Role of blood oxygen transport in setting octopods’ range limits

Michael Oellermann (1), Bernhard Lieb (2), Jan M. Strugnell (3), Jayson M. Semmens (4), Hans-O. Pörtner (5), Felix C. Mark (6)

1 Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany, Michael.Oellermann@awi.de

2 Institute of Zoology, Johannes Gutenberg-Universität, Müllerweg 6, 55099 Mainz, Germany, lieb@uni-mainz.de

3 Department of Genetics, La Trobe Institute for Molecular Sciences, La Trobe University, Bundoora, VIC 3086, Australia, J.Strugnell@latrobe.edu.au

4 Fisheries, Aquaculture and Coasts Centre, Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Hobart, Tas 7001, Australia, Jayson.Semmens@utas.edu.au

5 Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany, Hans.Poertner@awi.de

6 Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany, Felix.Christopher.Mark@awi.de

Predictions of octopods’ future responses to ocean warming and resulting range shifts rely on a mechanistic understanding of the physiological and genetic underpinnings that define temperature tolerance. Oxygen transport has been shown to fail first at thermal margins in various ectotherms. We thus analysed the major oxygen transporter of octopods, the blood pigment haemocyanin, to unravel properties shaping temperature tolerance. Functional comparisons of haemocyanin between cold- and warm-water octopods revealed limited capacity to release oxygen to tissues towards lower temperatures. Oxygen unloading was particularly poor in Antarctic octopods at 0°C but was compensated by high levels of dissolved oxygen, lowered oxygen affinity and higher oxygen carrying capacity compared to warm water octopods. While oxygen uptake by haemocyanin remained high towards warmer temperatures, oxygen unloading increased in all analysed octopods, which formed a significant cardio-circulatory buffer in polar octopods. Genetic comparisons of 28 octopods species of polar, temperate, subtropical and tropical origin indicated temperature dependent selection of amino acid properties at the protein`s surface. Net charges of surface residues were elevated in polar octopods suggesting that charge-charge interactions raise intrinsic pK values to stabilise quaternary structure against higher ambient pH present in cold waters. In conclusion, limited haemocyanin function towards colder temperatures highlights the general role of haemocyanin oxygen transport in constraining cold tolerance in octopods. Buffering of oxygen supply by haemocyanin at higher temperatures may extend warm tolerance and together with variable temperature-adaptive genetic traits may be key to determine future winners and losers in ecosystems facing radical environmental change.