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Gene Structure and Molecular Phylogeny of the Linker Chains from the Giant Annelid Hexagonal Bilayer Hemoglobins

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Abstract

Giant extracellular hexagonal bilayer hemoglobin (HBL-Hb), found only in annelids, is an ∼3500-kDa heteropolymeric structure involved in oxygen transport. The HBL-Hbs are comprised of globin and linker chains, the latter being required for the assembly of the quaternary structure. The linker chains, varying in size from 225 to 283 amino acids, have a conserved cysteine-rich domain within their N-terminal moiety that is homologous to the cysteine-rich modules constituting the ligand binding domain of the low-density lipoprotein receptor (LDLR) protein family found in many metazoans. We have investigated the gene structure of linkers from Arenicola marina, Alvinella pompejana, Nereis diversicolor, Lumbricus terrestris, and Riftia pachyptila. We found, contrary to the results obtained earlier with linker genes from N. diversicolor and L. terrestris, that in all of the foregoing cases, the linker LDL-A module is flanked by two phase 1 introns, as in the human LDLR gene, with two more introns in the 3′ side whose positions varied with the species. In addition, we obtained 13 linker cDNAs that have been determined experimentally or found in the EST database LumbriBASE. A molecular phylogenetic analysis of the linker primary sequences demonstrated that they cluster into two distinct families of linker proteins. We propose that the common gene ancestor to annelid linker genes exhibited a four-intron and five-exon structure and gave rise to the two families subsequent to a duplication event.

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Acknowledgments

We are indebted to Serge Vinogradov for his critical reading and comments on the manuscript. We thank the captains and crews of the NO L’Atalante and the pilots, cruises, and team of the submersibles Nautile and Alvin of the HOT 96, HOPE’99, LARVE99, and BIOSPEEDO. We thank the referees for helpful discussion. This work was supported by the CNRS, European grant FEDER presage 3814, and the Conseil Régional de Bretagne (contract A2C809).

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  1. Equipe Ecophysiologie: Adaptation et Evolution Moléculaires, UPMC—CNRS UMR 7144, Station Biologique, BP 74, 29682, Roscoff cedex, France

    Christine Chabasse, Xavier Bailly, Sophie Sanchez, Morgane Rousselot & Franck Zal

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  1. Christine Chabasse
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Chabasse, C., Bailly, X., Sanchez, S. et al. Gene Structure and Molecular Phylogeny of the Linker Chains from the Giant Annelid Hexagonal Bilayer Hemoglobins. J Mol Evol 63, 365–374 (2006). https://doi.org/10.1007/s00239-005-0198-9

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