Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut

mBio

Volumn 5, Issue 2, 2014, Pages

  Nuccio, Sean Paul ^a   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; COMPUTER MODEL; GENOME ANALYSIS; INFLAMMATION; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; SALMONELLA; SALMONELLA ENTERICA;

ANAEROBIOSIS; COMPUTATIONAL BIOLOGY; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; METABOLIC NETWORKS AND PATHWAYS; SALMONELLA;

EID: 84899761194     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00929-14     Document Type: Article

References (63)

1. Parkhill J, Wren BW, Thomson NR, Titball RW, Holden MT, Prentice MB, Sebaihia M, James KD, Churcher C, Mungall KL, Baker S, Basham D, Bentley SD, Brooks K, Cerdeño-Tárraga AM, Chillingworth T, Cronin A, Davies RM, Davis P, Dougan G, Feltwell T, Hamlin N, Holroyd S, Jagels K, Karlyshev AV, Leather S, Moule S, Oyston PC, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527. http://dx.doi.org/10.1038/ 35097083.
2. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O'Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852. http://dx.doi.org/10.1038/35101607.
3. Vissa VD, Brennan PJ. 2001. The genome of Mycobacterium leprae: a minimal mycobacterial gene set. Genome Biol. 2:reviews1023-reviews1023.8. http://dx.doi.org/10.1186/gb-2001-2-8-reviews1023.
4. Jin Q, Yuan Z, Xu J, Wang Y, Shen Y, Lu W, Wang J, Liu H, Yang J, Yang F, Zhang X, Zhang J, Yang G, Wu H, Qu D, Dong J, Sun L, Xue Y, Zhao A, Gao Y, Zhu J, Kan B, Ding K, Chen S, Cheng H, Yao Z, He B, Chen R, Ma D, Qiang B, Wen Y, Hou Y, Yu J. 2002. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K-12 and O157. Nucleic Acids Res. 30:4432-4441. http://dx.doi.org/10.1093/nar/gkf566.
5. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, Ward NL, Tettelin H, Davidsen TM, Beanan MJ, Deboy RT, Daugherty SC, Brinkac LM, Madupu R, Dodson RJ, Khouri HM, Lee KH, Carty HA, Scanlan D, Heinzen RA, Thompson HA, Samuel JE, Fraser CM, Heidelberg JF. 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. U. S. A. 100:5455-5460. http:// dx.doi.org/10.1073/pnas.0931379100.
6. McClelland M, Sanderson KE, Clifton SW, Latreille P, Porwollik S, Sabo A, Meyer R, Bieri T, Ozersky P, McLellan M, Harkins CR, Wang C, Nguyen C, Berghoff A, Elliott G, Kohlberg S, Strong C, Du F, Carter J, Kremizki C, Layman D, Leonard S, Sun H, Fulton L, Nash W, Miner T, Minx P, Delehaunty K, Fronick C, Magrini V, Nhan M, Warren W, Florea L, Spieth J, Wilson RK. 2004. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat. Genet. 36:1268-1274. http://dx.doi.org/ 10.1038/ng1470.
7. Kauffmann F. 1955. Differential diagnosis and pathogenicity of Salmonella Java and Salmonella Paratyphi B. Z. Hyg. Infektionskr. 141:546-550. (In German.) http://dx.doi.org/10.1007/BF02156850.
8. Bravo D, Silva C, Carter JA, Hoare A, Alvarez SA, Blondel CJ, Zaldívar M, Valvano MA, Contreras I. 2008. Growth-phase regulation of lipopolysaccharide O-antigen chain length influences serum resistance in serovars of Salmonella. J. Med. Microbiol. 57:938-946. http://dx.doi.org/ 10.1099/jmm.0.47848-0.
9. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Bäumler AJ. 2005. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect. Immun. 73:3358-3366. http://dx.doi.org/10.1128/ IAI.73.6.3358-3366.2005.
10. Stecher B, Barthel M, Schlumberger MC, Haberli L, Rabsch W, Kremer M, Hardt WD. 2008. Motility allows S. Typhimurium to benefit from the mucosal defence. Cell. Microbiol. 10:1166-1180. http://dx.doi.org/ 10.1111/j.1462-5822.2008.01118.x.
