Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae

Biology Direct

Volumn 10, Issue 1, 2015, Pages

  Pagnier, Isabelle ^a   Yutin, Natalya ^b   Croce, Olivier ^a   Makarova, Kira S ^b   Wolf, Yuri I ^b   Benamar, Samia ^a   Raoult, Didier ^a   Koonin, Eugene V ^b   La Scola, Bernard ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Amoeba; Bacterial replication; Intracellular bacteria

Indexed keywords

ACANTHAMOEBA CASTELLANII; AMOEBA (GENUS); BACTERIA (MICROORGANISMS); EUKARYOTA;

BACTERIAL DNA; BACTERIAL PROTEIN; CULTURE MEDIUM; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA; RIBOSOME RNA; TRANSFER RNA;

ACANTHAMOEBA CASTELLANII; BACTERIAL GENOME; CELL CULTURE TECHNIQUE; CELL DIVISION; CHEMISTRY; CULTURE MEDIUM; CYTOPLASM; DELTAPROTEOBACTERIA; DNA SEQUENCE; GENETICS; GENOMICS; HORIZONTAL GENE TRANSFER; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS;

ACANTHAMOEBA CASTELLANII; BACTERIAL PROTEINS; BASE SEQUENCE; CELL CULTURE TECHNIQUES; CELL DIVISION; CULTURE MEDIA; CYTOPLASM; CYTOSKELETAL PROTEINS; DELTAPROTEOBACTERIA; DNA, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL; RNA, TRANSFER; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84925635458     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/s13062-015-0043-z     Document Type: Article

References (73)

