The PVC superphylum: Exceptions to the bacterial definition?

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 104, Issue 4, 2013, Pages 451-466

  Fuerst, John A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Chlamydia; Compartmentalization; Lentisphaerae; Planctomycetes; PVC superphylum; Verrucomicrobia

Indexed keywords

PEPTIDOGLYCAN;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM; BACTERIUM IDENTIFICATION; CHLAMYDIA; CYTOPLASM; CYTOSKELETON; ENDOCYTOSIS; GEMMATA; GENETIC TRANSCRIPTION; LENTISPHAERAE; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PHYLOGENOMICS; PHYLUM; PLANCTOMYCETES; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; VERRUCOMICROBIA;

BACTERIA (MICROORGANISMS); CHLAMYDIA; CHLAMYDIAE; EUKARYOTA; GEMMATA OBSCURIGLOBUS; LENTISPHAERAE; PLANCTOMYCETES; VERRUCOMICROBIA;

BACTERIA; HUMANS; VERRUCOMICROBIA;

EID: 84890558962     PISSN: 00036072     EISSN: 15729699     Source Type: Journal    
DOI: 10.1007/s10482-013-9986-1     Document Type: Article

References (99)

1. Albrecht W, Fischer A et al (1987) Verrucomicrobium spinosum, an eubacterium representing an ancient line of descent. Syst Appl Microbiol 10:57-62
2. Belzer C, de Vos WM (2012) Microbes inside - from diversity to function: the case of Akkermansia. ISME J 6(8):1449-1458
3. Bode HB, Zeggel B et al (2003) Steroid biosynthesis in prokaryotes: identification of myxobacterial steroids and cloning of the first bacterial 2,3(S)-oxidosqualene cyclase from the myxobacterium Stigmatella aurantiaca. Mol Microbiol 47(2):471-481
4. Chistoserdova L, Jenkins C et al (2004) The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol Biol Evol 21(7):1234-1241
5. Cho JC, Vergin KL et al (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(6):611-621
6. Choi A, Yang SJ et al (2013) Lentisphaera marina sp. nov., and emended description of the genus Lentisphaera. Int J Syst Evol Microbiol 63(Pt 4):1540-1544
7. Choo YJ, Lee K et al (2007) Puniceicoccus vermicola gen. nov., sp. nov., a novel marine bacterium, and description of Puniceicoccaceae fam. nov., Puniceicoccales ord. nov., Opitutaceae fam. nov., Opitutales ord. nov. and Opitutae classis nov. in the phylum Verrucomicrobia. Int J Syst Evol Microbiol 57(Pt 3):532-537
8. de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8(5):395-403
9. DeGrasse JA, DuBois KN et al (2009) Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol Cell Proteomics 8(9):2119-2130
10. Devos DP (2012) Regarding the presence of membrane coat proteins in bacteria: confusion? What confusion? BioEssays 34(1):38-39
11. Devos D, Dokudovskaya S et al (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2(12):e380
12. Dunfield PF, Yuryev A et al (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450(7171):879-882
13. Dunfield PF, Tamas I et al (2012) Electing a candidate: a speculative history of the bacterial phylum OP10. Environ Microbiol 14(12):3069-3080
14. Everard A, Belzer C et al (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110(22):9066-9071
15. Fieseler L, Horn M et al (2004) Discovery of the novel candidate phylum Poribacteria in marine sponges. Appl Environ Microbiol 70(6):3724-3732
16. Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59:299-328
17. Fuerst JA, Sagulenko E (2010) Protein uptake by bacteria: an endocytosis-like process in the planctomycete Gemmata obscuriglobus. Commun Integr Biol 3(6):572-575
18. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9(6):403-413
19. Fuerst JA, Sagulenko E (2012) Keys to eukaryality: planctomycetes and ancestral evolution of cellular complexity. Front Microbiol 3:167
20. Fuerst JA, Sagulenko E (2013) Nested bacterial boxes: nuclear and other intracellular compartments in planctomycetes. J Mol Microbiol Biotechnol 23(1-2):95-103
21. Fuerst JA, Webb RI (1991) Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 88(18):8184-8188
22. Glockner FO, Kube M et al (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100(14):8298-8303
