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

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.

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

10.5194/bg-2018-3 ◽

2018 ◽

Cited By ~ 1

Author(s):

Dina Spungin ◽

Natalia Belkin ◽

Rachel Foster ◽

Marcus Stenegren ◽

Andrea Caputo ◽

...

Keyword(s):

Cell Death ◽

Organic Matter ◽

Pacific Ocean ◽

Programmed Cell Death ◽

South Pacific ◽

Sediment Traps ◽

Vertical Flux ◽

Physiological Status ◽

Chl A ◽

South Pacific Ocean

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 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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Supplementary material to "Programmed cell death in diazotrophs and the fate of organic matter in the Western Tropical South Pacific Ocean during the OUTPACE cruise"

10.5194/bg-2018-3-supplement ◽

2018 ◽

Author(s):

Dina Spungin ◽

Natalia Belkin ◽

Rachel Foster ◽

Marcus Stenegren ◽

Andrea Caputo ◽

...

Keyword(s):

Cell Death ◽

Organic Matter ◽

Pacific Ocean ◽

Programmed Cell Death ◽

South Pacific ◽

South Pacific Ocean ◽

Supplementary Material

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INTERACTIVE COMMENT on "Programmed cell death in diazotrophs and the fate of organic matter in the Western Tropical South Pacific Ocean during the OUTPACE cruise" By Spungin et al.

10.5194/bg-2018-3-rc2 ◽

2018 ◽

Author(s):

Anonymous

Keyword(s):

Cell Death ◽

Organic Matter ◽

Pacific Ocean ◽

Programmed Cell Death ◽

South Pacific ◽

South Pacific Ocean

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Biochemical characteristics and bacterial community structure of the sea surface microlayer in the South Pacific Ocean

Biogeosciences Discussions ◽

10.5194/bgd-4-2809-2007 ◽

2007 ◽

Vol 4 (4) ◽

pp. 2809-2844 ◽

Cited By ~ 6

Author(s):

I. Obernosterer ◽

P. Catala ◽

R. Lami ◽

J. Caparros ◽

J. Ras ◽

...

Keyword(s):

Organic Matter ◽

Microbial Community ◽

Pacific Ocean ◽

Organic Carbon ◽

South Pacific ◽

Leucine Incorporation ◽

Surface Microlayer ◽

South Pacific Ocean ◽

Subsurface Waters ◽

Card Fish

Abstract. The chemical and biological characteristics of the surface microlayer were determined during a transect across the South Pacific Ocean in October-December 2004. Concentrations of particulate organic carbon (1.3 to 7.6-fold) and nitrogen (1.4 to 7), and POC:PON ratios were consistently higher in the surface microlayer as compared to subsurface waters (5 m). The large variability in particulate organic matter enrichment was negatively correlated to wind speed. No enhanced concentrations of dissolved organic carbon were detectable in the surface microlayer as compared to 5 m, but chromophoric dissolved organic matter was markedly enriched (by 2 to 4-fold) at all sites. Based on pigment analysis and cell counts, no consistent enrichment of any of the major components of the autotrophic and heterotrophic microbial community was detectable. CE-SSCP fingerprints and CARD FISH revealed that the bacterial communities present in the surface microlayer had close similarity (>76%) to those in subsurface waters. By contrast, bacterial heterotrophic production (3H-leucine incorporation) was consistently lower in the surface microlayer than in subsurface waters. By applying CARD-FISH and microautoradiography, we observed that Bacteroidetes and Gammaproteobacteria dominated leucine uptake in the surface microlayer, while in subsurface waters Bacteroidetes and Alphaproteobacteria were the major groups accounting for leucine incorporation. Our results demonstrate that the microbial community in the surface microlayer closely resembles that of the surface waters of the open ocean. However, even short time periods in the surface microlayer result in differences in bacterial groups accounting for leucine incorporation, probably as a response to the differences in the physical and chemical nature of the two layers.

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Biochemical characteristics and bacterial community structure of the sea surface microlayer in the South Pacific Ocean

Biogeosciences ◽

10.5194/bg-5-693-2008 ◽

2008 ◽

Vol 5 (3) ◽

pp. 693-705 ◽

Cited By ~ 46

Author(s):

I. Obernosterer ◽

P. Catala ◽

R. Lami ◽

J. Caparros ◽

J. Ras ◽

...

