Comparative Genomics of Helicobacter pylori and the human-derived Helicobacter bizzozeronii CIII-1 strain reveal the molecular basis of the zoonotic nature of non-pylori gastric Helicobacter infections in humans

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Schott, Thomas ^a   Kondadi, Pradeep K ^a   Hänninen, Marja Liisa ^a   Rossi, Mirko ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; POLYSACCHARIDE LYASE; VIRULENCE FACTOR; BACTERIAL DNA;

ADULT; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM DETECTION; BACTERIUM ISOLATION; CASE REPORT; COMPARATIVE STUDY; DISEASE SEVERITY; DISEASE TRANSMISSION; DYSPEPSIA; ELECTRON TRANSPORT; ENERGY RESOURCE; FEMALE; GASTROINTESTINAL INFECTION; GENE IDENTIFICATION; GENE INSERTION SEQUENCE; GENE LOCATION; GENE SEQUENCE; GENOME ANALYSIS; HELICOBACTER BIZZOZERONII; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC PLASTICITY; PROPHAGE; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; ANIMAL; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELICOBACTER; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MOLECULAR GENETICS; PATHOGENICITY; ZOONOSIS;

ANIMALIA; CANDIDATUS HELICOBACTER HEILMANNII; HELICOBACTER; HELICOBACTER BIZZOZERONII; HELICOBACTER FELIS; HELICOBACTER PYLORI; HELICOBACTER SP.; NEGIBACTERIA;

ANIMALS; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; FEMALE; GENOME, BACTERIAL; HELICOBACTER; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; MIDDLE AGED; MOLECULAR SEQUENCE ANNOTATION; SEQUENCE ANALYSIS, DNA; ZOONOSES;

EID: 80055021587     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-534     Document Type: Article

References (90)

1. Suerbaum S, Josenhans C. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 2007, 5(6):441-452. 10.1038/nrmicro1658, 17505524.
2. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, Meyns T, Decostere A, Ducatelle R. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 2009, 22(2):202-23. 10.1128/CMR.00041-08, 2668234, 19366912.
3. Haesebrouck F, Pasmans F, Flahou B, Smet A, Vandamme P, Ducatelle R. Non-Helicobacter pylori Helicobacter Species in the Human Gastric Mucosa: A Proposal to Introduce the Terms H. heilmannii Sensu Lato and Sensu Stricto. Helicobacter 2011, 16(4):339-340. 10.1111/j.1523-5378.2011.00849.x, 21762276.
4. Baele M, Pasmans F, Flahou B, Chiers K, Ducatelle R, Haesebrouck F. Non-Helicobacter pylori helicobacters detected in the stomach of humans comprise several naturally occurring Helicobacter species in animals. FEMS Immunol Med Microbiol 2009, 55(3):306-313. 10.1111/j.1574-695X.2009.00535.x, 19243435.
5. Meining A, Kroher G, Stolte M. Animal reservoirs in the transmission of Helicobacter heilmannii. Results of a questionnaire-based study. Scand J Gastroenterol 1998, 33(8):795-798. 10.1080/00365529850171422, 9754724.
6. Jalava K, On SL, Harrington CS, Andersen LP, Hänninen ML, Vandamme P. A cultured strain of "Helicobacter heilmannii," a human gastric pathogen, identified as H. bizzozeronii: evidence for zoonotic potential of Helicobacter. Emerg Infect Dis 2001, 7(6):1036-1038. 10.3201/eid0706.010622, 2631917, 11747737.
7. Andersen LP, Boye K, Blom J, Holck S, Norgaard A, Elsborg L. Characterization of a culturable "Gastrospirillum hominis" (Helicobacter heilmannii) strain isolated from human gastric mucosa. J Clin Microbiol 1999, 37(4):1069-1076. 88651, 10074528.
8. Kivistö R, Linros J, Rossi M, Rautelin H, Hänninen ML. Characterization of multiple Helicobacter bizzozeronii isolates from a Finnish patient with severe dyspeptic symptoms and chronic active gastritis. Helicobacter 2010, 15(1):58-66. 10.1111/j.1523-5378.2009.00730.x, 20302591.
