Hopanoid lipids may facilitate aerobic nitrogen fixation in the ocean

Abstract

Cyanobacterial diazotrophs are considered to be the most important source of fixed N2in the open ocean. Biological N2fixation is catalyzed by the extremely O2-sensitive nitrogenase enzyme. In cyanobacteria without specialized N2-fixing cells (heterocysts), mechanisms such as decoupling photosynthesis from N2fixation in space or time are involved in protecting nitrogenase from the intracellular O2evolved by photosynthesis. However, it is not known how cyanobacterial cells limit O2diffusion across their membranes to protect nitrogenase in ambient O2-saturated surface ocean waters. Here, we explored all known genomes of the major marine cyanobacterial lineages for the presence of hopanoid synthesis genes, since hopanoids are a class of lipids that might act as an O2diffusion barrier. We found that, whereas all non−heterocyst-forming cyanobacterial diazotrophs had hopanoid synthesis genes, none of the marineSynechococcus,Prochlorococcus(non−N2-fixing), and marine heterocyst-forming (N2-fixing) cyanobacteria did. Finally, we conclude that hopanoid-enriched membranes are a conserved trait in non−heterocyst-forming cyanobacterial diazotrophs that might lower the permeability to extracellular O2. This membrane property coupled with high respiration rates to decrease intracellular O2concentration may therefore explain how non−heterocyst-forming cyanobacterial diazotrophs can fix N2in the fully oxic surface ocean.