The diverse and ubiquitous members of the SAR11 lineage (Alphaproteobacteria) represent up to 30–40% of the surface and mesopelagic oceanic microbial communities. However, the molecular and ecological mechanisms that differentiate closely related, yet distinct, SAR11 members that often co-occur under similar environmental conditions remain speculative. Recently, two mesopelagic and oxygen minimum zone (OMZ)-associated subclades of SAR11 (Ic and IIa.A) were described using single-cell amplified genomes (SAGs) linked to nitrate reduction in OMZs. In this current study, the collection of genomes belonging to these two subclades was expanded with thirteen new metagenome-assembled genomes (MAGs), thus providing a more detailed phylogenetic and functional characterization of these subclades. Gene content-based predictions of metabolic functions revealed similarities in central carbon metabolism between subclades Ic and IIa.A and surface SAR11 clades, with small variations in central pathways. These variations included more versatile sulfur assimilation pathways, as well as a previously predicted capacity for nitrate reduction that conferred unique versatility on mesopelagic-adapted clades compared to their surface counterparts. Finally, consistent with previously reported abundances of carbon monoxide (CO) in surface and mesopelagic waters, subclades Ia (surface) and Ic (mesopelagic) have the genetic potential to oxidize carbon monoxide (CO), presumably taking advantage of this abundant compound as an electron donor. Based on genomic analyses, environmental distribution and metabolic reconstruction, we propose two new SAR11 genera, Ca. Mesopelagibacter carboxydoxydans (subclade Ic) and Ca. Anoxipelagibacter denitrificans (subclade IIa.A), which represent members of the mesopelagic and OMZ-adapted SAR11 clades.