Environmental chlamydiae and amoebae
Environmental chlamydiae and amoebae
Disciplines
Biology (80%); Health Sciences (20%)
Keywords
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Evolution,
Intracellular bacteria,
Environmental chlmaydia,
Amoeba,
Symbiosis
Chlamydiae are a unique group of bacteria that infect and live exclusively within eukaryotic host cells. While chlamydial pathogens of humans and animals, such as Chlamydia trachomatis and Chlamydia pneumoniae, are known for more than 100 years, chlamydiae associated with protists have been identified only recently. This project aimed to improve our understanding of these environmental chlamydiae and their similarities with and differences to their pathogenic counterparts by a multiphasic molecular biology approach. We revealed that the diversity of chlamydiae in the environment exceeds the known diversity by orders of magnitude; a vast number of unknown chlamydiae is hidden primarily in marine environments. We developed and successfully applied novel methods to harvest this diversity by isolation of novel chlamydiae from complex environmental samples, resulting in the identification and characterization of several new environmental chlamydiae. Using state-of-the-art genomics analyses, we gained insights into the genetic repertoire of environmental chlamydiae, and we were able to highlight similarities and major differences with their pathogenic counterparts. Using this data we reconstructed the evolutionary history of chlamydiae and revealed that chlamydiae represent probably the oldest group of bacteria able to infect eukaryotic cells; an essential contribution of chlamydiae to the evolution of algae and plants, as suggested recently, seems plausible. Challenging long-standing text-book knowledge, we provide evidence that chlamydiae remain physiologically active even outside of their host cells, and we for the first time were able to demonstrate the presence of peptidoglycan in the cell wall of chlamydiae, a key component of the cell wall of most bacteria whose existence in chlamydiae has been debated controversially for decades. These findings do not only provide a fresh perspective on the cell biology of these bacteria but also have potential implications for anti-chlamydia therapy. Finally, the in-depths analyses of cell envelope associated proteins of environmental chlamydiae such as outer membrane proteins and nucleotide transport proteins provided new insights into the adaptation of chlamydiae to and the interaction with their different host cells. In summary, the knowledge gained in this project contributes to a better understanding of diversity, biology, host interaction and evolution of chlamydiae and demonstrated the power of comparative analysis of pathogens and symbionts.
- Universität Wien - 100%
- Hans-Werner Mewes, Technische Universität München - Germany
- Ekkehard Neuhaus, Universität Kaiserslautern - Germany
Research Output
- 10928 Citations
- 46 Publications
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2013
Title The Pine Bark Adelgid, Pineus strobi, Contains Two Novel Bacteriocyte-Associated Gammaproteobacterial Symbionts DOI 10.1128/aem.03310-13 Type Journal Article Author Toenshoff E Journal Applied and Environmental Microbiology Pages 878-885 Link Publication -
2013
Title Signature Protein of the PVC Superphylum DOI 10.1128/aem.02655-13 Type Journal Article Author Lagkouvardos I Journal Applied and Environmental Microbiology Pages 440-445 Link Publication -
2013
Title Identification and Characterization of a Novel Porin Family Highlights a Major Difference in the Outer Membrane of Chlamydial Symbionts and Pathogens DOI 10.1371/journal.pone.0055010 Type Journal Article Author Aistleitner K Journal PLoS ONE Link Publication -
2013
Title Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae DOI 10.1038/ismej.2013.142 Type Journal Article Author Lagkouvardos I Journal The ISME Journal Pages 115-125 Link Publication -
2013
Title Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling DOI 10.1186/gb-2013-14-2-r11 Type Journal Article Author Clarke M Journal Genome Biology Link Publication -
2013
Title Developmental cycle and host interaction of Rhabdochlamydia porcellionis, an intracellular parasite of terrestrial isopods DOI 10.1111/1462-2920.12252 Type Journal Article Author Sixt B Journal Environmental Microbiology Pages 2980-2993 -
2009
