Modulation of oxidative stress machinery determines the contrasting ability of cyanobacteria to adapt to Se(VI) or Se(IV)

Plant Physiol Biochem. 2024 Jun:211:108673. doi: 10.1016/j.plaphy.2024.108673. Epub 2024 May 1.

Abstract

Excess of selenium (Se) in aquatic ecosystems has necessitated thorough investigations into the effects/consequences of this metalloid on the autochthonous organisms exposed to it. The molecular details of Se-mediated adaptive response remain unknown in cyanobacteria. This study aims to uncover the molecular mechanisms driving the divergent physiological responses of cyanobacteria on exposure to selenate [Se(VI)] or selenite [Se(IV)], the two major water-soluble oxyanions of Se. The cyanobacterium, Anabaena PCC 7120, withstood 0.4 mM of Se(VI), whereas even 0.1 mM of Se(IV) was detrimental, affecting photosynthesis and enhancing endogenous ROS. Surprisingly, Anabaena pre-treated with Se(VI), but not Se(IV), showed increased tolerance to oxidative stress mediated by H2O2/methyl viologen. RNA-Seq analysis showed Se(VI) to elevate transcription of genes encoding anti-oxidant proteins and Fe-S cluster biogenesis, whereas the photosynthesis-associated genes, which were mainly downregulated by Se(IV), remained unaffected. Specifically, the content of typical 2-Cys-Prx (Alr4641), a redox-maintaining protein in Anabaena, was elevated with Se(VI). In comparison to the wild-type, the Anabaena strain over-expressing the Alr4641 protein (An4641+) showed enhanced tolerance to Se(VI) stress, whereas the corresponding knockdown-strain (KD4641) was sensitive to this stressor. Incidentally, among these strains, only An4641+ was better protected from the ROS-mediated damage caused by high dose of Se(VI). These results suggest that altering the content of the antioxidant protein 2-Cys-Prx, could be a potential strategy for modulating resistance to selenate. Thus, involvement of oxidative stress machinery appears to be the major determinant, responsible for the contrasting physiological differences observed in response to selenate/selenite in cyanobacteria.

Keywords: 2-Cys-Peroxiredoxin; Cyanobacteria; Differentially expressed genes; Oxidative stress; Photosynthesis; Selenium.

MeSH terms

  • Adaptation, Physiological / drug effects
  • Anabaena* / drug effects
  • Anabaena* / genetics
  • Anabaena* / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Gene Expression Regulation, Bacterial / drug effects
  • Oxidative Stress* / drug effects
  • Photosynthesis / drug effects
  • Reactive Oxygen Species / metabolism
  • Selenic Acid / metabolism
  • Selenic Acid / pharmacology
  • Selenious Acid / metabolism
  • Selenious Acid / pharmacology
  • Selenium / metabolism
  • Selenium / pharmacology

Substances

  • Bacterial Proteins
  • Selenium
  • Selenious Acid
  • Reactive Oxygen Species
  • Selenic Acid