Chapter 8 : Metabolites as Intercellular Signals for Regulation of Community-Level Traits

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Metabolites as Intercellular Signals for Regulation of Community-Level Traits, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815578/9781555814045_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555815578/9781555814045_Chap08-2.gif


This chapter describes work on new and emerging systems that describe roles for excreted cellular metabolites as intercellular signals. The therapeutic value of antibiotics is unquestionable; however, understanding the biological role of these compounds in natural settings may not be as intuitive as the definition of antibiotics would suggest. Increases in biofilm formation were correlated with a 10-fold increase in expression of the operon upon treatment with antibiotic. The internal concentration of polyamines is tightly regulated through a combination of biosynthesis, transport, and excretion. In , putrescine is synthesized either by decarboxylation of L-ornithine or decarboxylation of Larginine followed by removal of a urea molecule. is known to make and excrete both monorhamnolipids (mono-RHLs) and dirhamnolipids (di-RHLs), which have either one or two attached rhamnose groups, respectively. In , indole is imported from the extracellular environment predominantly by the Mtr permease whereas efflux of indole out of the cell is performed by the AcrEF pump. The chapter provides evidence that supports the role of various metabolites in the regulation of community-level traits, such as biofilm formation, swarming, and filamentation.

Citation: Monds R, O’Toole G. 2008. Metabolites as Intercellular Signals for Regulation of Community-Level Traits, p 105-129. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch8
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Achike, F. I.,, and C. Y. Kwan. 2003. Nitric oxide, human diseases and the herbal products that affect the nitric oxide signaling pathway. Clin. Exp. Pharmacol. Physiol. 30: 605615.
2. Aleshin, V. V.,, N. P. Zakataeva, and, V. A. Livshits. 1999. A new family of amino acid-efflux proteins. Trends Biochem. Sci. 24: 133135.
3. Baca-DeLancey, R. R.,, M. M. South,, X. Ding, and, P. N. Rather. 1999. Escherichia coli genes regulated by cell-to-cell signaling. Proc. Natl. Acad. Sci. USA 96: 46104614.
4. Bader, M. W.,, S. Sanowar,, M. E. Daley,, A. R. Schneider,, U. Cho,, W. Xu,, R. E. Klevit,, H. Le Moual, and, S. I. Miller. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122: 461472.
5. Barraud, N.,, D. J. Hassett,, S. H. Hwang,, S. A. Rice,, S. Kjelleberg, and, J. S. Webb. 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188: 73447353.
6. Boles, B. R.,, M. Thoendel, and, P. K. Singh. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57: 12101223.
7. Bomchil, N.,, P. Watnick, and, R. Kolter. 2003. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J. Bacteriol. 185: 13841390.
8. Boon, E. M.,, J. H. Davis,, R. Tran,, D. S. Karow,, S. H. Huang,, D. Pan,, M. M. Miazgowicz,, R. A. Mathies, and, M. A. Marletta. 2006. Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta1 H-NOX domain. J. Biol. Chem. 281: 2189221902.
9. Boon, E. M.,, and M. A. Marletta. 2005. Ligand specificity of H-NOX domains: from sGC to bacterial NO sensors. J. Inorg. Biochem. 99: 892902.
10. Boucher, R. C. 2004. New concepts of the pathogenesis of cystic fibrosis lung disease. Eur. Respir. J. 23: 146158.
11. Bredt, D. S. 1999. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 31: 577596.
12. Burkovski, A.,, and R. Kramer. 2002. Bacterial amino acid transport proteins: occurrence, functions, and significance for biotechnological applications. Appl. Microbiol. Biotechnol. 58: 265274.
13. Caiazza, N. C.,, and G. A. O’Toole. 2004. SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J. Bacteriol. 186: 44764485.
14. Caiazza, N. C.,, R. M. Shanks, and, G. A. O’Toole. 2005. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J. Bacteriol. 187: 73517361.
15. Camilli, A.,, and B. L. Bassler. 2006. Bacterial small-molecule signaling pathways. Science 311: 11131116.
16. Chant, E. L.,, and D. K. Summers. 2007. Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol. Microbiol. 63: 3543.
17. Chen, X.,, S. Schauder,, N. Potier,, A. Van Dorsselaer,, I. Pelczer,, B. L. Bassler, and, F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545549.
