Thiol/Disulfide System Plays a Crucial Role in Redox Protection in the Acidophilic Iron-Oxidizing Bacterium Leptospirillum ferriphilum

Abstract

Thiol/disulfide systems are involved in the maintenance of the redox status of proteins and other molecules that contain thiol/disulfide groups. Leptospirillum ferriphilum DSM14647, an acidophilic bacterium that uses Fe2+ as electron donor, and withstands very high concentrations of iron and other redox active metals, is a good model to study how acidophiles preserve the thiol/disulfide balance. We studied the composition of thiol/disulfide systems and their role in the oxidative stress response in this extremophile bacterium. Bioinformatic analysis using genomic data and enzymatic assays using protein extracts from cells grown under oxidative stress revealed that the major thiol/disulfide system from L. ferriphilum are a cytoplasmic thioredoxin system (composed by thioredoxins Trx and thioredoxin reductase TR), periplasmic thiol oxidation system (DsbA/DsbB) and a c-type cytochrome maturation system (DsbD/DsbE). Upon exposure of L. ferriphilum to reactive oxygen species (ROS)-generating compounds, transcriptional activation of the genes encoding Trxs and the TR enzyme, which results in an increase of the corresponding activity, was observed. Altogether these data suggest that the thioredoxin-based thiol/disulfide system plays an important role in redox protection of L. ferriphilum favoring the survival of this microorganism under extreme environmental oxidative conditions.

Oxidative Stress Induced by Metal Ions in Bioleaching of LiCoO2 by an Acidophilic Microbial Consortium

“…However, it is also found that there exist intracellular antioxidant enzyme systems (Rodrigues et al, 2010) and non-enzyme antioxidant components (Xu et al, 2016) in microorganisms to maintain the balance of ROS in cells. It is reported that the thiol/disulfide system plays a crucial role in red ox protection in L. ferriphilum (Javiera et al, 2012). Previous studies have shown that the intracellular ROS content could be regulated by exogenous chemicals such as cobalamin (Chen et al, 2016;Ferrer et al, 2016).…”

“…It is found that the increase of the intracellular ROS content resulted from Cu 2+ accumulation can lead to the death of A. ferrooxidans (Xia et al, 2011). Fortunately, it has been proven that an intracellular ROS scavenging system exists in Leptospirillum ferrooxidans to improve the damage resistance (Javiera et al, 2012). Exogenous cobalamin has also been used to decrease the ROS content in L. ferrooxidans, and to improve cell growth and survival (Ferrer et al, 2016).…”

“…A predicted gene encoding OxyR, a transcription factor that regulates the response to red ox stress was found in L. ferriphilum but not in A. ferrooxidans, suggesting that there are differences among the molecular mechanisms for the regulation of oxidative stress response from various microorganism (Cortés et al, 2011). Javiera et al (2012) suggested that L. ferriphilum is mainly protected by the thioredoxin-based thiol/disulfide system to survive under extreme oxidative environments. It was found in this study that exogenous GSH increased the activities of ROS scavenging enzymes in AMC to scavenge the excessive intracellular ROS content.…”

Deciphering the Role of Multiple Thioredoxin Fold Proteins of Leptospirillum sp. in Oxidative Stress Tolerance

“…is an autotrophic obligate acidophilic bacterium that catalyzes dissimilatory Fe(II) oxidation. It serves as a model bacterium to elucidate the mechanisms used by acidophilic microorganisms to thrive under highly oxidative conditions [16][17][18][19]. Thirteen tfp genes (formerly trx) coding for predicted TFPs have been identified in Leptospirillum spp.…”

“…Thirteen tfp genes (formerly trx) coding for predicted TFPs have been identified in Leptospirillum spp. [18]. Exposure of Leptospirillum ferriphilum to ROS-generating compounds resulted in a concomitant increase in thioredoxin activity.…”