Skip to main content
SpringerLink
Log in

Pro-oxidant Challenges and Antioxidant Adaptation of Pleuragramma antarctica in Platelet Ice

  • Chapter
  • First Online:
The Antarctic Silverfish: a Keystone Species in a Changing Ecosystem

Part of the book series: Advances in Polar Ecology ((AVPE,volume 3))

  • 800 Accesses

Abstract

Antarctic organisms developed specific adaptation mechanisms making these species able to survive to extreme environment conditions. Among fishes, Pleuragramma antarctica presents a specific peculiarity due to the occurrence of eggs with fully developed yolk-sac embryos below the platelet ice layer. This ice is an environment with strong pro-oxidant characteristics at the beginning of austral spring, when the rapid growth of algal ice communities, the massive release of nutrients and the photoactivation of dissolved organic carbon and nitrates represent an important sources for oxyradical formation. Such processes are concentrated in a short period of a few weeks, which overlaps with the final stage of development of P. antarctica embryos in platelet ice. For this reason, embryonated eggs of P. antarctica, before hatching, should possess adequate protection toward the marked and sudden increase of reactive oxygen species exposure. In this respect, molecular and functional characteristics of antioxidants in P. antarctica provide new insights on the modulation of the antioxidant defence pathway in response to varied environmental pro-oxidant challenge. To this aim, the main antioxidant components have been characterized in P. antarctica sampled from platelet ice in its nursery area in the Ross Sea, and data on nucleotide and protein sequences have been integrated with the analysis of regulation at transcriptional and functional levels. The results revealed a marked temporal increase of antioxidants in embryos of P. antarctica as adaptive counteracting response to oxidative conditions of platelet ice.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A 138:405–415

    Article  Google Scholar 

  • Abele D, Burlando B, Viarengo A et al (1998) Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp Biochem Physiol B 120:425–435

    Article  Google Scholar 

  • Ansaldo M, Luquet CM, Evelson PA et al (2000) Antioxidant levels from different Antarctic fish caught around South Georgia Island and Shag Rocks. Polar Biol 23:160–165

    Article  Google Scholar 

  • Bilyk KT, Cheng C-H (2013) Model of gene expression in extreme cold – reference transcriptome for the high-Antarctic cryopelagic notothenioid fish Pagothenia borchgrevinki. BMC Genomics 14:634

    Article  CAS  Google Scholar 

  • Brier S, Maria G, Carginale V et al (2007) Purification and characterization of pepsins A1 and A2 from the Antarctic rock cod Trematomus bernacchii. FEBS J 274:6152–6166

    Article  CAS  Google Scholar 

  • Brigelius-Flohé R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830:3289–3303

    Article  Google Scholar 

  • Camus L, Gulliksen B, Depledge MH et al (2005) Polar bivalves are characterized by high antioxidant defenses. Polar Res 24(1–2):111–118

    Article  Google Scholar 

  • Cassini A, Favero M, Albergoni A (1993) Comparative studies of antioxidant enzymes in red-blooded and white-blooded Antarctic teleost fish Pagothenia bernacchii and Chionodraco hamatus. Comp Biochem Physiol C 106:333–336

    Google Scholar 

  • Chen Z, Cheng C-HC, Zhang J et al (2008) Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 105:12944–12949

    Article  CAS  Google Scholar 

  • Coppe A, Agostini C, Marino IAM (2013) Genome evolution in the cold: Antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function. Genome Biol Evol 5:45–60

    Article  Google Scholar 

  • Cullinan SB, Gordan JD, Jin J et al (2004) The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol 24:8477–8486

    Article  CAS  Google Scholar 

  • D’Amico S, Claverie P, Collins T et al (2002) Molecular basis of cold adaptation. Philos Trans R Soc Lond B Biol Sci 357:917–925

    Article  Google Scholar 

  • Delille B, Jourdain B, Borges AV et al (2007) Biogas (CO2, O2, dimethylsulfide) dynamics in springs in Antarctic fast ice. Limnol Oceanogr 52:1367–1379

