OXIDATIVE STRESS INAQUATIC ECOSYSTEMS

OXIDATIVE STRESS INAQUATICECOSYSTEMS

Edited by Doris Abele, Jose Pablo Vazquez-Medina,and Tania Zenteno-Savın

A John Wiley & Sons, Ltd., Publication

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Library of Congress Cataloguing-in-Publication Data

Oxidative stress in aquatic ecosystems/[edited by] Doris Abele, Jose Pablo Vazquez-Medina, Tania Zenteno-Savın. – 1p. cm.

Includes index.ISBN 978-1-4443-3548-4 (hardback)

1. Aquatic ecology. 2. Aquatic biodiversity. 3. Oxidative stress. 4. Oxidation, Physiological. I. Abele, Doris. II. Vazquez-Medina,Jose Pablo. III. Zenteno-Savın, Tania.

QH541.5.W3O95 2012577.6′14--dc23

2011014027

A catalogue record for this book is available from the British Library.

This book is published in the following electronic formats: epdf 9781444345957; Wiley Online Library 9781444345988; epub9781444345964; MobiPocket 9781444345971

Set in 9/11pt Photina by Laserwords Private Limited, Chennai, India

1 2012

Contents

Contributors, ix

Acknowledgments, xv

List of Abbreviations, xix

INTRODUCTION TO OXIDATIVE STRESS INAQUATIC ECOSYSTEMS, 1Doris Abele, Jose Pablo Vazquez-Medina, and TaniaZenteno-Savın

PART I. CLIMATE REGIONS AND SPECIALHABITATS, 7

1. OXIDATIVE STRESS IN TROPICAL MARINEECOSYSTEMS, 9Michael P. Lesser

2. OXIDATIVE CHALLENGES IN POLARSEAS, 20Francesco Regoli, Maura Benedetti, Andreas Krell, and DorisAbele

3. OXIDATIVE STRESS IN ESTUARINEAND INTERTIDAL ENVIRONMENTS(TEMPERATE AND TROPICAL), 41Carolina A. Freire, Alexis F. Welker, Janet M. Storey, Kenneth B.Storey, and Marcelo Hermes-Lima

4. OXIDATIVE STRESS TOLERANCESTRATEGIES OF INTERTIDALMACROALGAE, 58Jose Aguilera and Ralf Rautenberger

5. OXIDATIVE STRESS IN AQUATIC PRIMARYPRODUCERS AS A DRIVING FORCE FORECOSYSTEM RESPONSES TO LARGE-SCALEENVIRONMENTAL CHANGES, 72Pauline Snoeijs, Peter Sylvander, and Norbert Haubner

6. MIGRATING TO THE OXYGEN MINIMUMLAYER: EUPHAUSIIDS, 89Nelly Tremblay, Tania Zenteno-Savın, Jaime Gomez-Gutierrez,and Alfonso N. Maeda-Martınez

7. OXIDATIVE STRESS IN SULFIDICHABITATS, 99Joanna Joyner-Matos and David Julian

8. IRON IN COASTAL MARINE ECOSYSTEMS:ROLE IN OXIDATIVE STRESS, 115Paula Mariela Gonzalez, Dorothee Wilhelms-Dick, Doris Abele,and Susana Puntarulo

9. OXIDATIVE STRESS INCORAL-PHOTOBIONT COMMUNITIES, 127Marco A. Linan-Cabello, Michael P. Lesser, Laura A.Flores-Ramırez, Tania Zenteno-Savın, and HectorReyes-Bonilla

PART II. AQUATIC RESPIRATION ANDOXYGEN SENSING, 139

10. PRINCIPLES OF OXYGEN UPTAKEAND TISSUE OXYGENATION INWATER-BREATHING ANIMALS, 141J. C. Massabuau and Doris Abele

11. OXIDATIVE STRESS IN SHARKSAND RAYS, 157Roberto I. Lopez-Cruz, Alcir Luiz Dafre, and Danilo WilhelmFilho

12. OXYGEN SENSING: THE ROLEOF REACTIVE OXYGEN SPECIES, 165Mikko Nikinmaa, Max Gassmann, and Anna Bogdanova

v

vi Contents

13. ISCHEMIA/REPERFUSION IN DIVINGBIRDS AND MAMMALS: HOW THEY AVOIDOXIDATIVE DAMAGE, 178Tania Zenteno-Savın, Jose Pablo Vazquez-Medina, NadiezhdaCantu-Medellın, Paul J. Ponganis, and Robert Elsner

PART III. MARINE ANIMAL MODELS FORAGING, DEVELOPMENT,AND DISEASE, 191

14. AGING IN MARINE ANIMALS, 193Eva E. R. Philipp, Julia Strahl, and Alexey A. Sukhotin

15. OXIDATIVE STRESS AND ANTIOXIDANTSYSTEMS IN CRUSTACEAN LIFECYCLES, 208Marıa Luisa Fanjul-Moles and Marıa E. Gonsebatt

16. TRANSFER OF FREE RADICALSBETWEEN PROTEINS AND MEMBRANELIPIDS: IMPLICATIONS FOR AQUATICBIOLOGY, 224Brenda Valderrama, Gustavo Rodrıguez-Alonso, and RebeccaPogni

17. IMMUNE DEFENSE OF MARINEINVERTEBRATES: THE ROLE OF REACTIVEOXYGEN AND NITROGEN SPECIES, 236Eva E. R. Philipp, Simone Lipinski, Jonathan Rast, and PhilipRosenstiel

18. ATTACK AND DEFENSE: REACTIVEOXYGEN AND NITROGEN SPECIESIN TELEOST FISH IMMUNE RESPONSEAND THE COEVOLVED EVASION OFMICROBES AND PARASITES, 247Katja Broeg and Dieter Steinhagen

PART IV. MARINE ANIMAL STRESSRESPONSE ANDBIOMONITORING, 261

19. STRESS EFFECTS ON METABOLISMAND ENERGY BUDGETS IN MOLLUSKS, 263Inna M. Sokolova, Alexey A. Sukhotin, and Gisela Lannig

20. STARVATION, ENERGETICS,AND ANTIOXIDANT DEFENSES, 281Amalia E. Morales, Amalia Perez-Jimenez, Miriam Furne, andHelga Guderley

21. ENVIRONMENTALLY INDUCEDOXIDATIVE STRESS IN FISH, 295Volodymyr I. Lushchak

22. CHEMICAL POLLUTANTSAND THE MECHANISMS OF REACTIVEOXYGEN SPECIES GENERATION IN AQUATICORGANISMS, 308Francesco Regoli

23. BIOMARKERS OF OXIDATIVE STRESS:BENEFITS AND DRAWBACKS FOR THEIRAPPLICATION IN BIOMONITORINGOF AQUATIC ENVIRONMENTS, 317Jose Marıa Monserrat, Rafaela Elias Letts, Josencler L. RibasFerreira, Juliane Ventura-Lima, Lılian L. Amado, Alessandra M.Rocha, Stefania Gorbi, Raffaella Bocchetti, Maura Benedetti, andFrancesco Regoli

PART V. METHODS OF OXIDATIVE STRESSDETECTION, 327

24. DETECTION OF REACTIVEMETABOLITES OF OXYGENAND NITROGEN, 329Matthew B. Grisham

25. ROLE OF SINGLET MOLECULAROXYGEN IN THE OXIDATIVE DAMAGETO BIOMOLECULES, 344Graziella Eliza Ronsein, Glaucia Regina Martinez, Eduardo Alvesde Almeida, Sayuri Miyamoto, Marisa Helena Gennari deMedeiros, and Paolo Di Mascio

