Age-dependent expression of stress and antimicrobial genes in the hemocytes and siphon tissue of the Antarctic bivalve, Laternula elliptica, exposed to injury and starvation

Cell Stress and Chaperones

Volumn 19, Issue 1, 2014, Pages 15-32

  Husmann, G ^a   Abele, D ^b   Rosenstiel, P ^a   Clark, M S ^c   Kraemer, L ^a   Philipp, E E R ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c BRITISH ANTARCTIC SURVEY   (United Kingdom)

Author keywords

Antioxidants; Climate change; Immune response; Transcriptome; Western Antarctic Peninsula

Indexed keywords

ACTIN; ANTIOXIDANT; CATALASE; CHITINASE; COMPLEMENTARY DNA; HEAT SHOCK PROTEIN 70; RNA 18S; SUPEROXIDE DISMUTASE; THEROMACIN; TISSUE INHIBITOR OF METALLOPROTEINASE; UNCLASSIFIED DRUG;

18S RRNA GENE; ACTIN GENE; AGE DISTRIBUTION; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTARCTICA; ANTIMICROBIAL GENE; ARTICLE; BIVALVE; BLOOD CELL; CATALASE GENE; CELLULAR STRESS RESPONSE; CLAM; CONTROLLED STUDY; DILUTION; ENVIRONMENTAL CHANGE; HIGH THROUGHPUT SCREENING; HSP70 GENE; IMMUNE RESPONSE; LATERNULA ELLIPTICA; MICROBIAL GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SEQUENCE; SEDIMENTATION; SIPHON TISSUE; SOD GENE; STARVATION; THEROMACIN GENE; TIMP GENE; TISSUE INJURY; UNINDEXED SEQUENCE; UPREGULATION;

ACTINS; AGING; ANIMALS; ANTARCTIC REGIONS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BIVALVIA; CATALASE; CHITINASE; DATABASES, GENETIC; GENE EXPRESSION REGULATION; HEMOCYTES; HSP70 HEAT-SHOCK PROTEINS; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; TISSUE INHIBITOR OF METALLOPROTEINASES; WOUNDS AND INJURIES;

EID: 84891064941     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-013-0431-1     Document Type: Article

References (93)

