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• W3010120900 abstract "•Abundant, diverse, and active chlamydiae are found in anoxic, deep-marine sediments•Several of the retrieved marine-sediment chlamydial genomes form new clades•These genomes encode features of symbionts, despite a lack of evidence for hosts•Chlamydiaceae did not evolve early and have relatives in marine sediment The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative abundances of up to 43% of the bacterial community, and a maximum diversity of 163 different species-level taxonomic units, these Chlamydiae represent important community members. Using genome-resolved metagenomics, we reconstructed 24 draft chlamydial genomes, expanding by over a third the known genomic diversity in this phylum. Phylogenomic analyses revealed several novel clades across the phylum, including a previously unknown sister lineage of the Chlamydiaceae, providing new insights into the origin of pathogenicity in this family. We were unable to identify putative eukaryotic hosts for these marine sediment chlamydiae, despite identifying genomic features that may be indicative of host-association. The high abundance and genomic diversity of Chlamydiae in these anoxic marine sediments indicate that some members could play an important, and thus far overlooked, ecological role in such environments and may indicate alternate lifestyle strategies. The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative abundances of up to 43% of the bacterial community, and a maximum diversity of 163 different species-level taxonomic units, these Chlamydiae represent important community members. Using genome-resolved metagenomics, we reconstructed 24 draft chlamydial genomes, expanding by over a third the known genomic diversity in this phylum. Phylogenomic analyses revealed several novel clades across the phylum, including a previously unknown sister lineage of the Chlamydiaceae, providing new insights into the origin of pathogenicity in this family. We were unable to identify putative eukaryotic hosts for these marine sediment chlamydiae, despite identifying genomic features that may be indicative of host-association. The high abundance and genomic diversity of Chlamydiae in these anoxic marine sediments indicate that some members could play an important, and thus far overlooked, ecological role in such environments and may indicate alternate lifestyle strategies. Chlamydiae is a bacterial phylum belonging to the larger Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) superphylum [1Wagner M. Horn M. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance.Curr. Opin. Biotechnol. 2006; 17: 241-249Crossref PubMed Scopus (299) Google Scholar, 2Devos D.P. Ward N.L. Mind the PVCs.Environ. Microbiol. 2014; 16: 1217-1221Crossref PubMed Scopus (11) Google Scholar], which also includes the phylum Lentisphaerae, and putatively Candidatus Omnitrophica. Chlamydiae are so far exclusively represented by obligate intracellular symbionts of eukaryotic hosts. Characterized members share a biphasic life cycle consisting of an infective extracellular non-replicating elementary body (EB) stage and intracellular replicative reticulate body (RB) stage [3Omsland A. Sixt B.S. Horn M. Hackstadt T. Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities.FEMS Microbiol. Rev. 2014; 38: 779-801Crossref PubMed Scopus (53) Google Scholar, 4Taylor-Brown A. Vaughan L. Greub G. Timms P. Polkinghorne A. Twenty years of research into Chlamydia-like organisms: a revolution in our understanding of the biology and pathogenicity of members of the phylum Chlamydiae.Pathog. Dis. 2015; 73: 1-15Crossref PubMed Scopus (60) Google Scholar, 5Elwell C. Mirrashidi K. Engel J. Chlamydia cell biology and pathogenesis.Nat. Rev. Microbiol. 2016; 14: 385-400Crossref PubMed Scopus (159) Google Scholar]. EBs can persist outside their eukaryotic host and are metabolically active [6Haider S. Wagner M. Schmid M.C. Sixt B.S. Christian J.G. Häcker G. Pichler P. Mechtler K. Müller A. Baranyi C. et al.Raman microspectroscopy reveals long-term extracellular activity of Chlamydiae.Mol. Microbiol. 