Hidden from plain sight: NovelChlamydiotadiversity emerging from screening genomic and metagenomic data

Abstract

AbstractChlamydiotaare an ancient and hyperdiverse Phylum of obligate intracellular bacteria. The best characterized representatives are pathogens or parasites of mammals, but it is thought that their most common hosts are microeukaryotes like Amoebozoa. The diversity in taxonomy, evolution, and function of non-pathogenicChlamydiotaare slowly being described. Here we use data mining techniques and genomic analysis to extend our current knowledge ofChlamydiotadiversity and its hosts, in particular the OrderParachlamydiales. We extract oneRhabdochlamydiaceaeand threeSimkaniaceaegenomes from NCBI Short Read Archive deposits of ciliate and algal genome sequencing projects. We then use these to identify a further 14 and 8 genomes respectively amongst existing, unidentified environmental assemblies. From these data we identify two novel clades with host associated data, for which we propose the names ‘CandidatusSacchlamydia’ (FamilyRhabdochlamydiaceae)and ‘CandidatusAmphrikania’ (FamilySimkaniaceae), as well as a third new clade of environmental MAGs ‘CandidatusAcheromydia’ (FamilyRhabdochlamydiaceae). The extent of uncharacterized diversity within theRhabdochlamydiaceaeandSimkaniaceaeis indicated by 16 of the 22 MAGs being evolutionarily distant from currently characterised genera. Within our limited data, we observe great predicted diversity inParachlamydialesmetabolism and evolution, including the potential for metabolic and defensive symbioses as well as pathogenicity. These data provide an imperative to link genomic diversity in metagenomics data to their associated eukaryotic host, and to develop onward understanding of the functional significance of symbiosis with this hyperdiverse clade.Graphical Abstract