9. Hänninen ML, Happonen I, Saari S, Jalava K. Culture and characteristics of Helicobacter bizzozeronii, a new canine gastric Helicobacter sp. Int J Syst Bacteriol 1996, 46(1):160-166. 10.1099/00207713-46-1-160, 8573490.
10. Happonen I, Linden J, Saari S, Karjalainen M, Hänninen ML, Jalava K, Westermarck E. Detection and effects of helicobacters in healthy dogs and dogs with signs of gastritis. J Am Vet Med Assoc 1998, 213(12):1767-1774.
11. De Bock M, Decostere A, Van den Bulck K, Baele M, Duchateau L, Haesebrouck F, Ducatelle R. The inflammatory response in the mouse stomach to Helicobacter bizzozeronii, Helicobacter salomonis and two Helicobacter felis Strains. J Comp Pathol 2005, 133(2-3):83-91. 10.1016/j.jcpa.2005.01.007, 15949811.
12. De Bock M, Decostere A, Hellemans A, Haesebrouck F, Ducatelle R. Helicobacter felis and Helicobacter bizzozeronii induce gastric parietal cell loss in Mongolian gerbils. Microbes Infect 2006, 8(2):503-510. 10.1016/j.micinf.2005.08.003, 16311055.
13. O'Toole PW, Snelling WJ, Canchaya C, Forde BM, Hardie KR, Josenhans C, Graham RL, McMullan G, Parkhill J, Belda E, Bentley SD. Comparative genomics and proteomics of Helicobacter mustelae, an ulcerogenic and carcinogenic gastric pathogen. BMC Genomics 2010, 11:164. 10.1186/1471-2164-11-164, 2846917, 20219135.
14. Eppinger M, Baar C, Linz B, Raddatz G, Lanz C, Keller H, Morelli G, Gressmann H, Achtman M, Schuster SC. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2006, 2(7):e120.. 1523251, 16789826.
15. Vermoote M, Vandekerckhove TT, Flahou B, Pasmans F, Smet A, De Groote D, Van Criekinge W, Ducatelle R, Haesebrouck F. Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet Res 2011, 42(1):51. 10.1186/1297-9716-42-51, 3065412, 21414191.
16. Arnold IC, Zigova Z, Holden M, Lawley TD, Rad R, Dougan G, Falkow S, Bentley SD, Muller A. Comparative whole genome sequence analysis of the carcinogenic bacterial model pathogen Helicobacter felis. Genome Biol Evol 2011, 3:302-308. 10.1093/gbe/evr022, 21402865.
17. Schott T, Rossi M, Hanninen ML. Genome sequence of Helicobacter bizzozeronii strain CIII-1, an isolate from human gastric mucosa. J Bacteriol 2011, 193(17):4565-4566. 10.1128/JB.05439-11, 21705603.
18. Sachs G, Weeks DL, Wen Y, Marcus EA, Scott DR, Melchers K. Acid acclimation by Helicobacter pylori. Physiology (Bethesda) 2005, 20:429-438.
19. Bury-Mone S, Mendz GL, Ball GE, Thibonnier M, Stingl K, Ecobichon C, Ave P, Huerre M, Labigne A, Thiberge JM, De Reuse H. Roles of alpha and beta carbonic anhydrases of Helicobacter pylori in the urease-dependent response to acidity and in colonization of the murine gastric mucosa. Infect Immun 2008, 76(2):497-509. 10.1128/IAI.00993-07, 2223474, 18025096.
20. Leduc D, Gallaud J, Stingl K, de Reuse H. Coupled amino acid deamidase-transport systems essential for Helicobacter pylori colonization. Infect Immun 2010, 78(6):2782-2792. 10.1128/IAI.00149-10, 2876568, 20368342.
21. Kanamori T, Kanou N, Kusakabe S, Atomi H, Imanaka T. Allophanate hydrolase of Oleomonas sagaranensis involved in an ATP-dependent degradation pathway specific to urea. FEMS Microbiol Lett 2005, 245(1):61-65. 10.1016/j.femsle.2005.02.023, 15796980.
