Chapter 20 : spp. in Microbial Populations and Communities: Molecular Interactions and Biological Importance

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spp. in Microbial Populations and Communities: Molecular Interactions and Biological Importance, Page 1 of 2

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This chapter emphasizes the underlying mechanisms that govern the physical and chemical interactions between organisms and their potential relevance to disease. Many biofilms within the host are not simply single species assemblages, but rather, dynamic polymicrobial communities. spp. in biofilms on medical devices are most often derived from the host’s own endogenous flora, and other microflora organisms, such as staphylococci, are also often associated with catheters in both the presence and absence of . Direct consequences of mixed infections could include enhancement of biofilm formation, antibiotic resistance or virulence factor production, or changes in immune responses or host tissues that result from simultaneous infection by bacteria and fungi. While frequently encounters large numbers of gram-positive bacteria in the oral, intestinal, and skin microfloras, a relatively small number of studies describe the molecular interactions that occur between and gram-positive microbes. A series of clinical trials have investigated the use of probiotics for the management of recurrent vulvovaginal candidiasis, and while the data are in conclusive, further in vitro and animal studies are warranted. Unicellular organisms often produce small, diffusible chemical signals, referred to as quorum-sensing molecules (QSMs), that coordinate group behavior within single-species populations.

Citation: Piispanen A, Hogan D. 2012. spp. in Microbial Populations and Communities: Molecular Interactions and Biological Importance, p 317-330. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch20

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Tumor Necrosis Factor alpha
Outer Membrane Protein A
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Relationships between and during infection in a murine model. (A) The presence of may modulate the host immune response, leading to decreased detection of (B) Alternatively, hyphae may promote increased colonization and dissemination. Dashed lines represent damage to the endothelial cells. doi:10.1128/9781555817176.ch20.f1

Citation: Piispanen A, Hogan D. 2012. spp. in Microbial Populations and Communities: Molecular Interactions and Biological Importance, p 317-330. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch20
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and -produced farnesol affects virulence in multiple ways. In biofilms, farnesol promotes upregulation of virulence factor production, particularly in LasR-defective strains, which are commonly observed in chronic lung infections associated with CF (left). When wild-type or LasR strains are at low densities, produced farnesol inhibits virulence factor production but may promote biofilm formation (right). doi:10.1128/9781555817176.ch20.f2

Citation: Piispanen A, Hogan D. 2012. spp. in Microbial Populations and Communities: Molecular Interactions and Biological Importance, p 317-330. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch20
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1. Aballay, A.,, P. Yorgey, and, F. M. Ausubel. 2000. Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr. Biol. 10: 15391542.
2. Adair, C. G.,, S. P. Gorman,, B. M. Feron,, L. M. Byers,, D. S. Jones,, C. E. Goldsmith,, J. E. Moore,, J. R. Kerr,, M. D. Curran,, G. Hogg,, C. H. Webb,, G. J. McCarthy, and, K. R. Milligan. 1999. Implications of endotracheal tube biofilm for ventilator-associated pneumonia. Intensive Care Med. 25: 10721076.
3. Adam, B.,, G. S. Baillie, and, L. J. Douglas. 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J. Med. Microbiol. 51: 344349.
4. Ahmad, S.,, Z. Khan,, A. S. Mustafa, and, Z. U. Khan. 2002. Seminested PCR for diagnosis of candidemia: comparison with culture, antigen detection, and biochemical methods for species identification. J. Clin. Microbiol. 40: 24832489.
5. Akagawa, G.,, S. Abe, and, H. Yamaguchi. 1995. Mortality of Candida albicans-infected mice is facilitated by superinfection of Escherichia coli or administration of its lipopolysaccharide. J. Infect. Dis. 171: 15391544.
6. Alem, M. A. S.,, M. D. Y. Oteef,, T. H. Flowers, and, L. J. Douglas. 2006. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot. Cell 5: 17701779.
7. Al-Fattani, M. A., and, L. J. Douglas. 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J. Med. Microbiol. 55: 9991008.
8. Al-Fattani, M. A., and, L. J. Douglas. 2004. Penetration of Candida biofilms by antifungal agents. Antimicrob. Agents Chemother. 48: 32913297.