    Article  CAS  Google Scholar 

  • Díaz A, Loewen PC, Fita I et al (2012) Thirty years of heme catalases structural biology. Arch Biochem Biophys 525:102110

    Article  Google Scholar 

  • Dinkova-Kostova AT, Holtzclaw WD, Kensler TW (2005) The role of Keap1 in cellular protective responses. Chem Res Toxicol 18:1779–1791

    Article  CAS  Google Scholar 

  • di Prisco G, Cocca E, Parker SK et al (2002) Tracking the evolutionary loss of hemoglobin expression by the white-blooded Antarctic icefishes. Gene 295:185–191

    Article  Google Scholar 

  • Epp O, Ladenstein R, Wendel A (1983) The refined structure of the selenoenzyme glutathione peroxidase at 0.2-nm resolution. Eur J Biochem 133:51–69

    Article  CAS  Google Scholar 

  • Evans CW, Williams DE, Vacchi M et al (2012) Metabolic and behavioural adaptations during early development of the Antarctic silverfish, Pleuragramma antarcticum. Polar Biol 35:891–898

    Article  Google Scholar 

  • Feller G, Gerday C (1997) Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci C 53:830–841

    Article  CAS  Google Scholar 

  • Fields PA, Houseman DE (2004) Decreases in activation energy and substrate affinity in cold-adapted A4-lactate dehydrogenase: evidence from the Antarctic notothenioid fish Chaenocephalus aceratus. Mol Biol Evol 21:2246–2255

    Article  CAS  Google Scholar 

  • Filho WD, Giuvili C, Boveris A (1993) Antioxidant defenses in marine fish. I. Teleost. Comp Biochem Physiol C106:409–414

    Google Scholar 

  • Fita I, Rossmann MG (1985) The active center of catalase. J Mol Biol 185:21–37

    Article  CAS  Google Scholar 

  • Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390

    Article  CAS  Google Scholar 

  • Fulgentini L, Passini V, Colombetti G et al (2015) UV radiation and visible light induce hsp70 gene expression in the Antarctic psychrophilic ciliate Euplotes focardii. Microb Ecol 70(2):372–379

    Article  CAS  Google Scholar 

  • Gerhard GS, Kauffman EJ, Grundy MA (2000) Molecular cloning and sequence analysis of the Danio rerio catalase gene. Comp Biochem Phys B 127:447–457

    Article  CAS  Google Scholar 

  • Giuliani ME, Regoli F (2014) Identification of the Nrf2-Keap1 pathway in the European eel Anguilla anguilla: role for a transcriptional regulation of antioxidant genes in aquatic organisms. Aquat Toxicol 150:117–123

    Article  CAS  Google Scholar 

  • Gleitz M, Vonderloeff MR, Thomas DN et al (1995) Comparison of summer and winter in organic carbon, oxygen and nutrient concentrations in Antarctic sea ice brine. Mar Chem 51:81–91

    Article  CAS  Google Scholar 

  • Guidetti P, Ghigliotti L, Vacchi M (2015) Insights on spatial distribution patterns of early stages of the Antarctic silverfish, Pleuragramma antarctica, in the platelet ice of Terra Nova Bay, Antarctica. Polar Biol 38(3):333–342

    Article  Google Scholar 

  • Hader D-P, Williamson CE, Wangberg S-A et al (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14(1):108–126

    Article  Google Scholar 

  • Hofmann GE, Buckley BA, Airaksinen S et al (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family nototheniidae). J Exp Biol 203:2331–2339

    CAS  Google Scholar 

  • Johnston IA, Calvo J, Guderley H et al (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    CAS  Google Scholar 

  • Katoh Y, Itoh K, Yoshida E et al (2001) Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 6:857–868

    Article  CAS  Google Scholar 

  • Kawall HG, Torres JJ, Sidell BD et al (2002) Metabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain. Mar Biol 140:279–286

    Article  Google Scholar 

  • Kobayashi M, Yamamoto M (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzym Regul 46:113–140