26. TOTAL OXYRADICAL SCAVENGINGCAPACITY ASSAY, 359Stefania Gorbi and Francesco Regoli

27. SPECTROPHOTOMETRIC ASSAYSOF ANTIOXIDANTS, 367Francesco Regoli, Raffaella Bocchetti, and Danilo WilhelmFilho

Contents vii

28. EVALUATION OF GLUTATHIONE STATUSIN AQUATIC ORGANISMS, 381Eduardo Alves de Almeida, Danilo Grunig Humberto Silva, AfonsoCelso Dias Bainy, Florencio Porto Freitas, Flavia Daniela Motta,Osmar Francisco Gomes, Marisa Helena Gennari de Medeiros,and Paolo Di Mascio

29. MEASUREMENT OF ANTIOXIDANTPIGMENTS AND VITAMINS INPHYTOPLANKTON, ZOOPLANKTON,AND FISH, 389Pauline Snoeijs, Norbert Haubner, Peter Sylvander, andXiang-Ping Nie

30. CAROTENOID ANALYSIS ANDIDENTIFICATION IN MARINE ANIMALS, 402Eduardo Alves de Almeida, Glaucia Regina Martinez, and PaoloDi Mascio

31. LINOLEIC ACID OXIDATION PRODUCTSAS BIOMARKERS OF OXIDATIVE STRESSIN VIVO, 412Etsuo Niki and Yasukazu Yoshida

32. THE CLASSIC METHODS TO MEASUREOXIDATIVE DAMAGE: LIPID PEROXIDES,THIOBARBITURIC-ACID REACTIVESUBSTANCES, AND PROTEIN CARBONYLS,420Volodymyr I. Lushchak, Halyna M. Semchyshyn, and Oleh V.Lushchak

33. PROTEIN CARBONYL MEASUREMENTBY ENZYME LINKED IMMUNOSORBENTASSAY, 432Betul Catalgol, Stefanie Grimm, and Tilman Grune

34. EVALUATION OF MALONDIALDEHYDELEVELS, 440Sayuri Miyamoto, Eduardo Alves de Almeida, Lılian Nogueira,Marisa Helena Gennari de Medeiros, and Paolo Di Mascio

35. THE USE OF ELECTRONPARAMAGNETIC RESONANCE IN STUDIESOF OXIDATIVE DAMAGE TO LIPIDSIN AQUATIC SYSTEMS, 448Gabriela Malanga and Susana Puntarulo

36. THE ASCORBYL RADICAL/ASCORBATERATIO AS AN INDEX OF OXIDATIVE STRESSIN AQUATIC ORGANISMS, 458Gabriela Malanga, Marıa Belen Aguiar, and Susana Puntarulo

37. EVALUATION OF OXIDATIVE DNADAMAGE IN AQUATIC ANIMALS: COMETASSAYS AND8-OXO-7,8-DIHIDRO-2′-DEOXYGUANOSINELEVELS, 465Jose Pedro Friedmann Angeli, Glaucia Regina Martinez, FlaviaDaniela Motta, Eduardo Alves de Almeida, Marisa HelenaGennari de Medeiros, and Paolo Di Mascio

38. EVALUATION OF DNA ADDUCTSFORMED BY LIPID PEROXIDATIONBY-PRODUCTS, 475Camila Carriao Machado Garcia, Jose Pedro Friedmann Angeli,Eduardo Alves de Almeida, Marisa Helena Gennari de Medeiros,and Paolo Di Mascio

39. METHODS TO QUANTIFY LYSOSOMALMEMBRANE STABILITY AND THEACCUMULATION OF LIPOFUSCIN, 487Katja Broeg and Stefania Gorbi

Index, 507

Color plate section appears between pages 250and 251

Contributors

DORIS ABELE Alfred Wegener Institute for Polar andMarine Research, Department of Functional Ecology, AmHandelshafen 12, 27570 Bremerhaven, Germany

JOSE AGUILERA Photobiology Laboratory, MedicalResearch Center, Department of Dermatology, Faculty ofMedicine, University of Malaga, 29071-Malaga, Spain

EDUARDO ALVES DE ALMEIDA Department ofChemistry and Environmental Sciences, IBILCE-UNESP,Sao Jose do Rio Preto, SP, Brazil

LILIAN L. AMADO Biological Sciences Institute, FederalUniversity of Rio Grande- FURG, Rio Grande, RS, Brazil;and Post-graduation Program in Physiological Sciences,Comparative Animal Physiology, FURG, Rio Grande, RS,Brazil

AFONSO CELSO DIAS BAINY Department of Bio-chemistry, Federal University of Santa Catarina, UFSC,Florianopolis, Santa Catarina, Brazil

MAURA BENEDETTI Department of Biochemistry,Biology and Genetics, Polytechnic University of Marches,Ancona, Italy

MARIA BELEN AGUIAR Physical Chemistry-PRALIB,School of Pharmacy and Biochemistry, University ofBuenos Aires, Junın 956, C1113AAD, Buenos Aires,Argentina

RAFFAELLA BOCCHETTI Department of Biochem-istry, Biology and Genetics, Polytechnic University ofMarches, Ancona, Italy

ANNA BOGDANOVA Institute of Veterinary Physiol-ogy, Vetsuisse Faculty and Zurich Center for IntegrativeHuman Physiology (ZIHP), University of Zurich, Win-terthurerstrasse 260, CH-8057 Zurich, Switzerland

KATJA BROEG Alfred Wegener Institute for Polar andMarine Research, Am Handelshafen 12, 27570 Bremer-haven, Germany

NADIEZHDA CANTU-MEDELLIN Northwestern Cen-ter for Biological Research, La Paz, Baja California Sur,23090, Mexico; and University of Alabama Birming-ham, Department of Pathology, Birmingham, AL, 35294,USA

BETUL CATALGOL Institute of Nutrition, FriedrichSchiller University, Jena, Germany; Institute of Biolog-ical Chemistry and Nutrition, University Hohenheim,Stuttgart, Germany; Department of Biochemistry,Faculty of Medicine, Marmara University, 34668Haydarpasa, Istanbul, Turkey

PAOLO DI MASCIO Department of Biochemistry, Insti-tute of Chemistry, University of Sao Paulo, Sao Paulo, SP,Brazil

ROBERT ELSNER University of Alaska Fairbanks,School for Fisheries and Ocean Science, Institute of MarineScience, Fairbanks, AK, 99775-7220, USA

MARIA LUISA FANJUL-MOLES National Autono-mous University of Mexico, School of Sciences, C.P.04510, Mexico, D. F.

