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Chlamydiae like Chlamydia trachomatis and Chlamydia psittaci are well-known human and animal pathogens. Yet, the chlamydiae are a much larger group of evolutionary ancient obligate intracellular bacteria that includes predominantly symbionts of protists and diverse animals. This makes them ideal model organisms to study evolutionary transitions from symbionts in microbial eukaryotes to pathogens of humans. To this end, comparative genome analysis has served as an important tool. Genome sequence data for many chlamydial lineages are, however, still lacking, hampering our understanding of their evolutionary history. Here, we determined the first high-quality draft genome sequence of the fish pathogen "Candidatus Clavichlamydia salmonicola", representing a separate genus within the human and animal pathogenic Chlamydiaceae. The "Ca. Clavichlamydia salmonicola" genome harbors genes that so far have been exclusively found in Chlamydia species suggesting that basic mechanisms important for the interaction with chordate hosts have evolved stepwise in the history of chlamydiae. Thus, the genome sequence of "Ca. Clavichlamydia salmonicola" allows to constrain candidate genes to further understand the evolution of chlamydial virulence mechanisms required to infect mammals., (© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

Aims: The order Chlamydiales comprises a broad range of bacterial pathogens and endosymbionts, which infect a wide variety of host species. Within this order, members of the family Parachlamydiaceae, which includes Parachlamydia and Neochlamydia species, have been particularly associated with infections in both humans and cattle, including having a potential pathogenic role in cases of bovine abortion. While the route of transmission has yet to be defined, it has been hypothesised that asymptomatic carriage and contamination of the immediate environment may be a route of inter-animal transmission. We investigated the asymptomatic carriage of Chlamydia-related organisms in healthy cattle., Methods & Results: DNA was isolated from nasal and rectal swabs obtained from 38 healthy dairy heifers. A Chlamydiales sp. 16S rRNA qPCR was performed on each sample. A total of 18/38 nasal samples and all 38/38 rectal samples were identified as positive for Chlamydiales sp. Each positive sample was sequenced confirming the presence of DNA belonging to the Parachlamydiaceae., Conclusions: The presence of Parachlamydiaceae DNA in nasal and rectal swab samples of healthy cattle provides evidence for the asymptomatic carriage of parachlamydial organisms within cattle., Significance & Impact of the Study: The study provides evidence of potential routes of environmental contamination that could provide a route for inter-animal and animal transmission of Parachlamydiaceae., (© 2021 The Society for Applied Microbiology.)

