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

Abstract

Specialized prokaryotes performing biological dinitrogen (N 2 ) 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 N 2 fixation. Here we added the photosynthesis inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) to estimate the N 2 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 N 2 fixation (samples not amended with DCMU) ranged from 0.66 to 1.32 nmol N L −1 d −1 . The addition of DCMU reduced N 2 fixation by >90%, suggesting that the contribution of heterotrophic diazotrophs to overall N 2 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. We tested the response of diazotrophs (in terms of nifH gene expression and bulk N 2 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 N 2 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.

Dissolved organic matter stimulates N2 fixation and nifH gene expression in Trichodesmium

“…Still, N 2 fixation models are mostly parameterized for Trichodesmium and its iron and phosphorus needs (Monteiro, Dutkiewicz and Follows 2011;Dutkiewicz et al 2012). The present study, and other recent studies (Benavides et al 2017(Benavides et al , 2018Rahav and Bar-Zeev 2017), indicate that taking the mixotrophic potential of diazotrophs into account will improve our understanding of their biogeography and seasonality. A development of biogeochemical models should in this context improve our ability to predict pools and fluxes of nitrogen in the global ocean.…”

“…The undetectable nifH gene expression at this station is likely explained by the fact that our sampling took place at noon, while UCYN-B primarily express nifH at night (Church et al 2005b). UCYN (Benavides et al 2018).…”

Untreated sewage outfalls do not promote Trichodesmium blooms in the coasts of the Canary Islands

“…4 b,c). Trichodesmium could have responded positively to DOP inputs as observed elsewhere 31 , 32 , but in our study DOP concentrations of clear and sewage waters were not significantly different (Table 1 ). We cannot exclude however, the possibility that there were toxic components in sewage waters that may have locally promoted the death of Trichodesmium close to the coast, as wastewaters are known to impair the metabolic activity of phytoplankton 33 .…”

Seasonal Shifts in Diazotrophs Players: Patterns Observed Over a Two-Year Time Series in the New Caledonian Lagoon (Western Tropical South Pacific Ocean)

“…Finally, due to the inability of UCYN-A to fix inorganic carbon (Tripp et al, 2010), it is likely that the high abundance of the symbiosis in lagoon waters is sustained by photosynthates of the haptophyte host and/or labile dissolved organic matter input from the Dumbea River. Indeed, a recent study reported an increase in N 2 fixation rates and UCYN-A nifH gene expression in the mouth of the Dumbea River compared to waters located close to the reef (Benavides et al, 2018). Surprisingly, Trichodesmium abundances were lower than those of the UCYN-A symbiosis (Figure 4).…”