LAURA A. FLORES-RAMIREZ University of Colima,Aquaculture and Biotechnology, FACIMAR, Manzanillo,Colima, Mexico

JOSE PEDRO FRIEDMANN ANGELI Department ofBiochemistry, Institute of Chemistry, Sao Paulo Univer-sity, Sao Paulo, SP, Brazil

CAROLINA A. FREIRE Department of Physiology,Section of Biological Sciences, Federal University ofParana, Curitiba, PR, Brazil

ix

x Contributors

FLORENCIO PORTO FREITAS Department of Bio-chemistry, Institute of Chemistry, University of Sao Paulo,Sao Paulo, Brazil

MIRIAM FURNE Department of Animal Biology, Univer-sity of Granada, Campus Universitario Fuentenueva s/n,18071 Granada, Spain

CAMILA CARRIAO MACHADO GARCIA Departmentof Biochemistry, Institute of Chemistry, University of SaoPaulo, Sao Paulo, SP, Brazil

MAX GASSMANN Institute of Veterinary Physiology,Vetsuisse Faculty and Zurich Center for Integrative HumanPhysiology (ZIHP), University of Zurich, Winterthur-erstrasse 260 CH-8057 Zurich, Switzerland

MARISA HELENA GENNARI DE MEDEIROS De-partment of Biochemistry, Institute of Chemistry, Uni-versity of Sao Paulo, Sao Paulo, SP, Brazil

OSMAR FRANCISCO GOMES Department of Bio-chemistry, Institute of Chemistry, University of Sao Paulo,Sao Paulo, Brazil

JAIME GOMEZ-GUTIERREZ Interdisciplinary Centerfor Marine Sciences, Department of Plankton and MarineEcology, La Paz, Baja California Sur 23096, Mexico

MARIA E. GONSEBATT Institute for BiomedicalResearch, National Autonomous University of Mex-ico, A.P. 70-228 Ciudad Universitaria, C.P. 04510,Mexico, D.F.

PAULA MARIELA GONZALEZ Physical Chemistry-PRALIB, School of Pharmacy and Biochemistry, Univer-sity of Buenos Aires, Junin 956, 1113 Buenos Aires,Argentina

STEFANIA GORBI Department of Biochemistry,Biology and Genetic, Polytechnic University of Marches,Ancona, Italy

STEFANIE GRIMM Institute of Nutrition, FriedrichSchiller University, Jena, Germany; and Institute of Bio-logical Chemistry and Nutrition, University Hohenheim,Stuttgart, Germany

MATTHEW B. GRISHAM Immunology and Inflamma-tion Research Group, Department of Molecular and CellularPhysiology, Louisiana State University Health SciencesCenter, Shreveport, LA, USA

TILMAN GRUNE Institute of Nutrition, FriedrichSchiller University, Jena, Germany

HELGA GUDERLEY Department of Biology, Universityof Laval, Quebec, Quebec, Canada G1K 7P4

NORBERT HAUBNER Department of Ecology and Evo-lution, Uppsala University, Villavagen 14, SE-752 36Uppsala, Sweden

MARCELO HERMES-LIMA Laboratory for Free Radi-cals, Department of Cellular Biology, University of Brasilia,Brasilia, DF, Brazil

JOANNA JOYNER-MATOS Department of Biology,Eastern Washington University, Cheney, WA, USA

DAVID JULIAN Department of Biology, University ofFlorida, Gainesville, FL, USA

ANDREAS KRELL Alfred Wegener Institute for Polarand Marine Research, 27570 Bremerhaven, Germany

GISELA LANNIG Alfred Wegener Institute for Polarand Marine Research in the Hermann von HelmholtzAssociation of National Research Centres e.V., IntegrativeEcophysiology, 27570 Bremerhaven, Germany

MICHAEL P. LESSER Department of Molecular, Cellu-lar and Biomedical Sciences, University of New Hampshire,Durham, NH 03824, USA

RAFAELA ELIAS LETTS Post-graduation programin Physiological Sciences, Comparative Animal Phys-iology, Federal University of Rio Grande – FURG,Rio Grande, RS, Brazil; Department of Biochemistry,Biology and Genetic, Polytechnic University of Marches,Ancona, Italy

MARCO A. LINAN-CABELLO University of Colima,Aquaculture and Biotechnology, FACIMAR, Manzanillo,Colima, Mexico

Contributors xi

SIMONE LIPINSKI Institute of Clinical MolecularBiology, Cell Biology Department, Christian-AlbrechtsUniversity Kiel, Schittenhelmstrasse 12, 24105 Kiel,Germany

ROBERTO I. LOPEZ-CRUZ Laboratory of Biochem-isty Research, Graduate School in Molecular Biomedicine,National School of Medicine and Homeopathy (ENMyH-IPN), Mexico D.F.

ALCIR LUIZ DAFRE Department of Physiological Sci-encies, Center of Biological Sciences, Federal University ofSanta Catarina, 88040-900 Florianopolis, SC, Brazil

OLEH V. LUSHCHAK Department of Biochemistry andBiotechnology, Vassyl Stefanyk Precarpathian NationalUniversity, 57 Shevchenko Str., 76025, Ivano-Frankivsk,Ukraine

VOLODYMYR I. LUSHCHAK Department of Biochem-istry and Biotechnology, Vassyl Stefanyk PrecarpathianNational University, 57 Shevchenko Str., 76025, Ivano-Frankivsk, Ukraine

ALFONSO N. MAEDA-MARTINEZ NorthwesternCenter for Biological Research (CIBNOR), La Paz, BajaCalifornia Sur 23090, Mexico

GABRIELA MALANGA Physical Chemistry-PRALIB,School of Pharmacy and Biochemistry, University ofBuenos Aires, Junin 956, C1113AAD, Buenos Aires,Argentina

GLAUCIA REGINA MARTINEZ Molecular Biology,Section for Biological Sciences, Federal University ofParana, Curitiba, PR, Brazil

J. C. MASSABUAU University of Bordeaux 1, CNRS,UMR 5805 EPOC, Place du Dr Peyneau, 33120, Arca-chon, France

SAYURI MIYAMOTO Department of Biochemistry,Institute of Chemistry, University of Sao Paulo, Sao Paulo,SP, Brazil

JOSE MONSERRAT Biological Sciences Institute,Federal University of Rio Grande- FURG, Rio Grande, RS,Brazil; Post-graduation program in Physiological Sciences,

Comparative Animal Physiology, Federal University ofRio Grande – FURG, Rio Grande, RS, Brazil

AMALIA E. MORALES Department of Animal Biology,University of Granada, Campus Universitario Fuentenuevas/n, 18071 Granada, Spain

FLAVIA DANIELA MOTTA Department of Biochem-istry, Institute of Chemistry, Universiy of Sao Paulo, SaoPaulo, Brazil

ETSUO NIKI National Institute of Advanced IndustrialScience and Technology, Health Research Institute, Osaka563–8577, Japan

MIKKO NIKINMAA Department of Biology, Universityof Turku, FI-20014, Turku, Finland

LILIAN NOGUEIRA Departament of Chemistry andEnvironmental Sciences, IBILCE-UNESP, Sao Jose do RioPreto, SP, Brazil

AMALIA PEREZ-JiMENEZ Department of AnimalBiology, University of Granada, Campus UniversitarioFuentenueva s/n, 18071 Granada, Spain

EVA E. R. PHILIPP Institute of Clinical Molecular Biol-ogy, Christian-Albrechts-University Kiel, Schittenhelm-strasse 12, 24105 Kiel, Germany

REBECCA POGNI Chemistry Department, Universityof Siena, Italy

PAUL J. PONGANIS Center for Marine Biotechnologyand Biomedicine, Scripps Institution of Oceanogra-phy, University of California San Diego, La Jolla,CA 92093-0204, USA