1. Adema CM, Vandeutekommulder EC, Vanderknaap WPW, Meuleman EA, Sminia T (1991) Generation of oxygen radicals in hemocytes of the snail Lymnaea stagnalis in relation to the rate of phagocytosis. Dev Comp Immunol 15(1-2):17-26
2. Ahn IY (1997) Feeding ecology of the Antarctic lamellibranch Laternula elliptica (Laternulidae) in Marian Cove vicinity, King George Island, during one austral summer. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 142-151
3. Anderson RS (1994) Hemocyte-derived reactive oxygen intermediate production in 4 bivalve mollusks. Dev Comp Immunol 18(2):89-96 (Pubitemid 24166338)
4. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26(1):32-46 (Pubitemid 33719668)
5. Atencio AG, Bertolin ML, Longhi L, Ferreyra GA, Ferrario ME, Schloss IR (2008) Spatial and temporal variability of chlorophyll-a and particulate organic matter in the sediments and the water column of Potter Cove (Antarctica). Reports on polar and marine research, vol 571. Alfred Wegener Institute for Polar and Marine Research, Bremerhaven
6. Bachere E, Mialhe E, Noel D, Boulo V, Morvan A, Rodriguez J (1995) Knowledge and research prospects in marine mollusk and crustacean immunology. Aquaculture 132(1-2):17-32
7. Badariotti F, Kypriotou M, Lelong C, Dubos MP, Renard E, Galera P, Favrel P (2006) The phylogenetically conserved molluscan chitinase-like protein 1 (Cg-Clp1), homologue of human HC-gp39, stimulates proliferation and regulates synthesis of extracellular matrix components of mammalian chondrocytes. J Biol Chem 40:29583-29596. doi: 10.1074/jbc.M605687200 (Pubitemid 44536966)
8. Badariotti F, Lelong C, Dubos MP, Favrel P (2007a) Characterization of chitinase-like proteins (Cg-Clp1 and Cg-Clp2) involved in immune defence of the mollusc Crassostrea gigas. FEBS J 274(14):3646-3654. doi: 10.1111/j.1742-4658. 2007.05898.x (Pubitemid 47052403)
9. Badariotti F, Thuau R, Lelong C, Dubos MP, Favrel P (2007b) Characterization of an atypical family 18 chitinase from the oyster Crassostrea gigas: evidence for a role in early development and immunity. Dev Comp Immunol 31(6):559-570. doi: 10.1016/j.dci.2006.09.002 (Pubitemid 46111082)
10. Ballarin L, Pampanin DM, Marin MG (2003) Mechanical disturbance affects haemocyte functionality in the Venus clam Chamelea gallina. Comp Biochem Physiol A 136(3):631-640. doi: 10.1016/S1095-6433(03)00216-2 (Pubitemid 37412393)
11. Barnes DKA, Conlan KE (2007) Disturbance, colonization and development of Antarctic benthic communities. Philos T R Soc B 362(1477):11-38. doi: 10.1098/rstb.2006.1951 (Pubitemid 47055510)
12. Barnes DKA, Kaiser S (2007) Melting of polar icecaps: impact on marine biodiversity. Encyclopedia of Life Support Systems (EOLSS). Developed under the auspices of the UNESCO, EOLSS Publishers, Oxford, UK
13. Barnes DKA, Souster T (2011) Reduced survival of Antarctic benthos linked to climate-induced iceberg scouring. Nat Clim Chang 1(7):365-368. doi: 10.1038/Nclimate1232
14. Beaz-Hidalgo R, Balboa S, Romalde JL, Figueras MJ (2010) Diversity and pathogenicity of Vibrio species in cultured bivalve molluscs. Env Microbiol Rep 2(1):34-43. doi: 10.1111/j.1758-2229.2010.00135.x
15. Bettencourt R, Roch P, Stefanni S, Rosa D, Colaco A, Santos RS (2007) Deep sea immunity: unveiling immune constituents from the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 64:108-127 (Pubitemid 46990516)
16. Bonneh-Barkay D, Zagadailov P, Zou HC, Niyonkuru C, Figley M, Starkey A, Wang GJ, Bissel SJ, Wiley CA, Wagner AK (2010) YKL-40 expression in traumatic brain injury: an initial analysis. J Neurotrauma 27(7):1215-1223. doi: 10.1089/neu.2010.1310
17. Brown KM, Fraser KPP, Barnes DKA, Peck LS (2004) Links between the structure of an Antarctic shallow-water community and ice-scour frequency. Oecologia 141(1):121-129. doi: 10.1007/s00442-004-1648-6 (Pubitemid 39320472)
