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J. Biol. Chem., Vol. 281, Issue 9, 5364-5372, March 3, 2006

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The Nerve Hemoglobin of the Bivalve Mollusc Spisula solidissima

MOLECULAR CLONING, LIGAND BINDING STUDIES, AND PHYLOGENETIC ANALYSIS^*

Sylvia Dewilde¹, Bettina Ebner, Evi Vinck^¶2, Kambiz Gilany, Thomas Hankeln, Thorsten Burmester^||, Jill Kreiling^**, Carol Reinisch^**, Jacques R. Vanfleteren, Laurent Kiger, Michael C. Marden, Christian Hundahl^¶¶, Angela Fago^¶¶, Sabine Van Doorslaer^¶, and Luc Moens³

From the Departments of Biomedical Sciences and ^¶Physics, University of Antwerp, 2610 Antwerp, Belgium, Institute of Molecular Genetics and ^||Institute of Zoology, Johannes Gutenberg University, 55099 Mainz, Germany, ^**Marine Biological Laboratory, Woods Hole, Massachusetts 02543, Department of Biology, Ghent University, 9000 Ghent, Belgium, Inserm U779, 94276 Le Kremlin-Bicêtre, France, and ^¶¶Zoophysiology, Institute of Biological Sciences, University of Aarhus, DK-8000 Aarhus C, Denmark

Members of the hemoglobin (Hb) superfamily are present in nerve tissue of several vertebrate and invertebrate species. In vertebrates they display hexacoordinate heme iron atoms and are typically expressed at low levels (µM). Their function is still a matter of debate. In invertebrates they have a hexa- or pentacoordinate heme iron, are mostly expressed at high levels (mM), and have been suggested to have a myoglobin-like function. The native Hb of the surf clam, Spisula solidissima, composed of 162 amino acids, does not show specific deviations from the globin templates. UV-visible and resonance Raman spectroscopy demonstrate a hexacoordinate heme iron. Based on the sequence analogy, the histidine E7 is proposed as a sixth ligand. Kinetic and equilibrium measurements show a moderate oxygen affinity (P₅₀ 0.6 torr) and no cooperativity. The histidine binding affinity is 100-fold lower than in neuroglobin. Phylogenetic analysis demonstrates a clustering of the S. solidissima nerve Hb with mollusc Hbs and myoglobins, but not with the vertebrate neuroglobins. We conclude that invertebrate nerve Hbs expressed at high levels are, despite the hexacoordinate nature of their heme iron, not essentially different from other intracellular Hbs. They most likely fulfill a myoglobin-like function and enhance oxygen supply to the neurons.

Received for publication, August 29, 2005 , and in revised form, December 7, 2005.

^* This study was supported in part by Inserm, University of Paris-XI, by European Union Grant QLG3-CT-2002-01548, the Deutsche Forschungsgemeinschaft (Ha2103/3 and Bu956/5), by the Fund for Scientific Research of Flanders Grant G.0468.03, and by the Danish Natural Science Research Council. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. SA and SB.

¹ A postdoctoral fellow of the Fund for Scientific Research of Flanders.

² A research assistant of the Fund for Scientific Research of Flanders.

³ To whom correspondence should be addressed: Dept. of Biomedical Sciences, University of Antwerp, Campus Drie eiken, Universiteitsplein 1, Antwerp B-2610, Belgium. Tel.: 32-3-8202323; Fax: 32-3-8202248; E-mail: luc.moens{at}ua.ac.be.

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