11. Rivera-Chávez F, Winter SE, Lopez CA, Xavier MN, Winter MG, Nuccio SP, Russell JM, Laughlin RC, Lawhon SD, Sterzenbach T, Bevins CL, Tsolis RM, Harshey R, Adams LG, Bäumler AJ. 2013. Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog. 9:e1003267. http://dx.doi.org/10.1371/journal.ppat.1003267.
12. Lockman HA, Curtiss R, III. 1990. Salmonella Typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect. Immun. 58:137-143.
13. Lockman HA, Curtiss R, III. 1992. Virulence of non-type 1-fimbriated and nonfimbriated nonflagellated Salmonella Typhimurium mutants in murine typhoid fever. Infect. Immun. 60:491-496.
14. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG, Leclerc JE, Ravel J, Cebula TA. 2011. Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J. Bacteriol. 193:3556-3568. http://dx.doi.org/10.1128/ JB.00297-11.
15. Tsolis RM, Adams LG, Ficht TA, Bäumler AJ. 1999. Contribution of Salmonella Typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67:4879-4885.
16. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Bäumler AJ. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426-429. http://dx.doi.org/10.1038/ nature09415.
17. Lopez CA, Winter SE, Rivera-Chávez F, Xavier MN, Poon V, Nuccio SP, Tsolis RM, Bäumler AJ. 2012. Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration. mBio 3(3):e00143-12. http://dx.doi.org/10.1128/mBio.00143-12.
18. Fischbach MA, Sonnenburg JL. 2011. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 10: 336-347. http://dx.doi.org/10.1016/j.chom.2011.10.002.
19. Maier RJ, Olczak A, Maier S, Soni S, Gunn J. 2004. Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72:6294-6299. http://dx.doi.org/10.1128/ IAI.72.11.6294-6299.2004.
20. Maier L, Vyas R, Cordova CD, Lindsay H, Schmidt TS, Brugiroux S, Periaswamy B, Bauer R, Sturm A, Schreiber F, von Mering C, Robinson MD, Stecher B, Hardt WD. 2013. Microbiota-derived hydrogen fuels Salmonella Typhimurium invasion of the gut ecosystem. Cell Host Microbe 14:641-651. http://dx.doi.org/10.1016/j.chom.2013.11.002.
21. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. U. S. A. 108:17480-17485. http://dx.doi.org/10.1073/pnas.1107857108.
22. Price-Carter M, Tingey J, Bobik TA, Roth JR. 2001. The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar Typhimurium on ethanolamine or 1,2-propanediol. J. Bacteriol. 183:2463-2475. http://dx.doi.org/10.1128/ JB.183.8.2463-2475.2001.
23. Deatherage Kaiser BL, Li J, Sanford JA, Kim YM, Kronewitter SR, Jones MB, Peterson CT, Peterson SN, Frank BC, Purvine SO, Brown JN, Metz TO, Smith RD, Heffron F, Adkins JN. 2013. A multi-omic view of host-pathogen-commensal interplay in Salmonella-mediated intestinal infection. PLoS One 8:e67155. http://dx.doi.org/10.1371/ journal.pone.0067155.
24. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, Sonnenburg JL. 2013. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:96-99. http://dx.doi.org/ 10.1038/502S96a.
25. Craig M, Sadik AY, Golubeva YA, Tidhar A, Slauch JM. 2013. Twinarginine translocation system (tat) mutants of Salmonella are attenuated due to envelope defects, not respiratory defects. Mol. Microbiol. 89: 887-902. http://dx.doi.org/10.1111/mmi.12318.
26. Muller L. 1923. Un nouveau milieu d'enrichissement pour la recherche du Bacille Typhique at Paratyphique. Comp. Rend. Soc. Biol. 89:434-437.
27. Krumwiede C, Kohn LA. 1917. A triple-sugar modification of the Russell double-sugar medium. J. Med. Res. 37:225-227.
28. Wilson WJ. 1923. Reduction of sulphites by certain bacteria in media containing a fermentable carbohydrate and metallic salts. J. Hyg. 21: 392-398. http://dx.doi.org/10.1017/S0022172400031594.