18. Bussell JA, Gidman EA, Causton DR, Gwynn-Jones D, Malham SK, Jones MLM, Reynolds B, Seed R (2008) Changes in the immune response and metabolic fingerprint of the mussel, Mytilus edulis (Linnaeus) in response to lowered salinity and physical stress. J Exp Mar Biol Ecol 358(1):78-85. doi: 10.1016/j.jembe.2008.01.018
19. Butt D, Aladaileh S, O'Connor WA, Raftos DA (2007) Effect of starvation on biological factors related to immunological defence in the Sydney rock oyster (Saccostrea glomerata). Aquaculture 264(1-4):82-91. doi: 10.1016/j.aquaculture. 2006.12.031 (Pubitemid 46365817)
20. Canesi L, Gallo G, Gavioli M, Pruzzo C (2002) Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc Res Techn 57(6):469-476. doi: 10.1002/Jemt.10100 (Pubitemid 34701147)
21. Canesi L, Barmo C, Fabbri R, Ciacci C, Vergani L, Roch P, Gallo G (2010) Effects of Vibrio challenge on digestive gland biomarkers and antioxidant gene expression in Mytilus galloprovincialis. Comp Biochem Phys C 152(3):399-406. doi: 10.1016/j.cbpc.2010.06.008
22. Chen L, Wu W, Dentchev T, Zeng Y, Wang JH, Tsui I, Tobias JW, Bennett J, Baldwin D, Dunaief JL (2004) Light damage induced changes in mouse retinal gene expression. Exp Eye Res 79(2):239-247. doi: 10.1016/j.exer.2004.05.002 (Pubitemid 39119413)
23. Chu FLE, Volety AK, Hale RC, Huang YQ (2002) Cellular responses and disease expression in oysters (Crassostrea virginica) exposed to suspended field - contaminated sediments. Mar Environ Res 53(1):17-35 (Pubitemid 32970719)
24. Clark MS, Peck LS (2009) HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a mini-review. Mar Genomics 2(1):11-18. doi: 10.1016/j.margen.2009.03.003
25. Clark MS, Bendell L, Power DM, Warner S, Elgar G, Ingleton PM (2002) Calcitonin: characterisation and expression in a teleost fish, Fugu rubripes. J Mol Endocrinol 28(2):111-123. doi: 10.1677/jme.0.0280111 (Pubitemid 34428761)
26. Clark MS, Fraser KPP, Peck LS (2008a) Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperones 13(1):39-49. doi: 10.1007/s12192-008-0014-8
27. Clark MS, Fraser KPP, Peck LS (2008b) Lack of an HSP70 heat shock response in two Antarctic marine invertebrates. Polar Biol 31(9):1059-1065. doi: 10.1007/s00300-008-0447-7
28. Clark MS, Thorne MAS, Vieira FA, Cardoso JCR, Power DM, Peck LS (2010) Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing. Bmc Genomics 11:362. doi: 10.1186/1471-2164-11-362
29. Clark MS, Husmann G, Thorne MAS, Burns G, Truebano M, Peck LS, Abele D, Philipp EER (2013) Hypoxia impacts large adults first: consequences in a warming world. Glob Change Biol doi: 10.1111/gcb.12197
30. Clarke A, Meredith MP, Wallace MI, Brandon MA, Thomas DN (2008) Seasonal and interannual variability in temperature, chlorophyll and macronutrients in northern Marguerite Bay, Antarctica. Deep-Sea Res II Top Stud Oceanogr 55(18-19):1988-2006
31. Cook AJ, Fox AJ, Vaughan DG, Ferrigno JG (2005) Retreating glacier fronts on the Antarctic Peninsula over the past half-century. Science 308(5721):541-544. doi: 10.1126/science.1104235 (Pubitemid 40570582)
32. Cummings V, Hewitt J, Van Rooyen A, Currie K, Beard S, Thrush S, Norkko J, Barr N, Heath P, Halliday NJ, Sedcole R, Gomez A, McGraw C, Metcalf V (2011) Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS One 6(1):e16069. doi: 10.1371/journal.pone.0016069
33. De Decker S, Saulnier D (2011) Vibriosis induced by experimental cohabitation in Crassostrea gigas: evidence of early infection and down-expression of immune-related genes. Fish Shellfish Immun 30(2):691-699. doi: 10.1016/j.fsi.2010.12.017
34. de Eguileor M, Tettamanti G, Grimaldi A, Boselli A, Scari G, Valvassori R, Cooper EL, Lanzavecchia G (1999) Histopathological changes after induced injury in leeches. J Invertebr Pathol 74(1):14-28 (Pubitemid 129498894)
35. De Zoysa M, Whang I, Lee Y, Lee S, Lee JS, Lee J (2009) Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress. Comp Biochem Phys B 154(4):387-395. doi: 10.1016/j.cbpb.2009.08.002