    Article  CAS  Google Scholar 

  • Kobayashi M, Itoh K, Suzuki T et al (2002) Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7:807–820

    Article  CAS  Google Scholar 

  • Kong X, Jiang H, Wang S et al (2013) Effects of copper exposure on the hatching status and antioxidant defense at different developmental stages of embryos and larvae of goldfish Carassius auratus. Chemosphere 92:1458–1464

    Article  CAS  Google Scholar 

  • Krapp RH, Baussant T, Berge J et al (2009) Antioxidant responses in the polar marine sea-ice amphipod Gammarus wilkitzkii to natural and experimentally increased UV levels. Aquat Toxicol 94:1–7

    Article  CAS  Google Scholar 

  • La Mesa M, Eastman JT (2012) Antarctic Silverfish: life strategies of a key species in the high-Antarctic ecosystem. Fish Fish 13:241–266

    Article  Google Scholar 

  • La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338

    Article  Google Scholar 

  • La Mesa M, Catalano B, Russo A et al (2010) Influence of environmental conditions on spatial distribution and abundance of early life stages of Antarctic silverfish, Pleuragramma antarcticum (Nototheniidae), in the Ross Sea. Antarct Sci 22:243–254

    Article  Google Scholar 

  • Liravi F, Salati AP, Asadi F et al (2014) Alterations in antioxidant defence in the early life stages of silver carp, Hypophthalmichthys molitrix. Prog Biol Sci 4:179–187

    Google Scholar 

  • Lister KN, Lamare MD, Burritt DJ (2010) Sea ice protects the embryos of the Antarctic sea urchin Sterechinus neumayeri from oxidative damage due to naturally enhanced levels of UV-B radiation. J Exp Biol 213:1967–1975

    Article  CAS  Google Scholar 

  • Lorentzen MS, Moe E, Jouve HM et al (2006) Cold adapted features of Vibrio salmonicida catalase: characterisation and comparison to the mesophilic counterpart from Proteus mirabilis. Extremophiles 10:427–440

    Article  CAS  Google Scholar 

  • Marx J-C, Collins T, D’Amico S et al (2007) Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol 9:293–304

    Article  CAS  Google Scholar 

  • Nahrgang J, Camus L, Broms F et al (2010) Seasonal baseline levels of physiological and biochemical parameters in polar cod (Boreogadus saida): implications for environmental monitoring. Mar Pollut Bull 60:1336–1345

    Article  CAS  Google Scholar 

  • Obermüller B, Karsten U, Abele D (2005) Response of oxidative stress parameters and sunscreening compounds in Arctic amphipods during experimental exposure to maximal natural UVB radiation. J Exp Mar Biol Ecol 323:100–117

    Article  Google Scholar 

  • Rautio M, Korhola A (2002) Effects of ultraviolet radiation and dissolved organic carbon on the survival of subarctic zooplankton. Polar Biol 25:460–468

    Google Scholar 

  • Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106–117

    Article  CAS  Google Scholar 

  • Regoli F, Principato G, Bertoli E et al (1997) Biochemical characterization of the antioxidant system in the scallop Adamussium colbecki, as a sentinel organism for monitoring the Antarctic environment. Polar Biol 17:251–258

    Article  Google Scholar 

  • Regoli F, Nigro M, Orlando E (1998) Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquat Toxicol 40:375–392

    Article  Google Scholar 

  • Regoli F, Nigro M, Bompadre S et al (2000a) Total oxidant scavenging capacity (TOSC) of microsomal and cytosolic fractions from Antarctic, Arctic and Mediterranean scallops: differentiation between three potent oxidants. Aquat Toxicol 49:13–25

    Article  CAS  Google Scholar 

  • Regoli F, Cerrano C, Chierici E et al (2000b) Susceptibility to oxidative stress of the Mediterranean demosponge Petrosia ficiformis: role of endosymbionts and solar irradiance. Mar Biol 137:453–461