SUSANA PUNTARULO Physical Chemistry-PRALIB,School of Pharmacy and Biochemistry, University ofBuenos Aires, Junin 956, 1113 Buenos Aires, Argentina

JONATHAN RAST Sunnybrook Health Sciences Cen-tre, Department of Medical Biophysics and Departmentof Immunology, University of Toronto, 2075 BayviewAvenue, Rm. S126B, Toronto, ON M4N 3M5, Canada

RALF RAUTENBERGER Institute for Polar Ecology,Christian Albrechts University of Kiel, Wischhofstraße

xii Contributors

1–3, 24148 Kiel, Germany; Department of MarineBotany, University of Bremen, Faculty of Biology andChemistry, 28359 Bremen, Germany; and Department ofBotany, University of Otago, Dunedin, 9016, New Zealand

FRANCESCO REGOLI Department of Biochem-istry, Biology and Genetics, Polytechnic University ofMarches, Ancona, Italy

HECTOR REYES-BONILLA Autonomous University ofBaja California Sur, La Paz, Baja California Sur, Mexico

JOSENCLER L. RIBAS FERREIRA Post-graduationprogram in Physiological Sciences, Comparative AnimalPhysiology, Federal University of Rio Grande – FURG,Rio Grande, RS, Brazil

ALESSANDRA M. ROCHA Post-graduation programin Physiological Sciences, Comparative Animal Physiology,Federal University of Rio Grande – FURG, Rio Grande, RS,Brazil

GUSTAVO RODRIGUEZ-ALONSO Department ofMolecular Medicine and Bioprocesses, Institute of Biotech-nology, Autonomous University of Mexico, Mexico;Faculty of Sciencies, Autonomous University of the Stateof Morelos, Mexico

GRAZIELLA ELIZA RONSEIN Department of Biochem-istry, Institute of Chemistry, University of Sao Paulo, SaoPaulo, SP, Brazil

PHILIP ROSENSTIEL Institute of Clinical MolecularBiology, Cell Biology Department, Christian-AlbrechtsUniversity Kiel, Schittenhelmstrasse 12, 24105 Kiel,Germany

HALYNA M. SEMCHYSHYN Department of Biochem-istry and Biotechnology, Vassyl Stefanyk PrecarpathianNational University, 57 Shevchenko Str., 76025, Ivano-Frankivsk, Ukraine

DANILO GRUNIG HUMBERTO SILVA Department ofChemistry and Environmental Sciences, IBILCE-UNESP,Sao Jose do Rio Preto, Sao Paulo, Brazil

PAULINE SNOEIJS Department of Systems Ecology,Stockholm University, Svante Arrhenius vag 21A, SE-10691 Stockholm, Sweden

INNA M. SOKOLOVA Department of Biology, Univer-sity of North Carolina at Charlotte, Charlotte, NC, USA

DIETER STEINHAGEN University of VeterinaryMedicine Hannover, Centre for Infection Medicine, FishDisease Research Unit, Buenteweg 17, 30559 Hannover,Germany

JANET M. STOREY Institute of Biochemistry, CarletonUniversity, Ottawa, ON, Canada

KENNETH B. STOREY Institute of Biochemistry, Car-leton University, Ottawa, ON, Canada

JULIA STRAHL Alfred Wegner Institute for Polar andMarine Research, Department of Functional Ecology, AmHandelshafen 12, 2570 Bremerhaven, Germany

ALEXEY A. SUKHOTIN White Sea Biological Station,Zoological Institute of Russian Academy of Sciences,199034 St. Petersburg, Russia

PETER SYLVANDER Department of Systems Ecology,Stockholm University, Svante Arrhenius vag 21A, SE-10691 Stockholm, Sweden

NELLY TREMBLAY Interdisciplinary Center for MarineSciences, Department of Plankton and Marine Ecology, Av.IPN, Col. Palo de Santa Rita s/n, La Paz, Baja CaliforniaSur, 23096, Mexico

BRENDA VALDERRAMA Department of MolecularMedicine and Bioprocesses, Institute of Biotechnology,Autonomous University of Mexico, Mexico

JOSE PABLO VAZQUEZ-MEDINA NorthwesternCenter for Biological Research (CIBNOR). Mar Bermejo195; Playa Palo Santa Rita, La Paz, Baja California Sur,23090, Mexico; School of Natural Sciences, University ofCalifornia Merced, Merced, CA 95343, USA

JULIANE VENTURA-LIMA Biological Sciences Insti-tute, Federal University of Rio Grande- FURG, Rio Grande,RS, Brazil; Post-graduation program in Physiological Sci-ences, Comparative Animal Physiology, Federal Universityof Rio Grande – FURG, Rio Grande, RS, Brazil

ALEXIS F. WELKER Laboratory for Free Radicals,Department of Cell Biology, University of Brasilia,

Contributors xiii

Brasilia, DF, Brazil; Faculty of Ceilandia, University ofBrasilia, DF, Brazil

DANILO WILHELM FILHO Department of Ecology andZoology, Center for Biological Sciences, Federal Universityof Santa Catarina, 88040-900 Florianopolis, SC, Brazil

DOROTHEE WILHELMS-DICK University of Bremen,Geoscience Department, Klagenfurter Straße, 28359 Bre-men, Germany

XIANG-PING NIE Department of Systems Ecology,Stockholm University, Svante Arrhenius vag 21A,

SE-106 91 Stockholm, Sweden; Department of Ecology,Jian University, 601 West Huangpu Street, Guangzhou510632, China

YASUKAZU YOSHIDA National Institute of AdvancedIndustrial Science and Technology, Health Research Insti-tute, Osaka 563–8577, Japan

TANIA ZENTENO-SAVIN Northwestern Center for Bio-logical Research (CIBNOR). Mar Bermejo 195; Playa PaloSanta Rita, La Paz, Baja California Sur, 23090, Mexico

Acknowledgments

Michael P. Lesser (Chapter 1) acknowledges the supportfrom various funding agencies including NOAA andNSF for research on coral reef bleaching. Additionally,the Coral Reef Targeted Research (CRTR) Program, apartnership between the Global Environmental Facilityand the World Bank provided funding and a challeng-ing environment to explore the underpinnings andramifications of global climate change on coral reefsaround the world.

Research in the Storey laboratory (Carolina A.Freire, Alexis F. Welker, Janet M. Storey, Kenneth B.Storey, and Marcelo Hermes-Lima, Chapter 3) is sup-ported by NSERC Canada; Kenneth B. Storey holdsthe Canada Research Chair in Molecular Physiology.Brazilian authors thank CNPq, INCT-CNPq Redoxoma,and DAAD (German Academic Exchange Service).

The work presented by Pauline Snoeijs, PeterSylvander, and Norbert Haubner in Chapter 5 and byPauline Snoeijs, Norbert Haubner, Peter Sylvanderand Xiang-Ping Nie in Chapter 29 was supportedby the research grants Formas 21.9/2003-1033,Formas 21.0/2004-0313, and EU Stukturstod FiV Dnr231-0692-04.

