Redox-dependent chaperone/peroxidase function of 2-Cys-Prx from the cyanobacterium Anabaena PCC7120: role in oxidative stress tolerance

Abstract

BackgroundCyanobacteria, progenitors of plant chloroplasts, provide a suitable model system for plants to study adaptation towards different abiotic stresses. Genome of the filamentous, heterocystous, nitrogen-fixing cyanobacterium Anabaena PCC7120 harbours a single gene (alr4641) encoding a typical 2-Cys-Peroxiredoxins (2-Cys-Prxs). 2-Cys-Prxs are thiol-based peroxidases that also function as molecular chaperones in plants and other systems. The Alr4641 protein from Anabaena PCC7120 shows high level biochemical similarities with the plant 2-Cys-Prx. The physiological role played by the Alr4641 protein in Anabaena was addressed in this study.ResultsIn Anabaena PCC7120, alr4641 transcript /Alr4641 protein was induced in response to abiotic stresses and its promoter was active in the vegetative cells as well as heterocysts. The wild-type Alr4641 protein or Alr4641 lacking the peroxidatic cysteine (Alr4641C56S) or the resolving cysteine (Alr4641C178S) existed as higher oligomers in their native form. The wild-type or the mutant Alr4641 proteins showed similar chaperone activity, but only the wild-type protein exhibited peroxidase activity indicating that unlike peroxidase activity, chaperone activity was not dependent on cysteines. In contrast to other 2-Cys-Prxs, chaperone/peroxidase activity of Alr4641 was dependent on its redox state and not oligomerization status. Alr4641 could protect plasmid DNA from oxidative damage and physically associate with NADPH-dependent thioredoxin reductase (NTRC). Like 2-Cys-Prxs from plants (e.g. rice), Alr4641 could detoxify various peroxides using NTRC as reductant. On exposure to H2O2, recombinant Anabaena PCC7120 strain over-expressing Alr4641 (An4641+) showed reduced content of reactive oxygen species (ROS), intact photosynthetic functions and consequently better survival than the wild-type Anabaena PCC7120, indicating that Alr4641 can protect Anabaena from oxidative stress.ConclusionsThe peroxidase/chaperone function of Alr4641, its inherent transcriptional/translational induction under different abiotic stresses and localization in both vegetative cells and heterocysts could be an adaptive strategy to battle various oxidative stresses that Anabaena encounters during its growth. Moreover, the recombinant Anabaena strain over expressing Alr4641 showed higher resistance to oxidative stress, suggesting its potential to serve as stress-tolerant biofertilizers in rice fields.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0444-2) contains supplementary material, which is available to authorized users.

Unraveling the mechanism responsible for the contrasting tolerance of Synechocystis and Synechococcus to Cr(VI): Enzymatic and non-enzymatic antioxidants

“…Among peroxidases, peroxiredoxins (Prxs) are the important hydroperoxide detoxification enzymes that have been characterized in cyanobacteria (Banerjee et al, 2013). In Anabaena, over-expression of 2-Cys-Prx resulted in increased resistance to oxidative stress mediated by H 2 O 2 (Banerjee et al, 2015). Similarly, the 2-Cys-Prx protein is proposed to play a major role in detoxification of H 2 O 2 in Synechocystis (Pascual et al, 2010).…”

A Salt-Inducible Mn-Catalase (KatB) Protects Cyanobacterium from Oxidative Stress

“…Thus, studying the detailed basis of oxidative stress resistance in Anabaena is essential for development of novel biofertilizers, which may be used under adverse conditions. The role played by various proteins in overcoming oxidative stress in the filamentous, heterocystous, nitrogen-fixing, cyanobacterium Anabaena PCC 7120 has garnered remarkable interest in the recent past (Cha et al, 2007;Agrawal et al, 2014;Panda et al, 2014;Banerjee et al, 2015;Tailor and Ballal, 2015).…”

“…Prxs such as All1541 and Alr4641 are induced by oxidizing agents, including H 2 O 2 (Banerjee et al, 2012a(Banerjee et al, , 2015, indicating that these Prxs may be the principal proteins that detoxify H 2 O 2 under normal conditions. However, the role of KatB becomes apparent when Anabaena PCC 7120 is stressed with salt, a stressor that activates KatB synthesis (Fig.…”

“…damage all the cellular components, leading to cell death. In Anabaena, the photosynthetic pigments appear to be particularly prone to bleaching on treatment with H 2 O 2 (Banerjee et al, 2012a(Banerjee et al, , 2015. In another cyanobacterium, Microcystis aeruginosa, treatment with H 2 O 2 led to enhanced ROS generation that destroyed pigment synthesis and membrane integrity (Qian et al, 2010).…”

“…In the context of reduced O 2 environment required in heterocysts, the absence of KatB may confer a distinct advantage, as oxygen is one of the products of catalase activity. Prxs like Alr4641 and Alr2375 are expressed in heterocysts (Banerjee et al, 2013(Banerjee et al, , 2015. Possibly, the above-mentioned proteins that detoxify H 2 O 2 without generating O 2 are better suited to function in heterocysts than catalases like KatB.…”