A Rickettsiales symbiont of amoebae with ancient features

Environmental Microbiology

Volumn 18, Issue 8, 2016, Pages 2326-2342

  Schulz, Frederik ^a   Martijn, Joran ^b   Wascher, Florian ^a   Lagkouvardos, Ilias ^a   Kostanjšek, Rok ^c   Ettema, Thijs J G ^b   Horn, Matthias ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAMOEBA; ALPHAPROTEOBACTERIA; BACTERIAL GENOME; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS;

ACANTHAMOEBA; ALPHAPROTEOBACTERIA; GENOME, BACTERIAL; PHYLOGENY; SYMBIOSIS;

EID: 85027954611     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12881     Document Type: Article

References (118)

1. Abby, S.S., and Rocha, E.P.C. (2012) The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet 8: e1002983.
2. Aistleitner, K., Heinz, C., Hörmann, A., Heinz, E., Montanaro, J., Schulz, F., et al. (2013) Identification and characterization of a novel porin family highlights a major difference in the outer membrane of chlamydial symbionts and pathogens. PLoS ONE 8: e55010.
3. Al-Quadan, T., Price, C.T., and Abu Kwaik, Y. (2012) Exploitation of evolutionarily conserved amoeba and mammalian processes by Legionella. Trends Microbiol 20: 299–306.
4. Altschul, S., Gish, W., and Miller, W. (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
5. Amann, R., and Binder, B. (1990) Combination of 16S rRNAtargeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919–1925.
6. Andersson, S.G.E. (1998) Bioenergetics of the obligate intracellular parasite Rickettsia prowazekii. Biochim Biophys Acta 1365: 105–111.
7. Andersson, S.G.E., Zomorodipour, A., Andersson, J.O., Sicheritz-Pontén, T., Alsmark, U.C.M., Podowski, R.M., et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133–140.
8. Angot, A., Vergunst, A., Genin, S., and Peeters, N. (2007) Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog 3: e3.
9. Azad, F., and Traub, R. (1985) Transmission of murine typhus rickettsiae by Xenopsylla cheopis, with notes on experimental infection and effects of temperature. Am J Trop Med Hyg 34: 555–563.
10. Backert, S., and Meyer, T.F. (2006) Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9: 207–217.
11. Badger, J.H., and Olsen, G.J. (1999) CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol 16: 512–524.
12. Bateman, A. (2002) The Pfam protein families database. Nucleic Acids Res 30: 276–280.
13. Besemer, J., Lomsadze, A., and Borodovsky, M. (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29: 2607–2618.
14. Beyer, A.R., Truchan, H.K., May, L.J., Walker, N.J., Borjesson, D.L., and Carlyon, J.A. (2014) The Anaplasma phagocytophilum effector AmpA hijacks host cell SUMOylation. Cell Microbiol 17: 504–519.
15. Bi, D., Liu, L., Tai, C., Deng, Z., Rajakumar, K., and Ou, H.-Y. (2013) SecReT4: a web-based bacterial type IV secretion system resource. Nucleic Acids Res 41: D660–D665.
16. Blanc, G., Ogata, H., Robert, C., Audic, S., Claverie, J.-M., and Raoult, D. (2007a) Lateral gene transfer between obligate intracellular bacteria: evidence from the Rickettsia massiliae genome. Genome Res 17: 1657–1664.
17. Blanc, G., Ogata, H., Robert, C., Audic, S., Suhre, K., Vestris, G., et al. (2007b) Reductive genome evolution from the mother of Rickettsia. PLoS Genet 3: e14.
18. Boscaro, V., Petroni, G., Ristori, A., Verni, F., and Vannini, C. (2013a) ‘Candidatus Defluviella procrastinata’ and ‘Candidatus Cyrtobacter zanobii’, two novel ciliate endosymbionts belonging to the ‘Midichloria Clade’. Microb Ecol 65: 302–310.
19. Boscaro, V., Schrallhammer, M., Benken, K.A., Krenek, S., Szokoli, F., Berendonk, T.U., et al. (2013b) Rediscovering the genus Lyticum, multiflagellated symbionts of the order Rickettsiales. Sci Rep 3: 3305.
20. Boussau, B., Karlberg, E.O., Frank, A.C., Legault, B.-A., and Andersson, S.G.E. (2004) Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc Natl Acad Sci USA 101: 9722–9727.
21. Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972–1973.
22. Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C.A., et al. (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 42: D459–D471.
