Indole negatively impacts predation by Bdellovibrio bacteriovorus and its release from the bdelloplast

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 1009-1022

  Dwidar, Mohammed ^a   Nam, Dougu ^a   Mitchell, Robert J ^a  

^a Ulsan National Institute of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); BDELLOVIBRIO BACTERIOVORUS; ESCHERICHIA; NEGIBACTERIA; SALMONELLA;

ANTIINFECTIVE AGENT; INDOLE; INDOLE DERIVATIVE;

BDELLOVIBRIO; DOWN REGULATION; DRUG EFFECTS; ESCHERICHIA COLI; FLAGELLUM; GENETICS; METABOLISM; PATHOGENICITY; RIBOSOME; VIROLOGY;

ANTI-BACTERIAL AGENTS; BDELLOVIBRIO; DOWN-REGULATION; ESCHERICHIA COLI; FLAGELLA; INDOLES; RIBOSOMES;

EID: 84926418600     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12463     Document Type: Article

References (41)

1. Afonina, I., Ankoudinova, I., Mills, A., Lokhov, S., Huynh, P., and Mahoney, W. (2007) Primers with 5′ flaps improve real-time PCR. Biotechniques 43: 770-774.
2. Atterbury, R.J., Hobley, L., Till, R., Lambert, C., Capeness, M.J., Lerner, T.R., etal. (2011) Effects of orally administered Bdellovibrio bacteriovorus on the well-being and Salmonella colonization of young chicks. Appl Environ Microbiol 77: 5794-5803.
3. Bansal, T., Englert, D., Lee, J., Hegde, M., Wood, T.K., and Jayaraman, A. (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157: H7 chemotaxis, colonization, and gene expression. Infect Immun 75: 4597-4607.
4. Bansal, T., Alaniz, R.C., Wood, T.K., and Jayaraman, A. (2010) The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci USA 107: 228-233.
5. Chant, E.L., and Summers, D.K. (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 63: 35-43.
6. Chu, W.H., Zere, T.R., Weber, M.M., Wood, T.K., Whiteley, M., Hidalgo-Romano, B., etal. (2012) Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl Environ Microbiol 78: 411-419.
7. Dashiff, A., and Kadouri, D.E. (2011) Predation of oral pathogens by Bdellovibrio bacteriovorus 109J. Mol Oral Microbiol 26: 19-34.
8. Dashiff, A., Junka, R.A., Libera, M., and Kadouri, D.E. (2011) Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. J Appl Microbiol 110: 431-444.
9. Domka, J., Lee, J., and Wood, T.K. (2006) YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol 72: 2449-2459.
10. Dwidar, M., Monnappa, A.K., and Mitchell, R.J. (2012a) The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus. BMB Rep 45: 71-78.
11. Dwidar, M., Hong, S., Cha, M., Jang, J., and Mitchell, R.J. (2012b) Combined application of bacterial predation and carbon dioxide aerosols to effectively remove biofilms. Biofouling 28: 671-680.
12. Dwidar, M., Leung, B.M., Yaguchi, T., Takayama, S., and Mitchell, R.J. (2013) Patterning bacterial communities on epithelial cells. PLoS ONE 8: e67165.
13. Engelking, H.M., and Seidler, R.J. (1974) The involvement of extracellular enzymes in the metabolism of Bdellovibrio. Arch Mikrobiol 95: 293-304.
14. Flannagan, R.S., Valvano, M.A., and Koval, S.F. (2004) Downregulation of the motA gene delays the escape of the obligate predator Bdellovibrio bacteriovorus 109J from bdelloplasts of bacterial prey cells. Microbiology 150: 649-656.
15. Fratamico, P.M., and Cooke, P.H. (1996) Isolation of Bdellovibrios that prey on Escherichia coli O157:H7 and Salmonella species and application for removal of prey from stainless steel surfaces. J Food Saf 16: 161-173.
16. Han, T.H., Lee, J.H., Cho, M.H., Wood, T.K., and Lee, J. (2011) Environmental factors affecting indole production in Escherichia coli. Res Microbiol 162: 108-116.
17. Hirakawa, H., Inazumi, Y., Masaki, T., Hirata, T., and Yamaguchi, A. (2005) Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55: 1113-1126.
18. Hong, F.X., Breitling, R., McEntee, C.W., Wittner, B.S., Nemhauser, J.L., and Chory, J. (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827.
19. Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