1. Bousseau B, Karlberg EO, Frank AC, Legault BA, Andersson SGE. Computational inference of scenarios for α-proteobacterial genome evolution. Proc Natl Acad Sci. 2004;26:9722-7.
2. Sakharkar KR, Dhar PK, Chow VTK. Genome reduction in prokaryotic obligatory intracellular parasites of humans: a comparative analysis. Int J Syst Evol Microbiol. 2004;54:1937-41.
3. Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D. Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct. 2009;4:13.
4. Greub G, Raoult D. History of the ADT/ATP-Translocase-Encoding Gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl Environ Microbial. 2003;69:5530-5.
5. Wolf YI, Aravind L, Koonin EV. Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 1999;15:173-5.
6. Levin BR, Cornejo OE. The population and evolutionary dynamics of homologous gene recombination in bacteria. PLoS Genet. 2009;5:e1000601.
7. Lukjansenko O, Wassenaar TM. Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol. 2010;60:702-20.
8. Fenchel T, Finlay BJ. The diversity of microbes: resurgence of the phenotype. Phil Trans R Soc. 2006;361:1965-73.
9. Merhej V, Notredame C, Royer-Carenzi M, Pontarotti P, Raoult D. The rhizome of life: the sympatric Rickettsia felis paradigm demonstrates the random transfer of DNA sequences. Mol Biol Evol. 2011;28:3213-23.
10. Moliner C, Fournier PE, Raoult D. Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev. 2010;34:281-94.
11. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, et al. Giant Marseillevirus highlights the role of amoeba as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci. 2009;106:21848-53.
12. Raoult D, Boyer M. Amoebae as genitors and reservoirs of giant viruses. Intervirology. 2010;53:321-9.
13. McLean JS, Lombardo MJ, Badger JH, Edlund A, Novotny M, Yee-Greenbaum J, et al. Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proc Natl Acad Sci U S A. 2013;110:E2390-9.
14. Gimenez DF. Staining Rickettsiae in Yolk-sac Cultures. Stain Technol. 1964;39:135-40.
15. Amann R, Springer N, Schönhuber W, Ludwig W, Schmid EN, Müller KD, et al. Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl Environ Microbiol. 1997;63:115-21.
16. Goy G, Croxatto A, Greub G. Waddlia chondrophila enters and multiplies within human macrophages. Microbes Infect. 2008;10:556-62.
17. Macalady JL, Jones DS, Lyon EH. Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol. 2007;9:1402-14.
18. Koonin EV, Wolf YI. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 2008;36:6688-719.
19. Schmitz-Esser S, Penz T, Spang A, Horn M. 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. 2011;26:270.
20. Yutin N, Puigbò P, Koonin EV, Wolf YI. Phylogenomics of prokaryotic ribosomal proteins. PLoS One. 2012;7:e36972.
21. Ogata H, La Scola B, Audic S, Renesto P, Blanc G, Robert C, et al. Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet. 2006;2:e76.
22. Thomas V, Greub G. Amoeba/amoebal symbiont genetic transfers: lessons from giant virus neighbours. Intervirology. 2010;53:254-67.
23. Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, et al. Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci. 2011;108:10296-301.
24. Klein CC, Cottret L, Kielbassa J, Charles H, Gautier C, Ribeiro De Vasconcelos AT, et al. Exploration of the core metabolism of symbiotic bacteria. BMC Genomics. 2012;31:438.
25. Malys N, McCarthy JE. Translation initiation: variations in the mechanism can be anticipated. Cell Mol Life Sci. 2011;68:991-1003.
26. Galli E, Gerdes K. Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol. 2010;76:1514-26.
27. McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 2011;10:13-26.
28. Galperin MY, Moroz OV, Wilson KS, Murzin AG. House cleaning, a part of good housekeeping. Mol Microbiol. 2006;59:5-19.
29. Voth DE. ThANKs for the repeat. Intracellular pathogens exploit a common eukaryotic domain. Cell Logist. 2011;1:128-32.
30. Dubreuil R, Segev N. Bringing host-cell takeover by pathogenic bacteria to center stage. Cell Logist. 2011;1:120-4.
31. Al-Khodor S, Price CT, Kalia A, Abu Kwaik Y. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 2010;18:132-9.
32. Alto NM, Orth K. Subversion of cell signaling by pathogens. Cold Spring Harb Perspect Biol. 2012;4:a006114.
33. Colson P, De Lamballerie X, Yutin N, Asgari S, Bigot Y, Bideshi DK, et al. "Megavirales", a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol. 2013;158:2517-21.
34. Barry M, van Buuren N, Burles K, Mottet K, Wang Q, Teale A. Poxvirus exploitation of the ubiquitin-proteasome system. Viruses. 2010;2:2356-80.
35. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ: SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell. 1996;86:263-74
36. Chung CH, Baek SH. Deubiquitinating enzymes: their diversity and emerging roles. Biochem Biophys Res Commun. 1999;266:633-40.
37. Hay RT. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 2007;17:370-6.
38. Yeh ET. SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem. 2009;284:8223-7.
39. Mossessova E, Lima CD. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell. 2000;5:865-76.
40. Everett RD, Boutell C, Hale BG. Interplay between viruses and host sumoylation pathways. Nat Rev Microbiol. 2013;11:400-11.
41. Huang W, Dolmer K, Gettins PG. NMR solution structure of complement-like repeat CR8 from the low density lipoprotein receptor-related protein. J Biol Chem. 1999;274:14130-6.
42. Springer TA. An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. J Mol Biol. 1998;283:837-62.
43. Makarova KS, Wolf YI, Koonin EV. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct. 2009;4:19.
44. Anderson JO, Andersson SG. Insights into the evolutionary process of genome degradation. Curr Opin Genet Dev. 1999;9:664-71.
45. Mercier R, Kawai Y, Errington J. Excess membrane synthesis drives a primitive mode of cell proliferation. Cell. 2013;152:997-1007.
46. Koonin EV, Mulkidjanian AY. Evolution of cell division: from shear mechanics to complex molecular machineries. Cell. 2013;152:942-4.
47. Luhrmann A, Noguiera CV, Carey KL, Roy CR. Inhibition of pathogen-induced apoptosis by Coxiella burnetti type IV effector protein. Proc Natl Acad Sci. 2010;107:18997-9001.
48. Lamb SA, Rhaman MM, Mc Fadden G. Recombinant myxoma virus lacking all poxvirus ankyrin-repeat proteins stimulates multiple cellular anti-viral pathways and exhibits a severe decrease in virulence. Virology. 2014;25:134-45.
49. Lagier JC, Armougom F, Million M, Hugon P, Pagnier I, Robert C, et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect. 2012;18:1185-93.
50. La Scola B, Mezi L, Weiller PJ, Raoult D. Isolation of Legionella anisa using an Amoebic Coculture procedure. J Clin Microbiol. 2001;39:365-6.
51. Fournier PE, El Karkouri K, Leroy Q, Robert C, Giumelli B, Renesto P, et al. Analysis of the Rickettsia africae genome reveals that virulence acquisition in Rickettsia species may be explained by genome reduction. BMC Genomics. 2009;10:166.
52. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005;437:376-80.
53. Chevreux B, Wetter T, Suhai S. Genome sequence assembly using trace signals and additional sequence information computer science and biology. Proceed German Conference Bioinformatics (GCB). 1999;99:45-56.
54. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2011;27:578-9.
55. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol. 2012;13:R56.
56. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-402.
57. Besemer J, Borodovsky M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res. 2005;33:W451-4.
58. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, Geer LY, et al. CDD: a Conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011;39:D225-9.
59. Schaffer AA, Wolf YI, Ponting CP, Koonin EV, Aravind L, Altschul SF. IMPALA: matching a protein sequence against a collection of PSI-BLAST-constructed position-specific score matrices. Bioinformatics. 1999;15:1000-11.
60. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003;11:41.
61. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33:W686-9.
62. Sonnhammer EL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol. 1998;6:175-82.
63. Wheeler D, Bhagwat M. BLAST QuickStart: example-driven web-based BLAST tutorial. Methods Mol Biol. 2007;395:149-76.
64. Peterson TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785-6.
65. Delorenzi M, Speed T. An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics. 2002;18:617-25.
66. Grigoriev A. Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res. 1998;26:2286-90.
67. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7.
68. Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG, Wolf YI, et al. Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J Gen Virol. 2009;90:2525-35.
69. Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5:e9490.
70. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27:1164-5.
71. Jobb G, von Haeseler A, Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 2004;28:18.
72. Stamatakis A, Ludwig T, Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 2005;21:456-63.
73. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590-6.