Title Comprehensive in silico prediction and analysis of chlamydial outer membrane proteins reflects evolution and life style of the Chlamydiae DOI 10.1186/1471-2164-10-634 Type Journal Article Author Heinz E Journal BMC Genomics Pages 634 Link Publication -
2009
Title Sequence-Based Prediction of Type III Secreted Proteins DOI 10.1371/journal.ppat.1000376 Type Journal Article Author Arnold R Journal PLoS Pathogens Link Publication -
2009
Title Diatom plastids depend on nucleotide import from the cytosol DOI 10.1073/pnas.0808862106 Type Journal Article Author Ast M Journal Proceedings of the National Academy of Sciences Pages 3621-3626 Link Publication -
2009
Title The Genome of the Amoeba Symbiont “Candidatus Amoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria DOI 10.1128/jb.01379-09 Type Journal Article Author Schmitz-Esser S Journal Journal of Bacteriology Pages 1045-1057 Link Publication -
2008
Title probeCheck – a central resource for evaluating oligonucleotide probe coverage and specificity DOI 10.1111/j.1462-2920.2008.01706.x Type Journal Article Author Loy A Journal Environmental Microbiology Pages 2894-2898 Link Publication -
2008
Title Chlamydia-like bacteria in respiratory samples of community-acquired pneumonia patients DOI 10.1111/j.1574-6968.2008.01099.x Type Journal Article Author Haider S Journal FEMS Microbiology Letters Pages 198-202 Link Publication -
2008
Title Diversity of Bacterial Endosymbionts of Environmental Acanthamoeba Isolates DOI 10.1128/aem.01093-08 Type Journal Article Author Schmitz-Esser S Journal Applied and Environmental Microbiology Pages 5822-5831 Link Publication -
2008
Title High genetic similarity between two geographically distinct strains of the sulfur-oxidizing symbiont ‘Candidatus Thiobios zoothamnicoli’ DOI 10.1111/j.1574-6941.2008.00628.x Type Journal Article Author Rinke C Journal FEMS Microbiology Ecology Pages 229-241 Link Publication -
2008
Title Lawsonia intracellularis Contains a Gene Encoding a Functional Rickettsia-Like ATP/ADP Translocase for Host Exploitation DOI 10.1128/jb.00391-08 Type Journal Article Author Schmitz-Esser S Journal Journal of Bacteriology Pages 5746-5752 Link Publication -
2008
Title Chlamydiae as Symbionts in Eukaryotes DOI 10.1146/annurev.micro.62.081307.162818 Type Journal Article Author Horn M Journal Annual review of microbiology Pages 113-131 -
2007
Title An Acanthamoeba sp. containing two phylogenetically different bacterial endosymbionts DOI 10.1111/j.1462-2920.2007.01268.x Type Journal Article Author Heinz E Journal Environmental Microbiology Pages 1604-1609 Link Publication -
2007
Title Enlightening Energy Parasitism by Analysis of an ATP/ADP Transporter from Chlamydiae DOI 10.1371/journal.pbio.0050231 Type Journal Article Author Trentmann O Journal PLoS Biology Link Publication -
2006
Title Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila DOI 10.1111/j.1365-2958.2006.05193.x Type Journal Article Author Haferkamp I Journal Molecular Microbiology Pages 1534-1545 Link Publication -
2006
Title Environmental chlamydia genomics. Type Book Chapter Author Chlamydia: Genomics And Pathogenesis. -
2006
Title probeBase—an online resource for rRNA-targeted oligonucleotide probes: new features 2007 DOI 10.1093/nar/gkl856 Type Journal Article Author Loy A Journal Nucleic Acids Research Link Publication -
2006
Title The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance DOI 10.1016/j.copbio.2006.05.005 Type Journal Article Author Wagner M Journal Current Opinion in Biotechnology Pages 241-249 -
2012
Title A Straightforward DOPE (Double Labeling of Oligonucleotide Probes)-FISH (Fluorescence In Situ Hybridization) Method for Simultaneous Multicolor Detection of Six Microbial Populations DOI 10.1128/aem.00977-12 Type Journal Article Author Behnam F Journal Applied and Environmental Microbiology Pages 5138-5142 Link Publication -
2014
Title Conserved features and major differences in the outer membrane protein composition of chlamydiae DOI 10.1111/1462-2920.12621 Type Journal Article Author Aistleitner K Journal Environmental Microbiology Pages 1397-1413 Link Publication -
2011
Title Simultaneous 16S and 18S rRNA fluorescence in situ hybridization (FISH) on LR White sections demonstrated in Vestimentifera (Siboglinidae) tubeworms DOI 10.1016/j.acthis.2011.03.008 Type Journal Article Author Schimak M Journal Acta Histochemica Pages 122-130 Link Publication -
2011
