The microbiota metabolite indole inhibits Salmonella virulence: Involvement of the PhoPQ two-component system

PLoS ONE

Volumn 13, Issue 1, 2018, Pages

  Kohli, Nandita ^a   Crisp, Zeni ^b   Riordan, Rebekah ^b   Li, Michael ^a   Alaniz, Robert C ^b   Jayaraman, Arul ^a,b  

^a Department of Electrical and Computer Engineering   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR GEL ELECTROPHORESIS; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL INVASION; CELL MOTILITY; CELL SURVIVAL; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; COORDINATION; DNA FRAGMENTATION; DOWN REGULATION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIUM CELL; ESCHERICHIA COLI O157; FEMALE; HOST CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPHOID CELL; MACROPHAGE; MESENTERY LYMPH NODE; MICROBIAL COMMUNITY; MICROENVIRONMENT; MICROFLORA; MOUSE; NEUROMODULATION; NONHUMAN; PLASMID; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TYPE III SECRETION SYSTEM; ANIMAL; CELL LINE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; METABOLISM; PATHOGENICITY; VIRULENCE;

BACTERIAL PROTEIN; INDOLE DERIVATIVE;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; INDOLES; MICE; MICROBIOTA; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 85040713985     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0190613     Document Type: Article

References (54)

1. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013; 13(11):790–801. https://doi.org/10.1038/nri3535 PMID: 24096337
2. Lawley TD, Walker AW. Intestinal colonization resistance. Immunology. 2013; 138(1):1–11. https://doi.org/10.1111/j.1365-2567.2012.03616.x PMID: 23240815
3. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk L-v. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond). 1971; 69(3):405–11.
4. Freter R, Brickner H, Botney M, Cleven D, Aranki A. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun. 1983; 39(2):676–85. PMID: 6339388
5. Wilson KH, Perini F. Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect Immun. 1988; 56(10):2610–4. PMID: 3417352
6. Bernet MF, Brassart D, Neeser JR, Servin AL. Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut. 1994; 35(4):483–9. PMID: 8174985
7. Lee YK, Puong KY, Ouwehand AC, Salminen S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J Med Microbiol. 2003; 52(Pt 10):925–30. https://doi.org/10.1099/jmm.0.05009-0 PMID: 12972590
8. Dabard J, Bridonneau C, Phillipe C, Anglade P, Molle D, Nardi M, et al. Ruminococcin A, a new lantibiotic produced by a Ruminococcus gnavus strain isolated from human feces. Appl Environ Microbiol. 2001; 67(9):4111–8. https://doi.org/10.1128/AEM.67.9.4111-4118.2001 PMID: 11526013
9. Gong HS, Meng XC, Wang H. Mode of action of plantaricin MG, a bacteriocin active against Salmonella typhimurium. J Basic Microbiol. 2010; 50 Suppl 1:S37–45. https://doi.org/10.1002/jobm.201000130PMID: 20967788
10. Rea MC, Sit CS, Clayton E, O’Connor PM, Whittal RM, Zheng J, et al. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci U S A. 2010; 107(20):9352–7. https://doi.org/10.1073/pnas.0913554107 PMID: 20435915
11. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, et al. Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol. 2006; 72 (1):946–9. https://doi.org/10.1128/AEM.72.1.946-949.2006 PMID: 16391141
12. Van Deun K, Pasmans F, Van Immerseel F, Ducatelle R, Haesebrouck F. Butyrate protects Caco-2 cells from Campylobacter jejuni invasion and translocation. Br J Nutr. 2008; 100(3):480–4. https://doi.org/10.1017/S0007114508921693 PMID: 18275629
13. Hung CC, Garner CD, Slauch JM, Dwyer ZW, Lawhon SD, Frye JG, et al. The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD. Mol Microbiol. 2013; 87 (5):1045–60. https://doi.org/10.1111/mmi.12149 PMID: 23289537
