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Phylogenomics of SAR116 clade reveals two subclades with different evolutionary trajectories and important role in the ocean sulfur cycle

Juan J. Roda-Garcia, Jose M. Haro-Moreno, Lukas A. Huschet, View ORCID ProfileFrancisco Rodriguez-Valera, View ORCID ProfileMario López-Pérez
doi: https://doi.org/10.1101/2021.05.06.443042
Juan J. Roda-Garcia
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan 03550, Alicante, Spain
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Jose M. Haro-Moreno
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan 03550, Alicante, Spain
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Lukas A. Huschet
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan 03550, Alicante, Spain
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Francisco Rodriguez-Valera
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan 03550, Alicante, Spain
bResearch Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology, Dolgoprudny, 141701 Russia
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Mario López-Pérez
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan 03550, Alicante, Spain
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  • For correspondence: mario.lopezp@umh.es
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ABSTRACT

The SAR116 clade within the class Alphaproteobacteria represents one of the most abundant groups of heterotrophic bacteria inhabiting the surface of the ocean. The small number of cultured representatives of SAR116 (only two to date) is a major bottleneck that has prevented an in-depth study at the genomic level to understand the relationship between genome diversity and its role in the marine environment. In this study, we use all publicly available genomes to provide a genomic overview of the phylogeny, metabolism and biogeography within the SAR116 clade. This increased genomic diversity revealed has led to the discovery of two subclades of SAR116 that, despite having similar genome size (ca. 2.4 Mb) and coexist in the same environment, display different properties in their genomic make up. One represents a novel subclade for which no pure cultures have been isolated and is composed mainly of single-amplified genomes (SAGs). Genomes within this subclade showed convergent evolutionary trajectories with more streamlining features, such as low GC content (ca. 30%), short intergenic spacers (<22 bp) and strong purifying selection (low dN/dS). Besides, they were more abundant in metagenomic databases recruiting also at the deep chlorophyll maximum. Less abundant and restricted to the upper photic layers of the global ocean, the other subclade of SAR116, enriched in MAGs, accommodated the only two pure cultures. Genomic analysis suggested that both clades have a significant role in the sulfur cycle with differences in the way in which both clades can metabolize the dimethylsulfoniopropionate (DMSP).

IMPORTANCE SAR116 clade of Alphaproteobacteria is an ubiquitous group of heterotrophic bacteria inhabiting the surface of the ocean, but the information about their ecology and population genomic diversity is scarce due to the difficulty of getting pure culture isolates. The combination of single-cell genomics and metagenomics has become an alternative approach to study this kind of microbes. Our results expand the understanding of the genomic diversity, distribution, and lifestyles within this clade and provide evidence of different evolutionary trajectories in the genome make-up of the two subclades that could serve to understand how evolutionary pressure can drive different adaptations to the same environment. Therefore, the SAR116 clade represents an ideal model organism for the study of the evolutionary streamlining of genomes in microbes that have relatively close relatedness to each other.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 09, 2021.
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Phylogenomics of SAR116 clade reveals two subclades with different evolutionary trajectories and important role in the ocean sulfur cycle
Juan J. Roda-Garcia, Jose M. Haro-Moreno, Lukas A. Huschet, Francisco Rodriguez-Valera, Mario López-Pérez
bioRxiv 2021.05.06.443042; doi: https://doi.org/10.1101/2021.05.06.443042
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Phylogenomics of SAR116 clade reveals two subclades with different evolutionary trajectories and important role in the ocean sulfur cycle
Juan J. Roda-Garcia, Jose M. Haro-Moreno, Lukas A. Huschet, Francisco Rodriguez-Valera, Mario López-Pérez
bioRxiv 2021.05.06.443042; doi: https://doi.org/10.1101/2021.05.06.443042

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