Abstract
A genome-wide investigation of the anhydrobiotic cyanobacterium Chroococcidiopsis sp. CCMEE 029 identified three genes coding superoxide dismutases (SODs) annotated as MnSODs (SodA2.1 and SodA2.2) and Cu/ZnSOD (SodC) as suggested by the presence of metal-binding motifs and conserved sequences. Structural bioinformatics analysis of the retrieved sequences yielded modeled MnSODs and Cu/ZnSOD structures that were fully compatible with their functional role. A signal-peptide bioinformatics prediction identified a Tat signal peptide at the N-terminus of the SodA2.1 that highlighted its transport across the thylakoid/cytoplasmic membranes and release in the periplasm/thylakoid lumen. Homologs of the Tat transport system were identified in Chroococcidiopsis sp. CCMEE 029, and the molecular docking simulation confirmed the interaction between the signal peptide of the SodA2.1 and the modeled TatC receptor, thus supporting the SodA2.1 translocation across the thylakoid/cytoplasmic membranes. No signal peptide was predicted for the MnSOD (SodA2.2) and Cu/ZnSOD, thus suggesting their occurrence as cytoplasmic proteins. No FeSOD homologs were identified in Chroococcidiopsis sp. CCMEE 029, a feature that might contribute to its desiccation tolerance since iron produces hydroxyl radical via the Fenton reaction. The overall-overexpression in response to desiccation of the three identified SOD-coding genes highlighted the role of SODs in the antioxidant enzymatic defense of this anhydrobiotic cyanobacterium. The periplasmic MnSOD protected the cell envelope against oxidative damage, the MnSOD localized in the thylakoid lumen scavengered superoxide anion radical produced during the photosynthesis, while the cytoplasmic MnSOD and Cu/ZnSOD reinforced the defense against reactive oxygen species generated at the onset of desiccation. Results contribute to decipher the desiccation-tolerance mechanisms of this cyanobacterium and allow the investigation of its oxidative stress response during future space experiments in low Earth orbit and beyond.
Highlights
Water removal induces damage at every level of the cellular organization, including membrane phase transition and oxidative damage to lipids, proteins, and DNA that are lethal to the majority of organisms (França et al, 2007)
The sodC was modeled using as a template the Cu/ZnSOD structure (PDB ID: 3KBF) from Caenorhabditis elegans, sharing about 40% of identity with the query
In order to unravel the role of superoxide dismutases (SODs) in the antioxidant defense of the anhydrobiotic cyanobacterium Chroococcidiopsis sp
Summary
Water removal induces damage at every level of the cellular organization, including membrane phase transition and oxidative damage to lipids, proteins, and DNA that are lethal to the majority of organisms (França et al, 2007). Among anhydrobiotic cyanobacteria Chroococcidiopsis strains isolated from hot and cold deserts have been extensively used to investigate the limit of microbial survival under laboratory simulated and space conditions (Billi, 2019). Chroococcidiopsis strains survived prolonged and extreme desiccation, like 4 years of air-drying under laboratory conditions (Billi, 2009; Fagliarone et al, 2020) and 18-month exposure to space vacuum in low Earth orbit outside the international space station (Mosca et al, 2021). Evidences for the presence of an efficient antioxidant defense in desert Chroococcidiopsis strains, including CCMEE 029, were provided by the absence of protein oxidation after exposure to desiccation and hydrogen peroxide treatment (Fagliarone et al, 2017), as well as by the reduced reactive oxygen species accumulation in cells air-dried for 4 years (Billi, 2009). Despite the relevance of the antioxidant defense, its role in the desiccation tolerance of desert strains of Chroococcidiopsis remains to be elucidated
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