23. Cho, N.-H., Kim, H.-R., Lee, J.-H., Kim, S.-Y., Kim, J., Cha, S., et al. (2007) The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host-cell interaction genes. Proc Natl Acad Sci USA 104: 7981–7986.
24. Collingro, A., Walochnik, J., Baranyi, C., Michel, R., Wagner, M., Horn, M., and Aspöck, H. (2004) Chlamydial endocytobionts of free-living amoebae differentially affect the growth rate of their hosts. Eur J Protistol 40: 57–60.
25. Collingro, A., Tischler, P., Weinmaier, T., Penz, T., Heinz, E., Brunham, R.C., et al. (2011) Unity in variety – the pangenome of the Chlamydiae. Mol Biol Evol 28: 3253–3270.
26. Daims, H., Brühl, A., Amann, R., Schleifer, K.H., andWagner, M. (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434–444.
27. Daims, H., Stoecker, K., and Wagner, M. (2005) Fluorescence in situ hybridization for the detection of prokaryotes. Mol Microb Ecol 213: 239.
28. Dale, C., Wang, B., Moran, N., and Ochman, H. (2003) Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20: 1188–1194.
29. Darby, A.C., Cho, N.-H., Fuxelius, H.-H., Westberg, J., and Andersson, S.G.E. (2007) Intracellular pathogens go extreme: genome evolution in the Rickettsiales. Trends Genet 23: 511–520.
30. Daugherty, R.M., Linka, N., Audia, J.P., Urbany, C., Neuhaus, H.E., and Winkler, H.H. (2004) The nucleotide transporter of Caedibacter caryophilus exhibits an extended substrate spectrum compared to the analogous ATP/ADP translocase of Rickettsia prowazekii. J Bacteriol 186: 3262–3265.
31. Dietrich, C., Heuner, K., Brand, B., Hacker, J., and Steiner, M. (2001) Flagellum of Legionella pneumophila positively affects the early phase of infection of eukaryotic host cells. Infect Immun 69: 2116–2122.
32. Domman, D., Collingro, A., Lagkouvardos, I., Gehre, L., Weinmaier, T., Rattei, T., et al. (2014) Massive expansion of ubiquitination-related gene families within the Chlamydiae. Mol Biol Evol 31: 2890–2904.
33. Dreher-Lesnick, S.M., Ceraul, S.M., Rahman, M.S., and Azad, A.F. (2008) Genome-wide screen for temperatureregulated genes of the obligate intracellular bacterium, Rickettsia typhi. BMC Microbiol 8: 61.
34. Driscoll, T., Gillespie, J.J., Nordberg, E.K., Azad, A.F., and Sobral, B.W. (2013) Bacterial DNA sifted from the Trichoplax adhaerens (Animalia: Placozoa) genome project reveals a putative rickettsial endosymbiont. Genome Biol Evol 5: 621–645.
35. Eddy, S.R. (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195.
36. Ettema, T.J.G., and Andersson, S.G.E. (2009) The alphaproteobacteria: the Darwin finches of the bacterial world. Biol Lett 5: 429–432.
37. Ferla, M.P., Thrash, J.C., Giovannoni, S.J., and Patrick, W.M. (2013) New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability. PLoS ONE 8: e83383.
38. Ferrantini, F., Fokin, S.I., Modeo, L., Andreoli, I., Dini, F., Görtz, H.-D., et al. (2009) ‘Candidatus Cryptoprodotis polytropus,’ a novel Rickettsia-like organism in the ciliated protist Pseudomicrothorax dubius (Ciliophora, Nassophorea). J Eukaryot Microbiol 56: 119–129.
39. Foster, P.G., and Hickey, D.A. (1999) Compositional bias may affect both DNA-based and protein-based phylogenetic reconstructions. J Mol Evol 48: 284–290.
40. Frank, A.C., Alsmark, C.M., Thollesson, M., and Andersson, S.G.E. (2005) Functional divergence and horizontal transfer of type IV secretion systems. Mol Biol Evol 22: 1325–1336.
41. Fritsche, T.R., Horn, M., Seyedirashti, S., Gautom, R.K., Schleifer, K.H., and Wagner, M. (1999) In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl Environ Microbiol 65: 206–212.
42. Gaspar, A.H., and Machner, M.P. (2014) VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc Natl Acad Sci USA 111: 4560–4565.
43. Georgiades, K., Madoui, M.-A., Le, P., Robert, C., and Raoult, D. (2011a) Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PLoS ONE 6: e24857.
