Molecular signatures for the pvc clade (planctomycetes, verrucomicrobia, chlamydiae, and lentisphaerae) of bacteria provide insights into their evolutionary relationships

Frontiers in Microbiology

Volumn 3, Issue SEP, 2012, Pages

  Gupta, Radhey S ^a   Bhandari, Vaibhav ^a   Naushad, Hafiz Sohail ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Chlamydia; Conserved signature indels; Lentisphaerae; Phylogenetic trees; Planctomycetes; PVC superphylum; Signature proteins; Verrucomicrobia

Indexed keywords

EID: 84875834208     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00327     Document Type: Article

References (98)

1. Agren, J., Sundstrom, A., Hafstrom, T., and Segerman, B. (2012). Gegenees: fragmented alignment of multiple genomes for determining phylogenomic distances and genetic signatures unique for specified target groups. PLoS ONE 7, e39107. doi:10.1371/journal.pone.0039107
2. Angiuoli, S. V., and Salzberg, S. L. (2011). Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics 27, 334-342.
3. Azuma, Y., Hirakawa, H., Yamashita, A., Cai, Y., Rahman, M. A., Suzuki, H., Mitaku, S., Toh, H., Goto, S., Murakami, T., Sugi, K., Hayashi, H., Fukushi, H., Hattori, M., Kuhara, S., and Shirai, M. (2006). Genome sequence of the cat pathogen, Chlamydophila felis. DNA Res. 13, 15-23.
4. Bernander, R., and Ettema, T. J. (2010). FtsZ-less cell division in archaea and bacteria. Curr. Opin. Microbiol. 13, 747-752.
5. Bertelli, C., Collyn, F., Croxatto, A., Ruckert, C., Polkinghorne, A., Kebbi-Beghdadi, C., Goesmann, A., Vaughan, L., and Greub, G. (2010). The Waddlia genome: a window into chlamydial biology. PLoS ONE 5, e10890. doi:10.1371/journal.pone.0010890
6. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17,540-552.
7. Cho, J. C., Vergin, K. L., Morris, R. M., and Giovannoni, S. J. (2004). Lentisphaera araneosa gen. nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae. Environ. Microbiol. 6, 611-621.
8. Chouari, R., Le Paslier, D., Dauga, C., Daegelen, P., Weissenbach, J., and Sghir, A. (2005). Novel major bacterial candidate division within a municipal anaerobic sludge digester. Appl. Environ. Microbiol. 71, 2145-2153.
9. Ciccarelli, F. D., Doerks, T., von Mering, C., Creevey, C. J., Snel, B., and Bork, P. (2006). Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287.
10. Clum, A., Tindall, B. J., Sikorski, J., Ivanova, N., Mavrommatis, K., Lucas, S., Glavina, T., Del, R., Nolan, M., Chen, F., Tice, H., Pitluck, S., Cheng, J. F., Chertkov, O., Brettin, T., Han, C., Detter, J. C., Kuske, C., Bruce, D., Goodwin, L., Ovchinikova, G., Pati, A., Mikhailova, N., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y. J., Jeffries, C. D., Chain, P., Rohde, M., Goker, M., Bristow, J., Eisen, J. A., Markowitz, V., Hugenholtz, P., Kyrpides, N. C., Klenk, H. P., and Lapidus, A. (2009). Complete genome sequence of Pirellula staleyi type strain (ATCC 27377). Stand. Genomic. Sci. 1, 308-316.
11. Collingro,A., Tischler, P.,Weinmaier, T., Penz, T., Heinz, E., Brunham, R. C., Read, T. D., Bavoil, P. M., Sachse, K., Kahane, S., Friedman, M. G., Rattei, T.,Myers,G.S.,and Horn,M. (2011). Unity in variety-the pan-genome of the Chlamydiae. Mol. Biol. Evol. 28, 3253-3270.
12. Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B., and AcunaGonzalez, J. (2003). N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606-608.
