Abstract
Proteobacteria constitute one of the most diverse and abundant groups of microbes on Earth. In productive marine environments like deep-sea hydrothermal systems, Proteobacteria are implicated in autotrophy coupled to sulfur, methane, and hydrogen oxidation, sulfate reduction, and denitrification. Beyond chemoautotrophy, little is known about the ecological significance of poorly studied Proteobacteria lineages that are globally distributed and active in hydrothermal systems. Here we apply multi-omics to characterize 51 metagenome-assembled genomes from three hydrothermal vent plumes in the Pacific and Atlantic Oceans that are affiliated with nine Proteobacteria lineages. Metabolic analyses revealed these organisms to contain a diverse functional repertoire including chemolithotrophic ability to utilize sulfur and C1 compounds, and chemoorganotrophic ability to utilize environment-derived fatty acids, aromatics, carbohydrates, and peptides. Comparative genomics with marine and terrestrial microbiomes suggests that lineage-associated functional traits could explain niche specificity. Our results shed light on the ecological functions and metabolic strategies of novel Proteobacteria in hydrothermal systems and beyond, and highlight the relationship between genome diversification and environmental adaptation.
Highlights
Proteobacteria constitute one of the most diverse microbial phyla and are successful in most biomes on Earth [1, 2]
We propose the names Marenostrumaceae for UBA2165; Hyrcanianaceae for group Casp-alpha2, Taraoceanobacteraceae for UBA11654, which was first reconstructed from Tara Ocean metagenome datasets [69]; Riflewellaceae for UBA4486 which was first described from terrestrial aquifer wells at Rifle, Colorado, USA [49]; Marinioligotrophales for the formerly OMG bacteria, the Oligotrophic Marine Gammaproteobacteria [70]; Planktothermales for UBA7887, which are reconstructed from hydrothermal plume environments [44]; and Kappaproteobacteria for the former LS-SOB group [44], which are ubiquitous in coastal systems and the ocean water column
Our research provides the first comprehensive study into the ecological functions and metabolic capacities of nine globally distributed proteobacterial lineages that are abundant and active in deep-sea hydrothermal systems
Summary
Proteobacteria constitute one of the most diverse microbial phyla and are successful in most biomes on Earth [1, 2]. Proteobacteria are abundant from pole to pole in the world’s oceans [3, 4], and from the surface to the deep oceans in vertical cross-sections [5, 6]. Proteobacteria display an enormous functional repertoire and comprise phototrophs, autotrophs, and heterotrophs. Heterotrophic Proteobacteria such as SAR11, SAR86, and Roseobacter are abundant and successful bacterioplankton lineages, which mainly rely on the availability of dissolved
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