Pseudo 2-fold symmetry in the copper-binding domain of arthropodan haemocyanins. Possible implications for the evolution of oxygen transport proteins.
Investigation of the copper-binding centre of Panulirus interruptus haemocyanin led to the discovery of a pseudo 2-fold axis relating two helical pairs surrounding and co-ordinating the two copper ions. The pseudo 2-fold symmetry relating one helical pair, co-ordinating Cu-A, to the second helical pair co-ordinating Cu-B is quite precise with 31 equivalent C alpha atoms having a root-mean-square deviation of only 1.47 A. The 2-fold consists of a rotation of 174.6 degrees and a translation parallel to the rotation axis of 0.7 A. After superposition of the helical pairs, the two copper ions are within 1.1 A and the three C alpha atoms of the histidine ligands of Cu-A are within a root-mean-square deviation of 1.0 A from the C alpha atoms of the histidine residues co-ordinating Cu-B. Of the superimposed residues, 26% are identical in sequence. These data suggest that the current oxygen-binding centre of arthropodan haemocyanins is the result of dimerization, gene duplication and gene fusion of an ancestral mono-copper-binding helical pair. This suggestion is supported by the recent discovery that in the sequence of functional domains of molluscan haemocyanins only amino acid sequence homology with the arthropodan Cu-B helical pair has been found and no evidence for similarity with a Cu-A binding helical pair was observed. This provides strong evidence that a mono-copper-binding helical pair has been the ancestor of both the arthropodan and molluscan haemocyanins. Turning to the Fe-binding helical pairs in haemerythrins, it appears that they are less similar to each other than the two Cu-binding helical pairs in arthropodan haemocyanins. Nevertheless, the Fe-B haemerythrin helical pair superimposes well onto the Cu-A helical pair of Panulirus haemocyanin. A root-mean-square deviation of 1.9 A for 24 equivalent C alpha carbon atoms is obtained, while Fe-B deviates 1.4 A from Cu-A after superposition of the helices. Moreover, the three histidine ligands of the Cu-A helical pair are equivalent with three histidine ligands of the Fe-B pair. The structural similarity and correspondence in metal-binding ligands suggests that both haemocyanins and haemerythrins have originated from an ancestral mono-metal-binding helical pair having two ligands provided by the first helix and one ligand by the second helix.(ABSTRACT TRUNCATED AT 400 WORDS)
Volbeda
A
A
Department of Chemistry, University of Groningen, The Netherlands.
Hol
W G
WG
D000595:Amino Acid Sequence; D000818:Animals; D001665:Binding Sites; D005075:Biological Evolution; D001692:Biological Transport; D003300:Copper / Q000378:metabolism*; D006422:Hemerythrin; D006433:Hemocyanins / Q000378:metabolism; D006454:Hemoglobins; D008969:Molecular Sequence Data; D008974:Mollusca / Q000378:metabolism; D008121:Nephropidae / Q000378:metabolism*; D010100:Oxygen / Q000378:metabolism; D011487:Protein Conformation; D011506:Proteins / Q000378:metabolism
D006422:Hemerythrin; D006454:Hemoglobins; D011506:Proteins; D003300:Copper; D006433:Hemocyanins; D010100:Oxygen