Positive selection in octopus haemocyanin indicates functional links to temperature adaptation

Oellermann, Michael, Strugnell, Jan M., Lieb, Bernhard, and Mark, Felix C. (2015) Positive selection in octopus haemocyanin indicates functional links to temperature adaptation. BMC Evolutionary Biology, 15 (133). pp. 1-18.

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Abstract

Background: Octopods have successfully colonised the world's oceans from the tropics to the poles. Yet, successful persistence in these habitats has required adaptations of their advanced physiological apparatus to compensate impaired oxygen supply. Their oxygen transporter haemocyanin plays a major role in cold tolerance and accordingly has undergone functional modifications to sustain oxygen release at sub-zero temperatures. However, it remains unknown how molecular properties evolved to explain the observed functional adaptations. We thus aimed to assess whether natural selection affected molecular and structural properties of haemocyanin that explains temperature adaptation in octopods.

Results: Analysis of 239 partial sequences of the haemocyanin functional units (FU) f and g of 28 octopod species of polar, temperate, subtropical and tropical origin revealed natural selection was acting primarily on charge properties of surface residues. Polar octopods contained haemocyanins with higher net surface charge due to decreased glutamic acid content and higher numbers of basic amino acids. Within the analysed partial sequences, positive selection was present at site 2545, positioned between the active copper binding centre and the FU g surface. At this site, methionine was the dominant amino acid in polar octopods and leucine was dominant in tropical octopods. Sites directly involved in oxygen binding or quaternary interactions were highly conserved within the analysed sequence.

Conclusions: This study has provided the first insight into molecular and structural mechanisms that have enabled octopods to sustain oxygen supply from polar to tropical conditions. Our findings imply modulation of oxygen binding via charge-charge interaction at the protein surface, which stabilize quaternary interactions among functional units to reduce detrimental effects of high pH on venous oxygen release. Of the observed partial haemocyanin sequence, residue 2545 formed a close link between the FU g surface and the active centre, suggesting a role as allosteric binding site. The prevalence of methionine at this site in polar octopods, implies regulation of oxygen affinity via increased sensitivity to allosteric metal binding. High sequence conservation of sites directly involved in oxygen binding indicates that functional modifications of octopod haemocyanin rather occur via more subtle mechanisms, as observed in this study.

Item ID: 46376
Item Type: Article (Research - C1)
ISSN: 1471-2148
Keywords: Cephalopoda, oxygen binding, net surface charge, cold tolerance
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Erratum: Michael Oellermann1, Jan M. Strugnell, Bernhard Lieb3 and Felix C. Mark1 http://dx.doi.org/10.1186/s12862-015-0536-5

The original version of this article [1] unfortunately contained a mistake. The presentation of Table 1 along with the table legend and footnote was incorrect in the HTML and PDF versions of this article. The corrected version is given in the uploaded file.

© 2015 Oellermann et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Funders: Journal of Experimental Biology Travelling fellowship, German Academic Exchange Service (DAAD), Deutsche Forschungsgemeinschaft (DFG)
Projects and Grants: DAAD D/11/43882, DFG MA4271/1-2 to FCM
Date Deposited: 16 Nov 2016 07:45
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 100%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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