Programmed cell death in diazotrophs and the fate of organic matter in the western tropical South Pacific Ocean during the OUTPACE cruise
Authors: Spungin Dina , Belkin Natalia , Foster Rachel A. , Stenegren Marcus , Caputo Andrea , Pujo-Pay Mireille , Leblond Nathalie , Dupouy Cécile , Bonnet Sophie , Berman-Frank Ilana 
Published: June 2018

Abstract. 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.