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Biochemical Characterization of a Novel Redox-Regulated Metacaspase in a Marine Diatom.

ABSTRACT: Programmed cell death (PCD) in marine microalgae was suggested to be one of the mechanisms that facilitates bloom demise, yet its molecular components in phytoplankton are unknown. Phytoplankton are completely lacking any of the canonical components of PCD, such as caspases, but possess metacaspases. Metacaspases were shown to regulate PCD in plants and some protists, but their roles in algae and other organisms are still elusive. Here, we identified and biochemically characterized a type III metacaspase from the model diatom Phaeodactylum tricornutum, termed PtMCA-IIIc. Through expression of recombinant PtMCA-IIIc in E. coli, we revealed that PtMCA-IIIc exhibits a calcium-dependent protease activity, including auto-processing and cleavage after arginine. Similar metacaspase activity was detected in P. tricornutum cell extracts. PtMCA-IIIc overexpressing cells exhibited higher metacaspase activity, while CRISPR/Cas9-mediated knockout cells had decreased metacaspase activity compared to WT cells. Site-directed mutagenesis of cysteines that were predicted to form a disulfide bond decreased recombinant PtMCA-IIIc activity, suggesting its enhancement under oxidizing conditions. One of those cysteines was oxidized, detected in redox proteomics, specifically in response to lethal concentrations of hydrogen peroxide and a diatom derived aldehyde. Phylogenetic analysis revealed that this cysteine-pair is unique and widespread among diatom type III metacaspases. The characterization of a cell death associated protein in diatoms provides insights into the evolutionary origins of PCD and its ecological significance in algal bloom dynamics.

SUBMITTER: Graff van Creveld S

PROVIDER: S-EPMC8455989 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Ocean-related global change has strongly affected the competition between key marine phytoplankton groups, such as diatoms and dinoflagellates, especially with the deleterious consequency of the increasing occurrence of harmful algal blooms. The dominance of diatoms generally shifts toward that of dinoflagellates in response to increasing temperature and reduced nutrient availability; however, contradictory findings have also been observed in certain sea areas. A key challenge in ecology and biogeochemistry is to quantitatively determine the effects of multiple environmental factors on the diatom-dinoflagellate community and the related changes in elemental and biochemical composition. Here, we test the interplay between temperature, nutrient concentrations and their ratios on marine diatom-dinoflagellate competition and chemical composition using bi-algal competition experiments. The ubiquitous diatom Phaeodactylum tricornutum and dinoflagellate Prorocentrum minimum were cultivated semi-continuously, provided with different N and P concentrations (three different levels) and ratios (10:1, 24:1, and 63:1 molar ratios) under three temperatures (12, 18, and 24°C). The responses of diatom-dinoflagellate competition were analyzed by a Lotka-Volterra model and quantified by generalized linear mixed models (GLMMs) and generalized additive models (GAMs). The changes in nutrient concentrations significantly affected diatom-dinoflagellate competition, causing a competitive superiority of the diatoms at high nutrient concentrations, independent of temperature and N:P supply ratios. Interestingly, the effect amplitude of nutrient concentrations varied with different temperatures, showing a switch back toward a competitive superiority of the dinoflagellates at the highest temperature and at very high nutrient concentrations. The ratios of particulate organic nitrogen to phosphorus showed significant negative correlations with increasing diatoms/dinoflagellates ratios, while lipid biomarkers (fatty acids and sterols) correlated positively with increasing diatoms/dinoflagellates ratios over the entire ranges of temperature, N and P concentrations and N:P ratios. Our results indicate that the integration of phytoplankton community structure and chemical composition provides an important step forward to quantitatively understand and predict how phytoplankton community changes affect ecosystem functions and biogeochemical cycles in the ocean.

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Biochemical Characterization of a Novel Redox-Regulated Metacaspase in a Marine Diatom.

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