Nelly Tremblay, Tania Zenteno-Savin, Jaime Gomez-Gutierrez, and Alfonso N. Maeda-Martınez (Chapter 6)wish to thank C.J. Robinson, the crews of the R/V ElPuma and R/V Francisco de Ulloa, and the graduatestudents and researchers at ICMyL-UNAM, UABCS,and CICIMAR-IPN for recording hydroacoustic, envi-ronmental information, and collecting zooplanktonsamples; N.O. Olguın-Monroy for technical help inthe biochemical analyses, O.Calvario M. for training inthe use of the Oxymat2000, and S. Martınez-Gomez, O.Angulo-Campillo, J. R. Morales, H. Urias-Leyva, andJ. Cruz for helping to sort out the krill specimensfrom the zooplankton samples. Nelly was supported bygraduate student grants Programa Institucional de For-macion de Investigadores (PIFI-IPN) and Secretarıa deRelaciones Exteriores. This research was supported byCICIMAR-IPN, CONACYT-FOSEMARNAT (2004-01-144), CONACYT- SAGARPA (S007-2005-1-11717),

CIBNOR (PC2.0, PC2.5, PC2.6), and ICMyL-UNAM(IN219502, IN210622).

Marco A. Linan-Cabello, Michael P. Lesser, LauraA. Flores-Ramırez, Tania Zenteno-Savın, and HectorReyes-Bonilla (Chapter 9) would like to thank everyonedirectly and indirectly involved in the research includedin this chapter, too many to be enumerated individu-ally. Research was supported by the Alvarez-Buylla deAldana Foundation, Universidad de Colima, PROMEPof the Secretarıa de Educacion Publica, Mexico (Marco),CIBNOR (Tania), and UABCS (Hector).

Work presented in Chapter 11 by Roberto I. Lopez-Cruz, Alcir Luiz Dafre, and Danilo Wilhelm Filho wasfunded by grants from CONACYT, CIBNOR, and afellowship from Programa de Estudios de Posgrado (CIB-NOR) (to Roberto). The authors wish to thank MarcoAntonio Salazar Bermudez (UABCS) for the artwork.

Mikko Nikinmaa (Chapter 12) is supported by theCentre of Excellence grants from the Academy ofFinland and the University of Turku, Max Gassmannand Anna Bogdanova (Chapter 12) are supportedby the Swiss National Science Foundation (#320030-125013, #310030-124970 and #310030-124970/1) and by the Zurich Center for IntegrativeHuman Physiology.

Research presented by Tania Zenteno-Savın, JosePablo Vazquez-Medina, Nadiezhda Cantu-Medellın,Paul J. Ponganis, and Robert Elsner (Chapter 13) wasfunded by grants from ONR, SEMARNAT-CONACYT,CIBNOR (to Tania), OPP 0944220 (to Paul), andfellowships from Programa de Estudios de Posgradoat CIBNOR (to Jose Pablo and Nadia). Jose Pablo iscurrently supported by UC-Mexus, CONACYT andSecretarıa de Educacion Publica fellowships.

While working on their manuscript (Chapter 14),Alexey A. Sukhotin was supported by Russian Foun-dation for Basic Research (grant #10-04-00316), JuliaStrahl by the German Science foundation (DFG), grantnumbers AB124/10-1 and DR262/10-1, and Eva E.R.Philipp by the DFG Cluster of Excellence ‘‘The FutureOcean.’’

xv

xvi Acknowledgments

The research presented in Chapter 15 by Marıa LuisaFanjul-Moles and Marıa E. Gonsebatt was partiallysupported by PAPIIT IN-207008 (Marıa Luisa) and byPAPIIT IN-207408 (Marıa Eugenia). Marıa Luisa andMarıa Eugenia thank Julio Prieto-Sagredo for his helpwith the figures.

Brenda Valderrama, Gustavo Rodrıguez-Alonso,and Rebecca Pogni (Chapter 16) were funded by theExecutive Program of Scientific and TechnologicalCooperation Mexico-Italy 2006–2009. Brenda andGustavo received additional support from the SNI-STUDENTS fund. Brenda and Gustavo acknowledgefinancial support from CONACYT.

While working on the manuscript Eva Phillip andPhilip Rosentiel (Chapter 17) were supported the by theGerman Science foundation (DFG) Cluster of Excellence‘‘The Future Ocean,’’ Eva Phillip and Simone Lipinski bythe Cluster of Excellence ‘‘Inflammation at Interfaces,’’and Simone Lipinsky by the DFG grant RO2994/5-1‘‘Reactive oxygen species as modulators and effectorsof epithelial defense: A role for Nod-like receptors.’’

Inna M. Sokolova, Alexey A. Sukhotin, and GiselaLannig (Chapter 19) the work of Amalia E. Morales,Amalia Perez-Jimenez, Miriam Furne, and Helga Gud-erley (Chapter 20) was primarily supported by NSERCof Canada, as well as by DFO, with strong collabora-tive support from Jean-Denis Dutil of DFO gratefullyacknowledge the following programs and organiza-tions for support during the work on this manuscript:NSF awards IOS-0921367 and IBN-0347238 to Inna,Russian Foundation for Basic Research Grant #10-04-00316 to Alexey and the PACES research program ofthe Alfred Wegener Institute to Gisela.

Volodymyr I. Lushchak (Chapters 21 and 32),Halyna M. Semchyshyn, and Oleh V. Lushchak(Chapter 32) wish to thank Nadia Semchuk whohelped with figures and artwork.

Jose Marıa Monserrat, Rafaela Elias Letts, Josen-cler L. Ribas Ferreira, Juliane Ventura-Lima, LılianL. Amado, Alessandra M. Rocha, Stefania Gorbi, Raf-faella Bocchetti, Maura Benedetti, and Francesco Regoli(Chapter 23) were supported by funds from the Brazil-ian agency CNPq (Productivity Research Fellowship) toJose and by a grant from the LASPAU/Fincyt PeruvianResearch Fund to Rafaela. Josencler and Alessandraare graduate fellows from CNPq and CAPES, respec-tively. Juliane receives a post-doctoral fellowship fromthe Brazilian Agency CAPES. The support from CAPES(PROCAD Program, Proc. 089/2007) is acknowledgedby Lılian and Jose.

Matthew B. Grisham (Chapter 24) wishes to thank allcurrent and former students and post-doctoral fellowswho contributed greatly to our understanding of therole of reactive oxygen and nitrogen species in acuteand chronic inflammation.

Work presented in Chapters 25 (Graziella ElizaRonsein, Glaucia Regina Martinez, Eduardo Alvesde Almeida, Sayuri Miyamoto, Marisa Helena Gennaride Medeiros, and Paolo Di Mascio), 28 (EduardoAlves de Almeida, Danilo Grunig Humberto Silva,Afonso Celso Dias Bainy, Florencio Porto Freitas,Flavia Daniela Motta, Osmar Francisco Gomes, MarisaHelena Gennari de Medeiros and Paolo Di Mascio), 30(Eduardo Alves de Almeida, Glaucia Regina Martinez,and Paolo Di Mascio), 34 (Sayuri Miyamoto, EduardoAlves de Almeida, Lılian Nogueira, Marisa HelenaGennari de Medeiros, and Paolo Di Mascio), 37 (JosePedro Friedmann Angeli, Glaucia Regina Martinez,Flavia Daniela Motta, Eduardo Alves de Almeida,Marisa Helena Gennari de Medeiros, and Paolo DiMascio) and 38 (Camila Carriao Machado Garcia, JosePedro Friedmann Angeli, Eduardo Alves de Almeida,Marisa Helena Gennari de Medeiros, and Paolo Di Mas-cio) was supported by the Brazilian research fundinginstitutions FAPESP (Fundacao de Amparo a Pesquisado Estado de Sao Paulo), CNPq (Conselho Nacionalpara o Desenvolvimento Cientıfico e Tecnologico),CAPES (Coordenacao de Aperfeicoamento de Pessoalde Nıvel Superior), Pro-Reitoria de Pesquisa USP,Instituto do Milenio: Redoxoma and INCT de ProcessosRedox em Biomedicina – Redoxoma. The authorsalso thank L’OREAL-UNESCO for Women in Science(Sayuri) and The John Simon Memorial GuggenheimFoundation (Paolo) for the fellowships provided.