23. Glockner J, Kube M et al (2010) Phylogenetic diversity and metagenomics of candidate division OP3. Environ Microbiol 12(5):1218-1229
24. Greub G, Raoult D (2002) Crescent bodies of Parachlamydia acanthamoeba and its life cycle within Acanthamoeba polyphaga: an electron micrograph study. Appl Environ Microbiol 68(6):3076-3084
25. Griffiths E, Gupta RS (2007) Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae. Microbiology 153(Pt 8):2648-2654
26. Gupta RS (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26
27. Gupta RS, Bhandari V et al (2012) Molecular signatures for the PVC clade (Planctomycetes, Verrucomicrobia, Chlamydiae, and Lentisphaerae) of bacteria provide insights into their evolutionary relationships. Front Microbiol 3:327
28. Hedlund BP, Gosink JJ et al (1997) Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prosthecobacter. Antonie Van Leeuwenhoek 72(1):29-38
29. Hou S, Makarova KS et al (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26
30. Hugenholtz P, Goebel BM et al (1998a) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180(18):4765-4774
31. Hugenholtz P, Pitulle C et al (1998b) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180(2):366-376
32. Jenkins C, Kedar V et al (2002) Gene discovery within the planctomycete division of the domain bacteria using sequence tags from genomic DNA libraries. Genome Biol 3(6): RESEARCH0031
33. Jenkins C, Samudrala R et al (2002) Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc Natl Acad Sci USA 99(26):17049-17054
34. Jogler C, Glockner FO et al (2011) Characterization of Planctomyces limnophilus and development of genetic tools for its manipulation establish it as a model species for the phylum Planctomycetes. Appl Environ Microbiol 77(16):5826-5829
35. Jogler C, Waldmann J et al (2012) Identification of proteins likely to be involved in morphogenesis, cell division, and signal transduction in Planctomycetes by comparative genomics. J Bacteriol 194(23):6419-6430
36. Kamneva OK, Liberles DA et al (2010) Genome-wide influence of indel substitutions on evolution of bacteria of the PVC superphylum, revealed using a novel computational method. Genome Biol Evol 2:870-886
37. Kamneva OK, Knight SJ et al (2012) Analysis of genome content evolution in PVC bacterial super-phylum: assessment of candidate genes associated with cellular organization and lifestyle. Genome Biol Evol 4(12):1375-1390
38. Khadem AF, Pol A et al (2010) Nitrogen fixation by the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV. Microbiology 156(Pt 4):1052-1059
39. König E, Schlesner H et al (1984) Cell-wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. Arch Microbiol 138(3):200-205
40. Kostanjsek R, Strus J et al (2004) Candidatus Rhabdochlamydia porcellionis, an intracellular bacterium from the hepatopancreas of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). Int J Syst Evol Microbiol 54(Pt 2):543-549
41. Kulichevskaya IS, Baulina OI et al (2009) Zavarzinella formosa gen. nov., sp. nov., a novel stalked, Gemmata-like planctomycete from a Siberian peat bog. Int J Syst Evol Microbiol 59(Pt 2):357-364
42. Lee KC, Webb RI et al (2009) Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol 9:5
43. Lienard J, Croxatto A et al (2011) Estrella lausannensis, a new star in the Chlamydiales order. Microbes Infect 13(14-15):1232-1241
44. Liesack W, Stackebrandt E (1989) Evidence for unlinked rrn operons in the planctomycete Pirellula marina. J Bacteriol 171(9):5025-5030
45. Liesack W, Konig H et al (1986) Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomyces group. Arch Microbiol 145(4):361-366
46. Limam RD, Bouchez T et al (2010) Detection of WWE2-related Lentisphaerae by 16S rRNA gene sequencing and fluorescence in situ hybridization in landfill leachate. Can J Microbiol 56(10):846-852
47. Lindsay MR, Webb RI et al (1995) Effects of fixative and buffer on morphology and ultrastructure of a fresh-water planctomycete, Gemmata obscuriglobus. J Microbiol Methods 21(1):45-54