36. Delaporte M, Soudant P, Moal J, Lambert C, Quere C, Miner P, Choquet G, Paillard C, Samain JF (2003) Effect of a mono-specific algal diet on immune functions in two bivalve species - Crassostrea gigas and Ruditapes philippinarum. J Exp Biol 206(17):3053-3064. doi: 10.1242/Jeb.00518 (Pubitemid 37073841)
37. Delaporte M, Soudant P, Lambert C, Moal J, Pouvreau S, Samain JF (2006) Impact of food availability on energy storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254(1-4):571-582. doi: 10.1016/j.aquaculture. 2005.10.006 (Pubitemid 43732333)
38. Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927-930 (Pubitemid 38204033)
39. Dominguez C, Eraso A (2007) Substantial changes happened during the last years in the icecap of King George, Insular Antarctica. Karst and Cryokarst, Studies of the Faculty of Earth Sciences, University of Silesia 45:87-110
40. Donaghy L, Lambert C, Choi KS, Soudant P (2009) Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): current knowledge and future prospects. Aquaculture 297(1-4):10-24. doi: 10.1016/j.aquaculture.2009.09.003
41. Fisher WS, Auffret M, Balouet G (1987) Response of European flat oyster (Ostrea edulis) hemocytes to acute salinity and temperature changes. Aquaculture 67(1-2):179-190
42. Hawley DM, Altizer SM (2011) Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25(1):48-60. doi: 10.1111/j.1365-2435.2010. 01753.x
43. Hegaret H, Wikfors GH, Soudant P, Delaporte M, Alix JH, Smith BC, Dixon MS, Quere C, Le Coz JR, Paillard C, Moal J, Samain JF (2004) Immunological competence of eastern oysters, Crassostrea virginica, fed different microalgal diets and challenged with a temperature elevation. Aquaculture 234(1-4):541-560. doi: 10.1016/j.aquaculture.2004.01.010 (Pubitemid 38484864)
44. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJA, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211-D215. doi: 10.1093/Nar/Gkn785
45. Husmann G, Philipp EER, Rosenstiel P, Vazquez S, Abele D (2011) Immune response of the Antarctic bivalve Laternula elliptica to physical stress and microbial exposure. J Exp Mar Biol Ecol 398(1-2):83-90. doi: 10.1016/j.jembe.2010.12.013
46. Ju ZL, Wells MC, Heater SJ, Walter RB (2007) Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia. Comp Biochem Phys C 145(1):134-144. doi: 10.1016/j.cbpc.2006.06.012 (Pubitemid 46210199)
47. Kadar E (2008) Haemocyte response associated with induction of shell regeneration in the deep-sea vent mussel Bathymodiolus azoricus (Bivalvia: Mytilidae). J Exp Mar Biol Ecol 362(2):71-78. doi: 10.1016/j.jembe.2008.05.014
48. Koutsogiannaki S, Kaloyianni M (2010) Signaling molecules involved in immune responses in mussels. Invertebr Surviv J 7:11-21
49. Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas J-L (2006) Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes Infect 8(12-13):2715-2724 (Pubitemid 44773719)
50. Lagente V, Boichot E (2010) Role of matrix metalloproteinases in the inflammatory process of respiratory diseases. J Mol Cell Cardiol 48(3):440-444. doi: 10.1016/j.yjmcc.2009.09.017
51. Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang MJ, He CH, Takyar S, Elias JA (2011) Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 73:479-501. doi: 10.1146/annurev-physiol-012110-142250
52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25(4):402-408. doi: 10.1006/meth.2001.1262 (Pubitemid 34164012)
53. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88(1):87-98 (Pubitemid 30121291)
54. Malham SK, Lacoste A, Gelebart F, Cueff A, Poulet SA (2003) Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata. J Exp Zool Part A 295A(2):136-144. doi: 10.1002/Jez.A.10222 (Pubitemid 37529111)
55. Momo F, Kowalke J, Schloss I, Mercuri G, Ferreyra G (2002) The role of Laternula elliptica in the energy budget of Potter Cove (King George Island, Antarctica). Ecol Model 155(1):43-51 (Pubitemid 34829505)
56. Monari M, Foschi J, Cortesi P, Rosmini R, Cattani O, Serrazanetti GP (2008) Chloramphenicol influence on antioxidant enzymes with preliminary approach on microsomal CYP1A immunopositive-protein in Chamelea gallina. Chemosphere 73(3):272-280. doi: 10.1016/j.chemosphere.2008.06.033