44. Georgiades, K., Merhej, V., El Karkouri, K., Raoult, D., and Pontarotti, P. (2011b) Gene gain and loss events in Rickettsia and Orientia species. Biol Direct 6: 6.
45. Gillespie, J.J., Brayton, K.A., Williams, K.P., Diaz, M.A.Q., Brown, W.C., Azad, A.F., and Sobral, B.W. (2010) Phylogenomics reveals a diverse Rickettsiales type IV secretion system. Infect Immun 78: 1809–1823.
46. Gillespie, J.J., Nordberg, E., Azad, A.F., and Sobral, B.W. (2012a) Phylogeny and Comparative Genomics: The Shifting Landscape in the Genomics Era. In Intracellular Pathogens II: Rickettsiales. Azad, A.F., and Palmer, G.H. (eds.). American Society of Microbiology, pp. 84–141.
47. Gillespie, J.J., Joardar, V., Williams, K.P., Driscoll, T., Hostetler, J.B., Nordberg, E., et al. (2012b) A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. J Bacteriol 194: 376–394.
48. Gillespie, J.J., Kaur, S.J., Rahman, M.S., Rennoll-Bankert, K., Sears, K.T., Beier-Sexton, M., and Azad, A.F. (2014) Secretome of obligate intracellular Rickettsia. FEMS Microbiol Rev 39: 47–80.
49. Gray, M.W. (1998) Rickettsia, typhus and the mitochondrial connection. Nature 396: 109–110.
50. Gray, M.W. (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4: a011403.
51. Griffiths-Jones, S., Moxon, S., Marshall, M., Khanna, A., Eddy, S.R., and Bateman, A. (2005) Rfam: annotating noncoding RNAs in complete genomes. Nucleic Acids Res 33: D121–D124.
52. Guy, L., Kultima, J.R., and Andersson, S.G.E. (2010) genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26: 2334–2335.
53. Guy, L., Saw, J.H., and Ettema, T.J.G. (2014) The archaeal legacy of Eukaryotes: a phylogenomic perspective. Cold Spring Harb Perspect Biol 6: a016022.
54. Haferkamp, I., Schmitz-Esser, S., Wagner, M., Neigel, N., Horn, M., and Neuhaus, H.E. (2006) Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol Microbiol 60: 1534–1545.
55. Horn, M. (2008) Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol 62: 113–131.
56. Horn, M., Fritsche, T.R., Gautom, R.K., Schleifer, K.-H., and Wagner, M. (1999) Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol 1: 357–367.
57. Huson, D.H., Mitra, S., Ruscheweyh, H.-J., Weber, N., and Schuster, S.C. (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21: 1552–1560.
58. Hyatt, D., Chen, G.-L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
59. Ishida, K., Sekizuka, T., Hayashida, K., Matsuo, J., Takeuchi, F., Kuroda, M., et al. (2014) Amoebal endosymbiont Neochlamydia genome sequence illuminates the bacterial role in the defense of the host amoebae against Legionella pneumophila. PLoS ONE 9: e95166.
60. Jehl, M.-A., Arnold, R., and Rattei, T. (2011) Effective – a database of predicted secreted bacterial proteins. Nucleic Acids Res 39: D591–D595.
61. Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30: 1236–1240.
62. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42: D199–D205.
63. Katoh, K., and Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
64. Kawafune, K., Hongoh, Y., Hamaji, T., and Nozaki, H. (2012) Molecular identification of rickettsial endosymbionts in the non-phagotrophic volvocalean green algae. PLoS ONE 7: e31749.
65. Kelley, D.R., Liu, B., Delcher, A.L., Pop, M., and Salzberg, S.L. (2012) Gene prediction with Glimmer for metagenomic sequences augmented by classification and clustering. Nucleic Acids Res 40: e9.
66. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639– 1645.
67. Ku, B., Lee, K.-H., Park, W.S., Yang, C.-S., Ge, J., Lee, S.-G., et al. (2012) VipD of Legionella pneumophila targets activated Rab5 and Rab22 to interfere with endosomal trafficking in macrophages. PLoS Pathog 8: e1003082.
68. Kurtz, S., Phillippy, A., Delcher, A.L., Smoot, M., Shumway, M., Antonescu, C., and Salzberg, S.L. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.
69. Kück, P., and Meusemann, K. (2010) FASconCAT: convenient handling of data matrices. Mol Phylogenet Evol 56: 1115–1118.