9. Allard, J. B.,, L. Rinaldi,, M. J. Wargo,, G. Allen,, S. Akira,, S. Uematsu,, M. E. Poynter,, D. A. Hogan,, M. Rincon, and, L. A. Whittaker. 2009. Th2 allergic immune response to inhaled fungal antigens is modulated by TLR-4-independent bacterial products. Eur. J. Immunol. 39: 776788.
10. Alonso-Valle, H.,, O. Acha,, J. D. García-Palomo,, C. Fariñas-Álvarez,, C. Fernández-Mazarrasa, and, M. C. Fariñas. 2003. Candidemia in a tertiary care hospital: epidemiology and factors influencing mortality. Eur. J. Clin. Microbiol. Infect. Dis. 22: 254257.
11. Azoulay, E.,, J.-F. Timsit,, M. Tafflet,, A. de Lassence,, M. Darmon,, J.-R. Zahar,, C. Adrie,, M. Garrouste-Orgeas,, Y. Cohen,, B. Mourvillier,, B. Schlemmer, andthe Outcomerea Study Group. 2006. Candida colonization of the respiratory tract and subsequent Pseudomonas ventilator-associated pneumonia. Chest 129: 110117.
12. Baena-Monroy, T.,, V. Moreno-Maldonado,, F. Franco-Martinez,, B. Aldape-Barrios,, G. Quindos, and, L. Sanchez-Vargas. 2005. Candida albicans, Staphylococcus aureus and Streptococcus mutans colonization in patients wearing dental prosthesis. Med. Oral Patol. Oral Cir. Bucal 10: E27–E39.
13. Bahn, Y.-S.,, M. Molenda,, J. F. Staab,, C. A. Lyman,, L. J. Gordon, and, P. Sundstrom. 2007. Genome-wide transcriptional profiling of the cyclic AMP-dependent signaling pathway during morphogenic transitions of Candida albicans. Eukaryot. Cell 6: 23762390.
14. Bahn, Y. S., and, P. Sundstrom. 2001. Cap1, an adenylate cyclase-associated protein gene, regulates bud-hypha transitions, filamentous growth, and cyclic AMP levels and is required for virulence of Candida albicans. J. Bacteriol. 183: 32113223.
15. Bamford, C. V.,, A. d’Mello,, A. H. Nobbs,, L. C. Dutton,, M. M. Vickerman, and, H. F. Jenkinson. 2009. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 77: 36963704.
16. Bandara, H. M. H. N.,, J. Y. Y. Yau,, R. M. Watt,, L. J. Jin, and, L. P. Samaranayake. 2009. Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation. J. Med. Microbiol. 58: 16231631.
17. Banerjee, M.,, D. S. Thompson,, A. Lazzell,, P. L. Carlisle,, C. Pierce,, C. Monteagudo,, J. L. Lopez-Ribot, and, D. Kadosh. 2008. Ume6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol. Biol. Cell 19: 13541365.
18. Bauernfeind, A.,, G. Emminger,, G. Horl,, S. Ott,, B. Przyklenk, and, C. Weisslein-Pfister. 1987. Bacteriological effects of anti-Pseudomonas aeruginosa chemotherapy in cystic fibrosis. Infection 15: 403406.
19. Beenken, K. E.,, J. S. Blevins, and, M. S. Smeltzer. 2003. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71: 42064211.
20. Biswas, S.,, P. Van Dijck, and, A. Datta. 2007. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev. 71: 348376.
21. Boon, C.,, Y. Deng,, L. H. Wang,, Y. He,, J. L. Xu,, Y. Fan,, S. Q. Pan, and, L. H. Zhang. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2: 2736.
22. Boris, S.,, J. E. Suarez,, F. Vazquez, and, C. Barbes. 1998. Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect. Immun. 66: 19851989.
23. Braun, B. R., and, A. D. Johnson. 1997. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277: 105109.
24. Breger, J.,, B. B. Fuchs,, G. Aperis,, T. I. Moy,, F. M. Ausubel, and, E. Mylonakis. 2007. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog. 3: e18.
25. Brehm-Stecher, B. F., and, E. A. Johnson. 2003. Sensitization of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol, and apritone. Antimicrob. Agents Chemother. 47: 33573360.
