The conundrum of marine N2 fixation

Abstract

Over the last 30 years, immense progress has been made in understanding the global significance of marine nitrogen (N₂) fixation. Development of enzymological, 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, geochemical 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 cyanobacterium, <i>Trichodesmium,</i> 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 N₂ fixers, including coccoid cyanobacteria and heterotrophic bacteria, cyanobacteria symbiotic with eukaryotic algae and the gut flora of zooplankton may account for much of the disparity. While their contribution 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 geochemically 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 individually 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, <i>Trichodesmium</i> 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?