Localization and Role of Manganese Superoxide Dismutase in a Marine Diatom

Wolfe-Simon, Felisa; Starovoytov, Valentin; Reinfelder, John R.; Schofield, Oscar; Falkowski, Paul G.

doi:10.1104/pp.106.088963

Cited by 81 publications

(67 citation statements)

References 64 publications

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“…Dramatic reductions in photosynthetic efficiency under Fe starvation signify uncoupled electron flow through photosystem II, ultimately leading to the production of ROS in oxygenic photoautotrophs (6), which in turn induces PCD (23,60). Indeed, we found highly elevated expression of a chloroplast-localized, Mn-SOD (64) in Fe-starved cell extracts by using Western blot analysis, diagnostic of a subcellular response to elevated ROS (48,64). PCD also has been observed under Fe starvation for the cyanobacterium Trichodesmium sp.…”

supporting

confidence: 54%

“…Transfer buffer consisted of (per 500 ml of MilliQ water) 15.0 g Tris base, 72.0 g glycine, and 5.0 g SDS. Membranes were probed with polyclonal antisera raised against a purified, recombinant metacaspase protein from Emiliania huxleyi (EhMC; titer, 1:500) (11), preimmune antisera (collected from the same rabbits prior to injection with purified EhMC; 1:500), or polyclonal antisera to purified recombinant T. pseudonana manganese superoxide dismutase (Mn-SOD; titer, 1:3,000) (64). Polyclonal goat anti-rabbit immunoglobulin G (IgG) horseradish peroxidase (HRP) (titer, 1:10,000; Pierce) and an HRP chemiluminescent substrate (Bio-Rad) was used for detection.…”

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confidence: 99%

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Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana

2008

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In the modern ocean, phytoplankton maintain extremely high primary production/biomass ratios, indicating that they bloom, die, and are replaced weekly. The molecular mechanisms regulating cellular mortality and turnover are largely unknown, even though they effectively short-circuit carbon export to the deep ocean and channel primary productivity to microbial food webs. Here, we present morphological, biochemical, and molecular evidence of caspase-mediated, autocatalytic programmed cell death (PCD) in the diatom Thalassiosira pseudonana in response to iron starvation. Transmission electron microscopy revealed internal degradation of nuclear, chloroplastic, and mitochondrial organelles, all while the plasma membranes remained intact. Cellular degradation was concomitant with dramatic decreases in photosynthetic efficiency, externalization of phosphatidylserine, and significantly elevated caspase-specific activity, with the addition of a broad-spectrum caspase inhibitor rescuing cells from death. A search of the T. pseudonana genome identified six distinct putative metacaspases containing a conserved caspase domain structure. Phytoplankton, or unicellular photoautotrophs that drift with the currents, represent the base of most marine food webs. Although they account for Ͻ1% of the Earth's biomass, they are responsible for nearly 50% of global annual carbonbased primary productivity (31). The steady-state maintenance of such a high production/biomass ratio implies that, on average, these organisms grow, die, and are replaced once every week (57). Substantial cell death via lysis documented in field populations of phytoplankton (1, 2, 14, 16, 58) challenges the long-held misconception among biological oceanographers that phytoplankton are immortal unless eaten by zooplankton grazers and highlights the importance of key death processes to marine ecosystems. Unfortunately, the mechanisms regulating phytoplankton cell death have received relatively little attention, even though they serve to couple primary production to microbial food webs (10), effectively short-circuiting carbon export to the deep ocean and stimulating upper ocean biogeochemical cycling (4, 10).Autocatalytic cell death triggered by specific environmental stresses (e.g., cell age, nutrient deprivation, high light levels, oxidative stress, and UV exposure) in prokaryotic and eukaryotic unicellular phytoplankton (6,10,42,51,59) provides a mechanism to explain the high lysis rates independent of viral attack or grazing. This cellular self destruction is analogous to programmed cell death (PCD) in multicellular organisms, a form of autocatalytic cell suicide in which an endogenous biochemical pathway leads to apoptotic-like morphological changes and, ultimately, cellular dissolution. PCD involves the expression and biochemical coordination of specialized cellular machinery, such as receptors, adaptors, signal kinases, proteases, and nuclear factors. A specific class of intracellular cysteinyl aspartate-specific proteases, termed caspases, is of particular...

