The effect of nutrients on carbon and nitrogen fixation by the UCYN-A–haptophyte symbiosis

Abstract

Symbiotic relationships between phytoplankton and N 2 -fixing microorganisms play a crucial role in marine ecosystems. The abundant and widespread unicellular cyanobacteria group A (UCYN-A) has recently been found to live symbiotically with a haptophyte. Here, we investigated the effect of nitrogen (N), phosphorus (P), iron (Fe) and Saharan dust additions on nitrogen (N 2 ) fixation and primary production by the UCYN-A-haptophyte association in the subtropical eastern North Atlantic Ocean using nifH expression analysis and stable isotope incubations combined with single-cell measurements. N 2 fixation by UCYN-A was stimulated by the addition of Fe and Saharan dust, although this was not reflected in the nifH expression. CO 2 fixation by the haptophyte was stimulated by the addition of ammonium nitrate as well as Fe and Saharan dust. Intriguingly, the single-cell analysis using nanometer scale secondary ion mass spectrometry indicates that the increased CO 2 fixation by the haptophyte in treatments without added fixed N is likely an indirect result of the positive effect of Fe and/or P on UCYN-A N 2 fixation and the transfer of N 2 -derived N to the haptophyte. Our results reveal a direct linkage between the marine carbon and nitrogen cycles that is fuelled by the atmospheric deposition of dust. The comparison of single-cell rates suggests a tight coupling of nitrogen and carbon transfer that stays balanced even under changing nutrient regimes. However, it appears that the transfer of carbon from the haptophyte to UCYN-A requires a transfer of nitrogen from UCYN-A. This tight coupling indicates an obligate symbiosis of this globally important diazotrophic association.

A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

“…These types of estimates have been done for several of the open ocean diazotrophs (Foster et al, 2011Krupke et al, 2015;Martínez-Pérez et al, 2016). For example, an estimate of 0.19 and 0.62 Tmol N yr −1 is provided by DDAs in the Atlantic and Pacific oceans, respectively, which is similar to 0.36-0.71 Tmol N yr −1 estimated for Trichodesmium spp.…”

Global distribution and vertical patterns of a prymnesiophyte–cyanobacteria obligate symbiosis

“…This is in agreement with a greater contribution of B. bigelowii reads in the 0.8-5 μm size fraction (as compared with the 5-20 μm fraction) in the Tara-Oceans metabarcoding data analyzed here, as well as of UCYN-A2 reads in the same smaller size fraction in metagenomic samples of the South Atlantic (Cornejo-Castillo et al, submitted). The hypothesis about the obligatory dependence of UCYN-A with its host (Tripp et al, 2010;Thompson et al, 2012;Bombar et al, 2014) has been recently reinforced with the strong coupling observed in the transfer of carbon and nitrogen metabolites between partner cells (Krupke et al, 2014b). On the other hand, the possibility of a freeliving population of the host could not be evaluated as the FISH probe used in previous studies (Krupke et al, 2014a) targeted the whole prymnesiophyte assemblage and not the specific host phylotypes.…”

Biological N2 Fixation in the Upwelling Region off NW Iberia: Magnitude, Relevance, and Players

“…Several studies performed in the North Atlantic reported that, after Trichodesmium, UCYN-A is the most abundant diazotrophic phylotype (Benavides and Voss, 2015;Ratten et al, 2015;Benavides et al, 2016). Even though it extends along a wide latitudinal and longitudinal range, it dominates mainly the eastern basin, where iron inputs by Saharan dust are higher (Benavides et al, 2013), which favors its growth and N 2 -fixing activity (Krupke et al, 2015).…”