Skip to main content

Advertisement

Log in

Cellular biomarkers to elucidate global warming effects on Antarctic sea urchin Sterechinus neumayeri

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Global warming is a reality and its effects have been widely studied. However, the consequences for marine invertebrates remain poorly understood. Thus, the present study proposed to evaluate the effect of elevated temperature on the innate immune system of Antarctic sea urchin Sterechinus neumayeri. Sea urchins were collected nearby Brazilian Antarctic Station “Comandante Ferraz” and exposed to 0 (control), 2 and 4°C for periods of 48 h, 2, 7 and 14 days. After the experimental periods, coelomic fluid was collected in order to perform the following analyses: coelomocytes differential counting, phagocytic response, adhesion and spreading coelomocytes assay, intranuclear iron crystalloid and ultra structural analysis of coelomocytes. The red sphere cell was considered a biomarker for heat stress, as they increased in acute stress. Besides that, a significant increase in phagocytic indexes was observed at 2°C coinciding with a significant increase of intranuclear iron crystalloid at the same temperature and same time period. Furthermore, significant alterations in cell adhesion and spreading were observed in elevated temperatures. The ultra structural analysis of coelomocytes showed no significant difference across treatments. This was the first time that innate immune response alterations were observed in response to elevated temperature in a Polar echinoid.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bachmann S, Pohla H, Goldschmid A (1980) Phagocytes in the axial complex of the sea urchin Sphaerechinus granularis (Lam.)—fine structure and X-ray microanalysis. Cell Tissue Res 31:109–120. doi:10.1007/BF00236924

    Google Scholar 

  • Beane WS, Voronina E, Wessel GM, McClay DR (2006) Lineage-specific expansions provide genomic complexity among sea urchin GTPases. Dev Biol 300:165–179. doi:10.1016/j.ydbio.2006.08.046

    PubMed  CAS  Google Scholar 

  • Beck G, Ellis T, Zhang HY, Lin WY, Beauregard K, Habicht GS, Truong N (2001) Nitric oxide production by coelomocytes of Asterias forbesi. Dev Comp Immunol 25:1–10. doi:10.1016/S0145-305X(00)00036-7

    PubMed  CAS  Google Scholar 

  • Bernstein L, Bosch P, Canziani O, Chen Z, Christ R, Davidson O, Hare W, Huq S, Karoly D, Kattsov V, Kundzewicz Z, Liu J, Lohmann U, Manning M, Matsuno T, Menne B, Metz M, Mirza M, Nicholls N, Nurse L, Pachauri R, Palutikof J, Parry M, Qin D, Ravindranath N, Reisinger A, Ren J, Riahi K, Rosenzweig C, Rusticucci M, Schneider S, Sokona Y, Solomon S, Stott P, Stouffer R, Sugiyama T, Swart R, Tirpak D, Vogel C, Yohe G (2007) Climate change 2007: synthesis report

  • Bertheussen K, Seljelid R (1978) Echinoid phagocytes in vitro. Exp Cel Res 111:401–412. doi:10.1016/0014-4827(78)90185-4

    CAS  Google Scholar 

  • Bindoff NL, Willebrand J, Artale V, Cazenave A, Gregory J, Gulev S, Hanawa K, Le Quéré C, Levitus S, Nojiri Y, Shum CK, Talley LD, Unnikrishnan A (2007) Observations: oceanic climate change and sea level. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

  • Borges JCS, Porto-Neto LR, Mangiaterra MBCD, Jensch-Junior BE, Silva JRMC (2002) Phagocytosis in vivo and in vitro in the Antarctic Sea Urchin Sterechinus neumayeri at 0°C. Polar Biol 25:891–897. doi:10.1007/s00300-002-0431-6

    Google Scholar 

  • Borges JCS, Branco PC, Pressinotti LN, Severino D, Silva JRMC (2010) Intranuclear crystalloids of Antarctic sea urchins as a biomarker for oil contamination. Polar Biol 33(6):843–849. doi:10.1007/s00300-009-0762-7

    Google Scholar 

  • Boureux A, Vignal E, Faure S, Fort P (2007) Evolution of the Rho Family of Ras-Like GTPases in Eukaryotes. Mol Biol Evol 24(1):203–216. doi:10.1093/molbev/msl145

    PubMed  CAS  Google Scholar 

  • Brock TD, Madigan MT, Martinko JM, Parker J (1994) Biology of microorganism, 7th edn. Prentice-Hall Inc, Englewood Cliffs

