Prof. Dr. Matthias Horn
Department of Microbial Ecology
Faculty Center of Ecology
Faculty of Life Sciences
University of Vienna
Althanstr. 14
A-1090 Wien
Austria
 
phone: +43 1 4277 54393
fax: +43 1 4277 54389
email:
 
 
Bacterial endosymbionts of free-living amoebae
The occurrence of bacterial endosymbionts in free-living amoebae has been known for decades, but their obligate intracellular lifestyle hampered their identification. Only recently, application of the full cycle rRNA approach including 16S rRNA gene sequencing and fluorescence in situ hybridization with 16S rRNA-targeted oligonucleotide probes assigned the symbionts of Acanthamoeba spp. and Hartmannella sp. to five different evolutionary lineages within the Proteobacteria, the Bacteroidetes, and the Chlamydiae, respectively. Several of these bacterial symbiont groups are most closely related to bacterial pathogens of humans, and it has been suggested that some of them should be considered potential emerging pathogens. Complete genome sequence analysis of a chlamydia-related symbiont of Acanthamoeba sp. showed that this endosymbiont uses similar mechanisms for interaction with its eukaryotic host cell as well known bacterial pathogens of humans. Furthermore, phylogenetic analysis suggested that these mechanisms have been invented by the ancestor of the amoeba symbionts in interplay with ancient unicellular eukaryotes.
 more ...
 
Topics
 Environmental chlamydiae
 Nucleotide transport proteins in environmental chlamydiae
 Environmental chlamydia genomics and post-genomics
 Whole genome analysis of 'Candidatus Amoebophilus asiaticus'
 
Publications in peer reviewed journals
  1. Toenshoff ER, Gruber D, Horn M. 2012. Coevolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ. Microbiol. , in press.
  2. Sixt BS, Hiess B, König L, Horn M. 2012. Lack of effective anti-apoptotic activities restricts growth of Parachlamydiaceae in insect cells. PLoS One : e29565.
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  3. Toenshoff ER, Penz T, Narzt T, Collingro A, Schmitz-Esser S, Pfeiffer S, Klepal W, Wagner M, Weinmaier T, Rattei T, Horn M. 2012. Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae) ISME J. 6: 384-396.
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  4. Schmitz-Esser S, Penz T, Spang A, Horn M. 2011. A bacterial genome in transition - an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus. BMC Evol. Biol. 11: 270.
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  5. Steger D, Berry D, Haider S, Horn M, Wagner M, Stocker R, Loy A. 2011. Systematic spatial bias in DNA microarray hybridization is caused by probe spot position-dependent variability in lateral diffusion. PloS One 6: e23727.
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  6. Gruber-Vodicka HR, Dirks U, Leisch N, Baranyi C, Stoecker K, Bulgheresi S, Heindl NR, Horn M, Lott C, Loy A, Wagner M, Ott J. 2011. Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. Proc. Natl. Acad. Sci. USA 108: 12078-12083.
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  7. Collingro A, Tischler P, Weinmaier T, Penz T, Heinz E, Brunham RC, Read TD, Bavoil PM, Sachse K, Kahane S, Friedman MG, Rattei T, Myers GSA, Horn M. 2011. Unity in variety - the pan-genome of the Chlamydiae. Mol. Biol. Evol. 28: 3253-3270.
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  8. Sixt BS, Heinz C, Pichler P, Heinz E, Montanaro J, Op den Camp HJM, Ammerer G, Mechtler K, Wagner M, Horn M. 2011. Proteomic analysis reveals a virtually complete set of proteins for translation and energy generation in elementary bodies of the amoeba symbiont Protochlamydia amoebophila. Proteomics 11: 1868-1892.
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  9. Knab S, Mushak TM, Schmitz-Esser S, Horn M, Haferkamp I. 2011. Nucleotide parasitism by Simkania negevensis (Chlamydiae). J. Bacteriol. 193: 225-235.
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  10. Heinz E, Pichler P, Heinz C, op den Camp HJM, Toenshoff ER, Ammerer G, Mechtler K, Wagner M, Horn M. 2010. Proteomic analysis of the outer membrane of Protochlamydia amoebophila elementary bodies. Proteomics 10: 4363-4376.
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  11. Penz T, Horn M, Schmitz-Esser S. 2010. The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" encodes an afp-like prophage possibly used for protein secretion. Virulence 1: 1-5.
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  12. Berry D, Horn M, Xi C, Raskin L. 2010. Mycobacterium avium infections of Acanthamoeba strains: host strain variability, grazing-acquired infections, and altered dynamics of inactivation with monochloramine. Appl. Environ. Microbiol. 76: 6685-6688.
