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Environmental chlamydiae and amoebae

Environmental chlamydiae and amoebae

Matthias Horn (ORCID: 0000-0002-8309-5855)
  • Grant DOI 10.55776/Y277
  • Funding program FWF START Award
  • Status ended
  • Start December 1, 2005
  • End June 30, 2013
  • Funding amount € 1,200,000

Disciplines

Biology (80%); Health Sciences (20%)

Keywords

    Evolution, Intracellular bacteria, Environmental chlmaydia, Amoeba, Symbiosis

Final report

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.

Research institution(s)
  • Universität Wien - 100%
International project participants
  • Hans-Werner Mewes, Technische Universität München - Germany
  • Ekkehard Neuhaus, Universität Kaiserslautern - Germany

Research Output

  • 10928 Citations
  • 46 Publications
Publications
  • 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

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