    Google Scholar 

  • Calich VLG, Purchio A, Paula CR (1978) A new fluorescent viability test for fungi cells. Mycopathol 66(3):175–177. doi:10.1007/BF00683967

    Google Scholar 

  • Caron E, Hall A (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282:1717–1721. doi:10.1126/science.282.5394.1717

    PubMed  CAS  Google Scholar 

  • Cuéllar-Mata P, Martínez-Cadena G, López-Godínez J, Obregón A, García-Soto J (2000) The GTP-binding protein RhoA localizes to the cortical granules of Strongylocentrotus purpuratus sea urchin egg in secreted during fertilization. Eur J Cell Biol 79(2):81–91. doi:10.1078/S0171-9335(04)70010-2

    PubMed  Google Scholar 

  • D’Andrea-Winslow L, Novitski AK (2008) Active bleb formation in abated Lytechinus variegatus red spherule cells after disruption of acto-myosin contractility. Integr Zool 3(2):115–122. doi:10.1111/j.1749-4877.2008.00086.x

    Google Scholar 

  • Ebert TA, Dixon JD, Schroeter SC, Kalvass PE, Richmond NT, Bradbury WA, Woodby DA (1999) Growth and mortality of red sea urchins Strongylocentrotus franciscanus across a latitudinal gradient. Mar Ecol Prog Ser 190:189–209. doi:10.2983/0730-8000-27.5.1291

    Google Scholar 

  • Freshney RI (1987) Culture of animal cells: a manual of basic technique, 2nd edn. New York

  • Hall A, Nobes CD (2000) Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci 29:965–970. doi:10.1098/rstb.2000.0632

    Google Scholar 

  • Harley CDG, Hughes AR, Hutgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9(2):228–241. doi:10.1111/j.1461-0248.2005.00871.x

    PubMed  Google Scholar 

  • Harvell CD, Kim K, Burkholder JM, Colwell RR, Epsterin PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–1510. doi:10.1126/science.285.5433.1505

    PubMed  CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risk for terrestrial and marine biota. Science 296:2158–2162. doi:10.1126/science.1063699

    PubMed  CAS  Google Scholar 

  • Hayat MA (1981) Fixation for electron microscopy. Academic Press, New York

    Google Scholar 

  • Hobaus E (1978) Studies on phagocytes of regular sea urchins (Echinoidea, Echinodermata) I—the occurrence of iron containing bodies within the nuclei of phagocytes. Zoo Anz 200:31–40. doi:10.1007/BF00236924

    Google Scholar 

  • Isaeva VV, Korenbaum ES (1990) Defence functions of coelomocytes and immunity of echinoderms. Sov J Mar Biol 15:353–363

    Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638. doi:10.1126/science.1059199

    PubMed  CAS  Google Scholar 

  • Jiravanichpaisal P, Söderhäll K, Söderhäll I (2004) Effect of water temperature on the immune response and infectivity pattern of white spot syndrome virus (WSSV) in freshwater crayfish. Fish Shell Immunol 17:265–275. doi:10.1016/j.fsi.2004.03.010

    CAS  Google Scholar 

  • Johnson PT (1969) The coelomic elements of sea urchins (Strongylocentrotus). I. The normal coelomocytes, their morphology and dynamics in hanging drop. J Invertebr Pathol 13:25–41. doi:10.1016/0022-2011(69)90236-5

    PubMed  CAS  Google Scholar 

  • Johnson PT (1971) Studies on disease urchins from Point Loma. In: Kelp habitat improvement project annual report, 1970–71. Calif. Inst. Technol., Pasadena

  • Jones GM, Hebda AJ, Scheibling RE, Miller RJ (1985) Histopathology of the disease causing mass mortality of sea urchins (Strongylocentrotus droebachiensis) in Nova Scotia. J Inv Pathol 45:260–271. doi:10.1016/0022-2011(85)90102-8

    CAS  Google Scholar 

  • Karasaki S (1965) Intranuclear crystal within the phagocytes of the ovary of Arbacia punctulata. J Cell Biol 25(1):654–660. doi:10.1083/jcb.25.3.654

    PubMed  CAS  Google Scholar 

  • Kawakami T, Tsushima M, Katabami Y, Mine M, Ishida A, Matsuno T (1998) Effect of beta, beta-carotene, beta-echinone, astaxanthin, fucosanthin, vitamin A and vitamin E on the biological defense of the sea urchin Pdseudocentrotus depressus. J Exp Mar Biol Ecol 226(2):165–174. doi:10.1056/NEJM199404143301501

