Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast

Abstract

An unusually high proportion of proteins encoded in Chlamydia genomes are most similar to plant proteins, leading to proposals that a Chlamydia ancestor obtained genes from a plant or plant-like host organism by horizontal gene transfer. However, during an analysis of bacterial-eukaryotic protein similarities, we found that the vast majority of plant-like sequences in Chlamydia are most similar to plant proteins that are targeted to the chloroplast, an organelle derived from a cyanobacterium. We present further evidence suggesting that plant-like genes in Chlamydia, and other Chlamydiaceae, are likely a reflection of an unappreciated evolutionary relationship between the Chlamydiaceae and the cyanobacteria-chloroplast lineage. Further analyses of bacterial and eukaryotic genomes indicates the importance of evaluating organellar ancestry of eukaryotic proteins when identifying bacteria-eukaryote homologs or horizontal gene transfer and supports the proposal that Chlamydiaceae, which are obligate intracellular bacterial pathogens of animals, are not likely exchanging DNA with their hosts.

Figure 1

Proportion of proteins, predicted from complete bacterial genomes, which share highest similarity to eukaryotic proteins (according to analysis with default stringency settings; see http://www.pathogenomics.bc.ca/BAE-watch.html). Results for those organisms with a higher proportion than expected are circled. Similar results are obtained when different stringency cutoffs are used (see Supplementary Material available online http://www.genome.org).

Figure 2

Unique shared-derived characters of the ribosomal super operon that unite cyanobacteria and Chlamydiaceae. Two unique shared-derived characters on the ribosomal super operon (the loss of ribosomal proteins S10 and S14) unite the Chlamydiaceae and cyanobacteria to the exclusion of other bacteria with genomes that have been completely sequenced (black boxes; note that S10 and S14 are present elsewhere on the chromosome). Loss of L30 (dashes; note that L30 does not appear to be present elsewhere in these genomes, according to TBLASTN analysis) is not a unique shared-derived character to the exclusion of all other bacteria but offers further support for a relationship between the Chlamydiaceae and cyanobacteria. In addition, all 10 chloroplast genomes examined (Porphyra purpurea chloroplast is shown as a representative) and an unfinished cyanobacterial genome (Synechococcus spp.) also share the same characters (i.e., loss of S10, S14, and L30 from the super operon); however, the chloroplasts are missing additional genes from this region (i.e., L15 in the region shown) that have been primarily transferred to the plant nucleus. Boxes with strikethroughs mark genes that have relocated in Deinococcus and Aquifex to form a separate operon. Note that the genome annotation for Aquifex did not report L29; however, we did positively identify this gene in Aquifex using TBLASTN. Another unique character uniting Chlamydiaceae, cyanobacteria, and the chloroplast, which is not illustrated in this figure, is that S10 is found as part of the separate S7/S12 operon in only the Chlamydiaceae, cyanobacteria, and chloroplast sequences examined.