18. Costacurta, A.,, and J. Vanderleyden. 1995. Synthesis of phytohormones by plant-associated bacteria. Crit. Rev. Microbiol. 21: 118.
19. Danhorn, T.,, M. Hentzer,, M. Givskov,, M. R. Parsek, and, C. Fuqua. 2004. Phosphorus limitation enhances biofilm formation of the plant pathogen Agrobacterium tumefaciens through the PhoR-PhoB regulatory system. J. Bacteriol. 186: 44924501.
20. Daniels, R.,, S. Reynaert,, H. Hoekstra,, C. Verreth,, J. Janssens,, K. Braeken,, M. Fauvart,, S. Beullens,, C. Heusdens,, I. Lambrichts,, D. E. De Vos,, J. Vanderleyden,, J. Vermant, and, J. Michiels. 2006. Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli. Proc. Natl. Acad. Sci. USA 103: 1496514970.
21. Davey, M. E.,, N. C. Caiazza, and, G. A. O’Toole. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185: 10271036.
22. Davies, J.,, G. B. Spiegelman, and, G. Yim. 2006. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9: 445453.
23. Deziel, E.,, F. Lepine,, S. Milot, and, R. Villemur. 2005. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149: 20052013.
24. Dietrich, L. E.,, A. Price-Whelan,, A. Petersen,, M. Whiteley, and, D. K. Newman. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61: 13081321.
25. Di Martino, P.,, R. Fursy,, L. Bret,, B. Sundararaju, and, R. S. Phillips. 2003. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can. J. Microbiol. 49: 443449.
26. Di Martino, P.,, A. Merieau,, R. Phillips,, N. Orange, and, C. Hulen. 2002. Isolation of an Escherichia coli strain mutant unable to form biofilm on polystyrene and to adhere to human pneumocyte cells: involvement of tryptophanase. Can. J. Microbiol. 48: 132137.
27. Domka, J.,, J. Lee,, T. Bansal, and, T. Wood. 2007. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ. Microbiol. 9: 332346.
28. Domka, J.,, J. Lee, and, T. K. Wood. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72: 24492459.
29. Dorel, C.,, P. Lejeune, and, A. Rodrigue. 2006. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res. Microbiol. 157: 306314.
30. Eggeling, L.,, and H. Sahm. 2003. New ubiquitous translocators: amino acid export by Corynebacterium glutamicum and Escherichia coli. Arch. Microbiol. 180: 155160.
31. Franke, I.,, A. Resch,, T. Dassler,, T. Maier, and, A. Bock. 2003. YfiK from Escherichia coli promotes export of O-acetylserine and cysteine. J. Bacteriol. 185: 11611166.
32. Fuqua, C.,, M. R. Parsek, and, E. P. Greenberg. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35: 439468.
33. Goh, E. B.,, G. Yim,, W. Tsui,, J. McClure,, M. G. Surette, and, J. Davies. 2002. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl. Acad. Sci. USA 99: 1702517030.
34. Gotz, F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43: 13671378.
35. Halim, V. A.,, A. Vess,, D. Scheel, and, S. Rosahl. 2006. The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol. 8: 307313.
36. Hamana, K.,, and S. Matsuzaki. 1985. Further study on polyamines in primitive unicellular eukaryotic algae. J. Biochem. 97: 13111315.
37. Hamana, K.,, T. Tanaka,, R. Hosoya,, M. Niitsu, and, T. Itoh. 2003. Cellular polyamines of the acidophilic, thermophilic and thermoacidophilic archaebacteria, Acidilobus, Ferroplasma, Pyrobaculum, Pyrococcus, Staphylothermus, Thermococcus, Thermodiscus and Vulcanisaeta. J. Gen. Appl. Microbiol. 49: 287293.
38. Hanzelka, B. L.,, and E. P. Greenberg. 1996. Quorum sensing in Vibrio fischeri: evidence that Sadenosylmethionine is the amino acid substrate for autoinducer synthesis. J. Bacteriol. 178: 52915294.
39. Hauser, G.,, and M. L. Karnovsky. 1957. Rhamnose and rhamnolipide biosynthesis by Pseudomonas aeruginosa. J. Biol. Chem. 224: 91105.