70. Lagesen, K., Hallin, P., Rødland, E.A., Staerfeldt, H.-H., Rognes, T., and Ussery, D.W. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100–3108.
71. Lagkouvardos, I., Weinmaier, T., Lauro, F.M., Cavicchioli, R., Rattei, T., and Horn, M. (2013) Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae. The ISME journal 8: 115–125.
72. Lartillot, N., Rodrigue, N., Stubbs, D., and Richer, J. (2013) PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol 62: 611–615.
73. Le, P.T., Ramulu, H.G., Guijarro, L., Paganini, J., Gouret, P., Chabrol, O., et al. (2012) An automated approach for the identification of horizontal gene transfers from complete genomes reveals the rhizome of Rickettsiales. BMC Evol Biol 12: 243.
74. Le, S.Q., and Gascuel, O. (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307–1320.
75. Li, L., Stoeckert, C.J., and Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.
76. Li, P.L., Everhart, D.M., and Farrand, S.K. (1998) Genetic and sequence analysis of the pTiC58 trb locus, encoding a mating-pair formation system related to members of the type IV secretion family. J Bacteriol 180: 6164–6172.
77. Linka, N., Hurka, H., Lang, B.F., Burger, G., Winkler, H.H., Stamme, C., et al. (2003) Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306: 27–35.
78. Liu, H., Bao, W., Lin, M., Niu, H., and Rikihisa, Y. (2012) Ehrlichia type IV secretion effector ECH0825 is translocated to mitochondria and curbs ROS and apoptosis by upregulating host MnSOD. Cell Microbiol 14: 1037–1050.
79. Lockwood, S., Voth, D.E., Brayton, K.A., Beare, P.A., Brown, W.C., Heinzen, R.A., and Broschat, S.L. (2011) Identification of Anaplasma marginale type IV secretion system effector proteins. PLoS ONE 6: e27724.
80. Lowe, T.M., and Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964.
81. McCutcheon, J.P., and Moran, N.A. (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13–26.
82. McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Lošo, T., Douglas, A.E., et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110: 3229–3236.
83. Mariconti, M., Epis, S., Sacchi, L., Biggiogera, M., Sassera, D., Genchi, M., et al. (2012) A study on the presence of flagella in the order Rickettsiales: the case of ‘Candidatus Midichloria mitochondrii’. Microbiology 158: 1677–1683.
84. Mavromatis, K., Doyle, C.K., Lykidis, A., Ivanova, N., Francino, M.P., Chain, P., et al. (2006) The genome of the obligately intracellular bacterium Ehrlichia canis reveals themes of complex membrane structure and immune evasion strategies. J Bacteriol 188: 4015–4023.
85. Montagna, M., Sassera, D., Epis, S., Bazzocchi, C., Vannini, C., Lo, N., et al. (2013) ‘Candidatus Midichloriaceae’ fam. nov. (Rickettsiales), an ecologically widespread clade of intracellular alphaproteobacteria. Appl Environ Microbiol 79: 3241–3248.
86. NCBI Resource Coordinators (2014) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 42: D7–D17.
87. Nurk, S., Bankevich, A., Antipov, D., Gurevich, A.A., Korobeynikov, A., Lapidus, A., et al. (2013) Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20: 714–737.
88. Ogata, H., La Scola, B., Audic, S., Renesto, P., Blanc, G., Robert, C., et al. (2006) Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet 2: e76.
89. Pan, X., Lührmann, A., Satoh, A., Laskowski-Arce, M.A., and Roy, C.R. (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320: 1651–1654.
90. Pilhofer, M., Aistleitner, K., Ladinsky, M.S., König, L., Horn, M., and Jensen, G.J. (2014) Architecture and host interface of environmental chlamydiae revealed by electron cryotomography. Environ Microbiol 16: 417–429.
91. Powell, S., Forslund, K., Szklarczyk, D., Trachana, K., Roth, A., Huerta-Cepas, J., et al. (2014) eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res 42: D231–D239.
92. Price, C.T.D., Al-Quadan, T., Santic, M., Rosenshine, I., and Kwaik, Y.A. (2011) Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science 334: 1553–1557.
93. Renvoisé, A., Merhej, V., Georgiades, K., and Raoult, D. (2011) Intracellular Rickettsiales: insights into manipulators of eukaryotic cells. Trends Mol Med 17: 573–583.
