Ecophysiology of the cosmopolitan OM252 bacterioplankton (Gammaproteobacteria)

Abstract

Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria. Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (Candidatus Halomarinus), sister to Litoricola, comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors, with subclade I genomes encoding the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance but a mesophilic temperature range for growth, with a maximum of 0.36 doublings/hr at 35{degrees}C. Cells were curved rod/spirillum-shaped, ~1.5 x 0.2 m. Growth on thiosulfate as the sole electron donor under autotrophic conditions was roughly one third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some Ca. Halomarinus organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. ImportanceMarine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria, has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic datasets, we examined the diversity within the OM252 clade, the distribution of these taxa in the worlds oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point towards the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly "heterotrophic" taxa.