Metacaspase involvement in programmed cell death of the marine cyanobacterium Trichodesmium

Abstract

Summary Metacaspases are cysteine specific proteases implicated in cell‐signalling, stress acclimation and programmed cell death (PCD) pathways in plants, fungi, protozoa, bacteria and algae. We investigated metacaspase‐like gene expression and biochemical activity in the bloom‐forming, N2‐fixing, marine cyanobacterium Trichodesmium, which undergoes PCD under low iron and high‐light stress. We examined these patterns with respect to in‐silico analyses of protein domain architectures that revealed a diverse array of regulatory domains within Trichodesmium metacaspases‐like (TeMC) proteins. Experimental manipulations of laboratory cultures and oceanic surface blooms of Trichodesmium from the South Pacific Ocean triggered PCD under Fe‐limitation and high light along with enhanced TeMC activity and upregulated expression of diverse TeMC representatives containing different regulatory domains. Furthermore, TeMC activity was significantly and positively correlated with caspase‐like activity, which has been routinely observed to increase with PCD induction in Trichodesmium. Although both TeMC and caspase‐like activities were stimulated upon PCD induction, inhibitor treatments of these proteolytic activities provided further evidence of largely distinct substrate specificities, even though some inhibitory crossover was observed. Our findings are the first results linking metacaspase expression and activity in PCD induced mortality in Trichodesmium. Yet, the role/s and specific activities of these different proteins remain to be elucidated.

Programmed Cell Death-Like and Accompanying Release of Microcystin in Freshwater Bloom-Forming Cyanobacterium Microcystis: From Identification to Ecological Relevance

“…A parallel elevation of the activity of caspase and the expression of metacaspase genes was observed in a marine cyanobacterium population that underwent apoptosis-like death [99]. In particular, the metacaspase TeMC of Trichodesmium was recently studied where it was found that the activity of metacaspase TeMC was significantly positively correlated with that of the caspase-like in the laboratory and field samples of Trichodesmium that underwent the apoptosis-like death [98]. This biochemical and physiological evidence directly linked the expression and activity of metacaspase with the occurrence of an apoptosis-like event in cyanobacterium, and this is similar to the PCD scenario in the marine diatom Phaeodactylum tricornutum [91] in which the PCD-associated role of metacaspase has been demonstrated by the overexpression and knockout experiment.…”

“…Of note, currently, research into the function of metacaspase in cyanobacteria remains in its infancy, and existing knowledge is based mainly on bioinformatics analysis [87,[94][95][96] and the biochemical and transcriptional exploration of limited laboratory and field samples [97], mainly in the freshwater bloom-forming cyanobacterium M. aeruginosa [56], and marine bloom-forming, filamentous cyanobacterium Trichodesmium [77,98]. The metacaspase gene is almost ubiquitous in the cyanobacteria except Prochlorococcus and some strains of Synechococcus; and it is relatively abundant in the filamentous diazotrophic cyanobacteria (e.g., Trichodesmium, Nostoc, and Anabaena).…”

Heat stress induces ferroptosis in a photosynthetic prokaryote

“…Metacaspases are cysteine specific proteases evolutionarily related to metazoan caspase proteases (Spungin et al, 2018) implicated in stress response and cell death in bacteria and phytoplankton. Caspase-like activities have been reported in Microcystis aeruginosa after treatments with pyrogallic acid, high light intensity or low phosphorus availability (He et al, 2016;Lu et al, 2017).…”

“…Trichodesmium spp. shows an increase in caspase-like activities under low iron and high-light stress (Asplund-Samuelsson et al, 2012;Berman-Frank et al, 2004Spungin et al, 2018).…”

“…Evidence has accumulated on controlled cell-death mechanisms triggered under unfavorable environmental conditions, such as nutrient deprivation, high-light-associated oxidative stress or osmotic stress that are indistinctly termed as PCD, apoptotic-like or necroticlike death. Such cell-death pathways involve morphological changes, accumulation of reactive oxygen species (ROS), DNA laddering, loss of plasma membrane integrity, and the coordinated participation of redox enzymes, metabolites and caspase-like proteases (Bidle, 2015;Durand et al, 2016;Spungin et al, 2018;Swapnil et al, 2017;Zhou et al, 2018). RCD has been proposed to optimize differentiation, dynamics and colony fitness in cyanobacteria (Bar-Zeev et al, 2013;Meeks and Elhai, 2002).…”