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Front Zool. 2015 Mar 11;12:6. doi: 10.1186/s12983-015-0097-x. eCollection 2015.

Blue blood on ice: modulated blood oxygen transport facilitates cold compensation and eurythermy in an Antarctic octopod.

Frontiers in zoology

Michael Oellermann, Bernhard Lieb, Hans-O Pörtner, Jayson M Semmens, Felix C Mark

Affiliations

  1. Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.
  2. Institute of Zoology, Johannes Gutenberg-Universität, Müllerweg 6, 55099 Mainz, Germany.
  3. Fisheries, Aquaculture and Coasts Centre, Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Hobart, Tasmania 7001 Australia.

PMID: 25897316 PMCID: PMC4403823 DOI: 10.1186/s12983-015-0097-x

Abstract

INTRODUCTION: The Antarctic Ocean hosts a rich and diverse fauna despite inhospitable temperatures close to freezing, which require specialist adaptations to sustain animal activity and various underlying body functions. While oxygen transport has been suggested to be key in setting thermal tolerance in warmer climates, this constraint is relaxed in Antarctic fishes and crustaceans, due to high levels of dissolved oxygen. Less is known about how other Antarctic ectotherms cope with temperatures near zero, particularly the more active invertebrates like the abundant octopods. A continued reliance on the highly specialised blood oxygen transport system of cephalopods may concur with functional constraints at cold temperatures. We therefore analysed the octopod's central oxygen transport component, the blue blood pigment haemocyanin, to unravel strategies that sustain oxygen supply at cold temperatures.

RESULTS: To identify adaptive compensation of blood oxygen transport in octopods from different climatic regions, we compared haemocyanin oxygen binding properties, oxygen carrying capacities as well as haemolymph protein and ion composition between the Antarctic octopod Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata. In the Antarctic Pareledone charcoti at 0°C, oxygen unloading by haemocyanin was poor but supported by high levels of dissolved oxygen. However, lower oxygen affinity and higher oxygen carrying capacity compared to warm water octopods, still enabled significant contribution of haemocyanin to oxygen transport at 0°C. At warmer temperatures, haemocyanin of Pareledone charcoti releases most of the bound oxygen, supporting oxygen supply at 10°C. In warm water octopods, increasing oxygen affinities reduce the ability to release oxygen from haemocyanin at colder temperatures. Though, unlike Eledone moschata, Octopus pallidus attenuated this increase below 15°C.

CONCLUSIONS: Adjustments of haemocyanin physiological function and haemocyanin concentrations but also high dissolved oxygen concentrations support oxygen supply in the Antarctic octopus Pareledone charcoti at near freezing temperatures. Increased oxygen supply by haemocyanin at warmer temperatures supports extended warm tolerance and thus eurythermy of Pareledone charcoti. Limited haemocyanin function towards colder temperatures in Antarctic and warm water octopods highlights the general role of haemocyanin oxygen transport in constraining cold tolerance in octopods.

Keywords: Cephalopod; Diffusion chamber; Eledone moschata; Haemocyanin; Hemocyanin; Octopus pallidus; Oxygen affinity; Oxygen carrying capacity; Pareledone charcoti

References

  1. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1237):655-66, discussion 666-7 - PubMed
  2. Comp Biochem Physiol A Mol Integr Physiol. 2002 Aug;132(4):739-61 - PubMed
  3. Mol Biol Evol. 2000 Apr;17(4):540-52 - PubMed
  4. Nature. 1954 May 8;173(4410):848-50 - PubMed
  5. Comp Biochem Physiol A Mol Integr Physiol. 2002 Aug;132(4):797-810 - PubMed
  6. Respir Physiol. 1972 Mar;14(1):219-36 - PubMed
  7. Acta Physiol (Oxf). 2011 Jul;202(3):549-62 - PubMed
  8. Arch Biochem Biophys. 1992 Jan;292(1):295-302 - PubMed
  9. PLoS One. 2013 May 28;8(5):e64120 - PubMed
  10. J Exp Biol. 2007 Jan;210(Pt 1):1-11 - PubMed
  11. Biochemistry. 1985 Aug 13;24(17):4582-6 - PubMed
  12. Comp Biochem Physiol A Mol Integr Physiol. 2002 Aug;132(4):789-95 - PubMed
  13. Gene. 2007 Aug 15;398(1-2):143-55 - PubMed
  14. Am J Physiol Regul Integr Comp Physiol. 2000 Nov;279(5):R1531-8 - PubMed
  15. J Exp Biol. 1988 Jul;137:549-63 - PubMed
  16. J Mol Biol. 1998 May 15;278(4):827-42 - PubMed
  17. J Exp Biol. 1998 Apr;201(Pt 8):1119-28 - PubMed
  18. J Exp Biol. 1977 Apr;67:77-88 - PubMed
  19. Experientia. 1992 May 15;48(5):473-5 - PubMed
  20. Am J Physiol. 1965 Nov;209(5):991-8 - PubMed
  21. Nucleic Acids Res. 2004 Mar 19;32(5):1792-7 - PubMed
  22. Science. 2001 Apr 27;292(5517):686-93 - PubMed
  23. Adv Mar Biol. 2006;50:191-265 - PubMed
  24. Science. 2012 Feb 17;335(6070):848-51 - PubMed
  25. Comp Biochem Physiol. 1962 Mar;5:161-76 - PubMed
  26. Comp Biochem Physiol A Comp Physiol. 1976;55(3):287-9 - PubMed
  27. J Exp Biol. 2014 May 1;217(Pt 9):1430-6 - PubMed
  28. Comp Biochem Physiol A Mol Integr Physiol. 2002 Oct;133(2):303-21 - PubMed
  29. Comp Biochem Physiol A Mol Integr Physiol. 2007 Feb;146(2):149-54 - PubMed
  30. J Exp Mar Bio Ecol. 2000 Mar 15;245(2):197-214 - PubMed
  31. Front Physiol. 2013 May 15;4:110 - PubMed
  32. Biol Bull. 2001 Feb;200(1):67-76 - PubMed
  33. J Exp Biol. 2006 May;209(Pt 10):1791-802 - PubMed
  34. Biochem Biophys Res Commun. 1993 Dec 15;197(2):927-31 - PubMed
  35. Anal Biochem. 1976 May 7;72:248-54 - PubMed
  36. Integr Comp Biol. 2007 Oct;47(4):645-55 - PubMed
  37. J Exp Biol. 1996;199(Pt 8):1845-55 - PubMed
  38. Bioinformatics. 2001 Aug;17(8):754-5 - PubMed
  39. Eur J Biochem. 1989 Feb 15;179(3):699-705 - PubMed
  40. Syst Biol. 2007 Aug;56(4):564-77 - PubMed
  41. Nat Methods. 2012 Jul 30;9(8):772 - PubMed
  42. Philos Trans R Soc Lond B Biol Sci. 2007 Dec 29;362(1488):2233-58 - PubMed
  43. Science. 2001 Sep 21;293(5538):2248-51 - PubMed

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