40. Heilmann, C.,, O. Schweitzer,, C. Gerke,, N. Vanittanakom,, D. Mack, and, F. Gotz. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20: 10831091.
41. Hoffman, L. R.,, D. A. D’Argenio,, M. J. MacCoss,, Z. Zhang,, R. A. Jones, and, S. I. Miller. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436: 11711175.
42. Igarashi, K.,, K. Ito, and, K. Kashiwagi. 2001. Polyamine uptake systems in Escherichia coli. Res. Microbiol. 152: 271278.
43. Igarashi, K.,, and K. Kashiwagi. 1999. Polyamine transport in bacteria and yeast. Biochem. J. 3: 633642.
44. Jarvis, F. G.,, and M. J. Johnson. 1949. A glycolipid produced by Pseudomonas aeruginosa. J. Am. Chem. Soc. 71: 41244126.
45. Karatan, E.,, T. R. Duncan, and, P. I. Watnick. 2005. NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J. Bacteriol. 187: 74347443.
46. Kashiwagi, K.,, S. Shibuya,, H. Tomitori,, A. Kuraishi, and, K. Igarashi. 1997. Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J. Biol. Chem. 272: 63186323.
47. Kawamura-Sato, K.,, K. Shibayama,, T. Horii,, Y. Iimuma,, Y. Arakawa, and, M. Ohta. 1999. Role of multiple efflux pumps in Escherichia coli in indole expulsion. FEMS Microbiol. Lett. 179: 345352.
48. Keller, L.,, and M. G. Surette. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4: 249258.
49. Klessig, D. F.,, J. Durner,, R. Noad,, D. A. Navarre,, D. Wendehenne,, D. Kumar,, J. M. Zhou,, J. Shah,, S. Zhang,, P. Kachroo,, Y. Trifa,, D. Pontier,, E. Lam, and, H. Silva. 2000. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA 97: 88498855.
50. Kohler, T.,, L. K. Curty,, F. Barja,, C. van Delden, and, J. C. Pechere. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182: 59905996.
51. Kutukova, E. A.,, V. A. Livshits,, I. P. Altman,, L. R. Ptitsyn,, M. H. Zyiatdinov,, I. L. Tokmakova, and, N. P. Zakataeva. 2005. The yeaS ( leuE) gene of Escherichia coli encodes an exporter of leucine, and the Lrp protein regulates its expression. FEBS Lett. 579: 46294634.
52. Lang, S.,, and D. Wullbrandt. 1999. Rhamnose lipids—biosynthesis, microbial production and application potential. Appl. Microbiol. Biotechnol. 51: 2232.
53. Langman, L. J.,, and B. M. Kapur. 2006. Toxicology: then and now. Clin. Biochem. 39: 498510.
54. Lau, G.,, D. Hassett,, H. Ran, and, F. Kong. 2004. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10: 599606.
55. Lee, J.,, A. Jayaraman, and, T. K. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7: 42.
56. Linares, J.,, I. Gustafsson,, F. Baquero, and, J. Martinez. 2006. Antibiotics as intermicrobial signaling agents instead of weapons. Proc. Natl. Acad. Sci. USA 103: 1948419489.
57. Livshits, V. A.,, N. P. Zakataeva,, V. V. Aleshin, and, M. V. Vitushkina. 2003. Identification and characterization of the new gene rhtA involved in threonine and homoserine efflux in Escherichia coli. Res. Microbiol. 154: 123135.
58. Lu, C. D.,, Y. Itoh,, Y. Nakada, and, Y. Jiang. 2002. Functional analysis and regulation of the divergent spuABCDEFGH-spuI operons for polyamine uptake and utilization in Pseudomonas aeruginosa PAO1. J. Bacteriol. 184: 37653773.
59. Madhani, H. D.,, and G. R. Fink. 1998. The control of filamentous differentiation and virulence in fungi. Trends Cell Biol. 8: 348353.
60. Maier, R. M.,, and G. Soberon-Chavez. 2000. Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl. Microbiol. Biotechnol. 54: 625633.