    Article  CAS  Google Scholar 

  • Regoli F, Nigro M, Chiantore M et al (2002) Seasonal variation of susceptibility to oxidative stress in Adamussium colbecki, a key bioindicator species for the Antarctic marine environment. Sci Total Environ 289:205–211

    Article  CAS  Google Scholar 

  • Regoli F, Nigro M, Chierici E et al (2004) Variations of antioxidant efficiency and presence of endosymbiotic diatoms in the Antarctic porifera Haliclona dancoi. Mar Environ Res 58:637–640

    Article  CAS  Google Scholar 

  • Regoli F, Nigro M, Benedetti M et al (2005) Antioxidant efficiency in early life stages of the Antarctic silverfish, Pleuragramma antarcticum: responsiveness to pro-oxidant conditions of platelet ice and chemical exposure. Aquat Toxicol 75:43–52

    Article  CAS  Google Scholar 

  • Regoli F, Benedetti M, Krell A et al (2011) Oxidative challenges in polar seas. In: Abele D, Vazquez-Medina JP, Zenteno-Savin T (eds) Oxidative stress in aquatic ecosystems. Wiley, Chichester, pp 20–40

    Chapter  Google Scholar 

  • Ren B, Huang W, Akesson B et al (1997) The crystal structure of seleno-glutathione peroxidase from human plasma at 2.9 A resolution. J Mol Biol 268:869–885

    Article  CAS  Google Scholar 

  • Riise EK, Lorentzen MS, Helland R et al (2007) The first structure of a cold-active catalase from Vibrio salmonicida at 1.96 A reveals structural aspects of cold adaptation. Acta Crystallogr D 63:135–148

    Article  CAS  Google Scholar 

  • Rocher C, Lalanne JL, Chaudiere J (1992) Purification and properties of a recombinant sulfur analog of murine selenium-glutathione peroxidase. Eur J Biochem 205:955–960

    Article  CAS  Google Scholar 

  • Ross JC, Vincent WF (1998) Temperature dependence of UV radiation effects on Antarctic cyanobacteria. J Phycol 34:118–125

    Article  Google Scholar 

  • Scott C, Falk-Petersen S, Gulliksen B et al (2001) Lipid indicators of the diet of the sympagic amphipod Gammarus wilkitzkii in the marginal ice zone and in open waters of Svalbard (Arctic). Polar Biol 24:572–576

    Article  Google Scholar 

  • Shick JM, Dykens JA (1985) Oxygen detoxification in algal-invertebrate symbioses from the Great Barrier Reef. Oecologia 66:33–64

    Article  CAS  Google Scholar 

  • Shin SC, Kim SJ, Lee JK et al (2012) Transcriptomics and comparative analysis of three Antarctic notothenioid fishes. PLoS One 7:1–9

    Google Scholar 

  • Skjærven KH, Penglase S, Olsvik PA et al (2013) Redox regulation in Atlantic cod (Gadus morhua) embryos developing under normal and heat-stressed conditions. Free Radic Biol Med 57:29–38

    Article  Google Scholar 

  • Storey KB, Storey JM (2013) Molecular biology of freezing tolerance. Compr Physiol 3:1283–1308

    Google Scholar 

  • Thomas DN, Kattner G, Engbrodt R et al (2001) Dissolved organic matter in Antarctic sea ice. Ann Glaciol 33:297–303

    Article  CAS  Google Scholar 

  • Timme-Laragy AR, Goldstone JV, Imhoff BR et al (2013) Glutathione redox dynamics and expression of glutathione-related genes in the developing embryo. Free Radic Biol Med 65:89–101

    Article  CAS  Google Scholar 

  • Tong KI, Katoh Y, Kusunoki H et al (2006) Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol Cell Biol 26:2887–2900

    Article  CAS  Google Scholar 

  • Tosatto SCE, Bosello V, Fogolari F et al (2008) The catalytic site of glutathione peroxidases. Antioxid Redox Signal 10:1515–1526