57. Montagnani C, Le Roux F, Berthe F, Escoubas JM (2001) Cg-TIMP, an inducible tissue inhibitor of metalloproteinase from the Pacific oyster Crassostrea gigas with a potential role in wound healing and defense mechanisms. FEBS Lett 500(1-2):64-70 (Pubitemid 32575320)
58. Montagnani C, Avarre JC, de Lorgeril J, Quiquand M, Boulo V, Escoubas JM (2007) First evidence of the activation of Cg-timp, an immune response component of pacific oysters, through a damage-associated molecular pattern pathway. Dev Comp Immunol 31(1):1-11. doi: 10.1016/j.dci.2006.04.002 (Pubitemid 44467970)
59. Morley NJ (2010) Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquat Toxicol 96(1):27-36. doi: 10.1016/j.aquatox.2009.09. 017
60. Morley SA, Peck LS, Tan KS, Martin SM, Portner HO (2007) Slowest of the slow: latitudinal insensitivity of burrowing capacity in the bivalve Laternula. Mar Biol 151(5):1823-1830. doi: 10.1007/s00227-007-0610-7 (Pubitemid 46789075)
61. Mydlarz LD, Jones LE, Harvell CD (2006) Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol S 37:251-288. doi: 10.1146/annurev.ecolsys.37.091305.110103 (Pubitemid 44907619)
62. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens HHH, Wagner H (2011) vegan: community ecology package. R package version 2.0-0. Available at http://CRAN.R-project.org/ package=vegan
63. Oliver LM, Fisher WS, Winstead JT, Hemmer BL, Long ER (2001) Relationships between tissue contaminants and defense-related characteristics of oysters (Crassostrea virginica) from five Florida bays. Aquat Toxicol 55(3-4):203-222 (Pubitemid 32928480)
64. Ottaviani E, Franchini A, Malagoli D (2010) Inflammatory response in molluscs: cross-taxa and evolutionary considerations. Curr Pharm Des 16(38):4160-4165
65. Oubella R, Maes P, Paillard C, Auffret M (1993) Experimentally induced variation in hemocyte density for Ruditapes philippinarum and R. decussatus (Mollusca, Bivalvia). Dis Aquat Organ 15(3):193-197
66. Park H, Ahn IY, Lee HE (2007) Expression of heat shock protein 70 in the thermally stressed Antarctic clam Laternula elliptica. Cell Stress Chaperones 12(3):275-282 (Pubitemid 351199390)
67. Park H, Ahn IY, Lee JK, Shin SC, Lee J, Choy EJ (2009) Molecular cloning, characterization, and the response of manganese superoxide dismutase from the Antarctic bivalve Laternula elliptica to PCB exposure. Fish Shellfish Immun 27(3):522-528. doi: 10.1016/j.fsi.2009.07.008
68. Peck LS (1998) Feeding, metabolism and metabolic scope in Antarctic marine ectotherms. In: Pörtner HO, Playle R (eds) Cold ocean physiology. Cambridge University Press, Cambridge, pp 365-390
69. Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25(1):31-40. doi: 10.1007/s003000100308 (Pubitemid 36058961)
70. Peck LS, Conway LZ (2000) The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. Geol Soc Lond Spec Publ 177(1):441-450. doi: 10.1144/gsl.sp.2000.177.01.29
71. Peck LS, Morley SA, Portner HO, Clark MS (2007) Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica. Oecologia 154(3):479-484. doi: 10.1007/s00442-007- 0858-0 (Pubitemid 350165634)
72. Peck LS, Veal R (2001) Feeding, metabolism and growth in the Antarctic limpet, Nacella concinna (Strebel 1908). Mar Biol 138(3):553-560. doi: 10.1007/s002270000486 (Pubitemid 32242970)
73. Peck LS, Ansell AD, Webb KE, Hepburn L, Burrows M (2004) Movements and burrowing activity in the Antarctic bivalve molluscs Laternula elliptica and Yoldia eightsi. Polar Biol 27(6):357-367 (Pubitemid 38784092)
74. Philipp EER, Abele D (2010) Masters of longevity: lessons from long-lived bivalves - a mini-review. Gerontology 56(1):55-65. doi: 10.1159/000221004
75. Philipp E, Brey T, Pörtner HO, Abele D (2005a) Chronological and physiological ageing in a polar and a temperate mud clam. Mech Ageing Dev 126(5):598-609. doi: 10.1016/j.mad.2004.12.003 (Pubitemid 40461959)
