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Positive Selection in the N-Terminal Extramembrane Domain of Lung Surfactant Protein C (SP-C) in Marine Mammals

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Abstract

Maximum-likelihood models of codon and amino acid substitution were used to analyze the lung-specific surfactant protein C (SP-C) from terrestrial, semi-aquatic, and diving mammals to identify lineages and amino acid sites under positive selection. Site models used the nonsynonymous/synonymous rate ratio (ω) as an indicator of selection pressure. Mechanistic models used physicochemical distances between amino acid substitutions to specify nonsynonymous substitution rates. Site models strongly identified positive selection at different sites in the polar N-terminal extramembrane domain of SP-C in the three diving lineages: site 2 in the cetaceans (whales and dolphins), sites 7, 9, and 10 in the pinnipeds (seals and sea lions), and sites 2, 9, and 10 in the sirenians (dugongs and manatees). The only semi-aquatic contrast to indicate positive selection at site 10 was that including the polar bear, which had the largest body mass of the semi-aquatic species. Analysis of the biophysical properties that were influential in determining the amino acid substitutions showed that isoelectric point, chemical composition of the side chain, polarity, and hydrophobicity were the crucial determinants. Amino acid substitutions at these sites may lead to stronger binding of the N-terminal domain to the surfactant phospholipid film and to increased adsorption of the protein to the air-liquid interface. Both properties are advantageous for the repeated collapse and reinflation of the lung upon diving and resurfacing and may reflect adaptations to the high hydrostatic pressures experienced during diving.

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Acknowledgments

We thank R. Adkins, D. Blair, R. Brumfield, C. Conroy, R. Elsner, F. Gulland, C. Kemper, T. Kuchel, D. Maver, J. Owens, D. Paetkau, C. Parmenter, D. Schulz, I. Smith; M. Webb, T. Zenteno-Savin, the North Slope Borough Department of Wildlife Management, and Inuit Eskimo hunters in Barrow, Alaska, for providing samples, and J. de Silva for help with the statistical analyses. The study was supported financially by the Australian Research Council, a University of Adelaide Postgraduate Scholarship, a Society for Experimental Biology Travel Grant, a Journal of Experimental Biology Travel Grant, a Research Abroad Travel Scholarship, and a D. R. Stranks Travelling Fellowship to N.J.F.

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Author notes

  1. Natalie J. Foot

    Present address: Department of Haematology, Hanson Institute, Institute of Medical and Veterinary Science, Adelaide, SA, 5000, Australia

  2. Sandra Orgeig

    Present address: Sansom Institute, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, SA, 5001, Australia

  3. Christopher B. Daniels

    Present address: School of Natural & Built Environments, University of South Australia, Adelaide, SA, 5001, Australia

Authors and Affiliations

  1. Discipline of Environmental Biology, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA, 5005, Australia

    Natalie J. Foot, Sandra Orgeig & Christopher B. Daniels

  2. Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA, 5005, Australia

    Sandra Orgeig, Stephen Donnellan & Christopher B. Daniels

  3. Evolutionary Biology Unit, South Australian Museum, Adelaide, SA, 5000, Australia

    Stephen Donnellan & Terry Bertozzi

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  1. Natalie J. Foot
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Correspondence to Sandra Orgeig.

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Reviewing Editor: Dr. Richard Kliman

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Foot, N.J., Orgeig, S., Donnellan, S. et al. Positive Selection in the N-Terminal Extramembrane Domain of Lung Surfactant Protein C (SP-C) in Marine Mammals. J Mol Evol 65, 12–22 (2007). https://doi.org/10.1007/s00239-006-0083-1

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