Genomic analysis of 61 Chlamydia psittaci strains reveals extensive divergence associated with host preference

Abstract

Background Chlamydia (C.) psittaci, the causative agent of avian chlamydiosis and human psittacosis, is a genetically heterogeneous species. Its broad host range includes parrots and many other birds, but occasionally also humans (via zoonotic transmission), ruminants, horses, swine and rodents. To assess whether there are genetic markers associated with host tropism we comparatively analyzed whole-genome sequences of 61 C. psittaci strains, 47 of which carrying a 7.6-kbp plasmid. Results Following clean-up, reassembly and polishing of poorly assembled genomes from public databases, phylogenetic analyses using C. psittaci whole-genome sequence alignment revealed four major clades within this species. Clade 1 represents the most recent lineage comprising 40/61 strains and contains 9/10 of the psittacine strains, including type strain 6BC, and 10/13 of human isolates. Strains from different non-psittacine hosts clustered in Clades 2– 4. We found that clade membership correlates with typing schemes based on SNP types, ompA genotypes, multilocus sequence types as well as plasticity zone (PZ) structure and host preference. Genome analysis also revealed that i) sequence variation in the major outer membrane porin MOMP can result in 3D structural changes of immunogenic domains, ii) past host change of Clade 3 and 4 strains could be associated with loss of MAC/perforin in the PZ, rather than the large cytotoxin, iii) the distinct phylogeny of atypical strains (Clades 3 and 4) is also reflected in their repertoire of inclusion proteins (Inc family) and polymorphic membrane proteins (Pmps). Conclusions Our study identified a number of genomic features that can be correlated with the phylogeny and host preference of C. psittaci strains. Our data show that intra-species genomic divergence is associated with past host change and includes deletions in the plasticity zone, structural variations in immunogenic domains and distinct repertoires of virulence factors.

Whole-genome sequencing of Chlamydia psittaci from Australasian avian hosts: A genomics approach to a pathogen that still ruffles feathers

“…Briefly, the genomes of two New Zealand ST27 pigeon strains were diverse yet closely related to the other pigeon ST27 strains, indicating some degree of clonality within this subclade, similar to that observed for the pigeon ST47 subclade. Furthermore, host tropism within the ‘pigeon-type’ PG4 seems more evident [12], with human and historical ferret-derived strains likely resulting from infection spillover from pigeons. However, these observations can only be adequately assessed when additional genomes from ‘pigeon-type’ subclades are provided.…”

“…Notably, SNVs identified in highly dense SNVs and/or predicted recombination regions were removed (i.e. the plasticity zone, major outer membrane protein [ omp A], polymorphic membrane protein [ pmp ] loci, and type III secretion system loci), similar to previous studies [3, 6, 7, 12, 14]. The filtered core-genome SNV alignment (16 595 SNVs) was run through jModelTest v2.1.10 [32], identifying the General Time Reversible (GTR) nucleotide substitution model as the best-fit evolutionary model.…”

“…While our focus was mainly on the phylogenomic diversity and relationships between avian and other host strains, a recent comparative genomic study by Sachse and colleagues thoroughly investigated C. psittaci genomic variable areas associated with phylogeny. Particularly for atypical strains (such as Ful127, Rostinovo-70, AMK), the areas driving phylogeny can include pmp (polymorphic membrane protein), Inc (inclusion membrane protein) and the PZ (plasticity zone) genes, in addition to unique sequences acquired due to recombination [12]. Cell biology studies also showed that different infectious potential and host tropism of avian and mammalian C. psittaci strains is associated with differences in their pmp gene repertoires [43].…”

“…Genomic studies further investigated and highlighted the intraspecies strain diversity of C. psittaci , providing novel insights into the evolution, genome content and phylogeny [1, 3, 6, 7, 12]. For example, Herrmann and colleagues successfully isolated and provided novel insights into the origin of fulmar-derived zoonotic strains from the Faroe Islands [13], whilst other genomic studies described the emergence and spillover into humans and horses of the global virulent and clonal ‘parrot-type 6BC’/sequence type (ST)24 strains [1, 6, 7, 14].…”

“…Extensive surveillance studies have revealed that C. psittaci has a broad host range globally (infecting >500 birds, small mammals, livestock and humans), making it the most diverse and significant veterinary pathogen with zoonotic potential of all chlamydial species [8][9][10][11]. Genomic studies further investigated and highlighted the intraspecies strain diversity of C. psittaci, providing novel insights into the evolution, genome content and phylogeny [1,3,6,7,12]. For example, Herrmann and colleagues successfully isolated and provided novel insights into the origin of fulmar-derived zoonotic strains from the Faroe Islands [13], whilst other genomic studies described the emergence and spillover into humans and horses of the global virulent and clonal 'parrot-type 6BC'/sequence type (ST)24 strains [1,6,7,14].…”