    Article  CAS  Google Scholar 

  • Ursini F, Maiorino M, Brigelius-Flohé R et al (1995) Diversity of glutathione peroxidase. Method Enzymol 252:38–53

    Article  CAS  Google Scholar 

  • Vacchi M, La Mesa M, Dalu M et al (2004) Early life stages in the life cycle of Antarctic silverfish, Pleuragramma antarcticum in Terra Nova Bay, Ross Sea. Antarct Sci 16:299–305

    Article  Google Scholar 

  • Vacchi M, Koubbi P, Ghigliotti L et al (2012a) Sea-ice interactions with polar fish-focus on the Antarctic silverfish life history. In: Verde C, di Prisco G (eds) Adaptation and evolution in marine environments, vol 1, from pole to pole. Springer, Berlin, pp 51–73

    Chapter  Google Scholar 

  • Vacchi M, DeVries A, Evans CW et al (2012b) A nursery area for the Antarctic silverfish Pleuragramma antarcticum at Terra Nova Bay (Ross Sea): first estimate of distribution and abundance of eggs and larvae under the seasonal sea-ice. Polar Biol 35:1573–1585

    Article  Google Scholar 

  • Viarengo A, Canesi L, Garcia Martinez P et al (1995) Pro-oxidant processes and antioxidant defence systems in the tissues of the Antarctic scallop (Adamussium colbecki) compared with the Mediterranean scallop (Pecten jacobeus). Comp Biochem Physiol B 111:119–126

    Article  Google Scholar 

  • Walczak R, Westhof E, Carbon P et al (1996) A novel RNA structural motif in the selenocysteine insertion element of eukaryotic selenoprotein mRNAs. RNA 2:367–379

    CAS  Google Scholar 

  • Wang W, Wang F, Ji X et al (2011) Cloning and characterization of a psychrophilic catalase gene from an Antarctic bacterium. Afr J Microbiol Res 5:3195–3199

    Article  CAS  Google Scholar 

  • Werner I (2000) Faecal pellet production by Arctic underice amphipods – transfer of organic matter through the ice/water interface. Hydrobiologia 426:89–96

    Article  CAS  Google Scholar 

  • Witas H, Gabryelak T, Matkovics B (1984) Comparative studies on superoxide dismutase and catalase activities in livers of fish and other Antarctic vertebrates. Comp Biochem Physiol C 77:409–411

    Article  CAS  Google Scholar 

  • Xu Q, C-HC C, Hu P et al (2008) Adaptive evolution of hepcidin genes in Antarctic notothenioid fishes. Mol Biol Evol 25:1099–1112

    Article  CAS  Google Scholar 

  • Yamamoto Y, Fujisawa A, Hara A et al (2001) An unusual vitamin E constituent provides antioxidant protection in marine organisms adapted to coldwater environments. Proc Natl Acad Sci U S A 98:13144–13148

    Article  CAS  Google Scholar 

  • Zhang J, Hosoya T, Maruyama A et al (2007) Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes. Biochem J 404:459–466

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy

    Maura Benedetti, Maria Elisa Giuliani & Francesco Regoli

Authors
  1. Maura Benedetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Elisa Giuliani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesco Regoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesco Regoli .

Editor information

Editors and Affiliations

  1. Institute of Marine Sciences (ISMAR) - CNR, Genoa, Italy

    Marino Vacchi

  2. Department of Earth, Environment and Life Sciences (DISTAV), University of Genoa, Genoa, Italy

    Eva Pisano

  3. Institute of Marine Sciences (ISMAR) - CNR, Genoa, Italy

    Laura Ghigliotti

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Benedetti, M., Giuliani, M.E., Regoli, F. (2017). Pro-oxidant Challenges and Antioxidant Adaptation of Pleuragramma antarctica in Platelet Ice. In: Vacchi, M., Pisano, E., Ghigliotti, L. (eds) The Antarctic Silverfish: a Keystone Species in a Changing Ecosystem. Advances in Polar Ecology, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-55893-6_4

Download citation

Publish with us

Policies and ethics

Search

Navigation