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  13. Heinz E, Rockey DD, Montanaro J, Aistleitner K, Wagner M, Horn M. 2010. Inclusion membrane proteins of Protochlamydia amoebophila UWE25 reveal a conserved mechanism for host cell interaction among the Chlamydiae. J. Bacteriol. 192: 5093-5102.
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  14. Haider S, Wagner M, Schmid MC, Sixt BS, Christian JG, Häcker G, Pichler P, Mechtler K, Müller A, Baranyi C, Toenshoff ER, Montanaro J, Horn M. 2010. Raman microspectroscopy reveals long-term extracellular activity of chlamydiae. Mol. Microbiol. 77: 687-700.
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     Supporting information [PDF]
     Highlighted in Nature [PDF]
     Highlighted by Faculty of 1000
  15. Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M. 2010. The genome of the amoeba symbiont 'Candidatus Amoebophilus asiaticus' reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J. Bacteriol. 192: 1045-1057.
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     Supplementary material [PDF]
  16. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, Wagner M. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12: 2070-2082.
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     Supplementary material [PDF]
  17. Heinz E, Tischler P, Rattei T, Myers G, Wagner M, Horn M. 2009. Comprehensive in silico prediction and analysis of chlamydial outer membrane proteins reflects evolution and life style of the Chlamydiae. BMC Genomics 10: 634.
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     Supporting information PDF]
  18. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, Behrens S, Niinikoski A, Mewes HW, Horn M, Rattei T. 2009. Sequence-based prediction of type III secreted proteins. PLoS Pathogens 5: e1000376.
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  19. Ast M, Gruber A, Schmitz-Esser S, Neuhaus HE, Kroth PG, Horn M, Haferkamp I. 2009. Diatom plastids depend on nucleotide import from the cytosol. Proc. Natl. Acad. Sci. USA 106: 3621-3626.
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     Supplementary online material [PDF]
  20. Rinke C, Schmitz-Esser S, Loy A, Horn M, Wagner M, Bright M. 2009. High genetic similarity between two geographically distinct strains of the sulfur-oxidizing symbiont 'Candidatus Thiobios zoothamnicoli' FEMS Microbiol. Ecol. 67: 229-41.
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  21. Schmitz-Esser S, Toenshoff ER, Haider S, Heinz E, Hoenninger VM, Wagner M, Horn M. 2008. Diversity of bacterial endosymbionts of environmental Acanthamoeba isolates. Appl. Environ. Microbiol. 74: 5822-5831.
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     Supplementary material (Table S1)
  22. Schmitz-Esser S, Haferkamp I, Knab S, Penz T, Ast M, Kohl C, Wagner M, Horn M. 2008. Lawsonia intracellularis encodes a functional rickettsia-like ATP/ADP translocase for host exploitation. J. Bacteriol. 190: 5746-5752.
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  23. Loy A, Arnold R, Tischler P, Rattei T, Wagner M, Horn M. 2008. probeCheck - a central resource for evaluating oligonucleotide probe coverage and specificity. Environ. Microbiol. 10: 2894-2896.
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  24. Horn M. 2008. Chlamydiae as symbionts in eukaryotes. Ann. Rev. Microbiol. 62: 113-131.
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  25. Haider S, Collingro A, Walochnik J, Wagner M, Horn M. 2008. Chlamydia-like bacteria in respiratory samples of community-acquired pneumonia patients. FEMS Microbiol. Lett. 281: 198-202.
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  26. Trentmann O, Horn M, van Scheltinga AC, Neuhaus HE, Haferkamp I. 2007. Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol. 9: e231.
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     Supporting information (Figs S1, S2)
  27. Heinz E, Kolarov I, Kästner C, Toenshoff ER, Wagner M, Horn M. 2007. An Acanthamoeba sp. containing two phylogenetically different bacterial endosymbionts Environ. Microbiol. 9: 1604-1609.
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  28. Loy A, Maixner F, Wagner M, Horn M. 2007. probeBase - an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res. 35: D800-D804.
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  29. Wagner M, Horn M. 2006. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17: 241-249.
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  30. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mave D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid MC, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D. 2006. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790-794.
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     Supplementary material [PDF]
  31. Haferkamp I, Schmitz-Esser S, Wagner M, Neigel N, Horn M, Neuhaus HE. 2006. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol. 60: 1534-1545.