14. Stecher B, Hardt WD. Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol. 2011; 14(1):82–91. https://doi.org/10.1016/j.mib.2010.10.003 PMID: 21036098
15. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun. 2008; 76(10):4726–36. https://doi.org/10.1128/IAI.00319-08 PMID: 18678663
16. Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun. 2005; 73(6):3228–41. https://doi.org/10.1128/IAI.73.6.3228-3241.2005 PMID: 15908347
17. Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 2001; 3(7):549–59. PMID: 11418329
18. Haraga A, Ohlson MB, Miller SI. Salmonellae interplay with host cells. Nature Reviews Microbiol. 2008; 6(1):53–66.
19. Sun Y, O’Riordan MX. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv Appl Microbiol. 2013; 85:93–118. https://doi.org/10.1016/B978-0-12-407672-3.00003-4 PMID: 23942149
20. Huang Y, Suyemoto M, Garner CD, Cicconi KM, Altier C. Formate acts as a diffusible signal to induce Salmonella invasion. J Bacteriol. 2008; 190(12):4233–41. https://doi.org/10.1128/JB.00205-08 PMID: 18424519
21. Lawhon SD, Maurer R, Suyemoto M, Altier C. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol. 2002; 46(5):1451–64. PMID: 12453229
22. Sridharan GV, Choi K, Klemashevich C, Wu C, Prabakaran D, Pan LB, et al. Prediction and quantification of bioactive microbiota metabolites in the mouse gut. Nat Commun. 2014; 5:5492. https://doi.org/10.1038/ncomms6492 PMID: 25411059
23. Bansal T, Englert D, Lee J, Hegde M, Wood TK, Jayaraman A. Differential effects of epinephrine, nor-epinephrine, and indole on Escherichia coli O157: H7 chemotaxis, colonization, and gene expression. Infect Immun. 2007; 75(9):4597–607. https://doi.org/10.1128/IAI.00630-07 PMID: 17591798
24. Oh S, Go GW, Mylonakis E, Kim Y. The bacterial signalling molecule indole attenuates the virulence of the fungal pathogen Candida albicans. J Appl Microbiol. 2012; 113(3):622–8. https://doi.org/10.1111/j.1365-2672.2012.05372.x PMID: 22726313
25. Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev. 2010; 34 (4):426–44. https://doi.org/10.1111/j.1574-6976.2009.00204.x PMID: 20070374
26. Vega NM, Allison KR, Samuels AN, Klempner MS, Collins JJ. Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. Proc Natl Acad Sci U S A. 2013; 110 (35):14420–5. https://doi.org/10.1073/pnas.1308085110 PMID: 23946425
27. Nikaido E, Yamaguchi A, Nishino K. AcrAB multidrug efflux pump regulation in Salmonella enterica serovar Typhimurium by RamA in response to environmental signals. J Biol Chem. 2008; 283(35):24245–53. https://doi.org/10.1074/jbc.M804544200 PMID: 18577510
28. Nikaido E, Giraud E, Baucheron S, Yamasaki S, Wiedemann A, Okamoto K, et al. Effects of indole on drug resistance and virulence of Salmonella enterica serovar Typhimurium revealed by genome-wide analyses. Gut Pathog. 2012; 4(1):5. https://doi.org/10.1186/1757-4749-4-5 PMID: 22632036
29. Bansal T, Alaniz RC, Wood TK, Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci U S A. 2010; 107 (1):228–33. https://doi.org/10.1073/pnas.0906112107 PMID: 19966295
30. Josenhans C, Suerbaum S. The role of motility as a virulence factor in bacteria. Int J Med Microbiol. 2002; 291(8):605–14. https://doi.org/10.1078/1438-4221-00173 PMID: 12008914
31. Miller SI, Mekalanos JJ. Constitutive expression of the PhoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol. 1990; 172(5):2485–90. PMID: 2185222
32. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987; 28(10):1221–7. PMID: 3678950
33. Argenzio RA, Southworth M. Sites of organic acid production and absorption in gastrointestinal tract of the pig. Am J Physiol. 1975; 228(2):454–60. https://doi.org/10.1152/ajplegacy.1975.228.2.454 PMID: 235219
