Environmental Chlamydia Genomics and Post-Genomics
 Environmental chlamydiae have been discovered as obligate endosymbionts of free-living amoebae and have been implicated as potential human pathogens. Phylogenetically the environmental chlamydiae form a deep branching novel lineage within the medically important order Chlamydiales. Despite their high diversity and ubiquitous distribution in clinical and environmental samples only limited information about genetics and ecology of these microorganisms was available until recently.
We have recently determined the complete genome sequence of a representative of environmental chlamydiae, the Parachlamydia-related strain UWE25, which is in the process of being validly described as Protochlamydia amoebophila (Horn et al., 2004).
The genome of this Acanthamoeba symbiont is about twice as large as the genomes of all pathogenic chlamydiae sequenced to date and thus represents the second largest genome of obligate intracellular bacteria. Nevertheless, many essential metaboli c pathways are truncated in the UWE25 genome. Similar to pathogenic chlamydiae, these environmental chlamydiae thus depend on the availability of host-derived metabolites that are imported into the chlamydial cell by a variety of transporters ( Nucleotide transport proteins in obligate intracellular bacteria). Taken together, these findings provide a rationale for the observed obligate intracellular life style of environmental chlamydiae and reveal striking similarities in the biology of environmental and pathogenic chlamydiae.
However, environmental chlamydiae seem to be more independent from their host cells than pathogenic chlamydiae, since they possess a complete TCA cycle and a more versatile respiratory chain. In addition, there seem to be notable differences in cell wall composition between environmental and pathogenic chlamydiae, as genomic analysis failed to identify homologues of the major outer membrane protein or polymorphic outer membrane proteins in UWE25.
Interestingly however, the environmental chlamydia strain UWE25 encodes several proteins that have been associated with virulence of pathogenic chlamydiae, including a type three secretion system, the chlamydial protease-like activity factor, and putative inclusion proteins. Although UWE25 additionally possesses a type four secretion system (that is absent in pathogenic chlamydiae), this suggests that in principle the interaction of environmental chlamydiae with their amoeba hosts resembles the interaction between pathogenic chlamydiae and animal or human cells.
A comprehensive online database containing the complete annotation and a variety of pre-calculated analyses, prediction results and sequence analysis tools is available. The environmental chlamydia genome database allows any user to add and improve the existing annotation.
Reconstructing the evolutionary history of chlamydiae
A major focus of our comparative genome sequence analysis of environmental and pathogenic chlamydiae was the evolution of chlamydiae and the inference of gene phylogenies. In this context, the high number of plant homologues in the UWE25 genome seemed intriguing and confirmed the previously hypothesized ancient relationship between chlamydiae, cyanobacteria and plastids (Brinkman et al., 2002). Phylogenetic reconstructions suggested that this relationship was rather complex and involved multiple lateral gene transfer events between these groups.
Consistent with the obligate intracellular life style of environmental and pathogenic chlamydiae, no traces of significant recent gene acquisition were detectable in the UWE25 genome. The genome of this amoebal symbiont thus opens a window on the genetic make-up of ancestral chlamydiae. Comparative and phylogenetic genome analysis revealed that the last common ancestor of both pathogenic and environmental chlamydiae, which lived around 700 million years ago, was already adapted to intracellular survival in early eukaryotes. Several virulence factors, like the type three secretion system, required for interaction of pathogenic chlamydiae with their hosts, evolved from genes of the last common chlamydial ancestor. Early members of the chlamydial evolutionary lineage were therefore major inventors of mechanisms for exploitation of eukaryotic cells as an ecological niche. Their analysis shed new light on the evolution of intracellular bacterial pathogens.
What's next?
The discovery of environmental chlamydiae opened a new possibility to investigate chlamydiae using a comparative approach. This approach already revealed novel insights into the biology and evolution of chlamydiae, which will be supplemented by future application of functional genomics, including global transcription and proteome analysis of environmental chlamydiae.
The ChlamydiaTaxogenomic project, currently underway at TIGR and aiming at complete genome sequencing of all remaining species within the phylum Chlamydiae will clearly lift comparative genome analysis of chlamydiae to the next level. Furthermore, genome sequencing of a representative of the natural hosts of environmental chlamydiae, Acanthamoeba castellanii, is in progress. The availability of this genome sequence will enable a more advanced and sophisticated comparison of the interaction of environmental and pathogenic chlamydiae with their respective host cells.
In addition, we are currently investigating the transcriptome and proteome of the environmental chlamydia UWE25, which is in the process of being described as Protochlamydia amoebophila.
[This text was modified from an abstract published in "Proceedings of the 5th Meeting of the European Society for Chlamydia Research", Budapest, September 2004.]
Investigated by: Matthias Horn, Astrid Collingro, Susanne Haider, Elena Tönshoff,
Barbara Sixt, Lena König, Ilias Lagkouvardos, Karin Aistleitner, Alexander Siegl, Birgit Hiess
This research is supported by:  
Links:
Environmental chlamydiae
Nucleotide transport proteins in environmental chlamydiae
Environmental chlamydia genome database
ChlamydiaeDB
References:
- Horn, M., Collingro, A., Schmitz-Esser, S., Beier, C.L., Purkhold, U., Fartmann, B., Brandt, P., Nyakatura, G.J., Droege, M., Frishman, D., Rattei, T., Mewes, H.-W., and Wagner, M. (2004). Illuminating the evolutionary history of chlamydiae. Science 304, 728-730.
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Supplementary material
Living Microbial Fossils. Movie showing environmental chlamydia UWE25 within
its amoeba host cells. © AAAS/Science. [Windows Media Player], [Quicktime]
- Brinkman, F. S., Blanchard, J. L., Cherkasov, A. & other authors (2002). Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res 12, 1159-1167.
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