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confidence: 54%

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confidence: 99%

Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana

2008

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“…SODs are vital to photosynthetic organisms, scavenging toxic superoxide radicals generated by multiple metabolic pathways including photosynthesis. Isoforms use different metals at the active site, influencing trace metal requirements (24). Presence of sodN, which encodes Ni-SOD, corresponds with absence of Fe-SOD-encoding genes in many marine bacterial genomes, and Ni-SOD seems to be more prevalent in open-ocean strains (25).…”

Section: Resultsmentioning

confidence: 99%

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Cuvelier

Allen

Monier

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

270

269

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Among eukaryotes, four major phytoplankton lineages are responsible for marine photosynthesis; prymnesiophytes, alveolates, stramenopiles, and prasinophytes. Contributions by individual taxa, however, are not well known, and genomes have been analyzed from only the latter two lineages. Tiny "picoplanktonic" members of the prymnesiophyte lineage have long been inferred to be ecologically important but remain poorly characterized. Here, we examine pico-prymnesiophyte evolutionary history and ecology using cultivation-independent methods. 18S rRNA gene analysis showed picoprymnesiophytes belonged to broadly distributed uncultivated taxa. Therefore, we used targeted metagenomics to analyze uncultured pico-prymnesiophytes sorted by flow cytometry from subtropical North Atlantic waters. The data reveal a composite nuclear-encoded gene repertoire with strong green-lineage affiliations, which contrasts with the evolutionary history indicated by the plastid genome. Measured pico-prymnesiophyte growth rates were rapid in this region, resulting in primary production contributions similar to the cyanobacterium Prochlorococcus. On average, picoprymnesiophytes formed 25% of global picophytoplankton biomass, with differing contributions in five biogeographical provinces spanning tropical to subpolar systems. Elements likely contributing to success include high gene density and genes potentially involved in defense and nutrient uptake. Our findings have implications reaching beyond pico-prymnesiophytes, to the prasinophytes and stramenopiles. For example, prevalence of putative Ni-containing superoxide dismutases (SODs), instead of Fe-containing SODs, seems to be a common adaptation among eukaryotic phytoplankton for reducing Fe quotas in low-Fe modern oceans. Moreover, highly mosaic gene repertoires, although compositionally distinct for each major eukaryotic lineage, now seem to be an underlying facet of successful marine phytoplankton.comparative genomics | primary production | prymnesiophytes | marine photosynthesis | haptophytes G lobal primary production is partitioned equally among terrestrial and marine ecosystems, each accounting for ≈50 gigatons of carbon per year (1). The phytoplankton responsible for marine primary production include the cyanobacteria, Prochlorococcus and Synechococcus, and a multitude of eukaryotic phytoplankton, such as diatoms, dinoflagellates, prasinophytes, and prymnesiophytes (2-4). Most oceanic phytoplankton are "picoplanktonic" (<2-3 μm diameter) and have high surface area to volume ratios, an advantage in open-ocean low-nutrient conditions (5-8). Despite the importance of eukaryotic phytoplankton to carbon cycling only six genomes have been sequenced and analyzed comparatively, all being from diatoms and prasinophytes. These revealed greater differentiation than anticipated on the basis of 18S rRNA gene analyses (9-11). The observed genomic divergence is associated with major differences in physiology and niche adaptation (10).Pigment-based estimates indicate that prymnesiophytes, also know...

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“…To investigate the effect of virus infection on an early antioxidant response, 2 sod2 paralogs and apx were also selected for monitoring. The precise site of activity of SOD2 (MnSOD) in E. huxleyi is unknown, and localization of various SOD isoforms vary greatly among photosynthetic organisms (Kitayama et al 1999, Li et al 2002, Pilon et al 2011; MnSOD is localized in the chloroplasts in the marine diatom Thalassiosira pseudo nana (Wolfe-Simon et al 2006) as a low-iron adaptation. Like T. pseudonana, the E. huxleyi pangenome lacks FeSOD isoforms (Read et al 2013), possessing instead 2 putative MnSOD paralogs based on the presence of 2 conserved residues at the active site cavity (Abreu & Cabelli 2010) as well as 2 putative Cu/ZnSOD paralogs.…”

Section: Selection Of Genes Involved In Psii Repair and Antioxidant Fmentioning

confidence: 99%

Differential gene expression is tied to photochemical efficiency reduction in virally infected Emiliania huxleyi

Gilg¹,

Archer²,

Floge³

et al. 2016

Mar. Ecol. Prog. Ser.

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Localization and Role of Manganese Superoxide Dismutase in a Marine Diatom

Cited by 81 publications

References 64 publications

Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana

Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Differential gene expression is tied to photochemical efficiency reduction in virally infected Emiliania huxleyi

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