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Evolution of Single-Domain Globins in Hydrothermal Vent Scale-Worms

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Abstract

Hypoxia at deep-sea hydrothermal vents represents one of the most basic challenges for metazoans, which then requires specific adaptations to acquire oxygen to meet their metabolic needs. Hydrothermal vent scale-worms (Polychaeta; Polynoidae) express large amounts of extracellular single- and multi-domain hemoglobins, in contrast with their shallow-water relatives that only possess intracellular globins in their nervous system (neuroglobins). We sequenced the gene encoding the single-domain (SD) globin from nine species of polynoids found in various vent and deep-sea reduced microhabitats (and associated constraints) to determine if the Polynoidae SD globins have been the targets of diversifying selection. Although extracellular, all the SD globins (and multi-domain ones) form a monophyletic clade that clusters within the intracellular globin group of other annelids, indicating that these hemoglobins have evolved from an intracellular myoglobin-like form. Positive selection could not be detected at the major ecological changes that the colonization of the deep-sea and hydrothermal vents represents. This suggests that no major structural modification was necessary to allow the globins to function under these conditions. The mere expression of these globins extracellularly may have been sufficiently advantageous for the polynoids living in hypoxic hydrothermal vents. Among hydrothermal vent species, positively selected amino acids were only detected in the phylogenetic lineage leading to the two mussel-commensal species (Branchipolynoe). In this lineage, the multiplicity of hemoglobins could have lessened the selective pressure on the SD hemoglobin, allowing the acquisition of novel functions by positive Darwinian selection. Conversely, the colonization of hotter environments (species of Branchinotogluma) does not seem to have required additional modifications.

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Acknowledgements

The authors would like to thank the crews of the ships and submersibles, as well as the chief scientists, of the cruises ATOS 2001 (project funded by Ifremer and INSU), Lau basin (projects funded by two NSF grants to C.R. Fisher (NSF OCE 0240985 and NSF OCE 0732333)), and EPR 2001 (project funded by a NSF Grant to C.R. Fisher (NSF OCE-0002729)). We would also like to thank Isabelle Boutet-Tanguy and Arnaud Tanguy for technical advice in lab, and Matthieu Bruneaux, Anis Bessadok, and Mirjam Czjzek for protein modeling advice. This work is part of the project HYPOXEVO (Région Bretagne), Deep-Sea Annelid Biodiversity and Evolution (Fondation Total), and was supported by the ESTeam research Marie Curie grant under the 6th framework program from the European Commission.

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Authors and Affiliations

  1. CNRS UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680, Roscoff, France

    J. Projecto-Garcia, A.-S. Le Port, D. Jollivet & S. Hourdez

  2. Laboratoire Adaptation et Diversité en Milieu Marin, Sorbonne Universités, UPMC Univ. Paris 06, Place Georges Teissier, 29680, Roscoff Cedex, France

    J. Projecto-Garcia, A.-S. Le Port, D. Jollivet & S. Hourdez

  3. Department of Biology and Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park, PA, 16802, USA

    T. Govindji & S. W. Schaeffer

  4. Ragsdale Lab, Myers Hall 100, Indiana University, 3rd St, Bloomington, IN, 47405, USA

    J. Projecto-Garcia

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  1. J. Projecto-Garcia
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  2. A.-S. Le Port
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Correspondence to J. Projecto-Garcia.

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Projecto-Garcia, J., Le Port, AS., Govindji, T. et al. Evolution of Single-Domain Globins in Hydrothermal Vent Scale-Worms. J Mol Evol 85, 172–187 (2017). https://doi.org/10.1007/s00239-017-9815-7

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