2010; 77: 687-700Crossref PubMed Scopus (72) Google Scholar, 7Sixt B.S. Siegl A. Müller C. Watzka M. Wultsch A. Tziotis D. Montanaro J. Richter A. Schmitt-Kopplin P. Horn M. Metabolic features of Protochlamydia amoebophila elementary bodies--a link between activity and infectivity in Chlamydiae.PLoS Pathog. 2013; 9: e1003553Crossref PubMed Scopus (0) Google Scholar], despite being unable to divide. Chlamydiaceae are a chlamydial family of well-known pathogens of humans and other animals [5Elwell C. Mirrashidi K. Engel J. Chlamydia cell biology and pathogenesis.Nat. Rev. Microbiol. 2016; 14: 385-400Crossref PubMed Scopus (159) Google Scholar, 8Bachmann N.L. Polkinghorne A. Timms P. Chlamydia genomics: providing novel insights into chlamydial biology.Trends Microbiol. 2014; 22: 464-472Abstract Full Text Full Text PDF PubMed Google Scholar, 9Nunes A. Gomes J.P. Evolution, phylogeny, and molecular epidemiology of Chlamydia.Infect. Genet. Evol. 2014; 23: 49-64Crossref PubMed Scopus (54) Google Scholar]. Members include the human pathogen Chlamydia trachomatis, which is the causative agent of sexually transmitted genital tract infections and trachoma (i.e., preventable blindness), and the zoonotic pathogens C. psittaci, C. abortus, and C. felis [9Nunes A. Gomes J.P. Evolution, phylogeny, and molecular epidemiology of Chlamydia.Infect. Genet. Evol. 2014; 23: 49-64Crossref PubMed Scopus (54) Google Scholar]. Chlamydiae also include environmental lineages [10Amann R. Springer N. Schönhuber W. Ludwig W. Schmid E.N. Müller K.D. Michel R. Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp.Appl. Environ. Microbiol. 1997; 63: 115-121Crossref PubMed Google Scholar, 11Horn M. Wagner M. Evidence for additional genus-level diversity of Chlamydiales in the environment.FEMS Microbiol. Lett. 2001; 204: 71-74Crossref PubMed Google Scholar, 12Lagkouvardos I. Weinmaier T. Lauro F.M. Cavicchioli R. Rattei T. Horn M. Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae.ISME J. 2014; 8: 115-125Crossref PubMed Scopus (59) Google Scholar] that primarily infect microbial eukaryotes [13Horn M. Chlamydiae as symbionts in eukaryotes.Annu. Rev. Microbiol. 2008; 62: 113-131Crossref PubMed Scopus (0) Google Scholar]. They have extended metabolic capabilities compared with their pathogenic relatives [3Omsland A. Sixt B.S. Horn M. Hackstadt T. Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities.FEMS Microbiol. Rev. 2014; 38: 779-801Crossref PubMed Scopus (53) Google Scholar, 4Taylor-Brown A. Vaughan L. Greub G. Timms P. Polkinghorne A. Twenty years of research into Chlamydia-like organisms: a revolution in our understanding of the biology and pathogenicity of members of the phylum Chlamydiae.Pathog. Dis. 2015; 73: 1-15Crossref PubMed Scopus (60) Google Scholar, 14Horn M. Collingro A. Schmitz-Esser S. Beier C.L. Purkhold U. Fartmann B. Brandt P. Nyakatura G.J. Droege M. Frishman D. et al.Illuminating the evolutionary history of chlamydiae.Science. 2004; 304: 728-730Crossref PubMed Scopus (306) Google Scholar, 15Collingro A. Tischler P. Weinmaier T. Penz T. Heinz E. Brunham R.C. Read T.D. Bavoil P.M. Sachse K. Kahane S. et al.Unity in variety--the pan-genome of the Chlamydiae.Mol. Biol. Evol. 2011; 28: 3253-3270Crossref PubMed Scopus (0) Google Scholar] and have provided first insights into the evolution of the pathogenic and obligate intracellular lifestyle characteristic of this phylum. Much of our current understanding of chlamydial biology and genomic diversity has been obtained using co-cultivation, selecting for representatives that can replicate in their respective eukaryotic hosts. However, cultivation-independent surveys indicate that Chlamydiae are found broadly distributed across diverse non-host-associated environments [12Lagkouvardos I. Weinmaier T. Lauro F.M. Cavicchioli R. Rattei T. Horn M. Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae.ISME J. 2014; 8: 115-125Crossref PubMed Scopus (59) Google Scholar, 16Schulz F. Eloe-Fadrosh E.A. Bowers R.M. Jarett J. Nielsen T. Ivanova N.N. Kyrpides N.C. Woyke T. Towards a balanced view of the bacterial tree of life.Microbiome. 2017; 5: 140Crossref PubMed Google Scholar] and that their ecological impacts may have thus far been ignored. It was recently reported that metagenomic surveys uncover a much wider taxonomic richness and phylogenetic diversity compared with amplicon studies [16Schulz F. Eloe-Fadrosh E.A. Bowers R.M. Jarett J. Nielsen T. Ivanova N.N. Kyrpides N.C. Woyke T. Towards a balanced view of the bacterial tree of life.Microbiome. 2017; 5: 140Crossref PubMed Google Scholar]. This is likely caused by mismatches of common PCR primers to 16S rRNA genes of Chlamydiae, hindering the amplification of a large fraction of representatives [12Lagkouvardos I. Weinmaier T. Lauro F.M. Cavicchioli R. Rattei T. Horn M. Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae.ISME J. 2014; 8: 115-125Crossref PubMed Scopus (59) Google Scholar, 16Schulz F. Eloe-Fadrosh E.A. Bowers R.M. Jarett J. Nielsen T. Ivanova N.N. Kyrpides N.C. Woyke T. Towards a balanced view of the bacterial tree of life.Microbiome. 2017; 5: 140Crossref PubMed Google Scholar]. However, the application of culture-independent methods has recently resulted in the reconstruction of the first chlamydial single-amplified genomes (SAGs) from marine waters [17Collingro A. Köstlbacher S. Mussmann M. Stepanauskas R. Hallam S.J. Horn M. Unexpected genomic features in widespread intracellular bacteria: evidence for motility of marine chlamydiae.ISME J. 2017; 11: 2334-2344Crossref PubMed Scopus (11) Google Scholar] and metagenome-assembled genomes (MAGs) from animal host-associated populations [18Taylor-Brown A. Pillonel T. Bridle A. Qi W. Bachmann N.L. Miller T.L. Greub G. Nowak B. Seth-Smith H.M.B. Vaughan L. Polkinghorne A. Culture-independent genomics of a novel chlamydial pathogen of fish provides new insight into host-specific adaptations utilized by these intracellular bacteria.Environ. Microbiol. 2017; 19: 1899-1913Crossref PubMed Scopus (8) Google Scholar, 19Taylor-Brown A. Pillonel T. Greub G. Vaughan L. Nowak B. Polkinghorne A. Metagenomic analysis of fish-associated Ca. Parilichlamydiaceae reveals striking metabolic similarities to the terrestrial Chlamydiaceae.Genome Biol. Evol. 2018; 10: 2587-2595Crossref PubMed Scopus (0) Google Scholar, 20Pillonel T. Bertelli C. Aeby S. de Barsy M. Jacquier N. Kebbi-Beghdadi C. Mueller L. Vouga M. Greub G. Sequencing the obligate intracellular Rhabdochlamydia helvetica within its tick host Ixodes ricinus to investigate their symbiotic relationship.Genome Biol. Evol. 2019; 11: 1334-1344Crossref PubMed Scopus (1) Google Scholar]. Additional chlamydial MAGs were reported in a variety of untargeted metagenomic surveys [21Pinto A.J. Marcus D.N. Ijaz U.Z. Bautista-de Lose Santos Q.M. Dick G.J. Raskin L. Metagenomic evidence for the presence of comammox nitrospira-like bacteria in a drinking water system.MSphere. 2015; 1 (e00054–e00015)PubMed Google Scholar, 22Zhang Y. Kitajima M. Whittle A.J. Liu W.T. Benefits of genomic insights and CRISPR-Cas signatures to monitor potential pathogens across drinking water production and distribution systems.Front. Microbiol. 2017; 8: 2036Crossref PubMed Scopus (3) Google Scholar, 23Kantor R.S. van Zyl A.W. van Hille R.P. Thomas B.C. Harrison S.T. Banfield J.F. Bioreactor microbial ecosystems for thiocyanate and cyanide degradation unravelled with genome-resolved metagenomics.Environ. Microbiol. 2015; 17: 4929-4941Crossref PubMed Scopus (43) Google Scholar, 24Anantharaman K. Brown C.T. Hug L.A. Sharon I. Castelle C.J. Probst A.J. Thomas B.C. Singh A. Wilkins M.J. Karaoz U. et al.Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system.Nat. Commun. 