The Rhabdochlamydiaceae family is one of the most widely distributed within the phylum Chlamydiae, but most of its members remain uncultivable. Rhabdochlamydia 16S rRNA was recently reported in more than 2% of 8,534 pools of ticks from Switzerland. Shotgun metagenomics was performed on a pool of five female Ixodes ricinus ticks presenting a high concentration of chlamydial DNA, allowing the assembly of a high-quality draft genome. About 60% of sequence reads originated from a single bacterial population that was named "Candidatus Rhabdochlamydia helvetica" whereas only few thousand reads mapped to the genome of "Candidatus Midichloria mitochondrii," a symbiont normally observed in all I. ricinus females. The 1.8 Mbp genome of R. helvetica is smaller than other Chlamydia-related bacteria. Comparative analyses with other chlamydial genomes identified transposases of the PD-(D/E)XK nuclease family that are unique to this new genome. These transposases show evidence of interphylum horizontal gene transfers between multiple arthropod endosymbionts, including Cardinium spp. (Bacteroidetes) and diverse proteobacteria such as Wolbachia, Rickettsia spp. (Rickettsiales), and Caedimonas varicaedens (Holosporales). Bacterial symbionts were previously suggested to provide B-vitamins to hematophagous hosts. However, incomplete metabolic capacities including for B-vitamin biosynthesis, high bacterial density and limited prevalence suggest that R. helvetica is parasitic rather than symbiotic to its host. The identification of novel Rhabdochlamydia strains in different hosts and their sequencing will help understanding if members of this genus have become highly specialized parasites with reduced genomes, like the Chlamydiaceae, or if they could be pathogenic to humans using ticks as a transmission vector., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Chlamydiae are an example of obligate intracellular bacteria that possess highly reduced, compact genomes (1.0-3.5 Mbp), reflective of their abilities to sequester many essential nutrients from the host that they no longer need to synthesize themselves. The Chlamydiae is a phylum with a very wide host range spanning mammals, birds, fish, invertebrates, and unicellular protists. This ecological and phylogenetic diversity offers ongoing opportunities to study intracellular survival and metabolic pathways and adaptations. Of particular evolutionary significance are Chlamydiae from the recently proposed Ca. Parilichlamydiaceae, the earliest diverging clade in this phylum, species of which are found only in aquatic vertebrates. Gill extracts from three Chlamydiales-positive Australian aquaculture species (Yellowtail kingfish, Striped trumpeter, and Barramundi) were subject to DNA preparation to deplete host DNA and enrich microbial DNA, prior to metagenome sequencing. We assembled chlamydial genomes corresponding to three Ca. Parilichlamydiaceae species from gill metagenomes, and conducted functional genomics comparisons with diverse members of the phylum. This revealed highly reduced genomes more similar in size to the terrestrial Chlamydiaceae, standing in contrast to members of the Chlamydiae with a demonstrated cosmopolitan host range. We describe a reduction in genes encoding synthesis of nucleotides and amino acids, among other nutrients, and an enrichment of predicted transport proteins. Ca. Parilichlamydiaceae share 342 orthologs with other chlamydial families. We hypothesize that the genome reduction exhibited by Ca. Parilichlamydiaceae and Chlamydiaceae is an example of within-phylum convergent evolution. The factors driving these events remain to be elucidated.

Many studies have aimed to set up boundaries for the classification and definition of prokaryotic genus and species classification; however, studies that focused on genus-level genomic differences for existing taxonomy systems are limited. Recently, a novel method was described for prokaryotic genus delineation using the percentage of conserved proteins (POCP) between two strains to estimate their evolutionary and phenotypic distance (Qin et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196: :2210-5). Here, we extended the POCP analysis of the order Chlamydiales and pairwise compared all currently recognized species and candidate species of the family Chlamydiaceae as well as some species from other families. Using the taxonomy advised by the International Committee on Systematics of Prokaryotes, subcommittee on the taxonomy of the Chlamydiae, POCP analysis revealed that all pairwise comparisons of species from different families resulted in values lower than 50%, the proposed threshold for genus boundary. In contrast, all interspecies pairwise comparisons of species from the single genus within the family Chlamydiaceae resulted in POCP values higher than 70%. We conclude that the recommended genus classification of the family Chlamydiaceae is rational and that POCP analyses can provide a robust genomic index for the taxonomy of members of the order Chlamydiales in terms of genus demarcation., (© FEMS 2016. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Waddlia chondrophila is a obligate intracellular bacterium belonging to the Chlamydiales order, a clade that also includes the well-known classical Chlamydia responsible for a number of severe human and animal diseases. Waddlia is an emerging pathogen associated with adverse pregnancy outcomes in humans and abortion in ruminants. Adhesion to the host cell is an essential prerequisite for survival of every strict intracellular bacteria and, in classical Chlamydia, this step is partially mediated by polymorphic outer membrane proteins (Pmps), a family of highly diverse autotransporters that represent about 15% of the bacterial coding capacity. Waddlia chondrophila genome however only encodes one putative Pmp-like protein. Using a proteomic approach, we identified several bacterial proteins potentially implicated in the adhesion process and we characterized their expression during the replication cycle of the bacteria. In addition, we demonstrated that the Waddlia Pmp-like autotransporter as well as OmpA2 and OmpA3, two members of the extended Waddlia OmpA protein family, exhibit adhesive properties on epithelial cells. We hypothesize that the large diversity of the OmpA protein family is linked to the wide host range of these bacteria that are able to enter and multiply in various host cells ranging from protozoa to mammalian and fish cells., (© FEMS 2015. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Mitochondrial genomes of lycophytes are surprisingly diverse, including strikingly different transfer RNA (tRNA) gene complements: No mitochondrial tRNA genes are present in the spikemoss Selaginella moellendorffii, whereas 26 tRNAs are encoded in the chondrome of the clubmoss Huperzia squarrosa. Reinvestigating the latter we found that trnL(gag) and trnS(gga) had never before been identified in any other land plant mitochondrial DNA. Sensitive sequence comparisons showed these two tRNAs as well as trnN(guu) and trnS(gcu) to be very similar to their respective counterparts in chlamydial bacteria. We identified homologs of these chlamydial-type tRNAs also in other lycophyte, fern, and gymnosperm DNAs, suggesting horizontal gene transfer (HGT) into mitochondria in the early vascular plant stem lineages. These findings extend plant mitochondrial HGT to affect individual tRNA genes, to include bacterial donors, and suggest that Chlamydiae on top of their recently proposed key role in primary chloroplast establishment may also have participated in early tracheophyte genome evolution., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

