Programmed cell death in diazotrophs and the fate of organic matter in the western tropical South Pacific Ocean during the OUTPACE cruise

Type Article
Date 2018-01-11
Language English
Author(s) Spungin Dina1, Belkin Natalia1, Foster Rachel2, Stenegren Marcus2, Caputo Andrea2, Pujo-Pay Mireille3, Leblond Nathalie4, Dupouy Cecile4, Bonnet Sophie5, Berman-Frank Ilana1
Affiliation(s) 1 : The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel
2 : Stockholm University, Department of Ecology, Environment and Plant Sciences. Stockholm, Sweden
3 : Laboratoire d’Océanographie Microbienne - UMR 7321, CNRS - Sorbonne Universités, UPMC Univ Paris 06, Observatoire Océanologique, 66650 Banyuls-sur-mer, France
4 : Observatoire Océanologique de Villefranche, Laboratoire d’Océanographie de Villefranche, UMR 7093, Villefranche-sur Mer, France
5 : Aix-Marseille Univ., Univ. Toulon, CNRS/INSU, IRD, UM 110, Mediterranean Institute of Oceanography (MIO) UM 110, 13288, Noumea, New Caledonia
Source Biogeosciences (1726-4170) (Copernicus GmbH), 2018-01-11 , Vol. 15 , N. 12 , P. 3893-3908
DOI 10.5194/bg-2018-3
Note Special issue Interactions between planktonic organisms and biogeochemical cycles across trophic and N2 fixation gradients in the western tropical South Pacific Ocean: a multidisciplinary approach (OUTPACE experiment) Editor(s): T. Moutin, S. Bonnet, K. Richards, D. G. Capone, E. Marañón, and L. Mémery

The fate of diazotroph (N2 fixers) derived carbon (C) and nitrogen (N) and their contribution to vertical export of C and N in the Western Tropical South Pacific Ocean was studied in OUTPACE (Oligotrophy to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine whether autocatalytic programmed cell death (PCD) is an important mechanism affecting diazotroph mortality and a factor regulating the vertical flux of organic matter and thus the fate of the blooms. We sampled at three long duration (LD) stations of 5 days each (LDA, LDB, and LDC) where drifting sediment traps were deployed at 150, 325 and 500 m depths. LDA and LDB were characterized by high chlorophyll a (Chl a) concentrations (0.2–0.6 µg L−1) and dominated by dense biomass of Trichodesmium as well as UCYN-B and diatom-diazotroph associations (Rhizosolenia with Richelia-detected by microscopy and het-1 nifH copies). Station LDC was located at an ultra-oligotrophic area of the South Pacific gyre with extremely low Chl a concentration (~ 0.02 µg L−1) with limited biomass of diazotrophs predominantly the unicellular UCYN-B. Our measurements of biomass from LDA and LDB yielded high activities of caspase-like and metacaspase proteases that are indicative of PCD in Trichodesmium and other phytoplankton. Metacaspase activity, reported here for the first time from oceanic populations, was highest at the surface of both LDA and LDB, where we also obtained high concentrations of transparent exopolymeric particles (TEP). TEP was negatively correlated with dissolved inorganic phosphorus and positively coupled to both the DOC and POC pools reflecting the typically high production of TEP under nutrient stress and its role as a source of sticky carbon facilitating aggregation and rapid vertical sinking. Evidence for bloom decline was observed at both LDA and LDB. However, the physiological status and rates of decline of the blooms differed between the stations, influencing the amount of accumulated diazotrophic organic matter and mass flux observed in the traps during our experimental time frame. At LDA sediment traps contained the greatest export of particulate matter and significant numbers of both intact and decaying Trichodesmium, UCYN-B, and het-1 compared to LDB where the bloom decline began only 2 days prior to leaving the station and to LDC where no evidence for bloom decline was seen. Substantiating previous findings from laboratory cultures linking PCD to carbon export in Trichodesmium, our results from OUTPACE indicate that induction of PCD by nutrient limitation in high biomass blooms such as Trichodesmium or diatom-diazotroph associations combined with high TEP production facilitates cellular aggregation and bloom termination, and expedites vertical flux to depth

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Spungin Dina, Belkin Natalia, Foster Rachel, Stenegren Marcus, Caputo Andrea, Pujo-Pay Mireille, Leblond Nathalie, Dupouy Cecile, Bonnet Sophie, Berman-Frank Ilana (2018). Programmed cell death in diazotrophs and the fate of organic matter in the western tropical South Pacific Ocean during the OUTPACE cruise. Biogeosciences, 15(12), 3893-3908. Publisher's official version : , Open Access version :