Betul Catalgol, Stefanie Grimm, and Tilman Grune(Chapter 33) thank COST (B35 and CM1001) forsupport.

Doris Abele thanks the Alfred-Wegener Institute ofPolar and Marine Research in Bremerhaven for sup-porting her oxidative stress working group and itsscientific works in the cold South for many years;and to her colleagues at the AWI, especially ThomasBrey, Christian Wiencke, Fritz Buchholz, and Vic-tor Smetacek for a creative and inspiring workingatmosphere. Doris gratefully acknowledges support byGerman Science Foundation (DFG) throughout hercareer track, during the time when we worked on thebook it was DFGAb124/10-1.

We would like to thank all co-authors for joiningthis venture and the effort each and every one of you

Acknowledgments xvii

invested in making this book reality. We appreciateyour straightforward cooperation and quick responsesto our (sometimes manic) e-mails. We are especiallyproud of the participation of young authors such asJulia Strahl, Nelly Tremblay, Dorothee Dick, PaulaGonzalez, Laura Flores-Ramırez, Gustavo Rodrıguez-Alonso, Josencler Ribas Ferreira, Alessandra Rocha,Juliane Ventura-Lima, Sayuri Miyamoto, DaniloGrunig Humberto Silva, Flavia Daniela Motta, RobertoLopez-Cruz, and Nadia Cantu-Medellın, who wrotebrilliant text passages. Tania and Jose Pablo wish tothank the so-called Secta de Estres Oxidativo for theirpatience, support and dedication.

Citlali Guerra, Stefanie Meyer, Michiel Rutgersvan der Loeff, and Gerhard Diekmann from theAlfred-Wegener Institute, Bremerhaven, and KaiBischoff from the University of Bremen, NormaOlguın-Monroy, Patricia Parrilla-Taylor, PaolaTenorio-Rodrıguez, Marcela Velez-Alavez, VanessaLabrada-Martagon, Ramon Gaxiola-Robles, and

Orlando Lugo-Lugo from Centro de InvestigacionesBiologicas del Noroeste (CIBNOR), kindly took thetime to review and improve chapters of the book. Thephotograph in the front cover was taken by RigobertoMoreno (www.rigobertomoreno.com) in the coast ofNayarit, Mexico. We enormously appreciate Rigo’skind contribution of his artwork for our book.

We dedicate this book to all our students and post-doctoral fellows, past, present and future, who are acontinuous source of inspiration, and who make all ourefforts worth the while.

As editors, Doris, Jose Pablo, and Tania acknowl-edge the support of our home institutions AWI, DFG,CIBNOR, UC-Merced, as well as the funding providedby DAAD, CONACYT, and Secretarıa de EducacionPublica for our research. The cover photograph wastaken by Rigoberto Moreno on the coast of Nayarit,Mexico. The editors appreciate Rigo’s kind contributionof his artwork for our book.

List ofAbbreviations

A •: ascorbyl radicalaaMF: alternatively activated macrophagesAA: arachidonic acidABC: ATP-binding cassetteAChE: acetylcholinesteraseAH •: ascorbateAMPK: adenosine monophosphate kinaseAMT: aminotriazoleAOX: total antioxidant capacityAPAF: poptosis protease-activating factorAPx: ascorbate peroxidaseAhR: aryl hydrocarbon receptorALAD: δ-aminolevulinic acid dehydrataseARNT: AhR nuclear translocatorARE: antioxidant response elementATP: adenosine triphosphateB[a]P: benzo[a]pyreneBHT: butylated hydroxytolueneBKD: bacterial kidney diseaseβ-OHBDH: β hydroxybutyrate dehydrogenasecaMF: classically activated macrophagescAMP: cyclic adenosine monophosphateCAR: constitutively active receptorCAT: catalaseCDK: cyclin-dependent kinasesCDOM: colored dissolved organic matterCFCs: chlorofluorocarbonsCGD: chronic granulomatous diseasecGMP: cyclic nucleotide guanosine monophosphateCHH: crustacean hyperglycemic hormoneCOX: cyclooxygenaseCPD: cyclobutane pyrimidine dimersCS: citrate synthaseCSF: colony-stimulating factorCu,Zn-SOD: copper and zinc-dependent superoxide

dismutaseCyt c: cytochrome cDBNBS: 3,5-dibromo-4-nitrosobenzensulfonate

DCFH-DA: 2′, 7′-dichlorofluorescin-diacetate(DCFH-DA)

DDC: diethyldithiocarbamateDEB: dynamic energy budgetDHAR: dehydroascorbate reductaseDMPO: 5,5-dimethyl-1-pyrroline-N-oxideDMSP: dimethylsulphoniopropionateDMT1: divalent metal cation transporter 1DNA: deoxyribonucleic acidDNIC: dinitrosyl iron complexDNPH: 2,4-dinitrophenylhydrazineDOM: dissolved organic matterDPX: DNA-protein cross-linksECM: extracellular matrixEC-SOD: extracellular superoxide dismutaseEDC: endocrine disrupting chemicalsELISA: enzyme linked immunosorbent assayEPR: electron paramagnetic resonanceEST: expressed sequence tagETC: electron transport chainFAD: flavin-adenine dinucleotideFAP: fluorescent age pigmentsFe-SOD: iron-containing superoxide dismutaseFOC: ferrous oxidation-xylenol orangeFOXO: forkhead box class OG6PDH: glucose-6-phosphate dehydrogenaseGCL glutamate-cysteine ligaseGGT: γ-glutamyl transpeptidaseGIH: gonad inhibiting hormoneGCL: glutamate-cysteine ligaseGR: glutathione disulphide reductaseGPx: glutathione peroxidaseGrx: glutaredoxinGSH: glutathioneGSSG: glutathione disulphideGST: glutathione S-transferaseGTP: guanosine triphosphateH2O2: hydrogen peroxide

xix

xx List of Abbreviations

H2S: hydrogen sulfideHCB: hexachlorobenzeneHGPRT: hypoxanthine guanine phosphoribosyl

transferaseHIF-1: hypoxia inducible factor 1HNE: 4-hydroxy-2-nonenalHO: heme oxygenaseHO •: hydroxyl radicalHO−: hydroxyide anionHO •