48. Lindsay MR, Webb RI et al (1997) Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiology 143:739-748
49. Lindsay MR, Webb RI et al (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175(6):413-429
50. Lonhienne TG, Sagulenko E et al (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107(29):12883-12888
51. Martin-Galiano AJ, Oliva MA et al (2011) Bacterial tubulin distinct loop sequences and primitive assembly properties support its origin from a eukaryotic tubulin ancestor. J Biol Chem 286(22):19789-19803
52. McCoy AJ, Adams NE et al (2006) l, l-diaminopimelate aminotransferase, a trans-kingdom enzyme shared by Chlamydia and plants for synthesis of diaminopimelate/lysine. Proc Natl Acad Sci USA 103(47):17909-17914
53. McInerney JO, Martin WF et al (2011) Planctomycetes and eukaryotes: a case of analogy not homology. BioEssays 33(11):810-817
54. Ouellette SP, Karimova G et al (2012) Chlamydia co-opts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol Microbiol 85(1):164-178
55. Palleja A, Garcia-Vallve S et al (2009) Adaptation of the short intergenic spacers between co-directional genes to the Shine-Dalgarno motif among prokaryote genomes. BMC Genomics 10:537
56. Patt TE, Hanson RS (1978) Intracytoplasmic membrane, phospholipid, and sterol content of Methylobacterium organophilum cells grown under different conditions. J Bacteriol 134(2):636-644
57. Pearson A, Budin M et al (2003) Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 100(26):15352-15357
58. Pilhofer M, Rosati G et al (2007) Coexistence of tubulins and ftsZ in different Prosthecobacter species. Mol Biol Evol 24(7):1439-1442
59. Pilhofer M, Rappl K et al (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(9):3192-3202
60. Pilhofer M, Ladinsky MS et al (2011) Microtubules in bacteria: ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol 9(12):e1001213
61. Pol A, Heijmans K et al (2007) Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450(7171):874-878
62. Qiu YL, Muramatsu M et al (2013) Oligosphaera ethanolica gen. nov., sp. nov., an anaerobic, carbohydrate-fermenting bacterium isolated from methanogenic sludge, and description of Oligosphaeria classis nov. in the phylum Lentisphaerae. Int J Syst Evol Microbiol 63(Pt 2):533-539
63. Rinke C, Schwientek P et al (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431-437
64. Santarella-Mellwig R, Franke J et al (2010) The compartmentalized bacteria of the planctomycetes-verrucomicrobia-chlamydiae superphylum have membrane coat-like proteins. PLoS Biol 8(1):e1000281
65. Santarella-Mellwig R, Pruggnaller S et al (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11(5):e1001565
66. Schlesner H (1987) Verrucomicrobium spinosum gen. nov., sp.nov., a fimbriated prosthecate bacterium. Syst Appl Microbiol 10:54-56
67. Schlieper D, Oliva MA et al (2005) Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci USA 102(26):9170-9175
68. Schouten S, Bowman JP et al (2000) Sterols in a psychrophilic methanotroph, Methylosphaera hansonii. FEMS Microbiol Lett 186(2):193-195
69. Sinninghe Damste JS, Rijpstra WI et al (2005) Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox). FEBS J 272(16):4270-4283
70. Speth DR, van Teeseling MC et al (2012) Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in planctomycetes and verrucomicrobia. Front Microbiol 3:304
71. Stackebrandt E, Wehmeyer U et al (1986) 16S ribosomal RNA- and cell wall analysis of Gemmata obscuriglobus, a new member of the order Planctomycetales. FEMS Microbiol Lett 37(3):289-292
72. Staley JT, Bouzek H et al (2005) Eukaryotic signature proteins of Prosthecobacter dejongeii and Gemmata sp. Wa-1 as revealed by in silico analysis. FEMS Microbiol Lett 243(1):9-14
73. Strous M, Pelletier E et al (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440(7085):790-794
74. Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18(10):464-470
