Tài liệu Báo cáo khoa học: Globin gene family evolution and functional diversification in annelids

Globin gene family evolution and functional diversification

in annelids

Xavier Bailly1,*,

, Christine Chabasse1,*, Ste´phane Hourdez1

, Sylvia Dewilde2

, Sophie Martial1

,

Luc Moens2 and Franck Zal1

1 Equipe Ecophysiologie: Adaptation et Evolution Mole´ culaires, UPMC – CNRS UMR 7144, Station Biologique, BP 74, Roscoff, France

2 Biochemistry Department, University of Antwerp, Belgium

Globins are heme-containing proteins that reversibly

bind oxygen and other gaseous ligands, and are wide￾spread in the three major kingdoms of life [1,2].

Despite the great diversity of their amino-acid

sequences, the basic functional unit is assumed to be a

monomeric globin with a specific and highly conserved

fold referred to as the ‘globin-fold’. On the basis of

this conserved basic structure and its prevalence in

living organisms, it has been suggested that globin

genes evolved from a common ancestral gene which,

after successive duplications and speciation events,

led to the genes that encode the widespread globin

superfamily [1–5].

Three types of globin have been described in anne￾lids: (a) noncirculating intracellular globin [e.g. myo￾globin (Mb) found in the cytoplasm of muscle cells]

[5,6]; (b) circulating intracellular globin [e.g. hemo￾globin (Hb) found in erythrocytes] [7]; (c) extracellu￾lar globin dissolved in circulating fluids [7,8]. These

three types of globin display diversity in sequence,

quaternary structure and functions such as binding

and transport of oxygen and hydrogen sulfide, and

activity of superoxide dismutase and mono-oxygenase

[8].

Annelid noncirculating intracellular globins are gen￾erally encountered as monomers [9,10], and only the

Keywords

annelid; dehaloperoxidase; extracellular

globin; intracellular globin; myoglobin

Correspondence

F. Zal, Equipe Ecophysiologie: Adaptation et

Evolution Mole´ culaires, UPMC – CNRS

UMR 7144, Station Biologique, BP 74,

29682 Roscoff cedex, France

Fax:. +33 (0) 2 98 29 23 24

Tel: +33 (0) 2 98 29 23 09

E-mail: [email protected]

Present address

Department of Cell Biology and Comparative

Zoology, Institute of Biology, University of

Copenhagen, Denmark

*These authors contributed equally to this

work

(Received 8 December 2006, revised 12

March 2007, accepted 20 March 2007)

doi:10.1111/j.1742-4658.2007.05799.x

Globins are the most common type of oxygen-binding protein in annelids.

In this paper, we show that circulating intracellular globin (Alvinella pom￾pejana and Glycera dibranchiata), noncirculating intracellular globin (Areni￾cola marina myoglobin) and extracellular globin from various annelids

share a similar gene structure, with two conserved introns at canonical

positions B12.2 and G7.0. Despite sequence divergence between intracellu￾lar and extracellular globins, these data strongly suggest that these three

globin types are derived from a common ancestral globin-like gene and

evolved by duplication events leading to diversification of globin types and

derived functions. A phylogenetic analysis shows a distinct evolutionary

history of annelid extracellular hemoglobins with respect to intracellular

annelid hemoglobins and mollusc and arthropod extracellular hemoglobins.

In addition, dehaloperoxidase (DHP) from the annelid, Amphitrite ornata,

surprisingly exhibits close phylogenetic relationships to some annelid intra￾cellular globins. We have characterized the gene structure of A. ornata

DHP to confirm assumptions about its homology with globins. It appears

that it has the same intron position as in globin genes, suggesting a com￾mon ancestry with globins. In A. ornata, DHP may be a derived globin

with an unusual enzymatic function.

Abbreviations

DHP, dehaloperoxidase; Hb, hemoglobin; HBL-Hb, hexagonal bilayer hemoglobin; Mb, myoglobin; nMb, nerve myoglobin.

FEBS Journal 274 (2007) 2641–2652 ª 2007 The Authors Journal compilation ª 2007 FEBS 2641