A mitochondrial origin for eukaryotic C2H2 zinc finger regulators?

1 discussed the phylogenetic distribution of C2H2 zinc finger transcriptional regulators, which were thought to be exclusively eukaryotic but have been recently found in several prokaryotes. These proteins display different regulatory roles in Sphingomonas aromaticivorans and some members of the symbiotic bacterial genera Rhizobium, Sinorhizobium and Agrobacterium. Distantly related proteins have been found also in the archaea Halobacterium salinarium, Haloferax mediterranei, and Methanococcus jannaschii 1. The restricted distribution of these proteins in bacteria, and their presence mostly in species living in intimate ecological relationship with eukaryotes, led these authors to propose that these bacteria acquired C2H2 zinc finger proteins by horizontal gene transfer (HGT) from eukaryotes. As phylogenetic analysis suggests that the bacterial sequences form a monophyletic group, the authors propose that this HGT was unique and predated the divergence of these bacterial species. We have analysed the opposite possibility, that is, that eukaryotes acquired C2H2 zinc finger regulators from bacteria, a scenario that Bouhouche et al. 1 proposed as a 'question for future research'. A BLAST search in the available ongoing genome sequence projects seeded with the Agrobacterium tumefaciens sequence allows the identification of C2H2 zinc finger homologues in three additional bacterial species: three copies in the prosthecate Caulobacter crescentus (E values between 1e-38 and 1e-31), three copies in the methanotroph Methylobacterium extorquens (E values between 9e-27 and 1e-10), and one copy in the facultative phototroph Rhodopseudomonas palustris (E value 4e-38) (Fig. 1). Two of these species often thrive in close contact with eukaryotes: C. crescentus as an algal epibiont and M. extorquens as a plant epibiont 2. The possibility for a eukaryote-to-bacteria HGT of the C2H2 zinc finger homologues thus remains open. Interestingly, despite the high overall similarity, these new sequences have zinc finger motifs different from the bacterial consensus X 2-Cys-X 2-Cys-X 9-His-X 3-His-X 2 , with the replacement of the second Cys by Asp in all sequences, and the replacement of the first Cys by Ser in all M. extorquens sequences and one C. crescentus sequence. The two His residues are more conserved, although the second is replaced by Lys, Arg or Gln in three of the sequences (data not shown). Although these zinc finger motifs are divergent, the presence of several copies in some species strongly suggests that they are functional. Interestingly, all the bacterial species carrying these genes belong to the ␣-subdivision of the proteobacteria from which mitochondria originated 3. These species cover a …