61. Matsui, H.,, V. E. Wagner,, D. B. Hill,, U. E. Schwab,, T. D. Rogers,, B. Button,, R. M. Taylor II,, R. Superfine,, M. Rubinstein,, B. H. Iglewski, and, R. C. Boucher. 2006. A physical linkage between cystic fibrosis airway surface dehydration and Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. USA 103: 1813118136.
62. Mavrodi, D.,, W. Blankenfeldt, and, L. Thomashow. 2006. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 44: 417445.
63. Monds, R. D.,, P. D. Newell,, R. H. Gross, and, G. A. O’Toole. 2007. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63: 656679.
64. Monds, R. D.,, P. D. Newell,, J. A. Schwartzman, and, A. O’Toole G. 2006. Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl. Environ. Microbiol. 72: 19101924.
65. Monds, R. D.,, M. W. Silby, and, H. K. Mahanty. 2001. Expression of the Pho regulon negatively regulates biofilm formation by Pseudomonas aureofaciens PA147–2. Mol. Microbiol. 42: 415426.
66. Navarro, L.,, P. Dunoyer,, F. Jay,, B. Arnold,, N. Dharmasiri,, M. Estelle,, O. Voinnet, and, J. D. Jones. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436439.
67. Ochsner, U. A.,, A. Fiechter, and, J. Reiser. 1994. Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J. Biol. Chem. 269: 1978719795.
68. Ochsner, U. A.,, T. Hembach, and, A. Fiechter. 1996. Production of rhamnolipid biosurfactants. Adv. Biochem. Eng. Biotechnol. 53: 89118.
69. Otto, K.,, and T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99: 22872292.
70. Patel, C. N.,, B. W. Wortham,, J. L. Lines,, J. D. Fetherston,, R. D. Perry, and, M. A. Oliveira. 2006. Polyamines are essential for the formation of plague biofilm. J. Bacteriol. 188: 23552363.
71. Patten, C. L.,, and B. R. Glick. 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 42: 207220.
72. Patten, C. L.,, and B. R. Glick. 2002. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 68: 37953801.
73. Price-Whelan, A.,, L. E. Dietrich, and, D. K. Newman. 2006. Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2: 7178.
74. Prithiviraj, B.,, H. P. Bais,, T. Weir,, B. Suresh,, E. H. Najarro,, B. V. Dayakar,, H. P. Schweizer, and, J. M. Vivanco. 2005. Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect. Immun. 73: 53195328.
75. Prusty, R.,, P. Grisafi, and, G. R. Fink. 2004. The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101: 41534157.
76. Rachid, S.,, K. Ohlsen,, W. Witte,, J. Hacker, and, W. Ziebuhr. 2000. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob. Agents Chemother. 44: 33573363.
77. Rahim, R.,, U. A. Ochsner,, C. Olvera,, M. Graninger,, P. Messner,, J. S. Lam, and, G. Soberon-Chavez. 2001. Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol. Microbiol. 40: 708718.
78. Rahme, L. G.,, F. M. Ausubel,, H. Cao,, E. Drenkard,, B. C. Goumnerov,, G. W. Lau,, S. Mahajan-Miklos,, J. Plotnikova,, M. W. Tan,, J. Tsongalis,, C. L. Walendziewicz, and, R. G. Tompkins. 2000. Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. USA 97: 88158821.
79. Rather, P. N. 2005. Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol. 7: 10651073.
80. Romling, U.,, M. Gomelsky, and, M. Y. Galperin. 2005. C-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57: 629639.
81. Ruiz, N.,, and T. J. Silhavy. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8: 122126.
82. Sanchez-Martinez, C.,, and J. Perez-Martin. 2001. Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis—similar inputs, different outputs. Curr. Opin. Microbiol. 4: 214221.
83. Shah, J. 2003. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6: 365371.
84. Soksawatmaekhin, W.,, A. Kuraishi,, K. Sakata,, K. Kashiwagi, and, K. Igarashi. 2004. Excretion and uptake of cadaverine by CadB and its physiological functions in Escherichia coli. Mol. Microbiol. 51: 14011412.
85. Sturgill, G.,, and P. N. Rather. 2004. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol. Microbiol. 51: 437446.
