Identification of novel factors involved in modulating motility of salmonella enterica serotype typhimurium

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Bogomolnaya, Lydia M ^a,b   Aldrich, Lindsay ^a   Ragoza, Yuri ^a   Talamantes, Marissa ^a   Andrews, Katharine D ^a   McClelland, Michael ^c   Andrews Polymenis, Helene L ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE MUTATION; GENOME; INOCULATION; OPEN READING FRAME; PHENOTYPE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SWIMMING; BACTERIAL GENE; CYTOLOGY; GENE DELETION; GENETICS; HUMAN; MICROBIOLOGY; SALMONELLOSIS;

GENE DELETION; GENES, BACTERIAL; HUMANS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 84932120863     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111513     Document Type: Article

References (84)

1. Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66.
2. Rabsch W, Tschape H, Baumler AJ (2001) Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3: 237-247.
3. Chevance FF, Hughes KT (2008) Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6: 455-465.
4. Wang Q, Frye JG, McClelland M, Harshey RM (2004) Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52: 169-187.
5. Ottemann KM, Miller JF (1997) Roles for motility in bacterial-host interactions. Mol Microbiol 24: 1109-1117.
6. Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57: 249-273.
7. Adler J (1966) Chemotaxis in bacteria. Science 153: 708-716.
8. Fraser GM, Hughes C (1999) Swarming motility. Curr Opin Microbiol 2: 630- 635.
9. Berg HC (2005) Swarming motility: it better be wet. Curr Biol 15: R599-R600.
10. Chen BG, Turner L, Berg HC (2007) The wetting agent required for swarming in Salmonella enterica serovar typhimurium is not a surfactant. J Bacteriol 189: 8750-8753.
11. Toguchi A, Siano M, Burkart M, Harshey RM (2000) Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J Bacteriol 182: 6308-6321.
12. Wang Q, Suzuki A, Mariconda S, Porwollik S, Harshey RM (2005) Sensing wetness: A new role for the bacterial flagellum. EMBO J 24: 2034-2042.
13. Girgis HS, Liu Y, Ryu WS, Tavazoie S (2007) A comprehensive genetic characterization of bacterial motility. PLoS Genet 3: 1644-1660.
14. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, et al. (2007) Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol 189: 950-957.
15. Santiviago CA, Reynolds MM, Porwollik S, Choi SH, Long F, et al. (2009) Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog 5: e1000477.
16. Bogomolnaya LM, Santiviago CA, Yang HJ, Baumler AJ, Andrews-Polymenis HL (2008) 'Form variation' of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine. Mol Microbiol 70: 1105- 1119.
17. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory.
18. Guard-Petter J (1997) Induction of flagellation and a novel agar-penetrating flagellar structure in Salmonella enterica grown on solid media: possible consequences for serological identification. FEMS Microbiol Lett 149: 173-180.
19. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
20. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, et al. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
21. Chilcott GS, Hughes KT (2000) Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64: 694-708.
22. Nevola JJ, Stocker BA, Laux DC, Cohen PS (1985) Colonization of the mouse intestine by an avirulent Salmonella typhimurium strain and its lipopolysaccharide- defective mutants. Infect Immun 50: 152-159.
23. Mariconda S, Wang Q, Harshey RM (2006) A mechanical role for the chemotaxis system in swarming motility. Mol Microbiol 60: 1590-1602.
24. Blair DF, Kim DY, Berg HC (1991) Mutant MotB proteins in Escherichia coli. J Bacteriol 173: 4049-4055.
25. Wang KC, Hsu YH, Huang YN, Yeh KS (2012) A previously uncharacterized gene stm0551 plays a repressive role in the regulation of type 1 fimbriae in Salmonella enterica serotype Typhimurium. BMC Microbiol 12: 111.
26. Ahmad I, Lamprokostopoulou A, Le Guyon S, Streck E, Barthel M, et al. (2011) Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS One 6: e28351.
27. Wolfe AJ, Visick KL (2008) Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190: 463-475.
28. Clegg S, Hughes KT (2002) FimZ is a molecular link between sticking and swimming in Salmonella enterica serovar Typhimurium. J Bacteriol 184: 1209- 1213.
29. Reynolds MM, Bogomolnaya L, Guo J, Aldrich L, Bokhari D, et al. (2011) Abrogation of the twin arginine transport system in Salmonella enterica serovar Typhimurium leads to colonization defects during infection. PLoS One 6: e15800.
30. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol Cell 38: 128-139.