75. Teeling H, Lombardot T et al (2004) Evaluation of the phylogenetic position of the planctomycete Rhodopirellula baltica SH 1 by means of concatenated ribosomal protein sequences, DNA-directed RNA polymerase subunit sequences and whole genome trees. Int J Syst Evol Microbiol 54(Pt 3):791-801
76. Teh AH, Saito JA et al (2011) Hell's Gate globin I: an acid and thermostable bacterial hemoglobin resembling mammalian neuroglobin. FEBS Lett 585(20):3250-3258
77. Thomas V, Casson N et al (2006) Criblamydia sequanensis, a new intracellular Chlamydiales isolated from Seine river water using amoebal co-culture. Environ Microbiol 8(12):2125-2135
78. Thrash JC, Cho JC et al (2010) Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J Bacteriol 192(11):2938-2939
79. van Niftrik L, Jetten MS (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76(3):585-596
80. van Niftrik LA, Fuerst JA et al (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233(1):7-13
81. van Niftrik L, Geerts WJ et al (2008) Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins. J Bacteriol 190(2):708-717
82. van Niftrik L, van Helden M et al (2010) Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium Candidatus Kuenenia stuttgartiensis. Mol Microbiol 77(3):701-715
83. van Teeseling MC, Neumann S et al (2013) The anammoxosome organelle is crucial for the energy metabolism of anaerobic ammonium oxidizing bacteria. J Mol Microbiol Biotechnol 23(1-2):104-117
84. Volkman JK (2003) Sterols in microorganisms. Appl Microbiol Biotechnol 60(5):495-506
85. Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17(3):241-249
86. Wang J, Jenkins C et al (2002) Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Appl Environ Microbiol 68(1):417-422
87. Weisburg WG, Hatch TP et al (1986) Eubacterial origin of chlamydiae. J Bacteriol 167(2):570-574
88. Welter-Stahl L, Ojcius DM et al (2006) Stimulation of the cytosolic receptor for peptidoglycan, Nod1, by infection with Chlamydia trachomatis or Chlamydia muridarum. Cell Microbiol 8(6):1047-1057
89. Wertz JT, Kim E et al (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(5):1544-1555
90. Wolf YI, Rogozin IB et al (2001) Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol Biol 1:8
91. Yee B, Lafi FF et al (2007) A canonical FtsZ protein in Verrucomicrobium spinosum, a member of the Bacterial phylum Verrucomicrobia that also includes tubulin-producing Prosthecobacter species. BMC Evol Biol 7:37
92. Yee B, Sagulenko E et al (2011) Making heads or tails of the HU proteins in the planctomycete Gemmata obscuriglobus. Microbiology 157(Pt 7):2012-2021
93. Yee B, Sagulenko E et al (2012) Electron tomography of the nucleoid of Gemmata obscuriglobus reveals complex liquid crystalline cholesteric structure. Front Microbiol 3:326
94. Yen TY, Pal S et al (2005) Characterization of the disulfide bonds and free cysteine residues of the Chlamydia trachomatis mouse pneumonitis major outer membrane protein. Biochemistry 44(16):6250-6256
95. Yildirim S, Yeoman CJ et al (2010) Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS ONE 5(11):e13963
96. Yoon J, Matsuo Y et al (2007a) Cerasicoccus arenae gen. nov., sp. nov., a carotenoid-producing marine representative of the family Puniceicoccaceae within the phylum Verrucomicrobia, isolated from marine sand. Int J Syst Evol Microbiol 57(Pt 9):2067-2072
97. Yoon J, Yasumoto-Hirose M et al (2007b) Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum Verrucomicrobia isolated from seawater in Japan. Int J Syst Evol Microbiol 57(Pt 5):959-963
98. Yoon J, Yasumoto-Hirose M et al (2007c) Pelagicoccus mobilis gen. nov., sp. nov., Pelagicoccus albus sp. nov. and Pelagicoccus litoralis sp. nov., three novel members of subdivision 4 within the phylum Verrucomicrobia, isolated from seawater by in situ cultivation. Int J Syst Evol Microbiol 57(Pt 7):1377-1385
99. Zoetendal EG, Plugge CM et al (2003) Victivallis vadensis gen. nov., sp. nov., a sugar-fermenting anaerobe from human faeces. Int J Syst Evol Microbiol 53(Pt 1):211-215