13. Devol, A. H. (2003). Nitrogen cycle: solution to a marine mystery. Nature 422, 575-576.
14. Dutilh, B. E., Snel, B., Ettema, T. J., and Huynen, M. A. (2008). Signature genes as a phylogenomic tool. Mol. Biol. Evol. 25, 1659-1667.
15. Fieseler, L., Horn, M., Wagner, M., and Hentschel, U. (2004). Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl. Environ. Microbiol. 70, 3724-3732.
16. Fox, A., Rogers, J. C., Gilbart, J., Morgan, S., Davis, C. H., Knight, S., and Wyrick, P. B. (1990). Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry. Infect. Immun. 58, 835-837.
17. Fuchsman, C. A., Staley, J. T., Oakley, B. B., Kirkpatrick, J. B., and Murray, J. W. (2012). Free-living and aggregate-associated planctomycetes in the Black Sea. FEMS Microbiol. Ecol. 80, 402-416.
18. Fuerst,J.A. (1995). The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiology 141(Pt 7), 1493-1506.
19. Fuerst, J. A., and Sagulenko, E. (2011). Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat. Rev. Microbiol. 9, 403-413.
20. Fuerst, J. A., and Webb, R. I. (1991). Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc. Natl. Acad. Sci. U.S.A. 88, 8184-8188.
21. Fukunaga, Y., Kurahashi, M., Sakiyama, Y., Ohuchi, M., Yokota, A., and Harayama, S. (2009). Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum Planctomycetes. J. Gen. Appl. Microbiol. 55, 267-275.
22. Gao, B., and Gupta, R. S. (2012). Microbial systematics in the postgenomics era. Antonie Van Leeuwenhoek 101, 45-54.
23. Gao, B., Mohan, R., and Gupta, R. S. (2009). Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int. J. Syst. Evol. Microbiol. 59, 234-247.
24. Glockner, F. O., Kube, M., Bauer, M., Teeling, H., Lombardot, T., Ludwig, W., Gade, D., Beck, A., Borzym, K., Heitmann, K., Rabus, R., Schlesner, H., Amann, R., and Reinhardt, R. (2003). Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl. Acad. Sci. U.S.A. 100, 8298-8303.
25. Glockner, J., Kube, M., Shrestha, P. M., Weber, M., Glockner, F. O., Reinhardt, R., and Liesack, W. (2010). Phylogenetic diversity and metagenomics of candidate division OP3. Environ. Microbiol. 12, 1218-1229.
26. Goker, M., Cleland, D., Saunders, E., Lapidus, A., Nolan, M., Lucas, S., Hammon,N.,Deshpande,S.,Cheng, J. F., Tapia, R., Han, C., Goodwin, L., Pitluck, S., Liolios, K., Pagani, I., Ivanova, N., Mavromatis, K., Pati,A., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y. J., Jeffries, C. D., Detter, J. C., Beck, B., Woyke, T., Bristow, J., Eisen, J. A., Markowitz, V., Hugenholtz, P., Kyrpides, N. C., and Klenk, H. P. (2011). Complete genome sequence of Isosphaera pallida type strain (IS1B). Stand. Genomic. Sci. 4, 63-71.
27. Griffiths, E., and Gupta, R. S. (2006). Lateral transfers of serine hydroxymethyltransferase (glyA) and UDP-N-acetylglucosamine enolpyruvyl transferase (murA) genes from free-living Actinobacteria to the parasitic chlamydiae. J. Mol. Evol. 63, 283-296.
28. Griffiths, E., and Gupta, R. S. (2007). Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae. Microbiology 153, 2648-2654.
29. Griffiths, E., Petrich, A. K., and Gupta, R. S. (2005). Conserved indels in essential proteins that are distinctive characteristics of chlamydiales and provide novel means for their identification. Microbiology 151, 2647-2657.
30. Griffiths, E., Ventresca, M. S., and Gupta, R. S. (2006). BLAST screening of chlamydial genomes to identify signature proteins that are unique for the chlamydiales, chlamydiaceae, Chlamydophila and Chlamydia groups of species. BMC Genomics 7, 14. doi:10.1186/14712164-7-14
31. Gupta, R. S. (1998). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria,and eukaryotes. Microbiol. Mol. Biol. Rev. 62, 1435-1491.
