Cyanobacteria from marine oxygen deficient zones encode both form I and form II rubiscos

Abstract

Cyanobacteria are highly abundant in the marine photic zone and primary drivers of the conversion of inorganic carbon to biomass. To date, all studied Cyanobacterial lineages encode carbon fixation machinery hinged upon form I rubisco enzymes within a CO2-concentrating carboxysome. Here, we report that the AMZ IB lineage of Prochlorococcus from global oxygen deficient zones (ODZs) harbor both form I and form II rubisco enzymes, the latter of which are typically non-carboxysomal and possess biochemical properties tuned towards low oxygen environments. Our analyses reveal that these cyanobacterial form II enzymes are functional in vitro and were likely acquired via lateral gene transfer from proteobacteria. Global metagenomic read recruitment demonstrates that Prochlorococcus with form II rubisco are essentially restricted to ODZs in the Eastern Tropical Pacific, suggesting that acquisition may confer an advantage specifically under low-O2 conditions. Populations of AMZ IB Prochlorococcus express both forms of rubisco in situ, with the highest form II rubisco expression at depths where both oxygen and light are particularly 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 the overall capacity of ODZs to sequester carbon.