2016; 7: 13219Crossref PubMed Scopus (288) Google Scholar, 25Probst A.J. Ladd B. Jarett J.K. Geller-McGrath D.E. Sieber C.M.K. Emerson J.B. Anantharaman K. Thomas B.C. Malmstrom R.R. Stieglmeier M. et al.Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface.Nat. Microbiol. 2018; 3: 328-336Crossref PubMed Scopus (37) Google Scholar, 26Tully B.J. Graham E.D. Heidelberg J.F. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans.Sci. Data. 2018; 5: 170203Crossref PubMed Scopus (81) Google Scholar, 27Baker B.J. Lazar C.S. Teske A.P. Dick G.J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria.Microbiome. 2015; 3: 14Crossref PubMed Google Scholar]. Nevertheless, the diversity, ecology, and biology of members of the Chlamydiae remain severely understudied, and the origins of host association and pathogenesis are currently unresolved. Here, we report the discovery of chlamydial lineages that dominate the microbial communities in anoxic marine sediments taken from near the Arctic Mid-Ocean Ridge [28Pedersen R.B. Rapp H.T. Thorseth I.H. Lilley M.D. Barriga F.J. Baumberger T. Flesland K. Fonseca R. Früh-Green G.L. Jorgensen S.L. Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge.Nat. Commun. 2010; 1: 126Crossref PubMed Scopus (114) Google Scholar]. Obtained MAGs greatly expand sequenced genomic diversity and indicate that chlamydiae play a previously unknown role in these environments. We have inferred a robust species phylogeny of the Chlamydiae phylum and identified several new clades. These include a group that shares a common ancestor with the pathogenic Chlamydiaceae, providing insights into their evolutionary history. Similar to “environmental” chlamydiae, marine sediment lineages generally have extended metabolic capabilities including the ability to use diverse carbon sources. While the new chlamydial MAGs encode host-association features found in other chlamydiae, such as markers of EB formation, secretion systems, and nucleotide transporters, we were unable to identify likely eukaryotic hosts in the sediment samples suggesting that at least some of these lineages may not be obligate symbionts of eukaryotes. Representing the first Chlamydiae-targeted metagenome-based investigation of a non-host-associated environment, our study broadens known phylogenetic and genomic diversity within the Chlamydiae phylum and provides additional insights into the evolution of pathogenic Chlamydiaceae. During a previous metagenomic study aimed at exploring microbial diversity of deep marine sediments from the Arctic Mid-Ocean Ridge [29Spang A. Saw J.H. Jørgensen S.L. Zaremba-Niedzwiedzka K. Martijn J. Lind A.E. van Eijk R. Schleper C. Guy L. Ettema T.J.G. Complex archaea that bridge the gap between prokaryotes and eukaryotes.Nature. 2015; 521: 173-179Crossref PubMed Scopus (479) Google Scholar], we detected several Chlamydiae-related contiguous sequences (contigs). This finding prompted us to systematically screen for Chlamydiae in marine sediment cores from a region surrounding Loki’s Castle hydrothermal vent field (Figure 1A). We extracted DNA from 69 sediment samples (Table S1), followed by screening using Chlamydiae-specific 16S rRNA gene primers. Chlamydiae were identified in 51 (74%) of the samples ranging in depth from 0.1 m to 9.4 m below seafloor (mbsf). Using bacterial-specific 16S rRNA gene amplicon sequencing (Figure S1; see STAR Methods), we investigated the microbial composition of 30 of these samples. We identified 252 operational taxonomic units (OTUs; clustered at 97% identity; Data S1) that could be reliably assigned to Chlamydiae. This analysis revealed notable differences in chlamydiae relative abundance and the number of OTUs between samples (Data S2A and S2B), with relative abundances of up to 43% and up to 163 OTUs (Figure 1B). Furthermore, we found that 155 of the 252 chlamydiae OTUs (hereafter referred to as “marine sediment chlamydiae”) could be identified in at least two samples and 30 OTUs in at least five samples. This indicates that many of the observed chlamydial lineages are common in this environment (Data S2A). The relative abundance of Chlamydiae was highest in anoxic sediment layers up to 1.2 m below the oxic-anoxic transition zone and was largely accounted for by chlamydial OTUs from previously unidentified groups (Data S1 and S2A). We further investigated the phylogenetic diversity of marine sediment chlamydiae by performing a 16S rRNA gene phylogenetic analysis including the presently reported chlamydial OTUs and diverse published chlamydiae sequences [12Lagkouvardos I. Weinmaier T. Lauro F.M. Cavicchioli R. Rattei T. Horn M. Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae.ISME J. 2014; 8: 115-125Crossref PubMed Scopus (59) Google Scholar]. This analysis revealed that the overall phylogenetic diversity of marine sediment chlamydiae spanned, and expanded, the known chlamydial diversity (Figure 1C), revealing several novel major clades. To obtain genomic information from these marine sediment chlamydiae, we employed a genome-resolved metagenomics approach (Figure S1) in which we generated 249.6 Gbp of paired-end reads from four sediment samples with a high relative abundance and phylogenetic diversity of chlamydial OTUs (Figure S1). Sequence assembly generated 5.85 Gbp of contigs larger than 1 Kbp. To assess the phylogenetic diversity of Chlamydiae-related sequences in these metagenome assemblies, we performed phylogenetic analyses of contigs containing 16S rRNA gene sequences or at least five genes of a conserved 15-ribosomal protein gene cluster (see STAR Methods). These analyses revealed numerous Chlamydiae-related contigs (Figure S1), most of which represented novel lineages. Contigs were binned into 24 highly complete (median 95% completeness; Data S3A) MAGs on the basis of their tetranucleotide frequencies and patterns of sequence coverage across samples. They differed markedly in predicted genome size (1.3-2.6 Mbp), GC-content (26.4%–48.9%), and gene content (Figures 2, 3, and S2; Data S3A).Figure 3Comparative Genomics Reveals Typical Chlamydial Features, yet More Diverse EcologyShow full captionPresence of selected proteins and pathways across Chlamydiae, including traits associated with the chlamydiae biphasic life cycle, central carbon metabolism, nucleotide and amino acid biosynthesis, motility, metal resistance, and nitrogen, sulfur, and phosphorus metabolism. Species representatives are color-coded according to Chlamydiae clades. Where relevant, the corresponding KEGG pathway module is indicated in brackets.See also Figure S2; Data S4.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Presence of selected proteins and pathways across Chlamydiae, including traits associated with the chlamydiae biphasic life cycle, central carbon metabolism, nucleotide and amino acid biosynthesis, motility, metal resistance, and nitrogen, sulfur, and phosphorus metabolism. Species representatives are color-coded according to Chlamydiae clades. Where relevant, the corresponding KEGG pathway module is indicated in brackets. See also Figure S2; Data S4. To robustly infer the evolutionary relationships of the marine sediment chlamydiae to known lineages (Data S3B and S3C), we performed in-depth phylogenomic analyses of concatenated conserved marker protein sequence datasets shared across the Chlamydiae phylum (Figure S3; Data S3D). We have broadly sampled chlamydial taxa and included all sequenced species representatives in our analyses (Data S3A and S3B) and applied phylogenomic approaches with the aim to detect and alleviate potential phylogenetic artifacts that can be caused by the inclusion of fast-evolving and compositionally biased lineages [30Philippe H. de Vienne D.M. Ranwez V. Roure B. Baurain D. Delsuc F. Pitfalls in supermatrix phylogenomics.Eur. J. Taxon. 