2: hydroperoxyl radicalHOAD: hepatic b-hydroxyacyl CoA dehydrogenaseHOCl: hypochlorous acidHOG: high-osmolarity glycerolHRE: hypoxia-response elementHS−: hydrosulphide anionHSF: heat shock inducing factorHSP: heat shock proteinsHSR: heat shock responseHX: hypoxanthineIMP: inosine monophophateIRP: iron-regulatory proteinsLDH: lactate dehydrogenaseLOX: lipoxygenaseLPO: lipid peroxidationLPS: lipopolysaccharideLOO •: peroxyl radicalLOOH: lipid peroxideLRR: leucine-rich repeatsMAA: mycosporine-like amino acidMAMP: microorganism-associated molecular

patternMAP: Mehler-ascorbate pathwayMAPK: mitogen-activated protein kinaseMDA: malondialdehydeMDAR: monodehydroascorbate reductaseMF: methyl farnesoateMHC: major histocompatibility complexMIH: molt inhibiting hormoneMLH: multilocus heterozygosityMn-SOD: manganese-dependent superoxide

dismutaseMNIC: mononitrosyl iron tris(thiolate) complexMNP: 2-methyl-2-nitroso propaneMPO: myeloperoxidaseMT: metallothioneinMV: methyl viologenMXR: multixenobiotic resistance proteinsNADH: nicotinamide adenine dinucleotide hydrogenNADPH: nicotinamide adenine dinucleotide

phosphate hydrogen

NCBI: National Center for BiotechnologyInformation

NF-κB: nuclear factor κBNO •: nitric oxide, nitrogen monoxideNLR: NOD-like receptorNOD: nucleotide-binding oligomerization domainNOS: nitric oxide synthaseNOX: NADPH oxidaseNQO1: NADPH-quinone reductase 1Nrf2: nuclear factor erythroid 2–related factor

8-oxodGuo: 8-oxo-7, 8-dihydro-2′-deoxyguano-sine

O •−2 : superoxide radical

1O2: singlet oxygenONOO−: peroxinitrite anionONOOH: peroxinitrous acidOP: organophosphatePAH: polycyclic aromatic hydrocarbonsPAMP: pathogen-associated molecular patternPAR: photosynthetic active radiationPB: phenobarbitolPBL: peripheral blood lymphocytesPBN: phenyl-t-butyl-nitronePCBs: polychlorinated biphenylsPCN: pregnenolone-16α-carbonitrilePCR: polymerase chain reactionPGG2: prostaglandin endoperoxide G2

PGH2: prostaglandin endoperoxide H2

PGHS: prostaglandin H synthasePGN: peptidoglycanPHD: prolyl hydroxylasesPO2 : oxygen partial pressurePOBN: α(4-pyridyl-1-oxide)-N-t-butyl nitronePOM: particulate organic matterPPAR: peroxisomal proliferator activated receptorPPRE: peroxisome proliferator responsive elementsproPO: prophenoloxidase systemPRR: pattern recognition receptorPrx: peroxiredoxinPS I: photosystem IPS II: photosystem IIPSSG: protein-glutathione mixed disulfidePSU: practical salinity unitsPUFA: polyunsaturated fatty acidpVHL: von Hippel-Lindau proteinPXR: pregnane X receptorR •: alkyl radicalRBC: red blood cellRNA: ribonucleic acidRNS: reactive nitrogen species

List of Abbreviations xxi

ROM: reactive oxygen metabolismRO •: alkoxy radicalROO •: peroxyl radicalROOH: lipid hydroperoxideROS: reactive oxygen speciesRPP: reversible protein phosphorylationRUBISCO: ribulose-1,5-carboxylase/oxygenaseRXR: retinoid X receptorS2−: sulphide anionSMR: standard metabolic rateSOD: superoxide dismutaseSRCR: scavenger receptor cysteine-richST: sulfotransferasesTBARS: thiobarbituric acid reactive substancesTCDD: 2,3,7,8-tetrachlorodibenzo-p-dioxinTF: transcription factorTfR: transferrin receptor

TLR: Toll-like receptorTNF-α:tumor necrosis factor alphaTOSC: total oxyradical scavenging capacityTrx: thioredoxinTSE: transmissible spongiform encephalopathiesUDP-GT: UDP-glucoronosyl transferasesUTR: untranslated regionUVR: ultraviolet radiationVEGF: vascular endothelial growth factorVHSV: viral haemorrhagic septicemia virusVSH: vitellogenesis-stimulating hormoneVTG: vitellogeninWSSV: white spot syndrome virusWWC: water–water cycleXDH: xanthine dehydrogenaseXO: xanthine oxidase

Introductionto Oxidative Stressin Aquatic Ecosystems

Doris Abele1, Jose Pablo Vazquez-Medina2,3,and Tania Zenteno-Savın2

1Alfred Wegener Institute for Polar and Marine Research, Bremerhaven,Germany2Centro de Investigaciones Biologicas del Noroeste, S.C. (CIBNOR), La Paz, BajaCalifornia Sur, Mexico3School of Natural Sciences, University of California Merced, Merced, CA, USA

A quatic ecosystems house a large biosphereof marine and freshwater organisms, highlydiverse in their tolerance of fluctuations in PO2

and temperature, two major modulators of metabolism.Often, both factors act in concert, and some of the mosthypoxia-tolerant fish and molluskan species are indeedfrom cold-water environments. Other marine inverte-brate and fish specialists thrive in the mixed waters athydrothermal vent sites, underwater volcanic outflowswhere warm and hydrogen-sulfide-enriched, deoxy-genated vent waters mix with colder and oxygenatedoceanic waters, and temperatures and oxygen concen-trations are extremely variable. Many vent species caneven deal with toxic hydrogen sulfide that threatensto inhibit their mitochondrial electron transporters.More than 700 Myr of aquatic evolution have fos-tered a huge variety of ectothermic life-forms that candeal with the most extreme and fluctuating environ-mental conditions. The discovery of many fascinatingunderwater biota has raised an interest in the res-piratory capacities of aquatic organisms and in howthey deal with, from our air breathing perspective,

Oxidative Stress in Aquatic Ecosystems, First Edition. Edited by Doris Abele, Jose Pablo Vazquez-Medina, and Tania Zenteno-Savın. 2012 by Blackwell Publishing Ltd.

way too little or way too much and fluctuant oxygenconcentrations. As long ago as 1982, James Dykens andMalcolm Shick (Nature 297, 579–580) discovered thathigh oxygen concentrations, produced by endosym-biontic microalgae, represent a toxic assault whichinduces antioxidant activities in the cnidarian hostcells. In 1984, Janice Blum and Irvin Fridovich inves-tigated the activities of superoxide dismutases (Cu,Zn-,Mn- and Fe-SOD) in tissues of the hydrothermal venttube worm Riftia pachyptila and the bivalve Calypto-gena magnifica (Archives of Biochemistry and Biophysics.228(2), 617–620). Superoxide dismutases detoxifysuperoxide anions (O •−

2 ) by adding another electronand converting O •−

2 to the less reactive, and thereforeless toxic reactive oxygen species (ROS) hydrogen per-oxide (H2O2). Both vent species rely largely on energyproduction by endosymbiontic sulfide-oxidizing bacte-ria but are still endowed with considerable SOD activity,just as are their sulfide-metabolizing endosymbionts,which feature a special procaryotic Fe-SOD isoform. Thecentral message of Blum and Fridovich’s paper is thatcellular antioxidants are ubiquitious and therefore not

1

2 D. Abele, J. P. Vazquez-Medina, and T. Zenteno-Savın

only present in organisms relying primarily on aerobicenergy production. Indeed, SOD enzyme forms de-veloped early in evolution when oxygen started toaccumulate: a toxicant in a primarily anoxic world.Together these two seminal papers started a whole newfield of research, relating oxidative stress and antioxi-dant parameters in marine and freshwater organismsto the conditions prevailing in different aquatic habitatsand microhabitats, such as the host cell environmentsof endosymbionts.