26. Burd, R. S.,, C. S. Raymond, and, D. L. Dunn. 1992. Endotoxin promotes synergistic lethality during concurrent Escherichia coli and Candida albicans infection. J. Surg. Res. 52: 537542.
27. Burns, J. L.,, J. M. Van Dalfsen,, R. M. Shawar,, K. L. Otto,, R. L. Garber,, J. M. Quan,, A. B. Montgomery,, G. M. Albers,, B. W. Ramsey, and, A. L. Smith. 1999. Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis. J. Infect. Dis. 179: 11901196.
28. Busscher, H. J.,, C. G. van Hoogmoed,, G. I. Geertsema-Doornbusch,, M. van der Kuijl-Booij, and, H. C. van der Mei. 1997. Streptococcus thermophilus and its biosurfactants inhibit adhesion by Candida spp. on silicone rubber. Appl. Environ. Microbiol. 63: 38103817.
29. Carlson, E. 1983. Effect of strain of Staphylococcus aureus on synergism with Candida albicans resulting in mouse mortality and morbidity. Infect. Immun. 42: 285292.
30. Carlson, E. 1983. Enhancement by Candida albicans of Staphylococcus aureus, Serratia marcescens, and Streptococcus faecalis in the establishment of infection in mice. Infect. Immun. 39: 193197.
31. Carlson, E. 1982. Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality. Infect. Immun. 38: 921924.
32. Carlson, E., and, G. Johnson. 1985. Protection by Candida albicans of Staphylococcus aureus in the establishment of dual infection in mice. Infect. Immun. 50: 655659.
33. Charlton, T. S.,, R. de Nys,, A. Netting,, N. Kumar,, M. Hentzer,, M. Givskov, and, S. Kjelleberg. 2000. A novel and sensitive method for the quantification of n-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ. Microbiol. 2: 530541.
34. Chen, H.,, M. Fujita,, Q. Feng,, J. Clardy, and, G. R. Fink. 2004. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc. Natl. Acad. Sci. USA 101: 50485052.
35. Chim, H.,, B. H. Tan, and, C. Song. 2007. Five-year review of infections in a burn intensive care unit: high incidence of Acinetobacter baumannii in a tropical climate. Burns 33: 10081014.
36. Cho, T.,, H. Hamatake,, H. Kaminishi,, Y. Hagihara, and, K. Watanabe. 1992. The relationship between cyclic adenosine 3‵,5‵-monophosphate and morphology in exponential phase Candida albicans. Med. Mycol. 30: 3542.
37. Chotirmall, S. H.,, E. O’Donoghue,, K. Bennett,, C. Gunaratnam,, S. J. O’Neill, and, N. G. McElvaney. 2010. Sputum Candida albicans presages FEV1 decline and hospitalized exacerbations in cystic fibrosis. Chest 138: 11861195.
38. Coco, B. J.,, J. Bagg,, L. J. Cross,, A. Jose,, J. Cross, and, G. Ramage. 2008. Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol. Immunol. 23: 377383.
39. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber, and, H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49: 711745.
40. Coudeyras, S.,, G. Jugie,, M. Vermerie, and, C. Forestier. 2008. Adhesion of human probiotic Lactobacillus rhamnosus to cervical and vaginal cells and interaction with vaginosis-associated pathogens. Infect. Dis. Obstet. Gynecol. 2008: 549640.
41. Csank, C., and, K. Haynes. 2000. Candida glabrata displays pseudohyphal growth. FEMS Microbiol. Lett. 189: 115120.
42. Cugini, C.,, M. W. Calfee,, J. M. Farrow III,, D. K. Morales,, E. C. Pesci, and, D. A. Hogan. 2007. Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol. Microbiol. 65: 896906.
43. Cugini, C.,, D. K. Morales, and, D. A. Hogan. 2010. Candida albicans-produced farnesol stimulates Pseudomonas quinolone signal production in LasR-defective Pseudomonas aeruginosa strains. Microbiology 156: 3096–3107.
44. Cugini, C.,, R. Kolter, and, D. A. Hogan. 2008. Interdomain cross talk, p. 419429. In S. C. Winans and, B. L. Bassler (ed.), Chemical Communications among Bacteria. ASM Press, Washington, DC.
45. Cushion, M. T.,, M. S. Collins, and, M. J. Linke. 2009. Biofilm formation by Pneumocystis spp. Eukaryot. Cell 8: 197206.