22. Cheng G, Shapir N, Sadowsky MJ, Wackett LP. Allophanate hydrolase, not urease, functions in bacterial cyanuric acid metabolism. Appl Environ Microbiol 2005, 71(8):4437-4445. 10.1128/AEM.71.8.4437-4445.2005, 1183272, 16085834.
23. Fischer W, Prassl S, Haas R. Virulence mechanisms and persistence strategies of the human gastric pathogen Helicobacter pylori. Curr Top Microbiol Immunol 2009, 337:129-171. 10.1007/978-3-642-01846-6_5, 19812982.
24. Rust M, Schweinitzer T, Josenhans C. Helicobacter flagella, motility and chemotaxis. Helicobacter pylori. Molecular genetics and cellular biology 2008, 61-86. Norwich: Caister Academic Press, Yamaoka Y.
25. Szurmant H, Ordal GW. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 2004, 68(2):301-319. 10.1128/MMBR.68.2.301-319.2004, 419924, 15187186.
26. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388(6642):539-547. 10.1038/41483, 9252185.
27. Kelly DJ. The physiology and metabolism of Campylobacter jejuni and Helicobacter pylori. Symp Ser Soc Appl Microbiol 2001, (30):16S-24S.
28. Schilling CH, Covert MW, Famili I, Church GM, Edwards JS, Palsson BO. Genome-scale metabolic model of Helicobacter pylori 26695. J Bacteriol 2002, 184(16):4582-4593. 10.1128/JB.184.16.4582-4593.2002, 135230, 12142428.
29. Doig P, de Jonge BL, Alm RA, Brown ED, Uria-Nickelsen M, Noonan B, Mills SD, Tummino P, Carmel G, Guild BC, Moir DT, Vovis GF, Trust TJ. Helicobacter pylori physiology predicted from genomic comparison of two strains. Microbiol Mol Biol Rev 1999, 63(3):675-707. 103750, 10477312.
30. Lemieux MJ, Huang Y, Wang DN. Glycerol-3-phosphate transporter of Escherichia coli: structure, function and regulation. Res Microbiol 2004, 155(8):623-629. 10.1016/j.resmic.2004.05.016, 15380549.
31. Kather B, Stingl K, van der Rest ME, Altendorf K, Molenaar D. Another unusual type of citric acid cycle enzyme in Helicobacter pylori: the malate:quinone oxidoreductase. J Bacteriol 2000, 182(11):3204-3209. 10.1128/JB.182.11.3204-3209.2000, 94508, 10809701.
32. Horswill AR, Escalante-Semerena JC. In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-methylcitrate dehydratase (PrpD) and aconitase Enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate. Biochemistry 2001, 40(15):4703-4713. 10.1021/bi015503b, 11294638.
33. Schneider BL, Ruback S, Kiupakis AK, Kasbarian H, Pybus C, Reitzer L. The Escherichia coli gabDTPC operon: specific gamma-aminobutyrate catabolism and nonspecific induction. J Bacteriol 2002, 184(24):6976-6986. 10.1128/JB.184.24.6976-6986.2002, 135471, 12446648.
34. Kalliri E, Mulrooney SB, Hausinger RP. Identification of Escherichia coli YgaF as an L-2-hydroxyglutarate oxidase. J Bacteriol 2008, 190(11):3793-3798. 10.1128/JB.01977-07, 2395033, 18390652.
35. Metzner M, Germer J, Hengge R. Multiple stress signal integration in the regulation of the complex sigma S-dependent csiD-ygaF-gabDTP operon in Escherichia coli. Mol Microbiol 2004, 51(3):799-811.
36. Barnard FM, Loughlin MF, Fainberg HP, Messenger MP, Ussery DW, Williams P, Jenks PJ. Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol Microbiol 2004, 51(1):15-32.
37. Brahmachary P, Wang G, Benoit SL, Weinberg MV, Maier RJ, Hoover TR. The human gastric pathogen Helicobacter pylori has a potential acetone carboxylase that enhances its ability to colonize mice. BMC Microbiol 2008, 8:14. 10.1186/1471-2180-8-14, 2244623, 18215283.
