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

Dina Spungin, Natalia Belkin, Rachel A. Foster, Marcus Stenegren, Andrea Caputo, Mireille Pujo-Pay, Nathalie Leblond, Ccile Dupouy, Sophie Bonnet, Ilana Berman-Frank

Research output: Contribution to journalArticlepeer-review


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 during OUTPACE (Oligotrophy to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine whether autocatalytic programmed cell death (PCD), occurring in some diazotrophs, 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 depth. 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 the filamentous cyanobacterium 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 were negatively correlated with dissolved inorganic phosphorus and positively coupled to both the dissolved and particulate organic carbon pools. Our results reflect the increase in TEP production 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 or bloom decline was seen. Substantiating previous findings from laboratory cultures linking PCD to carbon export in Trichodesmium, our results from OUTPACE indicate that nutrient limitation may induce PCD in high biomass blooms such as displayed by Trichodesmium or diatom-diazotroph associations. Furthermore, PCD combined with high TEP production will tend to facilitate cellular aggregation and bloom termination and will expedite vertical flux to depth.

Original languageEnglish
Pages (from-to)3893-3908
Number of pages16
Issue number12
StatePublished - 28 Jun 2018

Bibliographical note

Funding Information:
Acknowledgements. This research is a contribution of the OUTPACE (Oligotrophy from UlTra-oligotrophy PACific Experiment) project (, last access: June 2018) funded by the Agence Nationale de la Recherche (grant ANR-14-CE01-0007-01), the LEFE-CyBER program (CNRS-INSU), the Institut de Recherche pour le Développement (IRD), the GOPS program (IRD) and the CNES (BC T23, ZBC 4500048836). The OUTPACE cruise ( was managed by the MIO (OSU Institut Pytheas, AMU) from Marseilles (France). The authors thank the crew of the R/V L’Atalante for outstanding shipboard operations. Gilles Rougier and Marc Picheral are warmly thanked for their efficient help in CTD rosette management and data processing, as is Catherine Schmechtig for the LEFE-CyBER database management. Aurelia Lozingot is acknowledged for the administrative work. All data and metadata are available at the following web address: (last access: June 2018). We thank Olivier Grosso (MIO) and Sandra Hélias (MIO) for the phosphate data and François Catlotti (MIO) for the zooplankton data. The ocean color satellite products were provided by CLS in the framework of the CNES-OUTPACE project (PI Andrea Michelangelo Doglioli) and the video is courtesy of Alain de Verneil. Rachel A. Foster acknowledges Stina Höglund and the Image Facility of Stockholm University and the Wenner-Gren Institute for access and assistance in confocal microscopy. The participation of Natalia Belkin, Dina Spungin and Ilana Berman-Frank in the OUTPACE experiment was supported through a collaborative grant to Ilana Berman-Frank and Sophie Bonnet from Israel Ministry of Science and Technology Israel and the High Council for Science and Technology (HCST) France grant 2012/3-9246 and United States–Israel Binational Science Foundation (BSF) grant no. 2008048 to Ilana Berman-Frank. Rachel A. Foster was funded by the Knut and Alice Wallenberg Stiftelse and acknowledges the helpful assistance of Lotta Bernt-zon. This work is in partial fulfillment of the requirements for a PhD thesis for Dina Spungin at Bar-Ilan University.

Publisher Copyright:
© 2018 Author(s).

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Earth-Surface Processes


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