Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum

ABSTRACT Diverse bacterial and archaeal lineages drive biogeochemical cycles in the global ocean, but the evolutionary processes that have shaped their genomic properties and physiological capabilities remain obscure. Here we track the genome evolution of the globally abundant marine bacterial phylu...

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Autores principales:	Eric W. Getz, Saima Sultana Tithi, Liqing Zhang, Frank O. Aylward
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	bioenergetics candidate phyla evolutionary genomics genome streamlining microbial oceanography pangenomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1d4c9debe2b144a3966058afd0afcd1b
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spelling	oai:doaj.org-article:1d4c9debe2b144a3966058afd0afcd1b2021-11-15T15:58:20ZParallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum10.1128/mBio.01089-182150-7511https://doaj.org/article/1d4c9debe2b144a3966058afd0afcd1b2018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01089-18https://doaj.org/toc/2150-7511ABSTRACT Diverse bacterial and archaeal lineages drive biogeochemical cycles in the global ocean, but the evolutionary processes that have shaped their genomic properties and physiological capabilities remain obscure. Here we track the genome evolution of the globally abundant marine bacterial phylum Marinimicrobia across its diversification into modern marine environments and demonstrate that extant lineages are partitioned between epipelagic and mesopelagic habitats. Moreover, we show that these habitat preferences are associated with fundamental differences in genomic organization, cellular bioenergetics, and metabolic modalities. Multiple lineages present in epipelagic niches independently acquired genes necessary for phototrophy and environmental stress mitigation, and their genomes convergently evolved key features associated with genome streamlining. In contrast, lineages residing in mesopelagic waters independently acquired nitrate respiratory machinery and a variety of cytochromes, consistent with the use of alternative terminal electron acceptors in oxygen minimum zones (OMZs). Further, while epipelagic clades have retained an ancestral Na+-pumping respiratory complex, mesopelagic lineages have largely replaced this complex with canonical H+-pumping respiratory complex I, potentially due to the increased efficiency of the latter together with the presence of the more energy-limiting environments deep in the ocean’s interior. These parallel evolutionary trends indicate that key features of genomic streamlining and cellular bioenergetics have occurred repeatedly and congruently in disparate clades and underscore the importance of environmental conditions and nutrient dynamics in driving the evolution of diverse bacterioplankton lineages in similar ways throughout the global ocean. IMPORTANCE Understanding long-term patterns of microbial evolution is critical to advancing our knowledge of past and present role microbial life in driving global biogeochemical cycles. Historically, it has been challenging to study the evolution of environmental microbes due to difficulties in obtaining genome sequences from lineages that could not be cultivated, but recent advances in metagenomics and single-cell genomics have begun to obviate many of these hurdles. Here we present an evolutionary genomic analysis of the Marinimicrobia, a diverse bacterial group that is abundant in the global ocean. We demonstrate that distantly related Marinimicrobia species that reside in similar habitats have converged to assume similar genome architectures and cellular bioenergetics, suggesting that common factors shape the evolution of a broad array of marine lineages. These findings broaden our understanding of the evolutionary forces that have given rise to microbial life in the contemporary ocean.Eric W. GetzSaima Sultana TithiLiqing ZhangFrank O. AylwardAmerican Society for Microbiologyarticlebioenergeticscandidate phylaevolutionary genomicsgenome streamliningmicrobial oceanographypangenomicsMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	bioenergetics candidate phyla evolutionary genomics genome streamlining microbial oceanography pangenomics Microbiology QR1-502
spellingShingle	bioenergetics candidate phyla evolutionary genomics genome streamlining microbial oceanography pangenomics Microbiology QR1-502 Eric W. Getz Saima Sultana Tithi Liqing Zhang Frank O. Aylward Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
description	ABSTRACT Diverse bacterial and archaeal lineages drive biogeochemical cycles in the global ocean, but the evolutionary processes that have shaped their genomic properties and physiological capabilities remain obscure. Here we track the genome evolution of the globally abundant marine bacterial phylum Marinimicrobia across its diversification into modern marine environments and demonstrate that extant lineages are partitioned between epipelagic and mesopelagic habitats. Moreover, we show that these habitat preferences are associated with fundamental differences in genomic organization, cellular bioenergetics, and metabolic modalities. Multiple lineages present in epipelagic niches independently acquired genes necessary for phototrophy and environmental stress mitigation, and their genomes convergently evolved key features associated with genome streamlining. In contrast, lineages residing in mesopelagic waters independently acquired nitrate respiratory machinery and a variety of cytochromes, consistent with the use of alternative terminal electron acceptors in oxygen minimum zones (OMZs). Further, while epipelagic clades have retained an ancestral Na+-pumping respiratory complex, mesopelagic lineages have largely replaced this complex with canonical H+-pumping respiratory complex I, potentially due to the increased efficiency of the latter together with the presence of the more energy-limiting environments deep in the ocean’s interior. These parallel evolutionary trends indicate that key features of genomic streamlining and cellular bioenergetics have occurred repeatedly and congruently in disparate clades and underscore the importance of environmental conditions and nutrient dynamics in driving the evolution of diverse bacterioplankton lineages in similar ways throughout the global ocean. IMPORTANCE Understanding long-term patterns of microbial evolution is critical to advancing our knowledge of past and present role microbial life in driving global biogeochemical cycles. Historically, it has been challenging to study the evolution of environmental microbes due to difficulties in obtaining genome sequences from lineages that could not be cultivated, but recent advances in metagenomics and single-cell genomics have begun to obviate many of these hurdles. Here we present an evolutionary genomic analysis of the Marinimicrobia, a diverse bacterial group that is abundant in the global ocean. We demonstrate that distantly related Marinimicrobia species that reside in similar habitats have converged to assume similar genome architectures and cellular bioenergetics, suggesting that common factors shape the evolution of a broad array of marine lineages. These findings broaden our understanding of the evolutionary forces that have given rise to microbial life in the contemporary ocean.
format	article
author	Eric W. Getz Saima Sultana Tithi Liqing Zhang Frank O. Aylward
author_facet	Eric W. Getz Saima Sultana Tithi Liqing Zhang Frank O. Aylward
author_sort	Eric W. Getz
title	Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
title_short	Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
title_full	Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
title_fullStr	Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
title_full_unstemmed	Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
title_sort	parallel evolution of genome streamlining and cellular bioenergetics across the marine radiation of a bacterial phylum
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/1d4c9debe2b144a3966058afd0afcd1b
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_version_	1718427016145928192

Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum

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