Genome-Wide Identification and Bioinformatics Characterization of Superoxide Dismutases in the Desiccation-Tolerant Cyanobacterium Chroococcidiopsis sp. CCMEE 029

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.

Insights into the chaotropic tolerance of the desert cyanobacterium Chroococcidiopsis sp. 029 (Chroococcidiopsales, Cyanobacteria)

“…After 1 week of exposure, three sod genes were over‐expressed. Notably, the expression of the membrane‐bound Mn‐SOD ( sod A 2.1) was higher than that of the cytoplasmic Mn‐SOD and Cu/Zn‐SOD ( sod A 2.2 and sod C), thus suggesting its protective role in the periplasm/thylakoid lumen as had been previously reported in response to desiccation (Napoli et al., 2021). The relevance of the antioxidant defense in the perchlorate resistance was reinforced by the over‐expression of four catalases ( kat E, kat G, Mn CAT 1, and MnCAT 2), with the kat E gene upregulated after 1 h of exposure and throughout the 3 weeks of perchlorate exposure.…”

“…The gathered evidence suggested that the perchlorate resistance of this cyanobacterium might be a byproduct of its desiccation tolerance. Indeed, the perchlorate exposure triggered the upregulation of the trehalose and sucrose biosynthetic pathways and antioxidant defense system, both known to be over‐expressed during the desiccation response (Fagliarone et al., 2020; Napoli et al., 2021). The gene upregulation observed during the early phase of perchlorate exposure (1 h and 1 week), as well as after 2 and 3 weeks of culturing, provided insights into the responses toward this chaotropic agent, independently from the growth state, as the fold change of each gene transcript in perchlorate‐exposed cells was compared with that in control cells grown without perchlorate for the same amount of time.…”

Ecophysiological and genomic approaches to cyanobacterial hardening for soil restoration

“…One of the most known mechanisms against reactive oxygen species, the superoxide dismutase ( sod ), was also annotated (Suppl. Table 5), specifically, the combination of Fe and Mn SOD, which is the type found in filamentous nonheterocystous cyanobacteria (Napoli et al 2021). Other genes related to oxidative damage protection that were detected are: a methionine sulfoxide reductase ( msrA ), the Mn containing catalase (cat ), the DNA-binding protein ( dps ); and peroxiredoxin ( prx ).…”

“…Genes known to be involved in resistance mechanisms against stress (Rajeev et al 2013; Soule et al 2013; Shimura et al 2015; Al-Hosani et al 2015; Kopf et al 2015; Ferreira et al 2016; Sinetova et al 2016; Chrismas et al 2016, 2018; Klicki et al 2018; Shang et al 2019; Pathak et al 2019; Kvíderová et al 2019; Pereira et al 2009, 2019; Chatterjee et al 2020; Mosca et al 2021; Ye et al 2021; Napoli et al 2021) were searched in the generated contig database and classified in the following groups: (i) Production of the EPS matrix, (ii) Photoprotection, (iii) Oxidative stress protection, (iv) DNA repair and (v) Osmotic stress protection. When genes were not found in the database, they were searched manually using tblastn against the ULC029 assembled genome with an e-value threshold of 1e-5 and a score higher than 50 bits (following Pearson et al 2013).…”

Screening the Survival of Cyanobacteria Under Perchlorate Stress. Potential Implications for Mars In Situ Resource Utilization

“…As previously shown, cyanobacteria that belong to the genera Leptolyngbya and Chroococcidiopsis are rich in flavonoids (Ijaz and Hasnain, 2016 ). Further, Chroococcidiopsis species have demonstrated the overexpression of genes encoding SODs under oxidative stress induced by desiccation (Napoli et al , 2021 ).…”