Copper/Zinc superoxide dismutase: How likely is gene transfer from ponyfish toPhotobacterium leiognathi?

Abstract

The proposed transfer of the gene for Cu/Zn superoxide dismutase from the ponyfish to its symbiotic bacteriumPhotobacterium leiognathi has been evaluated by an extensive analysis of all available Cu/Zn superoxide dismutase sequences. By the use of four different computer programs, phylogenetic trees were constructed from the sequences of the superoxide dismutases of human, ox, pig, horse, swordfish, fruit fly, yeast, andNeurospora crassa to find out whether superoxide dismutase sequences can reliably be used for the reconstruction of genealogical relationships. All programs arrived at the same most parsimonious tree (one requiring 232 amino acid replacements), the topology of which conformed to established opinions about the phylogenetic relations among these eukaryotes, except that it placed humans closer to the artiodactyls ox and pig than it placed horses. This could be corrected at the cost of two amino acid replacements. The sequence ofP. leiognathi superoxide dismutase was then connected at all possible positions to the corrected eukaryotic tree. It was slighly more parsimonious to link the bacterial sequence to the root of the tree than to the fish branch: The former required 316 (or 317) amino acid replacements, versus 319 for the latter. This relative lack of discrimination between such distinct alternative topologies may be a general complication in the comparison of prokaryotic and eukaryotic proteins: Bacterial cytochrome c sequences also were found to be connected as parsimoniously to the root of the eukaryotic tree as to any terminal or ancestral branch. It was calculated that the rate of evolution of the bacterial superoxide dismutase gene, if transfer occurred 30 million years (Myr) ago, must have amounted to 487 amino acid replacements per 100 residues per 100 Myr. This is more than 5 times the highest rate observed in any protein (that found for fibrinopeptides), and even much higher than the maximum rate of protein evolution that can be deduced from the neutral mutation rate of unconstrained DNA. Also, no significant evidence that shared derived amino acid replacements are present in swordfish andP. leiognathi superoxide dismutase, as might be expected had gene transfer occurred, was found. On the basis of the available data it seems more reasonable to ascribe the isolated occurrence of Cu/Zn superoxide dismutase inP. leiognathi (as well as inCaulobacter crescentus) to irregular patterns of gene expression and inactivation in the course of divergent evolution than to undocumented processes of gene transfer from eukaryotes to prokaryotes.