    CAS  Google Scholar 

  • Kurihara K, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169. doi:10.3354/meps274161

    Google Scholar 

  • Lafferty KD, Porter JD, Ford SE (2004) Are diseases increasing in the ocean? Ann Rev Ecol Evol Syst 35:31–54. doi:10.1146/annurev.ecolsys.35.021103.105704

    Google Scholar 

  • Lambrechts A, Van Troys M, Ampe C (2004) The actin cytoskeleton in normal and pathological cell motility. Int J Biochem Cell Biol 36:1890–1909. doi:10.1016/j.biocel.2004.01.024

    PubMed  CAS  Google Scholar 

  • Lebedev AV, Levitskaya EL, Tikhonova EV, Ivanova EV (2001) Antioxidant properties, autooxidation, and mutagenic activity of echinochrome a compared with its etherified derivative. Biochem (Mosc) 66(8):885–893. doi:10.1023/A:1011904819563

    CAS  Google Scholar 

  • Maes P, Jangoux M (1984) The bald-sea-urchin disease: a biopathological approach. Helgol Mar Res 37:217–224. doi:10.1007/BF01989306

    Google Scholar 

  • Mangiaterra MBBCD, Silva JRMC (2001) Induced inflammatory process in the sea urchin (Lytechinus variegatus). J Inv Biol 120(2):178–184. doi:10.1111/j.1744-7410.2001.tb00122.x

    Google Scholar 

  • Matranga V, Toia G, Bonaventura R, Muller WEG (2000) Cellular and biochemical responses to environmental and experimentally induced stress in sea urchin coelomocytes. Cell Stress Chaperon 5(2):113–120. doi:csac.2000.158

    CAS  Google Scholar 

  • Matranga V, Pinsino A, Celi M, Natoli A, Bonaventura R, Schröder HC, Müller WEG (2005) Monitoring chemical and physical stress using immune cells. In: Matranga V (ed) Echinodermata. Springer, Berlin, pp 85–110

    Google Scholar 

  • Matranga V, Pinsino A, Celi M, Di Bella G, Natoli A (2006) Impacts of UV-B radiation on short term cultures of sea urchin coelomocytes. Mar Biol 149:25–34. doi:10.1007/s00227-005-0212-1

    CAS  Google Scholar 

  • McCallum H, Harvell D, Dobson A (2003) Rates of spread of marine pathogens. Ecol Lett 6(12):1062–1067. doi:10.1046/j.1461-0248.2003.00545.x

    Google Scholar 

  • McDowell M, Trump BF (1976) Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100:405–414

    PubMed  CAS  Google Scholar 

  • Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Let 32(19):5. doi:10.1029/2005GL024042

    Google Scholar 

  • Morris RL, Hoffman MP, Obar RA, McCafferty SS, Gibbons IR, Leone AD, Cool J, Allgood EL, Musante AM, Judkins KM, Rossetti BJ, Rawson AP, Burgess DR (2006) Analysis of cytoskeletal and motility proteins in the sea urchin genome assembly. Dev Biol 300(1):219–237. doi:10.1016/j.ydbio.2006.08.052

    PubMed  CAS  Google Scholar 

  • Mydlarz LD, Jones LE, Harvell CD (2006) Innate immunity, environmental drivers and disease ecology of marine and freshwater invertebrates. Ann Rev Ecol Evol Syst 37:251–288. doi:10.1146/annurev.ecolsys.37.091305.110103

    Google Scholar 

  • Nishimura Y, Nakano K, Mabuchi I (1998) Localization of Rho GTPase in sea urchin eggs. FEBS Let 441:121–126. doi:10.1016/S0014-5793(98)01531-2

    CAS  Google Scholar 

  • Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144(6):1235–1244. doi:10.1083/jcb.144.6.1235

    PubMed  CAS  Google Scholar 

  • Pancer Z, Rast JP, Davidson EH (1999) Origins of immunity: transcription factors and homologues of effector genes of the vertebrate immune system expressed in sea urchin coelomocytes. Immunogen 49:773–786. doi:10.1007/s002510050551

    CAS  Google Scholar 

  • Pinsino A, Della Torre C, Sammarini V, Bonaventura R, Amato E, Matranga V (2008) Sea urchin coelomocytes as a novel cellular biosensor of environmental stress: a field study in the Tremiti Island Marine Protected Area, Italy. Cell Biol Toxicol 24(6):541–552. doi:10.1007/s10565-008-9055-0