32. Gupta, R. S. (2010). "Applications of conserved indels for understanding microbial phylogeny,"in Molecular Phylogeny of Microorganisms, ed. A. Oren and R. T. Papke (Norfolk: Caister Academic Press), 135-150.
33. Gupta, R. S., and Bhandari, V. (2011). Phylogeny and molecular signatures for the phylum thermotogae and its subgroups. Antonie Van Leeuwenhoek 100, 1-34.
34. Gupta, R. S., and Griffiths, E. (2002). Critical issues in bacterial phylogeny. Theor. Popul. Biol. 61, 423-434.
35. Gupta, R. S., and Griffiths, E. (2006). Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol. 14, 527-535.
36. Gupta, R. S., and Mok, A. (2007). Phylogenomics and signature proteins for the alpha proteobacteria and its main groups. BMC Microbiol. 7, 106. doi:10.1186/1471-2180-7-106
37. Haukka, K., Kolmonen, E., Hyder, R., Hietala, J., Vakkilainen, K., Kairesalo, T., Haario, H., and Sivonen, K. (2006). Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb. Ecol. 51, 137-146.
38. Hedlund, B. P., Gosink, J. J., and Staley, J. T. (1996). Phylogeny of Prosthecobacter, the fusiform caulobacters: members of a recently discovered division of the bacteria. Int. J. Syst. Bacteriol. 46, 960-966.
39. Hedlund,B. P.,Gosink,J. J.,and Staley,J. T. (1997).Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prosthecobacter. Antonie Van Leeuwenhoek 72, 29-38.
40. 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.
41. Hou, S., Makarova, K. S., Saw, J. H., Senin, P., Ly, B. V., Zhou, Z., Ren, Y., Wang, J., Galperin, M. Y., Omelchenko, M.V.,Wolf,Y. I.,Yutin, N.,Koonin,E.V.,Stott,M. B.,Mountain, B. W., Crowe, M. A., Smirnova, A. V., Dunfield, P. F., Feng, L., Wang, L., and Alam, M. (2008). Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum verrucomicrobia. Biol. Direct 3, 26.
42. Hugenholtz, P., Pitulle, C., Hershberger, K. L., and Pace, N. R. (1998). Novel division level bacterial diversity in a Yellowstone hot spring. J. Bacteriol. 180, 366-376.
43. Janssen, P. H., Schuhmann, A., Morschel, E., and Rainey, F. A. (1997). Novel anaerobic ultramicrobacteria belonging to the Verrucomicrobiales lineage of bacterial descent isolated by dilution culture from anoxic rice paddy soil. Appl. Environ. Microbiol. 63, 1382-1388.
44. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G., and Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23, 403-405.
45. Jenkins, C., and Fuerst, J. A. (2001). Phylogenetic analysis of evolutionary relationships of the planctomycete division of the domain bacteria based on amino acid sequences of elongation factor Tu. J. Mol. Evol. 52, 405-418.
46. Kant, R., van Passel, M. W., Palva, A., Lucas, S., Lapidus, A., Glavina, D. R., Dalin, E., Tice, H., Bruce, D., Goodwin, L., Pitluck, S., Larimer, F. W., Land, M. L., Hauser, L., Sangwan, P., de Vos, W. M., Janssen, P. H., and Smidt, H. (2011a). Genome sequence of Chthoniobacter flavus Ellin428, an aerobic heterotrophic soil bacterium. J. Bacteriol. 193, 2902-2903.
47. Kant, R., van Passel, M. W., Sangwan, P., Palva, A., Lucas, S., Copeland, A., Lapidus, A., Glavina, D. R., Dalin, E., Tice, H., Bruce, D., Goodwin, L., Pitluck, S., Chertkov, O., Larimer, F. W., Land, M. L., Hauser, L., Brettin, T. S., Detter, J. C., Han, S., de Vos, W. M., Janssen, P. H., and Smidt, H. (2011b). Genome sequence of "Pedosphaera parvula" Ellin514, an aerobic Verrucomicrobial isolate from pasture soil. J. Bacteriol. 193, 2900-2901.