29. Malorny B, Bunge C, Helmuth R. 2003. Discrimination of d-tartratefermenting and-nonfermenting Salmonella enterica subsp. enterica isolates by genotypic and phenotypic methods. J. Clin. Microbiol. 41: 4292-4297. http://dx.doi.org/10.1128/JCM.41.9.4292-4297.2003.
30. Edwards PR, Moran AB. 1945. Salmonella cultures which resemble the Sendai type. J. Bacteriol. 50:257-260.
31. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell DJ, Wain J, Dolecek C, Achtman M, Dougan G. 2008. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat. Genet. 40:987-993. http://dx.doi.org/10.1038/ng.195.
32. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE. 2000. Host adapted serotypes of Salmonella enterica. Epidemiol. Infect. 125:229-255. http://dx.doi.org/10.1017/ S0950268899004379.
33. Chen HD, Jewett MW, Groisman EA. 2012. An allele of an ancestral transcription factor dependent on a horizontally acquired gene product. PLoS Genet. 8:e1003060. http://dx.doi.org/10.1371/journal.pgen.1003060.
34. Winter SE, Winter MG, Thiennimitr P, Gerriets VA, Nuccio SP, Rüssmann H, Bäumler AJ. 2009. The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol. Microbiol. 74:175-193. http://dx.doi.org/10.1111/ j.1365-2958.2009.06859.x.
35. Winter SE, Winter MG, Godinez I, Yang HJ, Russmann H, Andrews-Polymenis HL, Baumler AJ. 2010. A rapid change in virulence gene expression during the transition from the intestinal lumen into tissue promotes systemic dissemination of Salmonella. PLoS Pathog. 6:e1001060. http://dx.doi.org/10.1371/journal.ppat.1001060.
36. Murray GL, Attridge SR, Morona R. 2003. Regulation of Salmonella Typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol. Microbiol. 47: 1395-1406. http://dx.doi.org/10.1046/j.1365-2958.2003.03383.x.
37. Crawford RW, Keestra AM, Winter SE, Xavier MN, Tsolis RM, Tolstikov V, Bäumler AJ. 2012. Very long O-antigen chains enhance fitness during Salmonella-induced colitis by increasing bile resistance. PLoS Pathog. 8:e1002918. http://dx.doi.org/10.1371/journal.ppat.1002918.
38. Crawford RW, Wangdi T, Spees AM, Xavier MN, Tsolis RM, Bäumler AJ. 2013. Loss of very-long O-antigen chains optimizes capsule-mediated immune evasion by Salmonella enterica serovar Typhi. mBio 4(4):e00232-13. http://dx.doi.org/10.1128/mBio.00232-13.
39. Lawley TD, Bouley DM, Hoy YE, Gerke C, Relman DA, Monack DM. 2008. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect. Immun. 76:403-416. http://dx.doi.org/10.1128/IAI.01189-07.
40. Raffatellu M, Santos RL, Chessa D, Wilson RP, Winter SE, Rossetti CA, Lawhon SD, Chu H, Lau T, Bevins CL, Adams LG, Bäumler AJ. 2007. The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect. Immun. 75: 4342-4350. http://dx.doi.org/10.1128/IAI.01571-06.
41. Haneda T, Winter SE, Butler BP, Wilson RP, Tükel C, Winter MG, Godinez I, Tsolis RM, Bäumler AJ. 2009. The capsule-encoding viaB locus reduces intestinal inflammation by a Salmonella pathogenicity island 1-independent mechanism. Infect. Immun. 77:2932-2942. http:// dx.doi.org/10.1128/IAI.00172-09.
42. Stone WS. 1912. The medical of chronic typhoid infection (typhoid bacillus carriers). Am. J. Med. Sci. 143:544-557. http://dx.doi.org/10.1097/ 00000441-191204000-00009.
43. Shivaprasad HL. 2000. Fowl typhoid and pullorum disease. Rev. Sci. Tech. 19:405-424.
44. Nielsen LR, Schukken YH, Gröhn YT, Ersbøll AK. 2004. Salmonella Dublin infection in dairy cattle: risk factors for becoming a carrier. Prev. Vet. Med. 65:47-62. http://dx.doi.org/10.1016/j.prevetmed.2004.06.010.
45. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, Quail MA, Stevens M, Jones MA, Watson M, Barron A, Layton A, Pickard D, Kingsley RA, Bignell A, Clark L, Harris B, Ormond D, Abdellah Z, Brooks K, Cherevach I, Chillingworth T, Woodward J, Norberczak H, Lord A, Arrowsmith C, Jagels K, Moule S, Mungall K, Sanders M, Whitehead S, Chabalgoity JA, Maskell D, Humphrey T, Roberts M, Barrow PA, Dougan G, Parkhill J. 2008. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18:1624-1637. http://dx.doi.org/ 10.1101/gr.077404.108.
46. Deng W, Liou SR, Plunkett G, III, Mayhew GF, Rose DJ, Burland V, Kodoyianni V, Schwartz DC, Blattner FR. 2003. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J. Bacteriol. 185:2330-2337. http://dx.doi.org/10.1128/JB.185.7.2330-2337.2003.
47. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, Hou S, Layman D, Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E, Ryan E, Sun H, Florea L, Miller W, Stoneking T, Nhan M, Waterston R, Wilson RK. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856. http://dx.doi.org/10.1038/35101614.
48. Holt KE, Thomson NR, Wain J, Langridge GC, Hasan R, Bhutta ZA, Quail MA, Norbertczak H, Walker D, Simmonds M, White B, Bason N, Mungall K, Dougan G, Parkhill J. 2009. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics 10:36. http://dx.doi.org/10.1186/1471-2164-10-S3-S36.
49. Chiu CH, Su LH, Chu C. 2004. Salmonella enterica serotype Choleraesuis: epidemiology, pathogenesis, clinical disease, and treatment. Clin. Microbiol. Rev. 17:311-322. http://dx.doi.org/10.1128/ CMR.17.2.311-322.2004.
50. Liu WQ, Feng Y, Wang Y, Zou QH, Chen F, Guo JT, Peng YH, Jin Y, Li YG, Hu SN, Johnston RN, Liu GR, Liu SL. 2009. Salmonella Paratyphi C: genetic divergence from Salmonella Choleraesuis and pathogenic convergence with Salmonella Typhi. PLoS One 4:e4510. http://dx.doi.org/ 10.1371/journal.pone.0004510.
51. Magrane M, UniProt Consortium. 2011. UniProt Knowledgebase: a hub of integrated protein data. Database 2011:bar009. doi:10.1093/database/ bar009. PubMed.
52. Maglott D, Ostell J, Pruitt KD, Tatusova T. 2005. Entrez gene: genecentered information at NCBI. Nucleic Acids Res. 33:D54-D58. http:// dx.doi.org/10.1093/nar/gni052.
53. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P. 2012. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res. 40:D284-D289. http:// dx.doi.org/10.1093/nar/gkr1060.
54. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301. http://dx.doi.org/10.1093/ nar/gkr1065.
55. Haft DH, Selengut JD, White O. 2003. The TIGRFAMs database of protein families. Nucleic Acids Res. 31:371-373. http://dx.doi.org/ 10.1093/nar/gkg128.
56. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and psi-blast: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
57. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34:D32-D36. http://dx.doi.org/10.1093/nar/gkj014.
58. Marchler-Bauer A, Bryant SH. 2004. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32:W327-W331. http://dx.doi.org/ 10.1093/nar/gkh454.
59. Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28:27-30. http://dx.doi.org/10.1093/nar/ 28.7.e27.
60. Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunsalus RP, Paulsen I, Karp PD. 2013. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41:D605-D612. http://dx.doi.org/10.1093/nar/gks1027.
61. Nuccio SP, Bäumler AJ. 2007. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol. Mol. Biol. Rev. 71:551-575. http://dx.doi.org/10.1128/MMBR.00014-07.
62. Haraga A, Ohlson MB, Miller SI. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66. http://dx.doi.org/10.1038/ nrmicro1788.
63. Frye J, Karlinsey JE, Felise HR, Marzolf B, Dowidar N, McClelland M, Hughes KT. 2006. Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:2233-2243. http:// dx.doi.org/10.1128/JB.188.6.2233-2243.2006.