The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway

Abstract

We present experimental laboratory evidence and field observations of an autocatalyzed, programmed cell death (PCD) pathway in the nitrogen-fixing cyanobacterium Trichodesmium spp., which forms massive blooms in the subtropical and tropical oceans. The PCD pathway was induced in response to phosphorus and iron starvation as well as high irradiance and oxidative stress. Transmission electron microscopy revealed morphological degradation of internal components including thylakoids, carboxysomes, and gas vesicles, whereas the plasma membranes remained intact. Physiologically stressed cells displayed significantly elevated endonuclease activity and terminal d-UTP nick-end labeling. Nucleic acid degradation was concordant with increased immunoreactivity to human caspase-3 polyclonal antisera and enhanced cleavage of a caspase-specific substrate, DEVD. Caspase activity was positively correlated with mortality and was inhibited by the irreversible caspase inhibitor Z-VAD-FMK. A search of the Trichodesmium erythraeum genome identified several protein sequences containing a conserved caspase domain structure, including the histidine-and cysteine-containing catalytic diad found in true caspases, paracaspases, and metacaspases. Induction of PCD by caspase-like proteases in a bacterial photoautotroph with an ancient evolutionary history requires a reassessment about the origins and roles of cell death cascades. This process is a previously unappriciated mortality mechanism that can lead to the termination of natural Trichodesmium blooms and that can influence the fluxes of organic matter in the ocean.Planktonic marine cyanobacteria of the genus Trichodesmium form extensive blooms in the oligotrophic tropical and subtropical oceans, where they make significant contributions to global nitrogen fixation (Capone et al. 1997). Natural blooms and laboratory cultures of Trichodesmium often terminate abruptly, with cell lysis and biomass degradation occurring within 1-2 d (Ohki 1999). The mechanisms controlling the dramatic and abrupt termination of Trichodesmium blooms are not well understood, even though this termination drives nutrient flow and biogeochemical cycling of organic and inorganic matter produced by these organisms, including the redistribution of fixed nitrogen in the upper ocean and the flow of organic matter through ecosystem pathways like the grazer food chain, the microbial loop, and vertical sinking flux (Azam 1998).

Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa

“…These findings are in agreement with recent reports demonstrating that caspase activity is a common constituent not only in mammalian systems but in higher plants and lower algae as well (Korthout et al, 2000, Elbaz et al, 2002, Segovia et al, 2003. Our results, in conjunction with the recent caspase-like activity found in Trichodesmium (Berman-Frank et al, 2004), support the notion that PCD has an earlier evolutionary origin and broader significance than previously thought.…”

“…This process is termed oxidative cell stress (Van Camp et al, 1998). Aside from what has been documented in Trichodesmium (Berman-Frank et al, 2004), the involvement of oxidative stress on PCD has not been previously shown in other cyanobacterium.…”

“…Exposure of cells to low levels of physical and chemical stressors have been known to trigger apoptosis-like conditions in a variety of photosynthetic organisms including vascular plants (Lam and del Pozo, 2000;Lam et al, 2001), unicellular chlorophytes (Berges and Falkowski, 1998;Segovia et al, 2003), dinoflagellates (Vardi et al, 1999;, and cyanobacteria (Berman-Frank et al, 2004). Characteristics of cells undergoing PCD include chromatin condensation, shrinkage of the nucleus and cytoplasm (Danon et al, 2000), and ordered DNA fragmentation (Hoeberichts and Woitering, 2003).…”

“…The most recent findings of caspase activity in the marine cyanobacterium Trichodesmium spp. (Berman-Frank et al, 2004) prompted our investigation to utilize caspase activity as a proxy for PCD in M. aeruginosa (Hug et al, 1999, Liu et al, 1999. We demonstrated that caspase activity in stressed M. aeruginosa cells might be responsible for the onset of PCD when induced with H 2 O 2 as a result of oxidative stress (Fig.…”

Population dynamics and environmental conditions affecting Trichodesmium spp. (filamentous cyanobacteria) blooms in the south–west lagoon of New Caledonia

“…already by Lenes et al (2005) and Moutin et al (2005). This process could reduce growth rates, in a 483 way opposite to the nutrient increase effect described above, or induce mortality through a 484 "Programmed Cell Death" (PCD) pathway (Berman-Frank et al, 2004, 2007. Viral lysis (Ohki, 485 1999) and PCD, caused by other factors than nutrient depletion, as listed by Berman-Franck et al 486 (2004), are other possible processes.…”