research and analysis methods
Rhodobacteraceae
RNA
rRNA 16S
Sea-water
Seawater
Surface water
Taxonomy
Virulence factors
title Distinctive microbial community and genome structure in coastal seawater from a human-made port and nearby offshore island in northern Taiwan facing the Northwestern Pacific Ocean
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