86. Sturgill, G.,, C. M. Toutain,, J. Komperda,, G. A. O’Toole, and, P. N. Rather. 2004. Role of CysE in production of an extracellular signaling molecule in Providencia stuartii and Escherichia coli: loss of CysE enhances biofilm formation in Escherichia coli. J. Bacteriol. 186: 76107617.
87. Surette, M. G.,, M. B. Miller, and, B. L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. USA 96: 16391644.
88. Tabor, C. W.,, and H. Tabor. 1985. Polyamines in microorganisms. Microbiol. Rev. 49: 8199.
89. Theunis, M.,, H. Kobayashi,, W. J. Broughton, and, E. Prinsen. 2004. Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol. Plant Microbe Interact. 17: 11531161.
90. Toutain, C. M.,, M. E. Zegans, and, G. A. O’Toole. 2005. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J. Bacteriol. 187: 771777.
91. Vrljic, M.,, H. Sahm, and, L. Eggeling. 1996. A new type of transporter with a new type of cellular function: l-lysine export from Corynebacterium glutamicum. Mol. Microbiol. 22: 815826.
92. Walker, T. S.,, H. P. Bais,, E. Deziel,, H. P. Schweizer,, L. G. Rahme,, R. Fall, and, J. M. Vivanco. 2004. Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol. 134: 320331.
93. Wang, D.,, X. Ding, and, P. N. Rather. 2001. Indole can act as an extracellular signal in Escherichia coli. J. Bacteriol. 183: 42104216.
94. Waters, C. M.,, and B. L. Bassler. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319346.
95. Werner, E.,, F. Roe,, A. Bugnicourt,, M. J. Franklin,, A. Heydorn,, S. Molin,, B. Pitts, and, P. S. Stewart. 2004. Stratified growth in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 70: 61886196.
96. Winzer, K.,, K. R. Hardie, and, P. Williams. 2002. Bacterial cell-to-cell communication: sorry, can’t talk now—gone to lunch! Curr. Opin. Microbiol. 5: 216222.
97. Yamamoto, S.,, M. A. Chowdhury,, M. Kuroda,, T. Nakano,, Y. Koumoto, and, S. Shinoda. 1991. Further study on polyamine compositions in Vibrionaceae. Can. J. Microbiol. 37: 148153.
98. Yanofsky, C.,, V. Horn, and, P. Gollnick. 1991. Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J. Bacteriol. 173: 60096017.
99. Yim, G.,, H. H. Wang, and, J. Davies. 2006. The truth about antibiotics. Int. J. Med. Microbiol. 296: 163170.
100. Yoon, S. S.,, R. F. Hennigan,, G. M. Hilliard,, U. A. Ochsner,, K. Parvatiyar,, M. C. Kamani,, H. L. Allen,, T. R. DeKievit,, P. R. Gardner,, U. Schwab,, J. J. Rowe,, B. H. Iglewski,, T. R. McDermott,, R. P. Mason,, D. J. Wozniak,, R. E. Hancock,, M. R. Parsek,, T. L. Noah,, R. C. Boucher, and, D. J. Hassett. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3: 593603.
101. Yoshida, M.,, K. Kashiwagi,, A. Shigemasa,, S. Taniguchi,, K. Yamamoto,, H. Makinoshima,, A. Ishihama, and, K. Igarashi. 2004. A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J. Biol. Chem. 279: 4600846013.
102. Zakataeva, N. P.,, V. V. Aleshin,, I. L. Tokmakova,, P. V. Troshin, and, V. A. Livshits. 1999. The novel transmembrane Escherichia coli proteins involved in the amino acid efflux. FEBS Lett. 452: 228232.
103. Zakataeva, N. P.,, E. A. Kutukova,, S. V. Gronski,, P. V. Troshin,, V. A. Livshits, and, V. V. Aleshin. 2006. Export of metabolites by the proteins of the DMT and RhtB families and its possible role in intercellular communication. Mikrobiologiia 75: 509520.
104. Zhang, X. S.,, R. Garcia-Contreras, and, T. K. Wood. 2007 . YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J. Bacteriol. 189: 30513062.
105. Zumft, W. G. 2004. Denitrification by pseudomonads: control and assemply processes, p. 193–227. In J. L. Ramos (ed.), Pseudomonas, vol. 3. Kluwer Academic/Plenum Publishers, New York, NY.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error