The conundrum of marine N2 fixation

Over the last 30 years, immense progress has been made in understand- ing the global significance of marine nitrogen (N2) fixation. Development of enzymo- logical, isotopic and molecular techniques for identifying N2 fixers and quantifying N2 fixation rates, as well as more frequent and extensive field campaigns have fuelled such progress. Ship-based and laboratory experiments have revealed a large suite of previously unknown physiological characteristics of diazotrophs. More recently, geo- chemical estimates of N2 fixation, based upon N and phosphorus (P) stoichiometry, stable N isotope studies and carbon (C) anomalies in nutrient starved regions of the ocean, have provided basin and global- scale estimates of N2 fixation. While these achievements have revolutionized our understanding of the role N2 fixers play in global marine N and C cycles, there remain fundamental challenges in the study of N2 fixation. We here summarize the advances made and highlight the conundrums that remain regarding the basin and global scale quantification of N2 fixation, as well as the climatological, physical and biological factors that enable or constrain the distribution and growth of diazotrophs. Presently, direct estimates of N2 fixation, largely of the planktonic cyanobacte- rium, Trichodesmium, can account for only a quarter to one-half of the geochemically derived rates of N2 fixation in various ocean basins. This dichotomy may be partially a result of the spatial and temporal scales over which each approach integrates N2 fixation. However, recently discovered marine N2fixers, including coccoid cyanobacte- ria and heterotrophic bacteria, cyanobacteria symbiotic with eukaryotic algae and the gut flora of zooplankton may account for much of the disparity. While their contribu- tion to the marine N cycle is captured by broad scale geochemical derivations, robust direct estimates of N2 fixation for these members of the diazotrophic flora have not yet been obtained. Moreover, there is substantial uncertainty among the various geochemi- cally derived estimates of N2 fixation, each of which is highly sensitive to choices of parameters, such as domain area, used in their derivation. Recent findings from stable isotope studies imply that unraveling the pathway of recently fixed N through the N cycle remains a challenge. On a basin and global scale, iron (Fe) and P are thought to be primary chemical factors limiting N2 fixation. The climatological and biological forcings, which individu- ally or cumulatively promote diazotroph growth or trigger blooms, are still poorly understood. Improvements in coupled biological-physical and ecosystem models have allowed for the explicit representation of diazotrophs and, in particular, Trichodes- mium and thus hold great potential for unraveling the factors that constrain diazotroph distribution and growth. The role of N2 fixation in both the global N and C cycle, through both the inter-glacial and glacial cycles as well in the present day ocean, remains an open question. The emerging body of data on global rates of denitrification implies that the oceans are losing nitrate rapidly and, if true, either the rates of N2 fixation are even higher than we currently estimate or, on some time-scale, the total stock of nitrate in the oceans is more variable than expected. Each of these outcomes has direct implications for the air-sea partitioning of CO2 on climate time-scales. The question remains: does the importance of marine N2 fixation relative to denitrification oscillate over various timescales in response to climate forcing or is the N cycle in a homeostatic steady state?