46. Davis-Hanna, A.,, A. E. Piispanen,, L. I. Stateva, and, D. A. Hogan. 2008. Farnesol and dodecanol effects on the Candida albicans Ras1-camp signalling pathway and the regulation of morphogenesis. Mol. Microbiol. 67: 4762.
47. de Carvalho, F. G.,, D. S. Silva,, J. Hebling,, L. C. Spolidorio, and, D. M. P. Spolidorio. 2006. Presence of mutans streptococci and Candida spp. in dental plaque/dentine of carious teeth and early childhood caries. Arch. Oral Biol. 51: 10241028.
48. de Macedo, J. L., and, J. B. Santos. 2005. Bacterial and fungal colonization of burn wounds. Mem. Inst. Oswaldo Cruz 100: 535539.
49. Derengowski, L.,, C. De-Souza-Silva,, S. Braz,, T. Mello-De-Sousa,, S. Bao,, C. Kyaw, and, I. Silva-Pereira. 2009. Antimicrobial effect of farnesol, a Candida albicans quorum sensing molecule, on Paracoccidioides brasiliensis growth and morphogenesis. Ann. Clin. Microbiol. Antimicrob. 8: 13.
50. Deveau, A.,, A. E. Piispanen,, A. A. Jackson, and, D. A. Hogan. 2010. Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the Ras-cyclic AMP signaling pathway. Eukaryot. Cell 9: 569577.
51. Dichtl, K.,, F. Ebel,, F. Dirr,, F. H. Routier,, J. Heesemann, and, J. Wagener. 2010. Farnesol misplaces tip-localized Rho proteins and inhibits cell wall integrity signalling in Aspergillus fumigatus. Mol. Microbiol. 76: 11911204.
52. Dieterich, C.,, M. Schandar,, M. Noll,, F. J. Johannes,, H. Brunner,, T. Graeve, and, S. Rupp. 2002. In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148: 497506.
53. Dyess, D. L.,, R. N. Garrison, and, D. E. Fry. 1985. Candida sepsis: implications of polymicrobial blood-borne infection. Arch. Surg. 120: 345348.
54. Ehrhardt, A.,, G. R. Ehrhardt,, X. Guo, and, J. W. Schrader. 2002. Ras and relatives—job sharing and networking keep an old family together. Exp. Hematol. 30: 10891106.
55. Elahi, S.,, G. Pang,, R. Ashman, and, R. Clancy. 2005. Enhanced clearance of Candida albicans from the oral cavities of mice following oral administration of Lactobacillus acidophilus. Clin. Exp. Immunol. 141: 2936.
56. El-Azizi, M. A.,, S. E. Starks, and, N. Khardori. 2004. Interactions of Candida albicans with other Candida spp. and bacteria in the biofilms. J. Appl. Microbiol. 96: 10671073.
57. Elving, G.,, H. van der Mei,, H. Busscher,, R. van Weissenbruch, and, F. Albers. 2003. Influence of different combinations of bacteria and yeasts in voice prosthesis biofilms on air flow resistance. Antonie van Leeuwenhoek 83: 4555.
58. Elving, G. J.,, H. C. van der Mei,, H. J. Busscher,, R. van Weissenbruch, and, F. W. J. Albers. 2001. Air-flow resistances of silicone rubber voice prostheses after formation of bacterial and fungal biofilms. J. Biomed. Materials Res. 58: 421426.
59. Eubanks, P. J.,, C. de Virgilio,, S. Klein, and, F. Bongard. 1993. Candida sepsis in surgical patients. Am. J. Surg. 166: 617–619; discussion, 619–620.
60. Evans, M. E., and, M. Pollack. 1993. Effect of antibiotic class and concentration on the release of lipopolysaccha-ride from Escherichia coli. J. Infect. Dis. 167: 13361343.
61. Falagas, M. E.,, G. I. Betsi, and, S. Athanasiou. 2006. Probiotics for prevention of recurrent vulvovaginal candidiasis: a review. J. Antimicrob. Chemother. 58: 266272.
62. Fang, H. M., and, Y. Wang. 2006. RA domain-mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development. Mol. Microbiol. 61: 484496.