20. Iebba, V., Santangelo, F., Totino, V., Nicoletti, M., Gagliardi, A., De Biase, R.V., etal. (2013) Higher prevalence and abundance of Bdellovibrio bacteriovorus in the human gut of healthy subjects. PLoS ONE 8: e61608.
21. Kadouri, D., and O'Toole, G.A. (2005) Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 71: 4044-4051.
22. Kadouri, D.E., To, K., Shanks, R.M., and Doi, Y. (2013) Predatory bacteria: a potential ally against multidrug-resistant Gram-negative pathogens. PLoS ONE 8: e63397.
23. Karlin, D.A., Mastromarino, A.J., Jones, R.D., Stroehlein, J.R., and Lorentz, O. (1985) Fecal skatole and indole and breath methane and hydrogen in patients with large bowel polyps or cancer. J Cancer Res Clin Oncol 109: 135-141.
24. Kim, E.H., Dwidar, M., Mitchell, R.J., and Kwon, Y.N. (2013) Assessing the effects of bacterial predation on membrane biofouling. Water Res 16: 6024-6032.
25. Lambert, C., Evans, K.J., Till, R., Hobley, L., Capeness, M., Rendulic, S., etal. (2006) Characterizing the flagellar filament and the role of motility in bacterial prey penetration by Bdellovibrio bacteriovorus. Mol Microbiol 60: 274-286.
26. Lee, J.H., and Lee, J. (2010) Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34: 426-444.
27. Lee, J.T., Jayaraman, A., and Wood, T.K. (2007) Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7: 42.
28. Monnappa, A.K., Dwidar, M., and Mitchell, R.J. (2013) Application of bacterial predation to mitigate recombinant bacterial populations and their DNA. Soil Biol Biochem 57: 427-435.
29. Morehouse, K.A., Hobley, L., Capeness, M., and Sockett, R.E. (2011) Three motAB stator gene products in Bdellovibrio bacteriovorus contribute to motility of a single flagellum during predatory and prey-independent growth. J Bacteriol 193: 932-943.
30. Park, S., Kim, D., Mitchell, R.J., and Kim, T. (2011) A microfluidic concentrator array for quantitative predation assays of predatory microbes. Lab Chip 11: 2916-2923.
31. Schwudke, D., Linscheid, M., Strauch, E., Appel, B., Zahringer, U., Moll, H., etal. (2003) The obligate predatory Bdellovibrio bacteriovorus possesses a neutral lipid A containing alpha-D-Mannoses that replace phosphate residues: similarities and differences between the lipid As and the lipopolysaccharides of the wild type strain B.bacteriovorus HD100 and its host-independent derivative HI100. J Biol Chem 278: 27502-27512.
32. Sockett, R.E., and Lambert, C. (2004) Bdellovibrio as therapeutic agents: a predatory renaissance? Nat Rev Microbiol 2: 669-675.
33. Stolp, H., and Starr, M.P. (1963) Bdellovibrio Bacteriovorus gen. et sp. n., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29: 217-248.
34. Thomashow, M.F., and Cotter, T.W. (1992) Bdellovibrio host dependence - the search for signal molecules and genes that regulate the intraperiplasmic growth-cycle. J Bacteriol 174: 5767-5771.
35. Tomlin, K.L., Clark, S.R.D., and Ceri, H. (2004) Green and red fluorescent protein vectors for use in biofilm studies of the intrinsically resistant Burkholderia cepacia complex. J Microbiol Methods 57: 95-106.
36. Untergasser, A. (2008) RNAprep - Trizol combined with Columns [WWW document]. URL http://www.untergasser.de/lab/protocols/rna_prep_comb_trizol_v1_0.htm.
37. Vega, N.M., Allison, K.R., Samuels, A.N., Klempner, M.S., and Collins, J.J. (2013) Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. Proc Natl Acad Sci USA 110: 14420-14425.
38. Verklova, Z.S. (1973) Study of the virulence, toxicity and immunogenicity of different strains of Bdellovibrio bacteriovorus. Gig Sanit 38: 10-13.
39. Westergaard, J.M., and Kramer, T.T. (1977) Bdellovibrio and intestinal flora of vertebrates. Appl Environ Microbiol 34: 506-511.
40. Wood, T.K., Hong, S.H., and Ma, Q. (2011) Engineering biofilm formation and dispersal. Trends Biotechnol 29: 87-94.
41. Zuccato, E., Venturi, M., Dileo, G., Colombo, L., Bertolo, C., Doldi, S.B., and Mussini, E. (1993) Role of bile-acids and metabolic-activity of colonic bacteria in increased risk of colon cancer after cholecystectomy. Dig Dis Sci 38: 514-519.