2017; 283: 1-25Google Scholar] (Figure S4). Phylogenomic analyses recovered seven consistent and well-supported clades of high taxonomic rank within the Chlamydiae (Figures 2, S2, and S4). In addition to the Chlamydiaceae and the environmental chlamydiae, these include five clades that are mainly represented by MAGs (Chlamydiae Clades or “CC” I to IV and Candidatus “Anoxychlamydiales”). Anoxychlamydiales are unique among Chlamydiae because they have distinctive gene repertoires indicative of an anaerobic lifestyle and will be described in detail in a complementary study. We recognized two major sub-divisions: one comprised primarily of uncultured lineages CC-I (including Simkania negevensis), CC-II, CC-III, and Anoxychlamydiales and the second of Chlamydiaceae, environmental chlamydiae, and CC-IV. The latter forms a well-supported sister relationship with the Chlamydiaceae and is solely represented by novel MAGs from this study (Figures 2, S2, and S4). The newly reconstructed marine sediment chlamydiae genomes are phylogenetically diverse (Figures 2, S2, and S4), though most are placed within the two major clades CC-II and Anoxychlamydiales, which also include MAGs associated with estuary sediment, aquifer groundwater, a drinking water treatment plant, and ticks [20Pillonel T. Bertelli C. Aeby S. de Barsy M. Jacquier N. Kebbi-Beghdadi C. Mueller L. Vouga M. Greub G. Sequencing the obligate intracellular Rhabdochlamydia helvetica within its tick host Ixodes ricinus to investigate their symbiotic relationship.Genome Biol. Evol. 2019; 11: 1334-1344Crossref PubMed Scopus (1) Google Scholar, 21Pinto A.J. Marcus D.N. Ijaz U.Z. Bautista-de Lose Santos Q.M. Dick G.J. Raskin L. Metagenomic evidence for the presence of comammox nitrospira-like bacteria in a drinking water system.MSphere. 2015; 1 (e00054–e00015)PubMed Google Scholar, 24Anantharaman K. Brown C.T. Hug L.A. Sharon I. Castelle C.J. Probst A.J. Thomas B.C. Singh A. Wilkins M.J. Karaoz U. et al.Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system.Nat. Commun. 2016; 7: 13219Crossref PubMed Scopus (288) Google Scholar, 27Baker B.J. Lazar C.S. Teske A.P. Dick G.J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria.Microbiome. 2015; 3: 14Crossref PubMed Google Scholar]. Although generally compatible at the family level, our results are notably different at higher-level taxonomic classifications based on previously available genome data [31Pillonel T. Bertelli C. Greub G. Environmental metagenomic assemblies reveal seven new highly divergent chlamydial lineages and hallmarks of a conserved intracellular lifestyle.Front. Microbiol. 2018; 9: 79Crossref PubMed Scopus (9) Google Scholar]. In particular, previous studies have suggested that the Chlamydiaceae represents an early-diverging order in the Chlamydiae phylum [15Collingro A. Tischler P. Weinmaier T. Penz T. Heinz E. Brunham R.C. Read T.D. Bavoil P.M. Sachse K. Kahane S. et al.Unity in variety--the pan-genome of the Chlamydiae.Mol. Biol. Evol. 2011; 28: 3253-3270Crossref PubMed Scopus (0) Google Scholar, 18Taylor-Brown A. Pillonel T. Bridle A. Qi W. Bachmann N.L. Miller T.L. Greub G. Nowak B. Seth-Smith H.M.B. Vaughan L. Polkinghorne A. Culture-independent genomics of a novel chlamydial pathogen of fish provides new insight into host-specific adaptations utilized by these intracellular bacteria.Environ. Microbiol. 2017; 19: 1899-1913Crossref PubMed Scopus (8) Google Scholar, 19Taylor-Brown A. Pillonel T. Greub G. Vaughan L. Nowak B. Polkinghorne A. Metagenomic analysis of fish-associated Ca. Parilichlamydiaceae reveals striking metabolic similarities to the terrestrial Chlamydiaceae.Genome Biol. Evol. 2018; 10: 2587-2595Crossref PubMed Scopus (0) Google Scholar, 31Pillonel T. Bertelli C. Greub G. Environmental metagenomic assemblies reveal seven new highly divergent chlamydial lineages and hallmarks of a conserved intracellular lifestyle.Front. Microbiol. 2018; 9: 79Crossref PubMed Scopus (9) Google Scholar, 32Kamneva O.K. Knight S.J. Liberles D.A. Ward N.L. Analysis of genome content evolution in pvc bacterial super-phylum: assessment of candidate genes associated with cellular organization and lifestyle.Genome Biol. Evol. 2012; 4: 1375-1390Crossref PubMed Scopus (39) Google Scholar, 33Pillonel T. Bertelli C. Salamin N. Greub G. Taxogenomics of the order Chlamydiales.Int. J. Syst. Evol. Microbiol. 