63. Feng, Q.,, E. Summers,, B. Guo, and, G. Fink. 1999. Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J. Bacteriol. 181: 63396346.
64. Fitzsimmons, N., and, D. R. Berry. 1994. Inhibition of Candida albicans by Lactobacillus acidophilus: evidence for the involvement of a peroxidase system. Microbios 80: 125133.
65. Gaddy, J. A.,, A. P. Tomaras, and, L. A. Actis. 2009. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect. Immun. 77: 31503160.
66. Gale, C.,, D. Finkel,, N. Tao,, M. Meinke,, M. McClellan,, J. Olson,, K. Kendrick, and, M. Hostetter. 1996. Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proc. Natl. Acad. Sci. USA 93: 357361.
67. Gibson, J.,, A. Sood, and, D. A. Hogan. 2009. Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl. Environ. Microbiol. 75: 504513.
68. Hall-Stoodley, L.,, J. W. Costerton, and, P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95108.
69. Han, Y. W.,, W. Shi,, G. T. Huang,, S. Kinder Haake,, N. H. Park,, H. Kuramitsu, and, R. J. Genco. 2000. Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect. Immun. 68: 31403146.
70. Harcus, D.,, A. Nantel,, A. Marcil,, T. Rigby, and, M. Whiteway. 2004. Transcription profiling of cyclic AMP signaling in Candida albicans. Mol. Biol. Cell 15: 44904499.
71. Harriott, M. M., and, M. C. Noverr. 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob. Agents Chemother. 53: 39143922.
72. Hawser, S. P., and, L. J. Douglas. 1994. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect. Immun. 62: 915921.
73. Hazan, R.,, J. He,, G. Xiao,, V. Dekimpe,, Y. Apidianakis,, B. Lesic,, C. Astrakas,, E. Deziel,, F. Lepine, and, L. G. Rahme. 2010. Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog. 6: e1000810.
74. Hermann, C.,, J. Hermann,, U. Munzel, and, R. Rüchel. 1999. Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses 42: 619627.
75. Hess, D. J.,, M. J. Henry-Stanley,, C. M. Bendel,, B. Zhang,, M.-A. Johnson, and, C. L. Wells. 2009. Escherichia coli and TNF-α modulate macrophage phagocytosis of Candida glabrata. J. Surg. Res. 155: 217224.
76. Hockey, L. J.,, N. K. Fujita,, T. R. Gibson,, D. Rotrosen,, J. Z. Montgomerie, and, J. E. Edwards, Jr. 1982. Detection of fungemia obscured by concomitant bacteremia: in vitro and in vivo studies. J. Clin. Microbiol. 16: 10801085.
77. Hoffman, L. R.,, H. D. Kulasekara,, J. Emerson,, L. S. Houston,, J. L. Burns,, B. W. Ramsey, and, S. I. Miller. 2009. Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J. Cystic Fibrosis 8: 6670.
78. Hogan, D. A., and, R. Kolter. 2002. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 22292232.
79. Hogan, D. A.,, Å. Vik, and, R. Kolter. 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 54: 12121223.
80. Hogenauer, C.,, H. F. Hammer,, G. J. Krejs, and, E. C. Reisinger. 1998. Mechanisms and management of antibiotic-associated diarrhea. Clin. Infect. Dis. 27: 702710.
81. Holmes, A. R.,, P. K. Gopal, and, H. F. Jenkinson. 1995. Adherence of Candida albicans to a cell surface polysaccha-ride receptor on Streptococcus gordonii. Infect. Immun. 63: 18271834.
82. Holmes, A. R.,, R. McNab, and, H. F. Jenkinson. 1996. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect. Immun. 64: 46804685.
83. Hornby, J. M.,, E. C. Jensen,, A. D. Lisec,, J. J. Tasto,, B. Jahnke,, R. Shoemaker,, P. Dussault, and, K. W. Nickerson. 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67: 29822992.
84. Hornby, J. M., and, K. W. Nickerson. 2004. Enhanced production of farnesol by Candida albicans treated with four azoles. Antimicrob. Agents Chemother. 48: 23052307.
85. Hughes, W. T., and, H. K. Kim. 1973. Mycoflora in cystic fibrosis: some ecological aspects of Pseudomonas aeruginosa and Candida albicans. Mycopathol. Mycol. Appl. 50: 261269.
