Biogeochemical and biological impacts of diazotroph blooms in a low-nutrient, low-chlorophyll ecosystem: synthesis from the VAHINE mesocosm experiment (New Caledonia)

Abstract

Abstract. In marine ecosystems, biological N 2 fixation provides the predominant external source of nitrogen (N; 140 ± 50 Tg N yr −1 ), contributing more than atmospheric and riverine inputs to the N supply. Yet the fate and magnitude of the newly fixed N, or diazotroph-derived N (hereafter named DDN) in marine ecosystems is poorly understood. Moreover, whether the DDN is preferentially and directly exported out of the photic zone, recycled by the microbial loop and/or transferred into larger organisms remains unclear. These questions were investigated in the framework of the VAHINE (VAriability of vertical and tropHIc transfer of diazotroph derived N in the south wEst Pacific) project. Triplicate large volume (∼ 50 m 3 ) mesocosms were deployed in the tropical south-west Pacific coastal ocean (New Caledonia). The mesocosms were intentionally fertilized with ∼ 0.8 µM dissolved inorganic phosphorus (DIP) at the start of the experiment to stimulate diazotrophy. A total of 47 stocks, fluxes, enzymatic activities and diversity parameters were measured daily inside and outside the mesocosms by the 40 scientists involved in the project. The experiment lasted for 23 days and was characterized by two distinct and successive diazotroph blooms: a dominance of diatom-diazotroph associations (DDAs) during the first half of the experiment (days 2-14) followed by a bloom of unicellular cyanobacterial lineage C (UCYN-C during the second half of the experiment (days 15-23). These conditions provided a unique opportunity to compare the DDN transfer and export efficiency associated with different diazotrophs. Here we summarize the major experimental and modelling results obtained during the project and described in the VAHINE special issue, in particular those regarding the evolution of the main standing stocks, fluxes and biological characteristics over the 23-day experiment, the contribution of N 2 fixation to export fluxes, the DDN released to dissolved pool and its transfer to the planktonic food web (bacteria, phytoplankton, zooplankton). We then apply our Eco3M modelling platform to further infer the fate of DDN in the ecosystem and the role of N 2 fixation on productivity, food web structure and carbon export. Recommendations for future work are finally provided in the conclusion section.

Preface: The Oligotrophy to the UlTra-oligotrophy PACific Experiment (OUTPACE cruise, 18 February to 3 April 2015)

“…This result is in accordance with high export fluxes measured in the tropical North Atlantic when the diazotroph community is dominated by DDAs (Subramaniam et al, 2008;White et al, 2012). More recently, Berthelot et al (2015) and Bonnet et al (2016a) studied the fate of a bloom of unicellular diazotrophs from Group C (UCYN-C) during a mesocosm experiment in the New Caledonia lagoon after a phosphate enrichment and revealed that ∼ 10 % of UCYN-C from the water column was exported to the particle traps daily, representing as much as 22.4 ± 5.5 % of the total POC exported at the height of the UCYN-C bloom. A δ 15 N budget performed in the mesocosms confirmed the high contribution of N 2 fixation (56 %; Knapp et al, 2016) to export compared to other tropical and subtropical regions where active N 2 fixation contributes 10 to 25 % to export production (e.g., Altabet, 1988;Knapp et al, 2005) and exceptionally up to 92 % in the Arabian Sea (Gandhi et al, 2011;Kumar et al, 2017).…”

“…Mechanistically, the vertical downward flux was enabled by the aggregation of the small (5.7 ± 0.8 µm) UCYN-C cells into large (100-500 µm) aggregates. In addition to direct export of diazotrophs, the use of nanoSIMS (nanoscale secondary ion mass spectrometry) enabled the tracking of the fate of 15 N from both Trichodesmium (Bonnet et al, 2016b) and UCYN blooms (Berthelot et al, 2015;Bonnet et al, 2016c) and demonstrated that ∼ 8 % of N originating from N 2 fixation is quickly transferred to non-diazotrophic plankton, in particular diatoms, i.e., efficient C exporters to depth (Nelson et al, 1995) during Trichodesmium blooms (Bonnet et al, 2016b). This reveals that N 2 fixation can fuel large-size nondiazotrophic plankton growth in the water column, suggesting an indirect export pathway of organic matter sustained by N 2 fixation in the oligotrophic ocean.…”

Protistal Grazers Increase Grazing on Unicellular Cyanobacteria Diazotroph at Night

“…UCYN-C is the least studied and descriptions about UCYN-C are rare. These three groups of UCDs may form blooms or dominate diazotrophic community in oligotrophic waters (Robidart et al, 2014;Bonnet et al, 2016;Wilson et al, 2017). Among the groups of the UCDs, only the UCYN-B (i.e., Crocosphaera watsonii) is cultivated.…”

Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies

“…Trichodesmium has a ubiquitous distribution throughout tropical and subtropical oceans where it contributes substantial amounts of new nitrogen (N) to the oligotrophic near-surface ocean through dinitrogen (N 2 ) fixation [1,2]. In the North Pacific Subtropical Gyre, Trichodesmium is suggested to account for up to half of the biologically fixed N 2 [3], which generally mitigates N limitation, and even promotes the growth of a broader plankton community [4][5][6] and eventual carbon (C) export to the deep sea [7][8][9]. Trichodesmium grows as filaments, referred to as trichomes, which at times aggregate as millimetre-sized spindle-shaped (tufts) or spherical (puffs) colonies [10], often forming conspicuous blooms which can be observed from space [11].…”