In 2010, a Google Scholar search for ‘‘oxidativestress’’ and ‘‘marine’’ yielded 50,000 publication hits(‘‘oxidative stress’’ and ‘‘aquatic’’ 25,000 hits). Thisis indicative of the enormous interest and intensiveresearch in this field, which prompted us to initiatethis book project. There is also a growing interest inaquatic organisms as models for clinical and aging stud-ies, which is expected to boost comparative research.A great number of diseases in animals and humansinvolve oxidative stress phenomena, and many aquaticorganisms tolerate extreme states, which are patho-logical in humans (e.g. ischemia/reperfusion). Finally,global change and pollution massively threaten andchange the Earth’s ecosystems and, as over 70% ofour planet’s surface area is covered by water, aquaticspecies have become important sentinels and indicatorsof change. Since most forms of environmental and pol-lution stress eventually cause an imbalance betweenoxygen radical-producing and -scavenging processes,oxidative stress parameters are broadly employed inmarine and terrestrial impact studies.

In preparing the concept for this book, it seemedfundamental to determine how climate effects intropical versus polar habitats and natural scenarios inextreme environments shape the basic levels of oxida-tive stress parameters in aquatic ectotherms (Part I,Climate Regions and Special Habitats). Individualchapters focus on life strategies in special habitatsin terms of oxygen availability, such as the sulfidicsedimentary and hydrothermal vent environments, theoxygen minimum layer of the ocean, or the cnidarianhost cell of zooxanthellate endosymbionts. Fluctua-tions of abiotic parameters during tidal cycles conferstress hardening on intertidal species and populations;Chapter 3 delves into the effect of these fluctuationson antioxidant concentrations and enzyme activitiesin animals and plants from the higher littoral zone.Furthermore, long-term seasonal and climate relatedfluctuations modulate oxidative stress parameters inaquatic ecosystems, and Chapters 4 and 5 have a

special focus on the expected consequences for primaryproducers at the base of aquatic food chains.

Part II of this book addresses the specific features ofoxidative stress parameters with respect to respirationin water- and air-breathing aquatic animals. The res-piratory medium water contains 30 times less oxygenper liter than air, and water-breathing organisms aregenerally adapted to perform at these lower oxygenconcentrations. What this means for animal respira-tory performance, including active swimmers such assharks, and how cellular oxygen sensing mechanismshave evolved under aquatic conditions is explored inPart II (Aquatic Respiration and Oxygen Sensing).Furthermore, aquatic animals are increasingly dis-cussed and tested as model organisms for aging anddisease. The longest lived of all noncolonial organismsso far known is the hard clam Arctica islandica. Sev-eral authors have summarized what is new in the fieldof aging in marine ectotherms, a recent hot topic inaging research. Aquatic models for human diseases,including fish and invertebrate immune function andcellular signaling pathways, where ROS play differentroles in development of cancer, are reviewed in PartIII (Marine Animal Models for Aging, Development,and Disease). Many current papers on oxidative stressin aquatic organisms lack information about gender,reproductive or molting state, and age distributionin the experimental animals. While we know that inmany cases it is still difficult to supply these data, westrongly encourage choosing model species that helpus to understand the relevance of life-history-relatedphysiological change on oxidative stress parameters inaquatic ectotherms.

Part IV (Marine Animal Stress Response andBiomonitoring) delves into the general stress responsein aquatic fauna and the applicability of oxidative stressmarkers as indicators of environmental stress andpollution in biomonitoring studies. One important take-home message in many chapters, especially in this Part,is that it does not suffice for stress assessment to compareonly the levels of antioxidants, or measure the rates ofradical production alone. A stress response should becharacterized by measurements of different oxidativedamage markers and antioxidants, ideally comple-mented by a confirmation of higher radical productionunder stress. On one hand, the mere increase in antiox-idant activity of animal tissues is not a confirmation ofa physiological stress condition and, much to the con-trary, can indicate the activation of antioxidant defensesystems in control or anticipation of increased ROS

Introduction to Oxidative Stress In Aquatic Ecosystems 3

production. On the other hand, different toxicants caninterfere with each other, and a decline in antioxidantdefense systems or the absence of a stress signaling (e.g.for immune stimulation) are, in many cases, the resultof toxicant cross-effects, often worsening the situation.

The last and most comprehensive part of the book(Methods of Oxidative Stress Detection) presents anevaluation of classic and modern methods for theassessment of oxidative stress in aquatic animals andplant material. We asked experts in different analyt-ical fields to describe the relevant methods and theiranalytical background. Many of our colleagues notonly provide detailed measurement protocols but alsosuggest where to start troubleshooting. Importantly,the authors of the method chapters make sugges-tions concerning the applicability of different methods.Indeed, the classic methods to assess lipid or protein oxi-dation are widely used and applicable in environmentalstudies, in spite of known constraints with respect toaccuracy and specificity. More accurate techniques arenow available, including those for direct analysis of var-ious radical species or oxidative damage parameters,such as DNA adducts. Often these require complex andcostly analytical equipment, such as an EPR (electronparamagnetic resonance spectrometry) or chromatog-raphy with mass spectrometric detection. The authorsshare their expertise and at the same time evaluate theusefulness of alternative methods for different problemsin aquatic oxidative stress research.

New tools are also coming into reach for geneticand genomic stress research, which promise a rapidadvance in the understanding of molecular pathways inthe response of aquatic organisms to different stressorsand stress scenarios. At present, measurements of tran-script levels can be compared to the antioxidant enzymeactivities in most aquatic organisms, as a growingamount of partial or full sequences become available ingene banks. Antibodies for measuring antioxidant pro-tein levels are less available, perhaps because for manyquestions the catalytic activity seems more functionallyimportant than the amount of enzyme subunits presentin a sample. However, antibodies that tag regulatoryproteins and transcription factors in aquatic speciesare urgently needed for the mechanistic assessment ofstress response capacities in different species. Furtherwork is needed to verify the applicability of mammaliancell stress research kits designed to detect activity ofcellular processes, such as apoptosis and autophagy,in aquatic invertebrates, often genetically distant fromthe originally targeted model system.

In future research it will also be important toestablish closely related model species or single specieswith wide geographical distribution (migrating species)for functional studies of animal adaptation and effectsof climate change in marine and freshwater systems.Cultures of different cell types, such as hemocytes orliver cells of aquatic species, need to be establishedas test systems and for intercalibration of methodsamong laboratories. These mechanistic model systemsand the enormous advances in organic environmentalchemistry, especially with respect to identification andelucidation of chemical compound structures, can beinstrumental in the assessment of pollution and anthro-pogenic disturbance in aquatic habitats and, withina short time, will allow chemists to identify sourcesof pollution in the globally interconnected oceanicenvironments.

An important motivation for us as editors of this bookwas the great enthusiasm of our fellow authors. Thereadiness with which many young authors engagedwith this project was inspiring. We are especially proudof the fact that several chapters were co-authored orhave been reviewed by graduate students from differentlaboratories, who have greatly contributed to improvethe understandability of the text and the completenessof the experimental protocols.

We hope that this book can further stimulateresearch in the exciting field of oxygen toxicity, stressand molecular signaling in marine and freshwaterorganisms.

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