38. Kelly DJ. Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni. Campylobacter 2008, 41-62. Washington (DC): ASM press, Nachamkin I, Szymanski CM, Blaser MJ, 3.
39. Kelly DJ, Hughes NJ, Poole RK. Microaerobic Physiology: Aerobic Respiration, Anaerobic Respiration, and Carbon Dioxide Metabolism. Helicobacter pylori: Physiology and Genetics 2001, 113-124. Washington (DC): ASM Press, Mobley HLT, Mendz GL, Hazell SL.
40. Belzer C, Stoof J, van Vliet AH. Metal-responsive gene regulation and metal transport in Helicobacter species. Biometals 2007, 20(3-4):417-429. 10.1007/s10534-006-9028-9, 2798029, 17294126.
41. O'Toole PW, Clyne M. Cell Envelope. Helicobacter pylori: Physiology and Genetics 2001, 69-80. Washington (DC): ASM Press, Mobley HLT, Mendz GL, Hazell SL.
42. Alm RA, Bina J, Andrews BM, Doig P, Hancock RE, Trust TJ. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun 2000, 68(7):4155-4168. 10.1128/IAI.68.7.4155-4168.2000, 101716, 10858232.
43. De Bock M, D'Herde K, Duchateau L, Hellemans A, Decostere A, Haesebrouck F, Ducatelle R. The effect of Helicobacter felis and Helicobacter bizzozeronii on the gastric mucosa in Mongolian gerbils: a sequential pathological study. J Comp Pathol 2006, 135(4):226-236. 10.1016/j.jcpa.2006.08.003, 17069831.
44. Lanzoni A, Faustinelli I, Cristofori P, Luini M, Simpson KW, Scanziani E, Recordati C. Localization of Helicobacter spp. in the fundic mucosa of laboratory Beagle dogs: an ultrastructural study. Vet Res 2011, 42(1):42. 10.1186/1297-9716-42-42, 3056783, 21366900.
45. Costa AC, Figueiredo C, Touati E. Pathogenesis of Helicobacter pylori infection. Helicobacter 2009, 14(Suppl 1):15-20.
46. Vernikos GS, Parkhill J. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 2006, 22(18):2196-2203. 10.1093/bioinformatics/btl369, 16837528.
47. Kanipes MI, Guerry P. Role of microbial glycosylation in host cell invasion. Microbial glycobiology 2009, 871-883. London: Academic press, Elsevier, Moran AP, Holst O, Brennan PJ, von Itzstein M, 1.
48. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 2009, (37 Database):D233-8.
49. Logan SM, Schoenhofen IC, Soo EC. Glycosylation of bacterial and archaeal flagellins. Microbial Glycobiology. Structures, Relevance and Applications 2009, 129-146. London: Academic press, Elsevier, Moran AP, Holst O, Brennan PJ, von Itzstein M, 1.
50. Bergman M, Del Prete G, van Kooyk Y, Appelmelk B. Helicobacter pylori phase variation, immune modulation and gastric autoimmunity. Nat Rev Microbiol 2006, 4(2):151-159. 10.1038/nrmicro1344, 16415930.
51. Hynes SO, Ferris JA, Szponar B, Wadstrom T, Fox JG, O'Rourke J, Larsson L, Yaquian E, Ljungh A, Clyne M, Andersen LP, Moran AP. Comparative chemical and biological characterization of the lipopolysaccharides of gastric and enterohepatic helicobacters. Helicobacter 2004, 9(4):313-323. 10.1111/j.1083-4389.2004.00237.x, 15270745.
52. Bumann D, Aksu S, Wendland M, Janek K, Zimny-Arndt U, Sabarth N, Meyer TF, Jungblut PR. Proteome analysis of secreted proteins of the gastric pathogen Helicobacter pylori. Infect Immun 2002, 70(7):3396-3403. 10.1128/IAI.70.7.3396-3403.2002, 128097, 12065478.
53. Ilver D, Rappuoli R, Telford JL. Protein Export. Helicobacter pylori: Physiology and Genetics 2001, 219-226. Washington (DC): ASM Press, Mobley HLT, Mendz GL, Hazell SL.
54. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2(4):953-971. 10.1038/nprot.2007.131, 17446895.
55. Yu CS, Lin CJ, Hwang JK. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 2004, 13(5):1402-1406. 10.1110/ps.03479604, 2286765, 15096640.
56. Karnholz A, Hoefler C, Odenbreit S, Fischer W, Hofreuter D, Haas R. Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J Bacteriol 2006, 188(3):882-893. 10.1128/JB.188.3.882-893.2006, 1347336, 16428391.
57. Pathak SK, Basu S, Bhattacharyya A, Pathak S, Banerjee A, Basu J, Kundu M. TLR4-dependent NF-kappaB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J Immunol 2006, 177(11):7950-7958.
58. Suganuma M, Yamaguchi K, Ono Y, Matsumoto H, Hayashi T, Ogawa T, Imai K, Kuzuhara T, Nishizono A, Fujiki H. TNF-alpha-inducing protein, a carcinogenic factor secreted from H. pylori, enters gastric cancer cells. Int J Cancer 2008, 123(1):117-122. 10.1002/ijc.23484, 18412243.
59. Hoy B, Lower M, Weydig C, Carra G, Tegtmeyer N, Geppert T, Schroder P, Sewald N, Backert S, Schneider G, Wessler S. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep 2010, 11(10):798-804. 10.1038/embor.2010.114, 2948180, 20814423.
60. Linhardt RJ, Galliher PM, Cooney CL. Polysaccharide lyases. Appl Biochem Biotechnol 1986, 12(2):135-176.
61. Makris G, Wright JD, Ingham E, Holland KT. The hyaluronate lyase of Staphylococcus aureus - a virulence factor?. Microbiology 2004, 150(Pt 6):2005-2013.
62. Miller WG, Parker CT, Rubenfield M, Mendz GL, Wosten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G, Malek JA, Rogosin A, Stanker LH, Mandrell RE. The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One 2007, 2(12):e1358. 10.1371/journal.pone.0001358, 2147049, 18159241.
63. Power PM, Sweetman WA, Gallacher NJ, Woodhall MR, Kumar GA, Moxon ER, Hood DW. Simple sequence repeats in Haemophilus influenzae. Infect Genet Evol 2009, 9(2):216-228. 10.1016/j.meegid.2008.11.006, 2651432, 19095084.
64. Mrazek J. Analysis of distribution indicates diverse functions of simple sequence repeats in Mycoplasma genomes. Mol Biol Evol 2006, 23(7):1370-1385. 10.1093/molbev/msk023, 16618962.
65. Snyder LA, Loman NJ, Linton JD, Langdon RR, Weinstock GM, Wren BW, Pallen MJ. Simple sequence repeats in Helicobacter canadensis and their role in phase variable expression and C-terminal sequence switching. BMC Genomics 2010, 11:67. 10.1186/1471-2164-11-67, 2823697, 20105305.
66. Salaun L, Linz B, Suerbaum S, Saunders NJ. The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori. Microbiology 2004, 150(Pt 4):817-830.
67. Salaun L, Ayraud S, Saunders NJ. Phase variation mediated niche adaptation during prolonged experimental murine infection with Helicobacter pylori. Microbiology 2005, 151(Pt 3):917-923.
68. Jerome JP, Bell JA, Plovanich-Jones AE, Barrick JE, Brown CT, Mansfield LS. Standing genetic variation in contingency loci drives the rapid adaptation of Campylobacter jejuni to a novel host. PLoS One 2011, 6(1):e16399. 10.1371/journal.pone.0016399, 3025981, 21283682.
69. Ragan MA. Detection of lateral gene transfer among microbial genomes. Curr Opin Genet Dev 2001, 11(6):620-626. 10.1016/S0959-437X(00)00244-6, 11682304.
70. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 2011, 12(3):R30. 10.1186/gb-2011-12-3-r30, 3129680, 21443786.
