The balance between autotrophy and heterotrophy regulates the size of the ocean’s carbon sink. The contribution of a particular bacterial or archaeal lineage to carbon flux is determined by its metabolism, which may vary within lineages and may depend on environmental conditions. Members of the SUP05 clade are often described as a single lineage of chemoautotrophic gammaproteobacterial sulfur-oxidizers (GSOs). Like other SUP05, the Arctic96BD-19 subclade contains the genetic potential for carbon fixation through the Calvin cycle yet differs from other strictly chemoautotrophic SUP05 in its potential to also consume exogenous organic matter from surrounding seawater. The balance between organic carbon production and consumption in Arctic96BD-19 is not well understood and could have global implications to carbon cycling in the world’s oceans. Here we used genomic reconstructions, physiological growth experiments, and proteomics to characterize central carbon and energy processing of Ca. Thioglobus singularis strain PS1, a representative of the Arctic96BD-19 subclade of SUP05 that was isolated from Puget Sound, WA, USA. The addition of either complex organic matter from phytoplankton lysate or individual phytoplankton-derived organic compounds significantly enhanced the growth of PS1. Proteins involved in methylotrophic pathways for carbon assimilation and energy generation were significantly upregulated when lysate was added to the growth media, suggesting that PS1 uses methylated compounds derived from marine organisms. Although sulfur oxidation and carbon fixation are defining characteristics of the GSO clade, strain PS1 did not require reduced inorganic sulfur for growth and there was little evidence of carbon fixation. These data indicate that strain PS1 functions primarily as an organic carbon consumer, suggesting that the role of widespread Arctic96BD-19 may be largely heterotrophic.