94. Rodríguez-Ezpeleta, N., and Embley, T.M. (2012) The SAR11 group of alpha-proteobacteria is not related to the origin of mitochondria. PLoS ONE 7: e30520.
95. Rolando, M., and Buchrieser, C. (2014) Legionella pneumophila type IV effectors hijack the transcription and translation machinery of the host cell. Trends Cell Biol 24: 771–778.
96. Salichos, L., and Rokas, A. (2011) Evaluating ortholog prediction algorithms in a yeast model clade. PLoS ONE 6: e18755.
97. Santos, H.A., and Massard, C.L. (2014) The family Holosporaceae. In The Prokaryotes. Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds). Berlin, Germany: Springer, pp. 237–246.
98. Sassera, D., Beninati, T., Bandi, C., Bouman, E.A.P., Sacchi, L., Fabbi, M., and Lo, N. (2006) ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Syst Evol Microbiol 56: 2535–2540.
99. Sassera, D., Lo, N., Epis, S., and D’Auria, G. (2011) Phylogenomic evidence for the presence of a flagellum and cbb3 oxidase in the free-living mitochondrial ancestor. Mol Biol Evol 28: 3285–3296.
100. Sällström, B., and Andersson, S.G. (2005) Genome reduction in the α-Proteobacteria. Curr Opin Microbiol 8: 579–585.
101. Schmitz-Esser, S., Linka, N., Collingro, A., Beier, C.L., Neuhaus, H.E., Wagner, M., and Horn, M. (2004) ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J Bacteriol 186: 683–691.
102. Schmitz-Esser, S., Haferkamp, I., Knab, S., Penz, T., Ast, M., Kohl, C., et al. (2008a) Lawsonia intracellularis contains a gene encoding a functional rickettsia-like ATP/ADP translocase for host exploitation. J Bacteriol 190: 5746–5752.
103. Schmitz-Esser, S., Toenshoff, E.E.R., Haider, S., Heinz, E., Hoenninger, V.M., Wagner, M., et al. (2008b) Diversity of bacterial endosymbionts of environmental acanthamoeba isolates. Appl Environ Microbiol 74: 5822–5831.
104. Schmitz-Esser, S., Tischler, P., Arnold, R., Montanaro, J., Wagner, M., Rattei, T., and 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.
105. Schulz, F., Lagkouvardos, I., Wascher, F., Aistleitner, K., Kostanjšek, R., and Horn, M. (2014) Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. ISME J 8: 1634–1644.
106. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
107. UniProt Consortium (2014) Activities at the universal protein resource (UniProt). Nucleic Acids Res 42: D191–D198.
108. Vannini, C., Petroni, G., Verni, F., and Rosati, G. (2005) A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Microb Ecol 49: 434–442.
109. Vannini, C., Ferrantini, F., Schleifer, K.-H., Ludwig, W., Verni, F., and Petroni, G. (2010) Candidatus anadelfobacter veles’ and ‘Candidatus cyrtobacter comes,’ two new Rickettsiales species hosted by the protist ciliate Euplotes harpa (Ciliophora, Spirotrichea). Appl Environ Microbiol 76: 4047–4054.
110. Vannini, C., Boscaro, V., Ferrantini, F., Benken, K.A., Mironov, T.I., Schweikert, M., et al. (2014) Flagellar movement in two bacteria of the family Rickettsiaceae: a re-evaluation of motility in an evolutionary perspective. PLoS ONE 9: e87718.
111. Viklund, J., Ettema, T.J.G., and Andersson, S.G.E. (2012) Independent genome reduction and phylogenetic reclassification of the oceanic SAR11 clade. Mol Biol Evol 29: 599–615.
112. Wang, Z., and Wu, M. (2015) An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Sci Rep 5: 7949.
113. Weinert, L.A., Werren, J.H., Aebi, A., Stone, G.N., and Jiggins, F.M. (2009) Evolution and diversity of Rickettsia bacteria. BMC Biol 7: 6.
114. Werren, J.H., Baldo, L., and Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751.
115. Williams, K.P., Sobral, B.W., and Dickerman, A.W. (2007) A robust species tree for the alphaproteobacteria. J Bacteriol 189: 4578–4586.
116. Williams, K.P., Gillespie, J.J., Sobral, B.W.S., Nordberg, E.K., Snyder, E.E., Shallom, J.M., and Dickerman, A.W. (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192: 2305–2314.
117. Wu, M., and Scott, A.J. (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28: 1033–1034.
118. Zug, R., and Hammerstein, P. (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 7: e38544.