Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents

ABSTRACT Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial popu...

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Autores principales:	Alief Moulana, Rika E. Anderson, Caroline S. Fortunato, Julie A. Huber
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	hydrothermal vents metagenomics pangenome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/eed46d4d19364354b59c85f3384874ba
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spelling	oai:doaj.org-article:eed46d4d19364354b59c85f3384874ba2021-12-02T18:15:45ZSelection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents10.1128/mSystems.00673-192379-5077https://doaj.org/article/eed46d4d19364354b59c85f3384874ba2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00673-19https://doaj.org/toc/2379-5077ABSTRACT Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution. IMPORTANCE Microbes can alter their gene content through the gain and loss of genes. However, there is some debate as to whether natural selection or neutral processes play a stronger role in molding the gene content of microbial genomes. In this study, we examined variation in gene content for the Epsilonbacteraeota genus Sulfurovum from deep-sea hydrothermal vents, which are dynamic habitats known for extensive horizontal gene transfer within microbial populations. Our results show that natural selection is a strong driver of Sulfurovum gene content and that nutrient limitation in particular has shaped the Sulfurovum genome, leading to differences in gene content between ocean basins. Our results also suggest that recently acquired genes undergo stronger selection than genes that were acquired in the more distant past. Overall, our results highlight the importance of natural selection in driving the evolution of microbial populations in these dynamic habitats.Alief MoulanaRika E. AndersonCaroline S. FortunatoJulie A. HuberAmerican Society for Microbiologyarticlehydrothermal ventsmetagenomicspangenomeMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	hydrothermal vents metagenomics pangenome Microbiology QR1-502
spellingShingle	hydrothermal vents metagenomics pangenome Microbiology QR1-502 Alief Moulana Rika E. Anderson Caroline S. Fortunato Julie A. Huber Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
description	ABSTRACT Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution. IMPORTANCE Microbes can alter their gene content through the gain and loss of genes. However, there is some debate as to whether natural selection or neutral processes play a stronger role in molding the gene content of microbial genomes. In this study, we examined variation in gene content for the Epsilonbacteraeota genus Sulfurovum from deep-sea hydrothermal vents, which are dynamic habitats known for extensive horizontal gene transfer within microbial populations. Our results show that natural selection is a strong driver of Sulfurovum gene content and that nutrient limitation in particular has shaped the Sulfurovum genome, leading to differences in gene content between ocean basins. Our results also suggest that recently acquired genes undergo stronger selection than genes that were acquired in the more distant past. Overall, our results highlight the importance of natural selection in driving the evolution of microbial populations in these dynamic habitats.
format	article
author	Alief Moulana Rika E. Anderson Caroline S. Fortunato Julie A. Huber
author_facet	Alief Moulana Rika E. Anderson Caroline S. Fortunato Julie A. Huber
author_sort	Alief Moulana
title	Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
title_short	Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
title_full	Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
title_fullStr	Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
title_full_unstemmed	Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents
title_sort	selection is a significant driver of gene gain and loss in the pangenome of the bacterial genus <italic toggle="yes">sulfurovum</italic> in geographically distinct deep-sea hydrothermal vents
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/eed46d4d19364354b59c85f3384874ba
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Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus <italic toggle="yes">Sulfurovum</italic> in Geographically Distinct Deep-Sea Hydrothermal Vents

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