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Abstract Marine SAR116 bacterioplankton are ubiquitous in surface waters across global oceans and form their own order, Puniceispirillales, within the Alphaproteobacteria. To date no comparative physiology among diverse SAR116 isolates has been performed to capture the functional diversity within the clade, and further, diversity through the lens of metabolic potential and environmental preferences via clade-wide pangenomics continues to evolve with the addition of new genomes. Using high-throughput dilution-to-extinction cultivation, we isolated and genome sequenced five new and diverse SAR116 isolates from the northern Gulf of Mexico. Here we present a comparative physiological analysis of these SAR116 isolates, along with a pangenomic investigation of the SAR116 clade using a combination of metagenome-assembled genomes (MAGs, n = 258), single-amplified genomes (SAGs, n = 84), previously existing (n = 2), and new isolate genomes (n = 5), totaling 349 SAR116 genomes. Phylogenomic investigation supported the division of SAR116 into three distinct subclades, each with additional structure totaling 15 monophyletic groups. Our SAR116 isolates belonged to three groups within subclade I representing distinct genera with different morphologies and varied phenotypic responses to salinity and temperature. Overall, SAR116 genomes encoded differences in vitamin and amino acid synthesis, trace metal transport, and osmolyte synthesis and transport. They also had genetic potential for diverse sulfur oxidation metabolisms, placing SAR116 at the confluence of the organic and inorganic sulfur pools. SAR116 subclades showed distinct patterns in habitat preferences across open ocean, coastal, and estuarine environments, and three of our isolates represented the most abundant coastal and estuarine subclade. This investigation provides the most comprehensive exploration of SAR116 to date anchored by new culture genomes and physiology.
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Marine Synechococcus isolates representing globally abundant genomic lineages demonstrate a unique evolutionary path of genome reduction without a decrease in GC content
Summary Synechococcus, a genus of unicellular cyanobacteria found throughout the global surface ocean, is a large driver of Earth's carbon cycle. Developing a better understanding of its diversity and distributions is an ongoing effort in biological oceanography. Here, we introduce 12 new draft genomes of marineSynechococcusisolates spanning five clades and utilize ~100 environmental metagenomes largely sourced from the TARA Oceans project to assess the global distributions of the genomic lineages they and other reference genomes represent. We show that five newly provided clade‐II isolates are by far the most representative of the recoveredin situpopulations (most ‘abundant’) and have biogeographic distributions distinct from previously available clade‐II references. Additionally, these isolates form a subclade possessing the smallest genomes yet identified of the genus (2.14 ± 0.05Mbps; mean ± 1SD) while concurrently hosting some of the highest GC contents (60.67 ± 0.16%). This is in direct opposition to the pattern inSynechococcus’s nearest relative,Prochlorococcus– wherein decreasing genome size has coincided with a strongdecreasein GC content – suggesting this new subclade ofSynechococcusappears to have convergently undergone genomic reduction relative to the rest of the genus, but along a fundamentally different evolutionary trajectory.
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- PAR ID:
- 10461594
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Environmental Microbiology
- Volume:
- 21
- Issue:
- 5
- ISSN:
- 1462-2912
- Format(s):
- Medium: X Size: p. 1677-1686
- Size(s):
- p. 1677-1686
- Sponsoring Org:
- National Science Foundation
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