31. Kato Y, Sugiura M, Mizuno T, Aiba H (2007) Effect of the arcA mutation on the expression of flagella genes in Escherichia coli. Biosci Biotechnol Biochem 71: 77-83.
32. Simm R, Morr M, Kader A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
33. Zhao R, Amsler CD, Matsumura P, Khan S (1996) FliG and FliM distribution in the Salmonella typhimurium cell and flagellar basal bodies. J Bacteriol 178: 258-265.
34. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29: 22-28.
35. Ilg K, Endt K, Misselwitz B, Stecher B, Aebi M, et al. (2009) O-antigen-negative Salmonella enterica serovar Typhimurium is attenuated in intestinal colonization but elicits colitis in streptomycin-treated mice. Infect Immun 77: 2568- 2575.
36. Abeyrathne PD, Daniels C, Poon KK, Matewish MJ, Lam JS (2005) Functional characterization of WaaL, a ligase associated with linking O-antigen polysaccharide to the core of Pseudomonas aeruginosa lipopolysaccharide. J Bacteriol 187: 3002-3012.
37. Blondel CJ, Jimenez JC, Contreras I, Santiviago CA (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10: 354.
38. Folkesson A, Lofdahl S, Normark S (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153: 537- 545.
39. Gomez-Gomez JM, Manfredi C, Alonso JC, Blazquez J (2007) A novel role for RecA under non-stress: promotion of swarming motility in Escherichia coli K- 12. BMC Biol 5: 14.
40. Stafford GP, Hughes C (2007) Salmonella typhimurium flhE, a conserved flagellar regulon gene required for swarming. Microbiology 153: 541-547.
41. Lee J, Harshey RM (2012) Loss of FlhE in the flagellar Type III secretion system allows proton influx into Salmonella and Escherichia coli. Mol Microbiol 84: 550-565.
42. Morgenstein RM, Clemmer KM, Rather PN (2010) Loss of the waaL O-antigen ligase prevents surface activation of the flagellar gene cascade in Proteus mirabilis. J Bacteriol 192: 3213-3221.
43. Haneda T, Sugimoto M, Yoshida-Ohta Y, Kodera Y, Oh-Ishi M, et al. (2010) Comparative proteomic analysis of Salmonella enterica serovar Typhimurium ppGpp-deficient mutant to identify a novel virulence protein required for intracellular survival in macrophages. BMC Microbiol 10: 324.
44. Traxler MF, Summers SM, Nguyen H-T, Zacharia VM, Hightower GA, et al. (2008) The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Molecular microbiology 68: 1128-1148.
45. Suzuki H, Koyanagi T, Izuka S, Onishi A, Kumagai H (2005) The yliA, -B, -C, and -D genes of Escherichia coli K-12 encode a novel glutathione importer with an ATP-binding cassette. J Bacteriol 187: 5861-5867.
46. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, et al. (2011) PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun 79: 4286-4298.
47. Kim W, Surette MG (2004) Metabolic differentiation in actively swarming Salmonella. Mol Microbiol 54: 702-714.
48. Frye J, Karlinsey JE, Felise HR, Marzolf B, Dowidar N, et al. (2006) Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 2233-2243.
49. Wang Q, Mariconda S, Suzuki A, McClelland M, Harshey RM (2006) Uncovering a large set of genes that affect surface motility in Salmonella enterica serovar Typhimurium. J Bacteriol 188: 7981-7984.
50. Kohler T, Curty LK, Barja F, van Delden C, Pechere JC (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182: 5990-5996.
51. Chandra H, Khandelwal P, Khattri A, Banerjee N (2008) Type 1 fimbriae of insecticidal bacterium Xenorhabdus nematophila is necessary for growth and colonization of its symbiotic host nematode Steinernema carpocapsiae. Environ Microbiol 10: 1285-1295.
52. Stocker BAD, McDonough MW, Ambler RP (1961) A gene determining presence or absence of epsilon-N-methyl-lysine in Salmonella flagellar protein. Nature 189: 556-558.
53. Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, et al. (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16: 496-506.
54. Chaudhuri RR, Peters SE, Pleasance SJ, Northen H, Willers C, et al. (2009) Comprehensive identification of Salmonella enterica serovar typhimurium genes required for infection of BALB/c mice. PLoS Pathog 5: e1000529.
55. Morgan E, Campbell JD, Rowe SC, Bispham J, Stevens MP, et al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54: 994-1010.
56. Groisman EA, Mouslim C (2006) Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 4: 705-709.
57. Navarre WW, Halsey TA, Walthers D, Frye J, McClelland M, et al. (2005) Coregulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 56: 492-508.