Title Unity in Variety—The Pan-Genome of the Chlamydiae DOI 10.1093/molbev/msr161 Type Journal Article Author Collingro A Journal Molecular Biology and Evolution Pages 3253-3270 Link Publication -
2011
Title Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae) DOI 10.1038/ismej.2011.102 Type Journal Article Author Toenshoff E Journal The ISME Journal Pages 384-396 Link Publication -
2011
Title Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms DOI 10.1073/pnas.1105347108 Type Journal Article Author Gruber-Vodicka H Journal Proceedings of the National Academy of Sciences Pages 12078-12083 Link Publication -
2011
Title Proteomic analysis reveals a virtually complete set of proteins for translation and energy generation in elementary bodies of the amoeba symbiont Protochlamydia amoebophila DOI 10.1002/pmic.201000510 Type Journal Article Author Sixt B Journal PROTEOMICS Pages 1868-1892 -
2011
Title A bacterial genome in transition - an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus DOI 10.1186/1471-2148-11-270 Type Journal Article Author Schmitz-Esser S Journal BMC Evolutionary Biology Pages 270 Link Publication -
2014
Title Massive Expansion of Ubiquitination-Related Gene Families within the Chlamydiae DOI 10.1093/molbev/msu227 Type Journal Article Author Domman D Journal Molecular Biology and Evolution Pages 2890-2904 Link Publication -
2013
Title Architecture and host interface of environmental chlamydiae revealed by electron cryotomography DOI 10.1111/1462-2920.12299 Type Journal Article Author Pilhofer M Journal Environmental Microbiology Pages 417-429 Link Publication -
2013
Title Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ DOI 10.1038/ncomms3856 Type Journal Article Author Pilhofer M Journal Nature Communications Pages 2856 Link Publication -
2010
Title Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts DOI 10.1111/j.1462-2920.2009.02065.x Type Journal Article Author Webster N Journal Environmental Microbiology Pages 2070-2082 Link Publication -
2010
Title Raman microspectroscopy reveals long-term extracellular activity of chlamydiae DOI 10.1111/j.1365-2958.2010.07241.x Type Journal Article Author Haider S Journal Molecular Microbiology Pages 687-700 Link Publication -
2010
Title Proteomic aspects of Parachlamydia acanthamoebae infection in Acanthamoeba spp. DOI 10.1038/ismej.2010.68 Type Journal Article Author Leitsch D Journal The ISME Journal Pages 1366-1374 Link Publication -
2010
Title Nucleotide Parasitism by Simkania negevensis (Chlamydiae) DOI 10.1128/jb.00919-10 Type Journal Article Author Knab S Journal Journal of Bacteriology Pages 225-235 Link Publication -
2010
Title Proteomic analysis of the outer membrane of Protochlamydia amoebophila elementary bodies DOI 10.1002/pmic.201000302 Type Journal Article Author Heinz E Journal PROTEOMICS Pages 4363-4376 -
2013
Title 'Candidatus Branchiomonas cysticola' is a common agent of epitheliocysts in seawater-farmed Atlantic salmon Salmo salar in Norway and Ireland. DOI 10.3354/dao02563 Type Journal Article Author Mitchell S Journal Diseases of aquatic organisms Pages 35-43 Link Publication -
2012
Title Lessons from Environmental Chlamydiae. Type Book Chapter Author Siegl A -
2012
Title Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii DOI 10.1371/journal.pgen.1003012 Type Journal Article Author Penz T Journal PLoS Genetics Link Publication -
2012
Title Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies DOI 10.1093/nar/gks808 Type Journal Article Author Klindworth A Journal Nucleic Acids Research Link Publication -
2012
Title A Novel Betaproteobacterial Agent of Gill Epitheliocystis in Seawater Farmed Atlantic Salmon (Salmo salar) DOI 10.1371/journal.pone.0032696 Type Journal Article Author Toenshoff E Journal PLoS ONE Link Publication -
2012
Title Lack of Effective Anti-Apoptotic Activities Restricts Growth of Parachlamydiaceae in Insect Cells DOI 10.1371/journal.pone.0029565 Type Journal Article Author Sixt B Journal PLoS ONE Link Publication -
2010
Title Inclusion Membrane Proteins of Protochlamydia amoebophila UWE25 Reveal a Conserved Mechanism for Host Cell Interaction among the Chlamydiae DOI 10.1128/jb.00605-10 Type Journal Article Author Heinz E Journal Journal of Bacteriology Pages 5093-5102 Link Publication -
2010
Title The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" encodes an afp-like prophage possibly used for protein secretion DOI 10.4161/viru.1.6.13800 Type Journal Article Author Penz T Journal Virulence Pages 541-545 Link Publication