Marine Nitrogen Fixation: Organisms, Significance, Enigmas, and Future Directions

Dinitrogen (N2) fixation is an integral part of the marine nitrogen cycle and together with N losses through denitrification and anaerobic ammonia oxidation determines the size of the oceanic nitrogen pool. N2 fixation in the oceans is of a similar magnitude to anthropogenic N2 fixation, and yet many questions remain on what the major N2-fixing organisms are, and what controls their distributions and N2 fixation rates. Using molecular and metagenomic approaches, surprising discoveries have been made as many environmental microorganisms have yet to be obtained in pure culture. Cyanobacteria appear to be the main oceanic N2-fixers, with several key species that include the filamentous, colonial, nonheterocyst-forming Trichodesmium, heterocyst-forming strains that are symbiotic with diatoms, and unicellular types, which differ in their impacts on the ecosystem. Unusual microorganisms have been discovered, such as the UCYN-A cyanobacterium that lacks photosystem II, Rubisco and the TCA cycle, and challenges the definition of cyanobacteria. The genomic basis of lifestyles of cyanobacterial symbiotic diazotrophs has been revealed, which differ in their level of host dependency/streamlining. These discoveries challenge the previous understanding about key players, habitats, ecological community interactions, and overall magnitude of oceanic N2 fixation. It is accepted that N2 fixation is a key component of the marine nitrogen cycle, but rather than being an easily quantifiable process carried out by few species in well-constrained areas, the accumulating knowledge shows that we are just beginning to understand the impacts of diazotrophs in the pelagic ocean (and other) ecosystems. New methods and instrumentation, such as the Environmental Sample Processor, promise to provide higher resolution information on the temporal and spatial mesoscale variability of the different species and environmental controlling factors. Further progress is necessary if we are to better understand the role of N2 fixation in the ocean and its response to global environmental change.