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Cyanobacteria are highly abundant in the marine photic zone and primary drivers of the conversion of inorganic carbon into biomass. To date, all studied cyanobacterial lineages encode carbon fixation machinery relying upon form I Rubiscos within a CO₂-concentrating carboxysome. Here, we report that the uncultivated anoxic marine zone (AMZ) IB lineage of Prochlorococcus from pelagic oxygen-deficient zones (ODZs) harbors both form I and form II Rubiscos, the latter of which are typically noncarboxysomal and possess biochemical properties tuned toward low-oxygen environments. We demonstrate that these cyanobacterial form II enzymes are functional in vitro and were likely acquired from proteobacteria. Metagenomic analysis reveals that AMZ IB are essentially restricted to ODZs in the Eastern Pacific, suggesting that form II acquisition may confer an advantage under low-O₂conditions. AMZ IB populations express both forms of Rubisco in situ, with the highest form II expression at depths where oxygen and light are low, possibly as a mechanism to increase the efficiency of photoautotrophy under energy limitation. Our findings expand the diversity of carbon fixation configurations in the microbial world and may have implications for carbon sequestration in natural and engineered systems. 

ABSTRACT Oxygen deficient zones (ODZs) are subsurface marine systems that harbour distinct microbial communities, including populations of the picocyanobacteriaProchlorococcusthat can form a secondary chlorophyll maximum (SCM), and low‐oxygen tolerant strains of the globally abundant heterotrophPelagibacter(SAR11). Yet, the small labile molecules (metabolites) responsible for maintaining these ODZ communities are unknown. Here, we compared the metabolome of an ODZ to that of an oxygenated site by quantifying 87 metabolites across depth profiles in the eastern tropical North Pacific ODZ and the oxygenated waters of the North Pacific Gyre. Metabolomes were largely consistent between anoxic and oxic water columns. However, the osmolyte glycine betaine (GBT) was enriched in the oxycline and SCM of the ETNP, comprising as much as 1.2% of particulate organic carbon. Transcriptomes revealed two active GBT production pathways, glycine methylation (SDMT/bsmB) expressed byProchlorococcusand choline oxidation (betB) expressed by Gammaproteobacteria. GBT consumption through demethylation involved diverse microbial taxa, with SAR11 contributing nearly half of the transcripts for the initial step of GBT demethylation (BHMT), which is predicted to convert GBT and homocysteine into dimethylglycine and methionine, a compound SAR11 cannot otherwise produce. Thus, GBT connects the metabolisms of the dominant phototroph and heterotroph in the oceans. 

Summary Synechococcus, a genus of unicellular cyanobacteria found throughout the global surface ocean, is a large driver of Earth's carbon cycle. Developing a better understanding of its diversity and distributions is an ongoing effort in biological oceanography. Here, we introduce 12 new draft genomes of marineSynechococcusisolates spanning five clades and utilize ~100 environmental metagenomes largely sourced from the TARA Oceans project to assess the global distributions of the genomic lineages they and other reference genomes represent. We show that five newly provided clade‐II isolates are by far the most representative of the recoveredin situpopulations (most ‘abundant’) and have biogeographic distributions distinct from previously available clade‐II references. Additionally, these isolates form a subclade possessing the smallest genomes yet identified of the genus (2.14 ± 0.05Mbps; mean ± 1SD) while concurrently hosting some of the highest GC contents (60.67 ± 0.16%). This is in direct opposition to the pattern inSynechococcus’s nearest relative,Prochlorococcus– wherein decreasing genome size has coincided with a strongdecreasein GC content – suggesting this new subclade ofSynechococcusappears to have convergently undergone genomic reduction relative to the rest of the genus, but along a fundamentally different evolutionary trajectory.