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

  • J. Projecto-Garcia
  • A.-S. Le Port
  • T. Govindji
  • D. Jollivet
  • S. W. Schaeffer
  • S. Hourdez
Original Article

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.

Keywords

Extracellular globin Single-domain Positive selection Heme Oxygen affinity Polynoidae 

Supplementary material

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Supplementary material 1 (DOCX 35 KB)
239_2017_9815_MOESM2_ESM.pdf (268 kb)
Supplementary material 2 (PDF 268 KB)
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Supplementary material 3 (PDF 122 KB)
239_2017_9815_MOESM4_ESM.pdf (103 kb)
Supplementary material 4 (PDF 103 KB)

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Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.CNRS UMR 7144Station Biologique de RoscoffRoscoffFrance
  2. 2.Laboratoire Adaptation et Diversité en Milieu MarinSorbonne Universités, UPMC Univ. Paris 06Roscoff CedexFrance
  3. 3.Department of Biology and Institute of Molecular Evolutionary GeneticsPennsylvania State UniversityUniversity ParkUSA
  4. 4.Ragsdale Lab, Myers Hall 100Indiana UniversityBloomingtonUSA

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