Keyword(s):

Organic Matter ◽

Microbial Community ◽

Pacific Ocean ◽

Organic Carbon ◽

Surface Waters ◽

South Pacific ◽

Leucine Incorporation ◽

Surface Microlayer ◽

South Pacific Ocean ◽

Card Fish

Abstract. The chemical and biological characteristics of the surface microlayer were determined during a transect across the South Pacific Ocean in October-December 2004. Concentrations of particulate organic carbon (1.3 to 7.6-fold) and nitrogen (1.4 to 7-fold), and POC:PON ratios were consistently higher in the surface microlayer as compared to surface waters (5 m). The large variability in particulate organic matter enrichment was negatively correlated to wind speed. No enhanced concentrations of dissolved organic carbon were detectable in the surface microlayer as compared to 5 m, but chromophoric dissolved organic matter was markedly enriched (by 2 to 4-fold) at all sites. Based on pigment analysis and cell counts, no consistent enrichment of any of the major components of the autotrophic and heterotrophic microbial community was detectable. CE-SSCP fingerprints and CARD FISH revealed that the bacterial communities present in the surface microlayer had close similarity (>76%) to those in surface waters. By contrast, bacterial heterotrophic production (3H-leucine incorporation) was consistently lower in the surface microlayer than in surface waters. By applying CARD-FISH and microautoradiography, we observed that Bacteroidetes and Gammaproteobacteria dominated leucine uptake in the surface microlayer, while in surface waters Bacteroidetes and Alphaproteobacteria were the major groups accounting for leucine incorporation. Our results demonstrate that the microbial community in the surface microlayer closely resembles that of the surface waters of the open ocean. Even a short residence in the surface microlayer influences leucine incorporation by different bacterial groups, probably as a response to the differences in the physical and chemical nature of the two layers.

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Massive export of diazotrophs across the tropical south Pacific Ocean

10.1101/2021.05.07.442706 ◽

2021 ◽

Author(s):

Sophie Bonnet ◽

Mar Benavides ◽

Mercedes Camps ◽

Antoine Torremocha ◽

Olivier Grosso ◽

...

Keyword(s):

Pacific Ocean ◽

South Pacific ◽

Sediment Traps ◽

Marine Snow ◽

Turnover Rates ◽

Sequencing Data ◽

Particulate Nitrogen ◽

Nitrogen Export ◽

South Pacific Ocean ◽

Species Specific

Diazotrophs are widespread microorganisms that regulate marine productivity in 60% of our oceans by alleviating nitrogen limitation. Yet, their contribution to organic carbon and nitrogen export fluxes has never been quantified, making an assessment of their impact on the biological carbon pump impossible. Here, we examine species-specific fates of several groups of globally-distributed unicellular (UCYN) and filamentous diazotrophs in the mesopelagic ocean. We used an innovative approach consisting of the combined deployment of surface-tethered drifting sediment traps, Marine Snow Catcher, and Bottle-net, in which we performed nifH sequencing and quantitative PCR on major diazotroph groups across the subtropical South Pacific Ocean. nifH sequencing data from sediment traps deployed at 170 m, 270 m and 1000 m provide clear evidence that cyanobacterial and non-cyanobacterial diazotrophs are systematically present in sinking particles down to 1000 m, with export fluxes being the highest for the UCYN-A1 symbiosis, followed by UCYN-B or Trichodesmium (depending on station and depth), Gamma A and UCYN-C. Specific export turnover rates (a metric similar to the export efficiency adapted to organisms) point to a more efficient export of UCYN groups relative to the filamentous Trichodesmium. This is further confirmed by Marine Snow catcher data showing that the proportion of sinking cells was significantly higher for UCYN compared to Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were indeed recurrently found embedded in large (> 50 micrometers) seemingly organic aggregates, or organized into clusters of tens to hundreds of cells linked by an extracellular matrix, facilitating the export. Overall, diazotrophs accounted for 6-13% (170 m) to 45-100% (1000 m) of the total particulate nitrogen export fluxes in our study. We thus conclude that diazotrophs are important contributors to carbon sequestration in the subtropical South Pacific Ocean and need to be considered in future studies to improve the accuracy of current regional and global estimates of export.

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