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     Supplemental Material
  32. Rinke C, Schmitz-Esser S, Stoecker K, Nussbaumer AD , Molnár DA, Vanura K, Wagner M, Horn M, Ott J, Bright M. 2006. Candidatus Thiobios zoothamnicoli, an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl. Environ. Microbiol. 72: 2014-2021.
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  33. Collingro A, Toenshoff ER, Taylor MW, Fritsche TR, Wagner M, Horn M. 2005. 'Candidatus Protochlamydia amoebophila', an endosymbiont of Acanthamoeba spp. Int. J. Syst. Evol. Microbiol. 55: 1863-1866.
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  34. Everett KDE, Thao M, Horn M, Dyszynski GLE, Baumann P. 2005. Novel chlamydiae in whiteflies and scale insects: endosymbionts "Candidatus Fritschea bemisiae" strain Falk and "Candidatus Fritschea eriococci" strain Elm. Int. J. Syst. Evol. Microbiol. 55: 1581-1587.
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  35. Collingro A, Poppert S, Heinz E, Schmitz-Esser S, Essig A, Schweikert M, Wagner M, Horn M. 2005. Recovery of an environmental chlamydia strain from activated sludge by co-cultivation with Acanthamoeba sp. Microbiology 151: 301-309.
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  36. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y. 2005. Amoeba as training grounds intracellular bacterial pathogens. Appl. Environ. Microbiol. 71: 20-28.
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  37. Haferkamp I, Schmitz-Esser S, Linka N, Urbany C, Collingro A, Wagner M, Horn M, Neuhaus HE. 2004. A candidate NAD+ transporter in an intracellular bacterial symbiont related to chlamydiae. Nature 432: 622-625.
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     Supplementary material [PDF]
  38. Fokin SI, Przybos E, Chivilev SM, Beier CL, Horn M, Skotarczak B, Wodecka B, Fujishima M. 2004. Morphological and molecular investigations of Paramecium schewiakoffi sp. nov. (Ciliophora, Oligohymenophorea) and current status of distribution and taxonomy of Paramecium spp. Europ. J. Protist. 40: 225-243.
  39. Horn M, Wagner M. 2004. Bacterial endosymbionts of free-living amoebae. J. Euk. Microbiol. 51: 509-514.
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  40. Horn M, Collingro A, Schmitz-Esser S, Beier CL, Purkhold U, Fartmann B, Brandt P, Nyakatura GJ, Droege M, Frishman D, Rattei T, Mewes HW, Wagner M. 2004. Illuminating the evolutionary history of chlamydiae. Science 304: 728-730.
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     Supplementary material [PDF]
     Press release [PDF]
     Press release (German) [PDF]
     Movie showing environmental chlamydia UWE25 within its amoeba host cells.
        © AAAS/Science. [Windows Media Player]
     Movie showing environmental chlamydia UWE25 within its amoeba host cells.
        © AAAS/Science.[Quicktime]
     Environmental chlamydia genome database
  41. Fieseler L, Horn M, Wagner M, Hentschel U. 2004. Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl. Environ. Microbiol. 70: 3724-3732.
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  42. Collingro A, Walochnik J, Baranyi C, Michel R, Wagner M, Horn M, Aspöck H. 2004. Chlamydial endocytobionts of free-living amoebae differentially affect the growth rate of their hosts. Europ. J. Protist. 40: 57-60.
  43. Schmitz-Esser S, Linka N, Collingro A, Beier CL, Neuhaus HE, Wagner M, Horn M. 2004. ATP/ADP translocases: A common feature of obligate intracellular amoebal symbionts related to chlamydiae and rickettsiae. J. Bacteriol. 186: 683-691.
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     ARB/FastA database
  44. Hutter G, Schlagenhauf U, Valenza G, Horn M, Burgemeister S, Claus H, Vogel U. 2003. Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiology 149: 67-75.
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  45. Adamczyk J, Hesselsoe M, Iversen N, Horn M, Lehner A, Nielsen PH, Schloter M, Roslev P, Wagner M. 2003. The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function. Appl. Environ. Microbiol. 69: 6875-6887.
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  46. Wagner M, Horn M, Daims H . 2003. Fluorescence in situ hybridisation for the identification and charcterisation of prokaryotes. Curr. Opin. Microbiol. 6: 302-309.
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  47. Thoms C, Horn M, Wagner M, Hentschel U, Proksch P. 2003. Monitoring microbial diversity and natural products profiles of the sponge Aplysina cavernicola following transplantation. Marine Biology 142: 685-692.