76. Philipp E, Pörtner HO, Abele D (2005b) Mitochondrial ageing of a polar and a temperate mud clam. Mech Ageing Dev 126(5):610-619. doi: 10.1016/j.mad.2005.02.002 (Pubitemid 40461960)
77. Philipp E, Brey T, Voigt M, Abele D (2008) Growth and age of Laternula elliptica populations in Potter Cove, King-George Island. Reports on polar and marine research, vol 571. Alfred Wegener Institute for Polar and Marine Research, Bremerhaven
78. Philipp E, Husmann G, Abele D (2011) The impact of sediment deposition and iceberg scour on the Antarctic soft shell clam Laternula elliptica at King George Island, Antarctica. Antarct Sci 23:127-138
79. Philipp EER, Kraemer L, Mountfort D, Schilhabel M, Schreiber S, Rosenstiel P (2012a) The Transcriptome Analysis and Comparison Explorer - T-ACE: a platform-independent, graphical tool to process large RNAseq datasets of non-model organisms. Bioinformatics 28(6):777-783. doi: 10.1093/bioinformatics/ bts056
80. Philipp EER, Lipinski S, Rast J, Rosenstiel P (2012b) Immune defense of marine invertebrates: the role of reactive oxygen and nitrogen species. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in aquatic ecosystems. Blackwell, Chichester, p 524
81. Pöhlmann K, Koenigstein S, Alter K, Abele D, Held C (2011) Heat-shock response and antioxidant defense during air exposure in Patagonian shallow-water limpets from different climatic habitats. Cell Stress Chaperones 16(6):621-632. doi: 10.1007/s12192-011-0272-8
82. Pruzzo C, Gallo G, Canesi L (2005) Persistence of vibrios in marine bivalves: the role of interactions with haemolymph components. Environ Microbiol 7(6):761-772. doi: 10.1111/j.1462-2920.2005.00792.x (Pubitemid 40697634)
83. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol (Clifton, NJ) 132:365-386
84. Santoro MG (2000) Heat shock factors and the control of the stress response. Biochem Pharmacol 59(1):55-63
85. Schloss IR, Abele D, Moreau S, Demers S, Bers AV, González O, Ferreyra GA (2012) Response of phytoplankton dynamics to 19-year (1991-2009) climate trends in Potter Cove (Antarctica). J Mar Syst 92(1):53-66
86. Siciński J, Pabis K, Jazdzewski K, Konopacka A, Błazewicz-Paszkowycz M (2012) Macrozoobenthos of two Antarctic glacial coves: a comparison with non-disturbed bottom areas. Polar Biol 35(3):355-367. doi: 10.1007/s00300-011-1081-3
87. Song LS, Wu LT, Ni DJ, Chang YQ, Xu W, Xing KZ (2006) The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish Shellfish Immun 21(4):335-345. doi: 10.1016/j.fsi.2005.12.011 (Pubitemid 43974982)
88. Tirape A, Bacque C, Brizard R, Vandenbulcke F, Boulo V (2007) Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev Comp Immunol 31(9):859-873. doi: 10.1016/j.dci.2007.01.005 (Pubitemid 46584736)
89. Tomanek L (2011) Environmental proteomics: changes in the proteome of marine organisms in response to environmental stress, pollutants, infection, symbiosis, and development. Annu Rev Mar Sci 3:373-399. doi: 10.1146/annurev-marine-120709-142729
90. Turner J, Bindschadler RA, Convey P, Di Prisco G, Fahrbach E, Gutt J, Hodgson DA, Mayewski PA, Summerhayes CP (eds) (2009) Antarctic climate change and the environment. Scientific Committee on Antarctic Research, Cambridge
91. Venier P, Varotto L, Rosani U, Millino C, Celegato B, Bernante F, Lanfranchi G, Novoa B, Roch P, Figueras A, Pallavicini A (2011) Insights into the innate immunity of the Mediterranean mussel Mytilus galloprovincialis. BMC Genomics 12:69. doi: 10.1186/1471-2164-12-69
92. Xu W, Faisal M (2009) Identification of the molecules involved in zebra mussel (Dreissena polymorpha) hemocytes host defense. Comp Biochem Phys B 154 (1):143-149. doi: 10.1016/j.cbpb.2009.05.012
93. Xu QQ, Wang GL, Yuan HW, Chai Y, Xiao ZL (2010) cDNA sequence and expression analysis of an antimicrobial peptide, theromacin, in the triangle-shell pearl mussel Hyriopsis cumingii. Comp Biochem Phys B 157(1):119-126. doi: 10.1016/j.cbpb.2010.05.010