71. Debets-Ossenkopp YJ, Pot RG, van Westerloo DJ, Goodwin A, Vandenbroucke-Grauls CM, Berg DE, Hoffman PS, Kusters JG. Insertion of mini-IS605 and deletion of adjacent sequences in the nitroreductase (rdxA) gene cause metronidazole resistance in Helicobacter pylori NCTC11637. Antimicrob Agents Chemother 1999, 43(11):2657-2662. 89539, 10543743.
72. Kersulyte D, Kalia A, Gilman RH, Mendez M, Herrera P, Cabrera L, Velapatino B, Balqui J, Paredes Puente de V, Rodriguez Ulloa CA, Cok J, Hooper CC, Dailide G, Tamma S, Berg DE. Helicobacter pylori from Peruvian amerindians: traces of human migrations in strains from remote Amazon, and genome sequence of an Amerind strain. PLoS One 2010, 5(11):e15076. 10.1371/journal.pone.0015076, 2993954, 21124785.
73. Poly F, Read TD, Chen YH, Monteiro MA, Serichantalergs O, Pootong P, Bodhidatta L, Mason CJ, Rockabrand D, Baqar S, Porter CK, Tribble D, Darsley M, Guerry P. Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies. Infect Immun 2008, 76(12):5655-5667. 10.1128/IAI.00780-08, 2583572, 18809665.
74. Alm RA, Trust TJ. Analysis of the genetic diversity of Helicobacter pylori: the tale of two genomes. J Mol Med(Berl) 1999, 77(12):834-846.
75. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 2009, 323(5912):396-401. 10.1126/science.1163806, 2764309, 19150849.
76. Bose M, Barber RD. Prophage Finder: a prophage loci prediction tool for prokaryotic genome sequences. In Silico Biol 2006, 6(3):223-227.
77. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75. 10.1186/1471-2164-9-75, 2265698, 18261238.
78. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics 2000, 16(10):944-945. 10.1093/bioinformatics/16.10.944, 11120685.
79. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. The Pfam protein families database. Nucleic Acids Res 2010, (38 Database):D211-22.
80. Mulder N, Apweiler R. InterPro and InterProScan: tools for protein sequence classification and comparison. Methods Mol Biol 2007, 396:59-70. 10.1007/978-1-59745-515-2_5, 18025686.
81. Aoki KF, Kanehisa M. Using the KEGG database resource. Current Protocols in Bioinformatics 2005, Unit 1.12. London: John Wiley & Sons, Baxevanis AD, Stein LD, Stormo GD, Yates JR III.
82. Yu NY, Laird MR, Spencer C, Brinkman FS. PSORTdb--an expanded, auto-updated, user-friendly protein subcellular localization database for Bacteria and Archaea. Nucleic Acids Res 2011, (39 Database):D241-4.
83. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S. Prediction of twin-arginine signal peptides. BMC Bioinformatics 2005, 6:167. 10.1186/1471-2105-6-167, 1182353, 15992409.
84. Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 2003, 12(8):1652-1662. 10.1110/ps.0303703, 2323952, 12876315.
85. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13(9):2178-2189. 10.1101/gr.1224503, 403725, 12952885.
86. Lara-Ramirez EE, Segura-Cabrera A, Guo X, Yu G, Garcia-Perez CA, Rodriguez-Perez MA. New implications on genomic adaptation derived from the Helicobacter pylori genome comparison. PLoS One 2011, 6(2):e17300. 10.1371/journal.pone.0017300, 3046158, 21387011.
87. Tsirigos KD, Bagos PG, Hamodrakas SJ. OMPdb: a database of β-barrel outer membrane proteins from Gram-negative bacteria. Nucleic Acids Res 2011, (39 Database):D324-31.
88. Rasko DA, Myers GS, Ravel J. Visualization of comparative genomic analyses by BLAST score ratio. BMC Bioinformatics 2005, 6:2. 10.1186/1471-2105-6-2, 545078, 15634352.
89. Msatfinder. , http://www.genomics.ceh.ac.uk/cgi-bin/msatfinder/msatfinder.cgi
90. Langille MG, Brinkman FS. IslandViewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics 2009, 25(5):664-665. 10.1093/bioinformatics/btp030, 2647836, 19151094.