48. Konig, E., Schlesner, H., and Hirsch, P. (1984). Cell wall studies on budding bacteria of the planctomycetes/pasteuria group and on a Prosthecomicrobium sp. Arch. Microbiol. 138, 200-205.
49. Labutti, K., Sikorski, J., Schneider, S., Nolan, M., Lucas, S., Glavina, D. R., Tice, H., Cheng, J. F., Goodwin, L., Pitluck, S., Liolios, K., Ivanova, N., Mavromatis, K., Mikhailova, N., Pati, A., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y. J., Jeffries, C. D., Tindall, B. J., Rohde, M., Goker, M., Woyke, T., Bristow, J., Eisen, J. A., Markowitz, V., Hugenholtz, P., Kyrpides, N. C., Klenk, H. P., and Lapidus, A. (2010). Complete genome sequence of Planctomyces limnophilus type strain (Mu 290). Stand. Genomic. Sci. 3, 47-56.
50. Lee, K. C., Webb, R. I., Janssen, P. H., Sangwan, P., Romeo, T., Staley, J. T., and Fuerst, J. A. (2009). Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol. 9, 5. doi:10.1186/1471-2180-9-5
51. Liesack,W.,Konig,H.,Schlesner,H.,and Hirsch,P. (1986). Chemical compostion of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomycetes group. Arch. Microbiol. 145, 361-366.
52. Lindsay, M. R., Webb, R. I., and Fuerst, J. A. (1997). Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiology 143, 739-748.
53. Lonhienne, T. G., Sagulenko, E., Webb, R. I., Lee, K. C., Franke, J., Devos, D. P., Nouwens, A., Carroll, B. J., andFuerst,J.A. (2010). Endocytosislike protein uptake in the bacterium Gemmata obscuriglobus. Proc. Natl. Acad. Sci. U.S.A. 107, 12883-12888.
54. Martiny, A. C., Albrechtsen, H. J., Arvin, E., and Molin, S. (2005). Identification of bacteria in biofilm and bulk water samples from a nonchlorinated model drinking water distribution system: detection of a large nitrite-oxidizing population associated with Nitrospira spp. Appl. Environ. Microbiol. 71, 8611-8617.
55. Matsuno, K., and Sonenshein, A. L. (1999). Role of SpoVG in asymmetric septation in Bacillus subtilis. J. Bacteriol. 181, 3392-3401.
56. Mavromatis, K., Abt, B., Brambilla, E., Lapidus, A., Copeland, A., Deshpande, S., Nolan, M., Lucas, S., Tice, H., Cheng, J. F., Han, C., Detter, J. C., Woyke, T., Goodwin, L., Pitluck, S., Held, B., Brettin, T., Tapia, R., Ivanova, N., Mikhailova, N., Pati, A., Liolios, K., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y. J., Jeffries, C. D., Rohde, M., Goker, M., Bristow, J., Eisen, J. A., Markowitz, V., Hugenholtz, P., Klenk, H. P., and Kyrpides, N. C. (2010). Complete genome sequence of Coraliomargarita akajimensis type strain (04OKA010-24). Stand. Genomic. Sci. 2, 290-299.
57. McInerney, J. O., Martin, W. F., Koonin, E. V., Allen, J. F., Galperin, M. Y., Lane, N., Archibald, J. M., and Embley, T. M. (2011). Planctomycetes and eukaryotes: a case of analogy not homology. Bioessays 33, 810-817.
58. Mojica, S., Huot, C. H., Daugherty, S., Read, T. D., Kim, T., Kaltenboeck, B., Bavoil, P., and Myers, G. S. (2011). Genome sequence of the obligate intracellular animal pathogen Chlamydia pecorum E58. J. Bacteriol. 193, 3690.
59. Naushad, H. S., and Gupta, R. S. (2012). Molecular signatures (conserved indels) in protein sequences that are specific for the order pasteurellales and distinguish two of its main clades. Antonie Van Leeuwenhoek 101, 105-124.
