Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids

Previous work has shown that molecular phylogenies of plastids,cyanobacteria, and proteobacteria based on the rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) genes rbcL and rbcS are incongruentwith molecular phylogenies based on other genes and are also incompatiblewith structural and biochemical information. Although it has been muchspeculated that this is the consequence of a single horizontal genetransfer (of a proteobacterial or mitochondrial rubisco operon intoplastids of rhodophytic and chromophytic algae), neither this hypothesisnor the alternative hypothesis of ancient gene duplication have beenexamined in detail. We have conducted phylogenetic analyses of allavailable bacterial rbcL sequences, and representative plastid sequences,in order to explore these alternative hypothesis and fully examine thecomplexity of rubisco gene evolution. The rbcL phylogeny reveals asurprising number of gene relationships that are fundamentally incongruentwith organismal relationships as inferred from multiple lines of othermolecular evidence. On the order of six horizontal gene transfers areimplied by the form I (L8S8) rbcL phylogeny, two between cyanobacteria andproteobacteria, one between proteobacteria and plastids, and three withinproteobacteria. Alternatively, a single ancient duplication of the form Irubisco operon, followed by repeated and pervasive differential loss of oneoperon or the other, would account for much of this incongruity. In allprobability, the rubisco operon has undergone multiple events of bothhorizontal gene transfer and gene duplication in different lineages.