2015; 65: 1381-1393Crossref PubMed Scopus (27) Google Scholar]. In contrast, our phylogenetic analyses strongly support that Chlamydiaceae and CC-IV represent sister clades and together share a common ancestor with environmental chlamydiae (Figures 2, S2, and S4). The branch leading to the Chlamydiaceae family is relatively long, which may be due in part to their evolutionary transition to a parasitic lifestyle with a restricted animal host range. The inclusion of CC-IV in our analyses shortens the long branch to the Chlamydiaceae, and thus diminishes the risk of phylogenetic reconstruction artifacts that could have previously attracted the latter to the base of the phylum. Compared with prior analyses, our results indicate that Chlamydiaceae emerged relatively late in chlamydiae evolution and that features specifically associated with their pathogenicity likely evolved more recently than previously assumed. Additionally, in a recent study, the long-branching orphan lineage Chlamydiae bacterium RIFCSPHIGHO2_12_FULL_49_11 was inferred as the second-deepest branching lineage within Chlamydiae (after the divergence of Ca. Similichlamydia epinephelii) (Figure S2) and was proposed to form the new order Candidatus Novochlamydiales [31Pillonel T. Bertelli C. Greub G. Environmental metagenomic assemblies reveal seven new highly divergent chlamydial lineages and hallmarks of a conserved intracellular lifestyle.Front. Microbiol. 2018; 9: 79Crossref PubMed Scopus (9) Google Scholar]. However, in our analyses, this lineage is well-supported within the C-I, C-II, C-III, and Anoxychlamydiales sub-division (Figures 2 and S2) and may be closely related to the Simkaniaceae family (Figure 2). The prior finding of Chlamydiae bacterium RIFCSPHIGHO2_12_FULL_49_11 as a deep-branching Chlamydiae order may have been an artifact caused by long-branch attraction. Uncovering the sister relationship of CC-IV and the pathogenic Chlamydiaceae allowed us to re-evaluate the evolutionary events leading to their emergence. The genome sizes of CC-IV (1.3–2.1 Mbp) are smaller than those of environmental chlamydiae (2.1–3.4 Mbp) but larger than those of Chlamydiaceae (1–1.2 Mbp); suggesting that the latter have been subjected to genome reduction, a feature often observed in animal pathogens [34Toft C. Andersson S.G.E. Evolutionary microbial genomics: insights into bacterial host adaptation.Nat. Rev. Genet. 2010; 11: 465-475Crossref PubMed Scopus (211) Google Scholar]. We analyzed the presence and absence patterns of non-supervised orthologous groups (NOGs) and their functional categories in Chlamydiaceae, CC-IV, and environmental chlamydiae (Figures S2 and S5; Data S4A). Our results support previous reports indicating that the evolution of the Chlamydiaceae family was characterized by massive gene loss and functional streamlining [9Nunes A. Gomes J.P. Evolution, phylogeny, and molecular epidemiology of Chlamydia.Infect. Genet. Evol. 2014; 23: 49-64Crossref PubMed Scopus (54) Google Scholar, 14Horn M. Collingro A. Schmitz-Esser S. Beier C.L. Purkhold U. Fartmann B. Brandt P. Nyakatura G.J. Droege M. Frishman D. et al.Illuminating the evolutionary history of chlamydiae.Science. 2004; 304: 728-730Crossref PubMed Scopus (306) Google Scholar, 15Collingro A. Tischler P. Weinmaier T. Penz T. Heinz E. Brunham R.C. Read T.D. Bavoil P.M. Sachse K. Kahane S. et al.Unity in variety--the pan-genome of the Chlamydiae.Mol. Biol. Evol. 2011; 28: 3253-3270Crossref PubMed Scopus (0) Google Scholar, 35Subtil A. Coll" @default.
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• W3010120900 title "Marine Sediments Illuminate Chlamydiae Diversity and Evolution" @default.
• W3010120900 cites W104710838 @default.
• W3010120900 cites W1614139436 @default.
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