60. NCBI protein database. (2012). Available at: http://www.ncbi.nlm.nih.gov/protein. [accessed May 18, 2012].
61. NCBI Taxonomy. (2012). Available at: http://www.ncbi.nlm.nih.gov/taxonomy. [accessed May 18, 2012].
62. Pearson, A., Budin, M., and Brocks, J. J. (2003). Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc. Natl. Acad. Sci. U.S.A. 100, 15352-15357.
63. Petroni, G., Spring, S., Schleifer, K. H., Verni, F., and Rosati, G. (2000). Defensive extrusive ectosymbionts of Euplotidium (Ciliophora) that contain microtubule-like structures are bacteria related toVerrucomicrobia. Proc. Natl. Acad. Sci. U.S.A. 97, 1813-1817.
64. Pilhofer, M., Rappl, K., Eckl, C., Bauer, A. P., Ludwig, W., Schleifer, K. H., and Petroni, G. (2008). Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J. Bacteriol. 190, 3192-3202.
65. Pol, A., Heijmans, K., Harhangi, H. R., Tedesco, D., Jetten, M. S., and Op den Camp, H. J. (2007). Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450, 874-878.
66. Read, T. D., Brunham, R. C., Shen, C., Gill, S. R., Heidelberg, J. F., White, O., Hickey, E. K., Peterson, J., Utterback, T., Berry, K., Bass, S., Linher, K., Weidman, J., Khouri, H., Craven, B., Bowman, C., Dodson, R., Gwinn, M., Nelson, W., DeBoy, R., Kolonay, J.,McClarty,G.,Salzberg,S. L.,Eisen, J., and Fraser, C. M. (2000). Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28, 1397-1406.
67. Read, T. D., Myers, G. S., Brunham, R. C., Nelson, W. C., Paulsen, I. T., Heidelberg, J., Holtzapple, E., Khouri, H., Federova, N. B., Carty, H. A., Umayam, L. A., Haft, D. H., Peterson, J., Beanan, M. J., White, O., Salzberg, S. L., Hsia, R. C., McClarty, G., Rank, R. G., Bavoil, P. M., and Fraser, C. M. (2003). Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the chlamydiaceae. Nucleic Acids Res. 31, 2134-2147.
68. Rokas, A., Williams, B. L., King, N., and Carroll, S. B. (2003). Genomescale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798-804.
69. Sachse, K., Vretou, E., Livingstone, M., Borel, N., Pospischil, A., and Longbottom, D. (2009). Recent developments in the laboratory diagnosis of chlamydial infections.Vet. Microbiol. 135, 2-21.
70. Sahl, J. W., Matalka, M. N., and Rasko, D. A. (2012). Phylomark, a tool to identify conserved phylogenetic markers from whole-genome alignments. Appl. Environ. Microbiol. 78, 4884-4892.
71. Sangwan, P., Kovac, S., Davis, K. E., Sait, M., and Janssen, P. H. (2005). Detection and cultivation of soil verrucomicrobia. Appl. Environ. Microbiol 71, 8402-8410.
72. Santarella-Mellwig, R., Franke, J., Jaedicke, A., Gorjanacz, M., Bauer, U., Budd, A., Mattaj, I. W., and Devos, D. P. (2010). The compartmentalized bacteria of the planctomycetes-verrucomicrobiachlamydiae superphylum have membrane coat-like proteins. PLoS Biol. 8, e1000281. doi:10.1371/journal.pbio.1000281
73. Schofl, G., Voigt, A., Litsche, K., Sachse, K.,and Saluz,H. P. (2011). Complete genome sequences of four mammalian isolates of Chlamydophila psittaci. J. Bacteriol. 193, 4258.
74. Schulthess, B., Meier, S., Homerova, D., Goerke, C., Wolz, C., Kormanec, J., Berger-Bachi, B., and Bischoff, M. (2009). Functional characterization of the sigmaB-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob. Agents Chemother. 53, 1832-1839.