58. Monsieurs P, De Keersmaecker S, Navarre WW, Bader MW, De Smet F, et al. (2005) Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J Mol Evol 60: 462-474.
59. Shah DH, Lee MJ, Park JH, Lee JH, Eo SK, et al. (2005) Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCRbased signature-tagged mutagenesis. Microbiology 151: 3957-3968.
60. Yoon H, McDermott JE, Porwollik S, McClelland M, Heffron F (2009) Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PLoS Pathog 5: e1000306.
61. Waite RD, Rose RS, Rangarajan M, Aduse-Opoku J, Hashim A, et al. (2012) Pseudomonas aeruginosa possesses two putative type I signal peptidases, LepB and PA1303, each with distinct roles in physiology and virulence. J Bacteriol 194: 4521-4536.
62. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 3603-3612.
63. Kuchma SL, Ballok AE, Merritt JH, Hammond JH, Lu W, et al. (2010) Cyclicdi- GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J Bacteriol 192: 2950-2964.
64. Merritt JH, Brothers KM, Kuchma SL, O'Toole GA (2007) SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J Bacteriol 189: 8154- 8164.
65. Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, et al. (2010) Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di- GMP diguanylate cyclases. MBio 1.
66. Wang WB, Chen IC, Jiang SS, Chen HR, Hsu CY, et al. (2008) Role of RppA in the regulation of polymyxin b susceptibility, swarming, and virulence factor expression in Proteus mirabilis. Infect Immun 76: 2051-2062.
67. Clemmer KM, Rather PN (2008) The Lon protease regulates swarming motility and virulence gene expression in Proteus mirabilis. J Med Microbiol 57: 931- 937.
68. Liaw SJ, Lai HC, Ho SW, Luh KT, Wang WB (2001) Characterisation of pnitrophenylglycerol- resistant Proteus mirabilis super-swarming mutants. J Med Microbiol 50: 1039-1048.
69. Belas R, Schneider R, Melch M (1998) Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriol 180: 6126-6139.
70. Li B, Li N, Wang F, Guo L, Huang Y, et al. (2012) Structural insight of a concentration-dependent mechanism by which YdiV inhibits Escherichia coli flagellum biogenesis and motility. Nucleic Acids Res 40: 11073-11085.
71. Takaya A, Erhardt M, Karata K, Winterberg K, Yamamoto T, et al. (2012) YdiV: A dual function protein that targets FlhDC for ClpXP-dependent degradation by promoting release of DNA-bound FlhDC complex. Mol Microbiol 83: 1268-1284.
72. Wada T, Morizane T, Abo T, Tominaga A, Inoue-Tanaka K, et al. (2011) EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica Serovar Typhimurium. J Bacteriol 193: 1600-1611.
73. Simms AN, Mobley HL (2008) Multiple genes repress motility in uropathogenic Escherichia coli constitutively expressing type 1 fimbriae. J Bacteriol 190: 3747- 3756.
74. Simm R, Remminghorst U, Ahmad I, Zakikhany K, Romling U (2009) A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium. J Bacteriol 191: 3928- 3937.
75. Miller SI, Kukral AM, Mekalanos JJ (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 86: 5054-5058.
76. Groisman EA, Chiao E, Lipps CJ, Heffron F (1989) Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci U S A 86: 7077-7081.
77. Brinkman FS, Macfarlane EL, Warrener P, Hancock RE (2001) Evolutionary relationships among virulence-associated histidine kinases. Infect Immun 69: 5207-5211.
78. Alteri CJ, Lindner JR, Reiss DJ, Smith SN, Mobley HL (2011) The broadly conserved regulator PhoP links pathogen virulence and membrane potential in Escherichia coli. Mol Microbiol 82: 145-163.
79. Derzelle S, Turlin E, Duchaud E, Pages S, Kunst F, et al. (2004) The PhoPPhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186: 1270-1279.
80. Stewart MK, Cummings LA, Johnson ML, Berezow AB, Cookson BT (2011) Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. Proc Natl Acad Sci U S A 108: 20742-20747.
81. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, et al. (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.
82. Ledeboer NA, Frye JG, McClelland M, Jones BD (2006) Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect Immun 74: 3156-3169.
83. Yeh KS, Hancox LS, Clegg S (1995) Construction and characterization of a fimZ mutant of Salmonella typhimurium. J Bacteriol 177: 6861-6865.
84. Yeh KS, Tinker JK, Clegg S (2002) FimZ binds the Salmonella typhimurium fimA promoter region and may regulate its own expression with FimY. Microbiol Immunol 46: 1-10.