Unexpected genomic features in widespread intracellular bacteria: evidence for motility of marine chlamydiae

Abstract

Chlamydiae are obligate intracellular bacteria comprising important human pathogens and symbionts of protists. Molecular evidence indicates a tremendous diversity of chlamydiae particularly in marine environments, yet our current knowledge is based mainly on terrestrial representatives. Here we provide first insights into the biology of marine chlamydiae representing three divergent clades. Our analysis of single-cell amplified genomes revealed hallmarks of the chlamydial lifestyle, supporting the ancient origin of their characteristic developmental cycle and major virulence mechanisms. Surprisingly, these chlamydial genomes encode a complete flagellar apparatus, a previously unreported feature. We show that flagella are an ancient trait that was subject to differential gene loss among extant chlamydiae. Together with a chemotaxis system, these marine chlamydiae are likely motile, with flagella potentially playing a role during host cell infection. This study broadens our view on chlamydial biology and indicates a largely underestimated potential to adapt to different hosts and environments.

Marine sediments illuminate Chlamydiae diversity and evolution

“…However, the exact functions of these genes in Chlamydiaceae are currently unknown and our analyses suggest that they should represent a priority for future functional investigations. CC-IV genomes also encode homologs of several flagellar proteins (Supplementary Discussion), which clustered with flagellar components recently identified within distantly-related chlamydiae sampled from marine waters 19 (Supplementary Fig. 8), indicating motility as a sharp difference between CC-IV and Chlamydiaceae.…”

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

“…Others were sequenced as part of the microbial community of a biologically active filter of a water treatment plant ( n = 1) (Pinto et al, 2016 ), as part of an investigation of bacterial communities in estuary sediments ( n = 1) (Baker et al, 2015 ), and from an experimental bioreactor used to treat contaminated goldmine water ( n = 2) (Kantor et al, 2015 ). In addition, three single-cell amplified partial genomes from marine Chlamydiae (Collingro et al, 2017 ) and 25 previously published chlamydial genomes (Table 1 ) were studied. The latter contained a majority ( n = 20) of draft assemblies.…”

“…Those genomes are amplified from a single cell. Such approach frequently yield incomplete genomes (Collingro et al, 2017 ). Chlamydiales bacterium SCGC AG-110-M15 missed 55 of the 108 core proteins used to build the species phylogeny (50.9% of the dataset, Figure 1C ).…”

“…Single-cell genomics is another promising approach for the study of uncultivable organisms (Gawad et al, 2016 ). This technique allowed the recovery of partial genomes of three new chlamydial lineages from marine environments (Collingro et al, 2017 ).…”

Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis

“…These appendages likely serve different purposes and can be regulated separately [ 86 ]. The flagellum commonly plays a role in motility and generalized attachment to surfaces and other cells [ 87 ] and may do the same in Nanoarchaeota and other microbial symbionts [ 88 – 90 ]. Once Nanoarchaeota have formed a weak non-specific attachment to a potential host with the flagellum, the T4P systems might be responsible for sensing the suitability of the host and forming a more secure and specific attachment.…”