Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>

ABSTRACT Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. The genomic structures of 46 of these isolates were investigated through comparative geno...

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Autores principales: Jie Deng, Jennifer M. Auchtung, Konstantinos T. Konstantinidis, Ingrid Brettar, Manfred G. Höfle, James M. Tiedje
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Publicado: American Society for Microbiology 2019
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Acceso en línea:https://doaj.org/article/381f40c2320441f19f78a9056ebe2802
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spelling oai:doaj.org-article:381f40c2320441f19f78a9056ebe28022021-12-02T19:46:17ZGenomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>10.1128/mSystems.00560-192379-5077https://doaj.org/article/381f40c2320441f19f78a9056ebe28022019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00560-19https://doaj.org/toc/2379-5077ABSTRACT Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. The genomic structures of 46 of these isolates were investigated through comparative genomic hybridization (CGH), which revealed a gradient of genomic similarity, ranging from 65% to as high as 99%. The core genome of the S. baltica species was enriched in anaerobic respiration-associated genes. Auxiliary genes, most of which locate within a few genomic islands (GIs), were nonuniformly distributed among the isolates. Specifically, hypothetical and mobile genetic element (MGE)-associated genes dominated intraclade gene content differences, whereas gain/loss of functional genes drove gene content differences among less related strains. Among the major S. baltica clades, gene signatures related to specific redox-driven and spatial niches within the water column were identified. For instance, genes involved in anaerobic respiration of sulfur compounds may provide key adaptive advantages for clade A strains in anoxic waters where sulfur-containing electron acceptors are present. Genes involved in cell motility, in particular, a secondary flagellar biosynthesis system, may be associated with the free-living lifestyle by clade E strains. Collectively, this study revealed characteristics of genome variations present in the water column and active speciation of S. baltica strains, driven by niche partitioning and horizontal gene transfer (HGT). IMPORTANCE Speciation in nature is a fundamental process driving the formation of the vast microbial diversity on Earth. In the central Baltic Sea, the long-term stratification of water led to formation of a large-scale vertical redoxcline that provided a gradient of environmental niches with respect to the availability of electron acceptors and donors. The region was home to Shewanella baltica populations, which composed the dominant culturable nitrate-reducing bacteria, particularly in the oxic-anoxic transition zone. Using the collection of S. baltica isolates as a model system, genomic variations showed contrasting gene-sharing patterns within versus among S. baltica clades and revealed genomic signatures of S. baltica clades related to redox niche specialization as well as particle association. This study provides important insights into genomic mechanisms underlying bacterial speciation within this unique natural redoxcline.Jie DengJennifer M. AuchtungKonstantinos T. KonstantinidisIngrid BrettarManfred G. HöfleJames M. TiedjeAmerican Society for MicrobiologyarticleShewanella balticacomparative genomicsspeciationadaptationMicrobiologyQR1-502ENmSystems, Vol 4, Iss 5 (2019)
institution DOAJ
collection DOAJ
language EN
topic Shewanella baltica
comparative genomics
speciation
adaptation
Microbiology
QR1-502
spellingShingle Shewanella baltica
comparative genomics
speciation
adaptation
Microbiology
QR1-502
Jie Deng
Jennifer M. Auchtung
Konstantinos T. Konstantinidis
Ingrid Brettar
Manfred G. Höfle
James M. Tiedje
Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
description ABSTRACT Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. The genomic structures of 46 of these isolates were investigated through comparative genomic hybridization (CGH), which revealed a gradient of genomic similarity, ranging from 65% to as high as 99%. The core genome of the S. baltica species was enriched in anaerobic respiration-associated genes. Auxiliary genes, most of which locate within a few genomic islands (GIs), were nonuniformly distributed among the isolates. Specifically, hypothetical and mobile genetic element (MGE)-associated genes dominated intraclade gene content differences, whereas gain/loss of functional genes drove gene content differences among less related strains. Among the major S. baltica clades, gene signatures related to specific redox-driven and spatial niches within the water column were identified. For instance, genes involved in anaerobic respiration of sulfur compounds may provide key adaptive advantages for clade A strains in anoxic waters where sulfur-containing electron acceptors are present. Genes involved in cell motility, in particular, a secondary flagellar biosynthesis system, may be associated with the free-living lifestyle by clade E strains. Collectively, this study revealed characteristics of genome variations present in the water column and active speciation of S. baltica strains, driven by niche partitioning and horizontal gene transfer (HGT). IMPORTANCE Speciation in nature is a fundamental process driving the formation of the vast microbial diversity on Earth. In the central Baltic Sea, the long-term stratification of water led to formation of a large-scale vertical redoxcline that provided a gradient of environmental niches with respect to the availability of electron acceptors and donors. The region was home to Shewanella baltica populations, which composed the dominant culturable nitrate-reducing bacteria, particularly in the oxic-anoxic transition zone. Using the collection of S. baltica isolates as a model system, genomic variations showed contrasting gene-sharing patterns within versus among S. baltica clades and revealed genomic signatures of S. baltica clades related to redox niche specialization as well as particle association. This study provides important insights into genomic mechanisms underlying bacterial speciation within this unique natural redoxcline.
format article
author Jie Deng
Jennifer M. Auchtung
Konstantinos T. Konstantinidis
Ingrid Brettar
Manfred G. Höfle
James M. Tiedje
author_facet Jie Deng
Jennifer M. Auchtung
Konstantinos T. Konstantinidis
Ingrid Brettar
Manfred G. Höfle
James M. Tiedje
author_sort Jie Deng
title Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
title_short Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
title_full Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
title_fullStr Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
title_full_unstemmed Genomic Variations Underlying Speciation and Niche Specialization of <italic toggle="yes">Shewanella baltica</italic>
title_sort genomic variations underlying speciation and niche specialization of <italic toggle="yes">shewanella baltica</italic>
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/381f40c2320441f19f78a9056ebe2802
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