75. Shinzato, N., Muramatsu, M., Matsui, T., and Watanabe, Y. (2005). Molecular phylogenetic diversity of the bacterial community in the gut of the termite Coptotermes formosanus. Biosci. Biotechnol. Biochem. 69, 1145-1155.
76. Siegl, A., Kamke, J., Hochmuth, T., Piel, J., Richter, M., Liang, C., Dandekar, T., and Hentschel, U. (2011). Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME. J. 5, 61-70.
77. Staley, J. T., Fuerst, J. A., Giovannoni, S., and Schlesner, H. (1992). "The order Planctomycetales and the genera Planctomyces, Pirellula, Gemmata and Isosphaera," in The Prokaryotes, eds A. Balows, H. G. Truper, M. Dworkin, W. Harder, and K. H. Schleifer (New York: SpringerVerlag), 3710-3731.
78. Strous, M., Fuerst, J. A., Kramer, E. H., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T., Webb, R., Kuenen, J. G., and Jetten, M. S. (1999).Missinglithotrophidentified as new planctomycete. Nature 400, 446-449.
79. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M. W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., Barbe, V., Fonknechten, N., Vallenet, D., Segurens, B., Schenowitz-Truong, C., Medigue, C., Collingro, A., Snel, B., Dutilh, B. E., Op den Camp, H. J., van der, D. C., Cirpus, I., van de Pas-Schoonen, K. T., Harhangi, H. R., van Niftrik, L., Schmid, M., Keltjens, J., vand, V, Kartal, B., Meier, H., Frishman, D., Huynen, M. A., Mewes, H. W., Weissenbach, J., Jetten,M. S.,Wagner,M.,and Le Paslier, D. (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790-794.
80. Thomson, N. R., Holden, M. T., Carder, C., Lennard, N., Lockey, S. J., Marsh, P., Skipp, P., OConnor, C. D., Goodhead, I., Norbertzcak, H., Harris, B., Ormond, D., Rance, R., Quail, M. A., Parkhill, J., Stephens, R. S., and Clarke, I. N. (2008). Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18, 161-171.
81. Thomson, N. R., Yeats, C., Bell, K., Holden, M. T., Bentley, S. D., Livingstone, M., Cerdeno-Tarraga, A. M., Harris, B., Doggett, J., Ormond, D., Mungall, K., Clarke, K., Feltwell, T., Hance, Z., Sanders, M., Quail, M. A., Price, C., Barrell, B. G., Parkhill, J., and Longbottom, D. (2005). The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15, 629-640.
82. Thrash, J. C., Cho, J. C., Vergin, K. L., Morris, R. M., and Giovannoni, S. J. (2010). Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J. Bacteriol. 192, 2938-2939.
83. van de Graaf, A. A., Mulder, A., de Bruijn,P.,Jetten, M. S.,Robertson,L. A., and Kuenen, J. G. (1995). Anaerobic oxidation of ammonium is a biologically mediated process. Appl. Environ. Microbiol 61, 1246-1251.
84. van Niftrik, L., Geerts, W. J., van Donselaar, E. G., Humbel, B. M., Webb, R. I., Harhangi, H. R., Camp, H. J., Fuerst, J. A., Verkleij, A. J., Jetten, M. S., and Strous, M. (2009). Cell division ring, a new cell division protein and vertical inheritance of a bacterial organelle in anammox planctomycetes. Mol. Microbiol 73, 1009-1019.
85. van Passel, M. W., Kant, R., Palva, A., Copeland, A., Lucas, S., Lapidus, A., Glavina, D. R., Pitluck, S., Goltsman, E., Clum, A., Sun, H., Schmutz, J., Larimer, F. W., Land, M. L., Hauser, L., Kyrpides, N., Mikhailova, N., Richardson, P. P., Janssen, P. H., de Vos, W. M., and Smidt, H. (2011a). Genome sequence of the verrucomicrobium Opitutus terrae PB90-1, an abundant inhabitant of rice paddy soil ecosystems. J. Bacteriol. 193, 2367-2368.
