The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective

ABSTRACT The SAR11 clade of Alphaproteobacteria is the most abundant group of planktonic cells in the near-surface epipelagic waters of the ocean, but the mechanisms underlying its exceptional success have not been fully elucidated. Here, we applied a metagenomic approach to explore microdiversity p...

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Autores principales:	Mario López-Pérez, Jose M. Haro-Moreno, Felipe Hernandes Coutinho, Manuel Martinez-Garcia, Francisco Rodriguez-Valera
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	SAR11 microdiversity evolution metagenomics homologous recombination intrapopulation diversity Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6dbcbc8c7e0a466cb68ace65bc129787
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spelling	oai:doaj.org-article:6dbcbc8c7e0a466cb68ace65bc1297872021-12-02T19:47:33ZThe Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective10.1128/mSystems.00605-202379-5077https://doaj.org/article/6dbcbc8c7e0a466cb68ace65bc1297872020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00605-20https://doaj.org/toc/2379-5077ABSTRACT The SAR11 clade of Alphaproteobacteria is the most abundant group of planktonic cells in the near-surface epipelagic waters of the ocean, but the mechanisms underlying its exceptional success have not been fully elucidated. Here, we applied a metagenomic approach to explore microdiversity patterns by measuring the accumulation of synonymous and nonsynonymous mutations as well as homologous recombination in populations of SAR11 from different aquatic habitats (marine epipelagic, bathypelagic, and surface freshwater). The patterns of mutation accumulation and recombination were compared to those of other groups of representative marine microbes with multiple ecological strategies that share the same marine habitat, namely, Cyanobacteria (Prochlorococcus and Synechococcus), Archaea (“Candidatus Nitrosopelagicus” and Marine Group II Thalassoarchaea), and some heterotrophic marine bacteria (Alteromonas and Erythrobacter). SAR11 populations showed widespread recombination among distantly related members, preventing divergence leading to a genetically stable population. Moreover, their high intrapopulation sequence diversity with an enrichment in synonymous replacements supports the idea of a very ancient divergence and the coexistence of multiple different clones. However, other microbes analyzed seem to follow different evolutionary dynamics where processes of diversification driven by geographic and ecological instability produce a higher number of nonsynonymous replacements and lower intrapopulation sequence diversity. Together, these data shed light on some of the evolutionary and ecological processes that lead to the large genomic diversity in SAR11. Furthermore, this approach can be applied to other similar microbes that are difficult to culture in the laboratory, but abundant in nature, to investigate the underlying dynamics of their genomic evolution. IMPORTANCE As the most abundant bacteria in oceans, the Pelagibacterales order (here SAR11) plays an important role in the global carbon cycle, but the study of the evolutionary forces driving its evolution has lagged considerably due to the inherent difficulty of obtaining pure cultures. Multiple evolutionary models have been proposed to explain the diversification of distinct lineages within a population; however, the identification of many of these patterns in natural populations remains mostly enigmatic. We have used a metagenomic approach to explore microdiversity patterns in their natural habitats. Comparison with a collection of bacterial and archaeal groups from the same environments shows that SAR11 populations have a different evolutionary regime, where multiple genotypes coexist within the same population and remain stable over time. Widespread homologous recombination could be one of the main driving factors of this homogenization.Mario López-PérezJose M. Haro-MorenoFelipe Hernandes CoutinhoManuel Martinez-GarciaFrancisco Rodriguez-ValeraAmerican Society for MicrobiologyarticleSAR11microdiversityevolutionmetagenomicshomologous recombinationintrapopulation diversityMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	SAR11 microdiversity evolution metagenomics homologous recombination intrapopulation diversity Microbiology QR1-502
spellingShingle	SAR11 microdiversity evolution metagenomics homologous recombination intrapopulation diversity Microbiology QR1-502 Mario López-Pérez Jose M. Haro-Moreno Felipe Hernandes Coutinho Manuel Martinez-Garcia Francisco Rodriguez-Valera The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
description	ABSTRACT The SAR11 clade of Alphaproteobacteria is the most abundant group of planktonic cells in the near-surface epipelagic waters of the ocean, but the mechanisms underlying its exceptional success have not been fully elucidated. Here, we applied a metagenomic approach to explore microdiversity patterns by measuring the accumulation of synonymous and nonsynonymous mutations as well as homologous recombination in populations of SAR11 from different aquatic habitats (marine epipelagic, bathypelagic, and surface freshwater). The patterns of mutation accumulation and recombination were compared to those of other groups of representative marine microbes with multiple ecological strategies that share the same marine habitat, namely, Cyanobacteria (Prochlorococcus and Synechococcus), Archaea (“Candidatus Nitrosopelagicus” and Marine Group II Thalassoarchaea), and some heterotrophic marine bacteria (Alteromonas and Erythrobacter). SAR11 populations showed widespread recombination among distantly related members, preventing divergence leading to a genetically stable population. Moreover, their high intrapopulation sequence diversity with an enrichment in synonymous replacements supports the idea of a very ancient divergence and the coexistence of multiple different clones. However, other microbes analyzed seem to follow different evolutionary dynamics where processes of diversification driven by geographic and ecological instability produce a higher number of nonsynonymous replacements and lower intrapopulation sequence diversity. Together, these data shed light on some of the evolutionary and ecological processes that lead to the large genomic diversity in SAR11. Furthermore, this approach can be applied to other similar microbes that are difficult to culture in the laboratory, but abundant in nature, to investigate the underlying dynamics of their genomic evolution. IMPORTANCE As the most abundant bacteria in oceans, the Pelagibacterales order (here SAR11) plays an important role in the global carbon cycle, but the study of the evolutionary forces driving its evolution has lagged considerably due to the inherent difficulty of obtaining pure cultures. Multiple evolutionary models have been proposed to explain the diversification of distinct lineages within a population; however, the identification of many of these patterns in natural populations remains mostly enigmatic. We have used a metagenomic approach to explore microdiversity patterns in their natural habitats. Comparison with a collection of bacterial and archaeal groups from the same environments shows that SAR11 populations have a different evolutionary regime, where multiple genotypes coexist within the same population and remain stable over time. Widespread homologous recombination could be one of the main driving factors of this homogenization.
format	article
author	Mario López-Pérez Jose M. Haro-Moreno Felipe Hernandes Coutinho Manuel Martinez-Garcia Francisco Rodriguez-Valera
author_facet	Mario López-Pérez Jose M. Haro-Moreno Felipe Hernandes Coutinho Manuel Martinez-Garcia Francisco Rodriguez-Valera
author_sort	Mario López-Pérez
title	The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
title_short	The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
title_full	The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
title_fullStr	The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
title_full_unstemmed	The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective
title_sort	evolutionary success of the marine bacterium sar11 analyzed through a metagenomic perspective
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/6dbcbc8c7e0a466cb68ace65bc129787
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The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective

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