  48. Loy A, Horn M, Wagner M.. 2003. probeBase - an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res. 31: 514-516.
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  49. Beier CL, Horn M, Michel R, Schweikert M, Gortz HD, Wagner M. 2002. The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl. Environ. Microbiol. 68: 6043-6050.
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  50. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS. 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68: 4431-4440.
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  51. Poppert S, Essig A, Marre R, Wagner M, Horn M. 2002. Detection and differentiation of chlamydiae by fluorescence in situ hybridization (FISH). Appl. Environ. Microbiol. 68: 4081-4089.
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  52. Skriwan C, Fajardo M, Hagele S, Horn M, Wagner M, Michel R, Krohne G, Schleicher M, Hacker J, Steinert M. 2002. Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int. J. Med. Microbiol. 291: 615-624.
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  53. Horn M, Fritsche TR, Linner T, Gautom RK, Harzenetter MD, Wagner M. 2002. Obligate bacterial endosymbionts of Acanthamoeba spp. related to the ß-subclass of Proteobacteria: proposal of 'Candidatus Procabacter acanthamoebae' gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 52: 599–605.
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  54. Horn M, Wagner M. 2001. Evidence for additional genus-level diversity of Chlamydiales in the environment. FEMS Microbiol. Lett. 204: 71-74.
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  55. Horn M, Harzenetter MD, Linner T, Schmid EN, Muller KD, Michel R, Wagner M. 2001. Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus'. Environ. Microbiol. 3: 440-449.
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  56. Kanagawa T, Kamagata Y, Aruga S, Kohno T, Horn M, Wagner M. 2000. Phylogenetic relationships of filamentous bacteria of the Eikelboom Type 021N isolated from bulking activated sludge and development of an encompassing set of 021N-specific oligonucleotide probes. Appl. Environ. Microbiol. 66: 5043-5052.
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  57. Fritsche TR, Horn M, Wagner M, Herwig RP, Schleifer KH, Gautom RK. 2000. Phylogenetic diversity among geographically dispersed Chlamydiales endosymbionts recovered from clinical and environmental isolates of Acanthamoeba spp. Appl. Environ. Microbiol. 66: 2613-2619.
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  58. Horn M, Wagner M, Muller KD, Schmid EN, Fritsche TR, Schleifer KH, Michel R. 2000. Neochlamydia hartmannellae gen. nov. sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology 146: 1231-1239.
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  59. Horn M, Fritsche TR, Gautom RK, Schleifer KH, Wagner M. 1999. Novel Bacterial Endosymbionts of Acanthamoeba isolates related to the Paramecium Symbiont Caedibacter caryophilus. Environ. Microbiol. 1: 357-367.
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  60. Fritsche TR, Horn M, Seyedirashti S, Gautom RK, Schleifer KH, Wagner M. 1999. In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the Rickettsiales. Appl. Environ. Microbiol. 65: 206-212.
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Book chapters and other publications
  1. Horn M, Collingro A, Schmitz-Esser S, Wagner M. 2006. Environmental chlamydia genomics. In Chlamydia: genomics and pathogenesis, pp. 25-44. (Bavoil PM, Wyrick PB, ed.). Horizon Scientific Press, Norfolk.
     Order information
  2. Horn M, Wagner M. 2005. Die Evolution der Chlamydien - Einblicke in die Entwicklungsgeschichte bedeutender bakterieller Krankheitserreger. GenomXpress Sonderausgabe 3: 50.
  3. Collingro A, Horn M. 2005. Chlamydien als Symbionten frei lebender Amöben. BioSpektrum 4: 393-394.
  4. Collingro A, Horn, M, Wagner M. 2004. Die Evolution der Chlamydien - Einblicke in die Entwicklungsgeschichte bedeutender bakterieller Krankheitserreger aus einer genomischen Perspektive. GenomXPress 2: 13-14.
  5. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M. 2003. Microbial diversity of sponges. In Marine Molecular Biotechnology., pp. 59-88. (Müller WEG, ed.). Springer-Verlag, Berlin Heidelberg.
  6. Hu J, Limaye AP, Fritsche TR, Horn M, Juretschko S, Gautom R. 2001. Direct detection of Legionellae in respiratory tract specimens using fluorescence in situ hybridization. In Legionella., pp. 221-224. (Marre R, ed.). Amer. Soc. Microbiol. Press, Washington, D.C..
  7. Horn M, Wagner M. 2001. Dasein im Verborgenem. Bakterien, die in Acanthamöben leben. Biologie in unserer Zeit 31: 160-168.
  8. Schleifer KH, Horn M. 2000. Mikrobielle Vielfalt. Biologen heute 452: 1-5.
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