86. van Passel, M. W., Kant, R., Palva, A., Lucas, S., Copeland, A., Lapidus, A., Glavina, D. R., Dalin, E., Tice, H., Bruce, D., Goodwin, L., Pitluck, S., Davenport, K. W., Sims, D., Brettin, T. S., Detter, J. C., Han, S., Larimer, F. W., Land, M. L., Hauser, L., Kyrpides, N., Ovchinnikova, G., Richardson, P. P., de Vos, W. M., Smidt, H., and Zoetendal, E. G. (2011b). Genome sequence of Victivallis vadensis ATCC BAA-548, an anaerobic bacterium from the phylum Lentisphaerae, isolated from the human gastrointestinal tract. J. Bacteriol. 193, 2373-2374.
87. Vandekerckhove, T. T., Coomans, A., Cornelis, K., Baert, P., and Gillis, M. (2002). Use of the Verrucomicrobiaspecific probe EUB338-III and fluorescent in situ hybridization for detection of "Candidatus Xiphinematobacter" cells in nematode hosts. Appl. Environ. Microbiol. 68, 3121-3125.
88. Wagner, M., and Horn, M. (2006). The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17, 241-249.
89. Wang, M., Ahrne, S., Jeppsson, B., and Molin, G. (2005). Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol. Ecol. 54, 219-231.
90. Ward, N., Staley, J. T., Fuerst, J. A., Giovannoni, S., Schlesner, H., and Stackebrandt, E. (2006). The Order Plancktomycetales, including the genera Planctomycetes, Pirellula, Gemmata, Isosphaera and the Candidatus genera Brocadia, Kuenenia and Scalindua," in The Prokaryotes, eds M. Dworkin, S. Falkow, K. H. Schleifer, and E. Stackebrandt (New York: Springer), 757-793.
91. Ward, N. L. (2011). "Class I. Planctomycetia class.nov," in Bergeys Manual of Systematic Bacteriology, eds N. R. Krieg, J. T. Staley, D. R. Brown, B. P. Hedlund, B. J. Paster, N. L. Ward, W. Ludwig, and W. B. Whitman (New York: Springer-Verlag), 879.
92. Ward,N. L.,Rainey,F. A.,Hedlund,B. P., Staley, J. T., Ludwig, W., and Stackebrandt, E. (2000). Comparative phylogenetic analyses of members of the order Planctomycetales and the divisionVerrucomicrobia:23S rRNA gene sequence analysis supports the 16S rRNA gene sequence-derived phylogeny. Int. J. Syst. Evol. Microbiol. 50(Pt 6), 1965-1972.
93. Weisburg, W. G., Hatch, T. P., and Woese, C. R. (1986). Eubacterial origin of chlamydiae. J. Bacteriol. 167, 570-574.
94. Wertz, J. T., Kim, E., Breznak, J. A., Schmidt, T. M., and Rodrigues, J. L. (2012). Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl. Environ. Microbiol. 78, 1544-1555.
95. Woese, C. R. (1987). Bacterial evolution.Microbiol. Rev. 51, 221-271.
96. Wu,M.,and Eisen,J.A. (2008).A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9, R151.
97. Yoon, J., Matsuo,Y., Adachi, K., Nozawa, M., Matsuda, S., Kasai, H., and Yokota, A. (2008). Description of Persicirhabdus sediminis gen. nov., sp. nov., Roseibacillus ishigakijimensis gen. nov., sp. nov., Roseibacillus ponti sp. nov.,Roseibacillus persicicus sp. nov., Luteolibacter pohnpeiensis gen. nov., sp. nov. and Luteolibacter algae sp. nov.,six marine members of the phylum "Verrucomicrobia," and emended descriptions of the class Verrucomicrobiae, the order Verrucomicrobiales and the family Verrucomicrobiaceae. Int. J. Syst. Evol. Microbiol. 58, 998-1007.
98. Zoetendal, E. G., Plugge, C. M., Akkermans, A. D., and de Vos, W. M. (2003).Victivallis vadensis gen. nov., sp. nov., a sugar-fermenting anaerobe from human faeces. Int. J. Syst. Evol. Microbiol. 53, 211-215.