Distribution of diverse nitrogen fixers in the global ocean

Abstract

[1] We employ a global three-dimensional model to simulate diverse phytoplanktonic diazotrophs (nitrogen fixers) in the oceans. In the model, the structure of the marine phytoplankton community self-assembles from a large number of potentially viable physiologies. Amongst them, analogs of Trichodesmium, unicellular diazotrophs and diatom-diazotroph associations (DDA) are successful and abundant. The simulated biogeography and nitrogen fixation rates of the modeled diazotrophs compare favorably with a compilation of published observations, which includes both traditional and molecular measurements of abundance and activity of marine diazotrophs. In the model, the diazotroph analogs occupy warm subtropical and tropical waters, with higher concentrations and nitrogen fixation rates in the tropical Atlantic Ocean and the Arabian Sea/Northern Indian Ocean, and lower values in the tropical and subtropical South Pacific Ocean. The three main diazotroph types typically co-exist in the model, although Trichodesmium analogs dominate the diazotroph population in much of the North and tropical Atlantic Ocean and the Arabian Sea, while unicellular-diazotroph analogs dominate in the South Atlantic, Pacific and Indian oceans. This pattern reflects the relative degree of nutrient limitation by iron or phosphorus. The model suggests in addition that unicellular diazotrophs could add as much new nitrogen to the global ocean as Trichodesmium.

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

“…If Crocosphaera watsonii had evolved hotbunking from an ancestor that maintained its metalloenzymes through the diel, how would the trade-off between lower iron requirement and higher energetic cost affect where Crocosphaera would be competitive relative to its progenitor and other diazotrophs? A numerical global ocean circulation and ecosystem model (10,42) is a useful tool to explore the implications of hotbunking on Crocosphera's habitat and nitrogen fixation rates in the global ocean. Our model resolves several phytoplankton types competing for resources, including analogs of several nondiazotrophs types, and unicellular and colonial marine diazotrophs, analogous to Crocosphaera and Trichodesmium, respectively.…”

“…The physical circulation flow fields and diffusion, constrained by observations (47), transport the organic and inorganic components of the ecosystem model. The ecosystem model was adapted from Monteiro et al (10) and includes several types of autotrophs including several nondiazotrophs (analogs of diatoms, other large eukaryotes, Prochlorococcus, and other small With increased α (a smaller cost to growth) and a decreased γ (a lower requirement for iron) there are more regions where diazotrophy is supported, there is higher biomass of unicellular diazotrophs, and consequently higher total global autotrophic nitrogen fixation rates. If the energetic cost is low enough the hotbunking diazotrophs outcompete the control group everywhere (white regions of B).…”

“…Instead, iron is considered the critical micronutrient for marine diazotrophs due to their use of the ironnitrogenase protein complex containing a homodimeric iron protein with a 4Fe∶4S metallocluster (NifH) and a heterotetrameric molybdenum-iron protein with an 8Fe∶7S P cluster and a 7 Fe and 1 Mo MoFe cofactor (NifDK, α and β subunits) (7,8) (Table S1). Field experiments and models both predict the distribution of oceanic nitrogen fixation to be primarily constrained by the availability of iron (2,(9)(10)(11). Despite this importance of iron on marine nitrogen fixation, there is a limited understanding of how marine diazotrophs have adapted to this low iron environment (12)(13)(14)(15)(16)(17).…”

High levels of heterogeneity in diazotroph diversity and activity within a putative hotspot for marine nitrogen fixation

“…N 2 fixed by diverse diazotrophic taxa may have different fates within the marine environment (Glibert and Bronk 1994;Mulholland, 2007;Foster et al, 2011;Karl et al, 2012;, and therefore characterisation of the composition of active N 2 -fixing assemblages, combined with size-fractionated N 2 fixation rates, is necessary to determine the differential contribution of newly fixed N to pelagic ecosystems. Here we report changes in the biogeographical distribution and activity of diazotrophs across a broad tropical region, which has been identified as a potential global 'hotspot' for marine N 2 fixation (Montoya et al, 2004;Monteiro et al, 2010;Luo et al, 2014).…”

“…Additionally, ecosystem models predict cyanobacterial diazotrophs will be abundant in northern Australian waters (Monteiro et al, 2010). Indeed, Trichodesmium has long been recognised as an important member of the phytoplankton in this region (Hallegraeff and Jeffrey, 1984;Burford et al, 1995Burford et al, , 2009, and unicellular diazotrophs are assumed to be highly active here as well (Montoya et al, 2004).…”