The type three secretion system (T3SS) operons of Chlamydiales bacteria are distributed in different clusters along their chromosomes and are conserved at both the level of sequence and genetic organization. A complete characterization of the temporal expression of multiple T3SS components at the transcriptional and protein levels has been performed in Parachlamydia acanthamoebae, replicating in its natural host cell Acanthamoeba castellanii. The T3SS components were classified in four different temporal clusters depending on their pattern of expression during the early, mid- and late phases of the infectious cycle. The putative T3SS transcription units predicted in Parachlamydia are similar to those described in Chlamydia trachomatis, suggesting that T3SS units of transcriptional expression are highly conserved among Chlamydiales bacteria. The maximal expression and activation of the T3SS of Parachlamydia occurred during the early to mid-phase of the infectious cycle corresponding to a critical phase during which the intracellular bacterium has (1) to evade and/or block the lytic pathway of the amoeba, (2) to differentiate from elementary bodies (EBs) to reticulate bodies (RBs), and (3) to modulate the maturation of its vacuole to create a replicative niche able to sustain efficient bacterial growth., (© 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.)

Under the endosymbiont hypothesis, over a billion years ago a heterotrophic eukaryote entered into a symbiotic relationship with a cyanobacterium (the cyanobiont). This partnership culminated in the plastid that has spread to forms as diverse as plants and diatoms. However, why primary plastid acquisition has not been repeated multiple times remains unclear. Here, we report a possible answer to this question by showing that primary plastid endosymbiosis was likely to have been primed by the secretion in the host cytosol of effector proteins from intracellular Chlamydiales pathogens. We provide evidence suggesting that the cyanobiont might have rescued its afflicted host by feeding photosynthetic carbon into a chlamydia-controlled assimilation pathway.

The idea of an endosymbiotic origin of plastids has become incontrovertible, but many important aspects of plastid origins remain obscured in the mists of more than a billion years of evolutionary history. This commentary provides a critical summary of a recent proposal that primary plastid endosymbiosis was facilitated by the secretion into the host cytosol of effector proteins from intracellular Chlamydiales pathogens that allowed the host to utilize carbohydrates exported from the incipient plastid. Although not without flaws, the model provides an explanation for why primary plastids have evolved so rarely and why Archaeplastida, among all phagotrophic eukaryotes, succeeded in establishing primary plastids.

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.

The medically important order Chlamydiales has long been considered to contain a few closely related bacteria which occur exclusively in animals and humans. This perception of diversity and habitat had to be revised with the recent identification of the genera Simkania, Waddlia, Parachlamydia, and Neochlamydia with the latter two comprising endosymbionts of amoebae. Application of a newly developed PCR assay for the specific amplification of a near full length 16S rDNA fragment of these novel Chlamydia-related bacteria on activated sludge samples revealed the existence of at least four additional, previously unknown evolutionary lineages of Chlamydiales (each showing less than 92% 16S rRNA sequence similarity with all recognized members of this order). These findings suggest that some waste water treatment plants represent reservoirs for a diverse assemblage of environmental chlamydiae, a discovery which might also be of relevance from the viewpoint of human public health.