Unity in Variety--The Pan-Genome of the Chlamydiae

Abstract

Chlamydiae are evolutionarily well-separated bacteria that live exclusively within eukaryotic host cells. They include important human pathogens such as Chlamydia trachomatis as well as symbionts of protozoa. As these bacteria are experimentally challenging and genetically intractable, our knowledge about them is still limited. In this study, we obtained the genome sequences of Simkania negevensis Z, Waddlia chondrophila 2032/99, and Parachlamydia acanthamoebae UV-7. This enabled us to perform the first comprehensive comparative and phylogenomic analysis of representative members of four major families of the Chlamydiae, including the Chlamydiaceae. We identified a surprisingly large core gene set present in all genomes and a high number of diverse accessory genes in those Chlamydiae that do not primarily infect humans or animals, including a chemosensory system in P. acanthamoebae and a type IV secretion system. In S. negevensis, the type IV secretion system is encoded on a large conjugative plasmid (pSn, 132 kb). Phylogenetic analyses suggested that a plasmid similar to the S. negevensis plasmid was originally acquired by the last common ancestor of all four families and that it was subsequently reduced, integrated into the chromosome, or lost during diversification, ultimately giving rise to the extant virulence-associated plasmid of pathogenic chlamydiae. Other virulence factors, including a type III secretion system, are conserved among the Chlamydiae to variable degrees and together with differences in the composition of the cell wall reflect adaptation to different host cells including convergent evolution among the four chlamydial families. Phylogenomic analysis focusing on chlamydial proteins with homology to plant proteins provided evidence for the acquisition of 53 chlamydial genes by a plant progenitor, lending further support for the hypothesis of an early interaction between a chlamydial ancestor and the primary photosynthetic eukaryote.

CRISPR system acquisition and evolution of an obligate intracellularChlamydia-related bacterium

“…amoebophila genome has a genomic island (Pam100G) that encodes a type IV secretion system of the F-type that might be involved in conjugative DNA transfer (Greub et al 2004). A similar system is also found on the plasmid of Simkania negevensis (Collingro et al 2011) and a partial operon was described in Parachlamydia acanthamoebae ), suggesting active DNA transfer capabilities in the ancestor of the Chlamydiales and some of its descendants.…”

“…amoebophila UWE25 chromosome (Greub et al 2004), the plasmids of S. negevensis (Collingro et al 2011) and Rubidus massiliensis, and the remnants traU, traN and traF present in members of the family Parachlamydiaceae Collingro et al 2011) (fig. 3).…”

Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum

“…(SI Appendix, Table S5). A recent study reported that an obligate endosymbiont, Candidatus Ameobophilus asiaticus, of a free-living amoeba, also lacking almost all amino acid biosynthesis pathways, contains a large fraction of proteins with eukaryotic domains (67,68). It was demonstrated that these domains are also significantly enriched in the genomes of other amoeba-associated bacteria (including Legionella pneumophilia, Ricksettsia bellii, Francisella tularensis, and M. avium).…”

Structural and Biochemical Characterization of Chlamydia trachomatis Hypothetical Protein CT263 Supports That Menaquinone Synthesis Occurs through the Futalosine Pathway

“…Chlamydia genomes have undergone a large degree of reductive evolution, Chlamydiaceae more so than environmental Chlamydiales given the 2-3 times smaller genomes found within that order (62). The environmental Chlamydiales are significantly more metabolically flexible than Chlamydiaceae, encoding additional genes involved in sugar utilization, a complete TCA cycle, and an expanded electron transport chain, among other pathways (61).…”