Dissolved Organic Matter Influences N2 Fixation in the New Caledonian Lagoon (Western Tropical South Pacific)

Hila Elifantz,Mar Benavides,Ilana Berman-Frank,Sophie Bonnet,Cécile Dupouy,Chloé Martias

doi:10.3389/fmars.2018.00089

Abstract

Specialized prokaryotes performing biological dinitrogen (N2) fixation ('diazotrophs') provide an important source of fixed nitrogen in oligotrophic marine ecosystems such as tropical and subtropical oceans. In these waters, cyanobacterial photosynthetic diazotrophs are well known to be abundant and active, yet the role and contribution of non-cyanobacterial diazotrophs are currently unclear. The latter are not photosynthetic (here called 'heterotrophic') and hence require external sources of organic matter to sustain N2 fixation. Here we added the photosynthesis inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) to estimate the N2 fixation potential of heterotrophic diazotrophs as compared to autotrophic ones. Additionally, we explored the influence of dissolved organic matter (DOM) on these diazotrophs along a coast to open ocean gradient in the surface waters of a subtropical coral lagoon (New Caledonia). Total N2 fixation (samples not amended with DCMU) ranged from 0.66 to 1.32 nmol N L-1 d-1. The addition of DCMU reduced N2 fixation by >90%, suggesting that the contribution of heterotrophic diazotrophs to overall N2 fixation activity was minor in this environment. Higher contribution of heterotrophic diazotrophs occurred in stations closer to the shore and coincided with the decreasing lability of DOM, as shown by various colored DOM and fluorescent DOM (CDOM and FDOM) indices. This suggests that heterotrophic N2 fixation is favored when labile DOM compounds are available. We tested the response of diazotrophs (in terms of nifH gene expression and bulk N2 fixation rates) upon the addition of a mix of carbohydrates ('DOC' treatment), amino acids ('DON' treatment), and phosphonates and phosphomonesters ('DOP' treatment). While nifH expression increased significantly in Trichodesmium exposed to the DOC treatment, bulk N2 fixation rates increased significantly only in the DOP treatment. The lack of nifH expression by gammaproteobacteria, in any of the DOM addition treatments applied, questions the contribution of non-cyanobacterial diazotrophs to fixed nitrogen inputs in the New Caledonian lagoon. While the metabolism and ecology of heterotrophic diazotrophs is currently elusive, a deeper understanding of their ecology and relationship with DOM is needed in the light of increased DOM inputs in coastal zones due to anthropogenic pressure.

Highlights

Biological dinitrogen (N2) fixation provides an important source of fixed nitrogen to fuel primary production in the oceans (Karl et al, 2002), being especially critical in areas devoid of other significant fixed nitrogen sources such as the oligotrophic subtropical gyres
colored DOM (CDOM) absorption at 442 nm and 350 nm (a442 and a350) presented lower values at station 2 and 3 as compared to the values recorded at Stations 1 and 4 (Table 1) which indicated a decrease in CDOM concentrations
CDOM at 442 nm and 350 nm is strongly photodegraded with a low aromaticity

Summary

Introduction

Biological dinitrogen (N2) fixation provides an important source of fixed nitrogen to fuel primary production in the oceans (Karl et al, 2002), being especially critical in areas devoid of other significant fixed nitrogen sources such as the oligotrophic subtropical gyres. Several filamentous cyanobacteria are able to obtain energy from dissolved organic matter-DOM- (Rippka et al, 1979), and several reports have shown that the most abundant photoautotrophs in the world’s oceans (Prochlorococcus and Synechococcus) harbor the genes necessary to use amino acids, peptides and sugars (Yelton et al, 2016). As evidence accumulates, it seems that the ability of using DOM as an alternative source of nutrients under limiting situations is common in various planktonic groups (Stoecker et al, 2017). Previous work has shown that N2 fixation activity is stimulated by DOM additions (Bonnet et al, 2013; Rahav et al, 2013, 2015), and correlates with labile DOM compounds in environments where non-cyanobacterial (non-photosynthetic) diazotrophs predominate, such as the aphotic mesopelagic layer (Benavides et al, 2015), or the surface ultraoligotrophic eastern Mediterranean Sea (Rahav et al, 2016)

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Discussion

Conclusion