Phylogenetic analysis of cnidarian peroxiredoxins and stress-responsive expression in the estuarine sea anemone Nematostella vectensis

Comp Biochem Physiol A Mol Integr Physiol. 2018 Jul:221:32-43. doi: 10.1016/j.cbpa.2018.03.009. Epub 2018 Mar 19.

Abstract

Peroxiredoxins (PRXs) are a family of antioxidant enzymes present in all domains of life. To date, the diversity and function of peroxiredoxins within animals have only been studied in a few model species. Thus, we sought to characterize peroxiredoxin diversity in cnidarians and to gain insight into their function in one cnidarian-the sea anemone Nematostella vectensis. Phylogenetic analysis using all six known PRX subfamilies (PRX1-4, PRX5, PRX6, PRXQ/AHPE1, TPX, BCP-PRXQ) revealed that like bilaterians, cnidarians contain representatives from three subfamilies (PRX1-4, PRX5, PRX6). Within the PRX1-4 subfamily, cnidarian sequences fall into two clades: PRX4, and a cnidarian-specific clade, which we term CNID-PRX. This phylogenetic analysis demonstrates that the three PRX subfamilies present in Bilateria were also present in the last common ancestor of the Cnidaria and Bilateria, and further that diversification of the PRX1-4 subfamily has occurred within the cnidarian lineage. We next examined the impact of decreased salinity, increased temperature, and peroxide exposure on the expression of four prx genes in N. vectensis (cnid-prx, prx4, prx5, and prx6). These genes exhibited unique expression patterns in response to these environmental stressors. Expression of prx4 decreased with initial exposure to elevated temperature, cnid-prx increased with exposure to elevated temperatures as well as with hydrogen peroxide exposure, and expression of all prxs transiently decreased with reduced salinity. Predicted subcellular localization patterns also varied among PRX proteins. Together these results provide evidence that peroxiredoxins in N. vectensis serve distinct physiological roles and lay a groundwork for understanding how peroxiredoxins mediate cnidarian developmental processes and environmental responses.

Keywords: Antioxidant; Cnidaria; Evolution; Heat stress; Nematostella vectensis; Oxidative stress; Peroxide; Peroxiredoxin; Reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Estuaries*
  • Evolution, Molecular
  • Gene Expression Regulation, Developmental*
  • Gene Expression Regulation, Enzymologic*
  • Hydrogen Peroxide / metabolism
  • Oxidative Stress
  • Peroxiredoxins / chemistry
  • Peroxiredoxins / classification*
  • Peroxiredoxins / genetics
  • Peroxiredoxins / metabolism
  • Phylogeny*
  • Protein Conformation
  • Reactive Oxygen Species / metabolism
  • Salt Stress
  • Sea Anemones / enzymology*
  • Sea Anemones / genetics
  • Sea Anemones / metabolism
  • Sea Anemones / physiology
  • Stress, Physiological / genetics*
  • Subcellular Fractions / enzymology
  • Temperature

Substances

  • Antioxidants
  • Reactive Oxygen Species
  • Hydrogen Peroxide
  • Peroxiredoxins