34. Argenzio RA, Southworth M, Stevens CE. Sites of organic acid production and absorption in the equine gastrointestinal tract. Am J Physiol. 1974; 226(5):1043–50. https://doi.org/10.1152/ajplegacy.1974.226.5.1043 PMID: 4824856
35. Linden SK, Sheng YH, Every AL, Miles KM, Skoog EC, Florin TH, et al. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog. 2009; 5(10): e1000617. https://doi.org/10.1371/journal.ppat.1000617 PMID: 19816567
36. Snell EE. Tryptophanase: structure, catalytic activities, and mechanism of action. Adv Enzymol Relat Areas Mol Biol. 1975; 42:287–333. PMID: 236639
37. Whitt DD, Demoss RD. Effect of microflora on the free amino acid distribution in various regions of the mouse gastrointestinal tract. Appl Microbiol. 1975; 30(4):609–15. PMID: 1190761
38. Darkoh C, Chappell C, Gonzales C, Okhuysen P. A rapid and specific method for the detection of indole in complex biological samples. Appl Environ Microbiol. 2015; 81(23):8093–7. https://doi.org/10.1128/AEM.02787-15 PMID: 26386049
39. Kingsley RA, Humphries AD, Weening EH, De Zoete MR, Winter S, Papaconstantinopoulou A, et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun. 2003; 71(2):629–40. https://doi.org/10.1128/IAI.71.2.629-640.2003 PMID: 12540539
40. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Baumler AJ. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun. 2005; 73(6):3358–66. https://doi.org/10.1128/IAI.73.6.3358-3366.2005PMID: 15908362
41. Lostroh CP, Lee CA. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 2001; 3(14–15):1281–91. PMID: 11755416
42. Carter PB, Collins FM. The route of enteric infection in normal mice. J Exp Med. 1974; 139(5):1189–203. PMID: 4596512
43. Kanamaru K, Kanamaru K, Tatsuno I, Tobe T, Sasakawa C. SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol. 2000; 38(4):805–16. PMID: 11115115
44. Lee J, Jayaraman A, Wood TK. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 2007; 7:42. https://doi.org/10.1186/1471-2180-7-42 PMID: 17511876
45. Bajaj V, Lucas RL, Hwang C, Lee CA. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol. 1996; 22(4):703–14. PMID: 8951817
46. Groisman EA, Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol. 2006; 4(9):705–9. https://doi.org/10.1038/nrmicro1478 PMID: 16894339
47. Roediger WE. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut. 1980; 21(9):793–8. PMID: 7429343
48. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001; 81(3):1031–64. https://doi.org/10.1152/physrev.2001.81.3.1031 PMID: 11427691
49. Altier C, Suyemoto M, Lawhon SD. Regulation of Salmonella enterica Serovar Typhimurium Invasion Genes by csrA. Infect Immun. 2000; 68(12):6790–7. PMID: 11083797
50. Santiviago CA, Reynolds MM, Porwollik S, Choi SH, Long F, Andrews-Polymenis HL, et al. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog. 2009; 5(7):e1000477. https://doi.org/10.1371/journal.ppat.1000477PMID: 19578432
51. Bogomolnaya LM, Santiviago CA, Yang HJ, Baumler AJ, Andrews-Polymenis HL.’Form variation’ of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine. Mol Microbiol. 2008; 70(5):1105–19. https://doi.org/10.1111/j.1365-2958.2008.06461.x PMID: 18826410
52. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000; 97(12):6640–5. https://doi.org/10.1073/pnas. 120163297 PMID: 10829079
53. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, et al. Complete set of ORF clones of Escherichia coli ASKA library (A complete set of E. coli K-12 ORF archive): Unique resources for biological research. DNA Res. 2005; 12(5):291–9. https://doi.org/10.1093/dnares/dsi012PMID: 16769691
54. CT Method. Methods. 2001; 25(4):402–8. https://doi.org/10.1006/meth.2001.1262 PMID: 11846609