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The SUP05 clade of gammaproteobacteria (Thioglobaceae) comprises both primary producers and primary consumers of organic carbon in the oceans. Host-associated autotrophs are a principal source of carbon and other nutrients for deep-sea eukaryotes at hydrothermal vents, and their free-living relatives are a primary source of organic matter in seawater at vents and in marine oxygen minimum zones. Similar to other abundant marine heterotrophs, such as SAR11 and Roseobacter, heterotrophic Thioglobaceae use the dilute pool of osmolytes produced by phytoplankton for growth, including methylated amines and sulfonates. Heterotrophic members are common throughout the ocean, and autotrophic members are abundant at hydrothermal vents and in anoxic waters; combined, they can account for more than 50% of the total bacterial community. Studies of both cultured and uncultured representatives from this diverse family are providing novel insights into the shifting biogeochemical roles of autotrophic and heterotrophic bacteria that cross oxic-anoxic boundary layers in the ocean.

A hallmark of the SUP05 clade of marine Gammaproteobacteria is the ability to use energy obtained from reduced inorganic sulfur to fuel autotrophic fixation of carbon using RuBisCo. However, some SUP05 also have the genetic potential for heterotrophic growth, raising questions about the roles of SUP05 in the marine carbon cycle. We used genomic reconstructions, physiological growth experiments and proteomics to characterize central carbon and energy metabolism in Candidatus Thioglobus singularis strain PS1, a representative from the SUP05 clade that has the genetic potential for autotrophy and heterotrophy. Here, we show that the addition of individual organic compounds and 0.2 μm filtered diatom lysate significantly enhanced the growth of this bacterium. This positive growth response to organic substrates, combined with expression of a complete TCA cycle, heterotrophic pathways for carbon assimilation, and methylotrophic pathways for energy conversion demonstrate strain PS1's capacity for heterotrophic growth. Further, our inability to verify the expression of RuBisCO suggests that carbon fixation was not critical for growth. These results highlight the metabolic diversity of the SUP05 clade that harbours both primary producers and consumers of organic carbon in the oceans and expand our understanding of specific pathways of organic matter oxidation by the heterotrophic SUP05., (© 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.)