Genomic and phenotypic characterization of 26 novel marine bacterial strains with relevant biogeochemical roles and widespread presence across the global ocean

30 pages, 7 figures, 2 tables, supplementary material https://www.frontiersin.org/articles/10.3389/fmicb.2024.1407904/full#supplementary-material.-- Data availability statement: The 16S rRNA gene Sanger sequences can be found in GenBank under accessions OP342948, OP342988, OP343012, OP343046, OP343076, OP343113, OP343172, OP343188, OP343189, OP343191, OP343207, OP343250, OP343258, OP343310, OP343522, OP343883, OP343904, OP343913, OP344205, OP344261, OP344277, OP344279, OP344286, OP344303, OP344346, and OP344367. The genome sequences used in this study can be found in GenBank under BioProject PRJNA1016293. The Tara Oceans metagenomic datasets can be found in ENA under BioProject PRJEB1787 and PJREB9740

Prokaryotes dominate global oceans and shape biogeochemical cycles, yet most taxa remain uncultured and uncharacterized as of today. Here we present the characterization of 26 novel marine bacterial strains from a large isolate collection obtained from Blanes Bay (NW Mediterranean) microcosm experiments made in the four seasons. Morphological, cultural, biochemical, physiological, nutritional, genomic, and phylogenomic analyses were used to characterize and phylogenetically place the novel isolates. The strains represent 23 novel bacterial species and six novel genera: three novel species pertaining to class Alphaproteobacteria (families Rhodobacteraceae and Sphingomonadaceae), six novel species and three new genera from class Gammaproteobacteria (families Algiphilaceae, Salinispheraceae, and Alteromonadaceae), 13 novel species and three novel genera from class Bacteroidia (family Flavobacteriaceae), and one new species from class Rhodothermia (family Rubricoccaceae). The bacteria described here have potentially relevant roles in the cycles of carbon (e.g., carbon fixation or energy production via proteorhodopsin), nitrogen (e.g., denitrification or use of urea), sulfur (oxidation of sulfur compounds), phosphorus (acquisition and use of different forms of phosphorus and remodeling of membrane phospholipids), and hydrogen (oxidation of hydrogen to obtain energy). We mapped the genomes of the presented strains to the Tara Oceans metagenomes to reveal that these strains were globally distributed, with those of the family Flavobacteriaceae being the most widespread and abundant, while Rhodothermia being the rarest and most localized. While molecular-only approaches are also important, our study stresses the importance of culturing as a powerful tool to further understand the functioning of marine bacterial communities

This research was supported by grants RTI2018-101025-B-I00, PID2021-125469NB-C31, and PID2021-125469NB-C32 funded by the Spanish Ministry of Science and Innovation and AICO2020-181 funded by Generalitat Valenciana. This study acknowledges the Severo Ochoa Center of Excellence accreditation (CEX2019-000928-S). XR-V was supported by a Spanish FPU grant

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