CRISPR System Acquisition and Evolution of an Obligate IntracellularChlamydia-Related Bacterium

Abstract

Recently, a new Chlamydia-related organism, Protochlamydia naegleriophila KNic, was discovered within a Naegleria amoeba. To decipher the mechanisms at play in the modeling of genomes from the Protochlamydia genus, we sequenced the full genome of Pr. naegleriophila, which includes a 2,885,090 bp chromosome and a 145,285 bp megaplasmid. For the first time within the Chlamydiales order, we describe the presence of a clustered regularly interspaced short palindromic repeats (CRISPR) system, the immune system of bacteria, located on the chromosome. It is composed of a small CRISPR locus comprising eight repeats and associated cas-cse genes of the subtype I-E. A CRISPR locus is also present within Chlamydia sp. Diamant, another Pr. naegleriophila strain, suggesting that the CRISPR system was acquired by a common ancestor of Pr. naegleriophila, after its divergence from Pr. amoebophila. Both nucleotide bias and comparative genomics approaches identified probable horizontal gene acquisitions within two and four genomic islands in Pr. naegleriophila KNic and Diamant genomes, respectively. The plasmid encodes an F-type conjugative system highly similar to 1) that found in the Pam100G genomic island of Pr. amoebophila UWE25 chromosome, as well as on the plasmid of Rubidus massiliensis and 2) to the three genes remaining in the chromosome of Parachlamydia acanthamoebae strains. Therefore, this conjugative system was likely acquired on an ancestral plasmid before the divergence of Parachlamydiaceae. Overall, this new complete Pr. naegleriophila genome sequence enables further investigation of the dynamic processes shaping the genomes of the family Parachlamydiaceae and the genus Protochlamydia.

Environmental Metagenomic Assemblies Reveal Seven New Highly Divergent Chlamydial Lineages and Hallmarks of a Conserved Intracellular Lifestyle

“…The genomes of Simkania negevensis and several Parachlamydiaceae strains encode an apparently complete type IV secretion system (T4SS) located either on the chromosome or on a plasmid (Bertelli et al, 2016 ) that may be involved in conjugative DNA transfer (Greub et al, 2004 ). Several strains of Parachlamydia acanthamoebae encode remnants of the T4SS in their genome (Greub et al, 2009 ; Bertelli et al, 2016 ). No traces of T4SS genes could be found in any other chlamydial lineages (Figure 6 ).…”

“…On the other hand, the F-like conjugative DNA transfer system identified by Greub et al ( 2004 ) in Protochlamydia amobophila was restricted to Simkaniaceae and Parachlamydiaceae (Bertelli et al, 2016 ). Since then, multiple genomes belonging to the family Parachlamydiaceae were sequenced from strains in pure culture, including one representative of a new genus named Rubidus (Domman et al, 2014 ; Ishida et al, 2014 ; Yamaguchi et al, 2015 ; Yamane et al, 2015 ; Bertelli et al, 2016 ; Bou Khalil et al, 2016 , 2017 ; Fukumoto et al, 2016 ). In addition, genome sequences representing two distinct genera of the family Criblamydiaceae were recently released (Bertelli et al, 2014 , 2015 ).…”

Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae

“…2016 ). Additionally, the level of shared synteny decreases with increased genetic distance ( Bertelli et al. 2016 ), so unsurprisingly, there is very little synteny between Ca .…”

Coevolving Plasmids Drive Gene Flow and Genome Plasticity in Host-Associated Intracellular Bacteria

“…Intriguingly, all other chlamydial families with cultured representatives have members with plasmids up to 145.3 kb in size. 46 , 47 , 48 , 49 , 50 , 51 , 52 Despite the heterogeneity in plasmid size and gene content, based on the presence of conserved plasmid genes it has been proposed that all chlamydial plasmids originated from a single plasmid in the last common ancestor (LCA) of the phylum Chlamydiae. 50 …”