    PubMed  CAS  Google Scholar 

  • Plytycz B, Seljelid R (1993) Bacterial clearance by the sea urchin Strongylocentrotus droebachiensis. Dev Comp Immunol 17:283–289. doi:10.1016/0145-305X(93)90047-T

    PubMed  CAS  Google Scholar 

  • Rabinovitch M (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5:85–88. doi:10.1016/S0962-8924(00)88955-2

    PubMed  CAS  Google Scholar 

  • Reynolds ES (1963) The use of the lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    PubMed  CAS  Google Scholar 

  • Ridley AJ (2001) Rho GTPases and cell migration. J Cell Sci 114:2713–2722

    PubMed  CAS  Google Scholar 

  • Scheibling RE, Feehan C, Lauzon-Guay JS (2010) Disease outbreaks associated with recent hurricanes cause mass mortality of sea urchins in Nova Scotia. Mar Ecol Prog Ser 408:109–116. doi:10.3354/meps08579

    Google Scholar 

  • Sea Urchin Genome Sequencing Consortium, Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI et al (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314(5801):941–952. doi:10.1126/science.1133609

    PubMed  Google Scholar 

  • Secombes CJ (1996) The non-specific immune system: cellular defenses. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, UK, pp 63–95

    Google Scholar 

  • Secombes CJ, Fletcher TC (1992) The role of phagocytes in the protective mechanisms of fish. Ann Rev Fish Disease 2:53–71. doi:10.1016/0959-8030(92)90056-4

    Google Scholar 

  • Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110:C09S08. doi:10.1029/2004JC002618

  • Silva JRMC, Peck L (2000) Induced in vitro phagocytosis of the Antarctic starfish Odontaster validus (Koehler, 1906) at 0°C. Polar Biol 23(4):225–230. doi:10.1007/s003000050438

    Google Scholar 

  • Silva JRMC, Vellutini BC, Porto Neto LR, Pressinotti LN, Ramos MC, Cooper EL, Hernandez-Blazquez FJ, Jensch Junior BE, Borges JCS (2007) Resposta imune inespecífica de animais ectotérmicos Antárticos sob temperatura polares. Oecol Bras 11(1):110–112. doi:10.4257/oeco.2007.1101.11

    Google Scholar 

  • Smith LC, Britten RJ, Davidson EH (1992) SpCoel1, a sea urchin profilin gene expressed specifically in coelomocytes in response to injury. Mol Biol Cell 3:403–414

    PubMed  CAS  Google Scholar 

  • Smith LC, Rast JP, Brocton V, Terwilleger DP, Nair SV, Bucley KM, Majestke AJ (2006) The sea urchin immune system. ISJ 3:25–29

    Google Scholar 

  • Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT (2009) Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Nature Lett 457:459–462. doi:10.1038/nature07669

    CAS  Google Scholar 

  • Tajima K, Takeuchi K, Takahata M, Hasegawa M, Watanabe S, Iqbal MM, Ezura Y (2000) Seasonal occurrence of the pathogenic Vibrio sp. of the disease of sea urchin Strongylocentrotus intermedius occurring of low water temperature and the preservation methods of the disease. Grad Sch Fisheries Sci 66(5):799–804

    Google Scholar 

  • Tajima K, Silva JRMC, Lawrence JM (2007) Immunological Response to bacterial disease. In: Lawrence JM (ed) Edible sea urchin: biology and ecology. Elsevier, UK, pp 167–182

    Google Scholar 

  • Tauber AI, Chernyak L (1997) Metchnikoff and the origins of immunology, from metaphor to theory. Oxford University Press, New York

    Google Scholar 

Download references

Acknowledgments

The authors want to express their acknowledgements to Secirm (Secretaria Interministerial para os Recursos do Mar) and the Brazilian Navy for logistical support in Antarctica, CEBIMar-USP for supporting the pilot experiments and to FAPESP, CAPES and CNPq for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paola Cristina Branco.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Branco, P.C., Pressinotti, L.N., Borges, J.C.S. et al. Cellular biomarkers to elucidate global warming effects on Antarctic sea urchin Sterechinus neumayeri . Polar Biol 35, 221–229 (2012). https://doi.org/10.1007/s00300-011-1063-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-011-1063-5

Keywords

Navigation