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MBE Advance Access published online on January 5, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi077
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Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved.
Accepted December 23, 2004

Research Article

Putting the Brakes on Snake Venom Evolution: the Unique Molecular Evolutionary Patterns of Aipysurus eydouxii (Marbled sea snake) Phospholipase A2 Toxins

Min Li 1, Bryan G. Fry 2, and R. Manjunatha Kini 3*

1 Department of Biological Science, Faculty of Science, National University of Singapore, Singapore, 119260
2 Australian Venom Research Unit, Department of Pharmacology, School of Medicine, University of Melbourne, Parkville, Victoria, 3010 Australia; Population and Evolutionary Genetics Unit, Museum Victoria, GPO Box 666E, Melbourne VIC 3001 Australia
3 Department of Biological Science, Faculty of Science, National University of Singapore, Singapore, 119260; Department of Biochemistry and Molecular Biophysics, Virginia Commonwealth University, Medical College of Virginia, Richmond, VA 23298-0614

* To whom correspondence should be addressed.
R. Manjunatha Kini, E-mail: dbskinim{at}nus.edu.sg


  Abstract

Accelerated evolution of toxins is a unique feature of venoms, with the toxins evolving via the birth-and-death mode of molecular evolution. The venoms of sea snakes, however, are remarkably simple in comparison to that of land snakes, which contain highly complex venoms. Aipysurus eydouxii (Marbled sea snake) is a particularly unique sea snake, feeding exclusively upon fish eggs. Secondary to this ecological change, the fangs have been lost and the venom glands greatly atrophied. We recently showed that the only neurotoxin (a three finger toxin) gene found in the sea snake Aipysurus eydouxii has a dinucleotide deletion resulting in the loss of neurotoxic activity. During these studies, we isolated and identified a number of cDNA clones encoding isozymes of phospholipase A2 (PLA2) toxins from its venom gland. Sixteen unique PLA2 clones were sequenced from the cDNA library and TA-cloning of RT-PCR products. Phylogenetic analysis of these clones revealed that less diversification of the PLA2 toxins has occurred in the A. eydouxii venom gland in comparison to equivalent terrestrial and other marine snakes. As there is no longer a positive selection pressure acting upon the venom, mutations have accumulated in the toxin coding regions that would have otherwise had a deleterious effect upon the ability to use the venom for prey capture. Such mutations include substitutions of highly conserved residues; in one clone the active site His48 is replaced by Arg and in two other clones highly conserved cysteine residues are replaced. These mutations significantly affect the functional and structural properties of these PLA2 enzymes respectively. Thus in A. eydouxii, the loss of the main neurotoxin is accompanied by a much slower rate of molecular evolution of the PLA2 toxins as a consequence of the snake's shift in ecological niche. This is the first case of decelerated evolution of toxins in snake venom.

Keywords: gene duplication; sea snake; venom gland; phospholipase A2; evolution of toxins.
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