86. Inoue, Y.,, A. Shiraishi,, T. Hada,, K. Hirose,, H. Hamashima, and, J. Shimada. 2004. The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiol. Lett. 237: 325331.
87. Jabra-Rizk, M. A.,, W. A. Falkler, Jr.,, W. G. Merz,, J. I. Kelley,, A. A. M. A. Baqui, and, T. F. Meiller. 1999. Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J. Clin. Microbiol. 37: 14641468.
88. Jabra-Rizk, M. A.,, T. F. Meiller,, C. E. James, and, M. E. Shirtliff. 2006. Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial susceptibility. Antimicrob. Agents Chemother. 50: 14631469.
89. Jain, P.,, I. Akula, and, T. Edlind. 2003. Cyclic AMP signaling pathway modulates susceptibility of Candida species and Saccharomyces cerevisiae to antifungal azoles and other sterol biosynthesis inhibitors. Antimicrob. Agents Chemother. 47: 31953201.
90. Jamieson, D. J.,, D. W. Stephen, and, E. C. Terriere. 1996. Analysis of the adaptive oxidative stress response of Candida albicans. FEMS Microbiol. Lett. 138: 8388.
91. Jenkinson, H. F.,, H. C. Lala, and, M. G. Shepherd. 1990. Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect. Immun. 58: 14291436.
92. Kadosh, D., and, A. D. Johnson. 2005. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16: 29032912.
93. Kaewsrichan, J.,, K. Peeyananjarassri, and, J. Kongprasertkit. 2006. Selection and identification of anaerobic lactobacilli producing inhibitory compounds against vaginal pathogens. FEMS Immunol. Med. Microbiol. 48: 7583.
94. Kamaguchi, A.,, H. Baba,, M. Hoshi, and, K. Inomata. 1994. Coaggregation between Porphyromonas gingivalis and mutans streptococci. Microbiol. Immunol. 38: 457460.
95. Kamaguchi, A.,, K. Nakayama,, S. Ichiyama,, R. Nakamura,, T. Watanabe,, M. Ohta,, H. Baba, and, T. Ohyama. 2003. Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr. Microbiol. 47: 485491.
96. Kerr, J. R. 1994. Suppression of fungal growth exhibited by Pseudomonas aeruginosa. J. Clin. Microbiol. 32: 525527.
97. Klaerner, H. G.,, M. E. Uknis,, R. D. Acton,, P. S. Dahlberg,, C. Carlone-Jambor, and, D. L. Dunn. 1997. Candida albicans and Escherichia coli are synergistic pathogens during experimental microbial peritonitis. J. Surg. Res. 70: 161165.
98. Klotz, S. A.,, B. S. Chasin,, B. Powell,, N. K. Gaur, and, P. N. Lipke. 2007. Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn. Microbiol. Infect. Dis. 59: 401406.
99. Klotz, S. A.,, N. K. Gaur,, R. De Armond,, D. Sheppard,, N. Khardori,, J. E. Edwards,, P. N. Lipke, and, M. ElAzizi. 2007. Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med. Mycol. 45: 363370.
100. Krom, B. P.,, K. Buijssen,, H. J. Busscher, and, H. C. van der Mei. 2009. Candida biofilm analysis in the artificial throat using FISH. Methods Mol. Biol. 499: 4554.
101. Kruppa, M.,, B. P. Krom,, N. Chauhan,, A. V. Bambach,, R. L. Cihlar, and, R. A. Calderone. 2004. The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot. Cell 3: 10621065.
102. Kuroda, M.,, S. Nagasaki, and, T. Ohta. 2007. Sesquiterpene farnesol inhibits recycling of the c55 lipid carrier of the murein monomer precursor contributing to increased susceptibility to β-lactams in methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 59: 425432.
103. Labrousse, A.,, S. Chauvet,, C. Couillault,, C. L. Kurz, and, J. J. Ewbank. 2000. Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr. Biol. 10: 15431545.
104. Lamont, R. J., and, H. F. Jenkinson. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62: 12441263.
105. Langford, M. L.,, A. L. Atkin, and, K. W. Nickerson. 2009. Cellular interactions of farnesol, a quorum-sensing molecule produced by Candida albicans. Future Microbiol. 4: 13531362.
106. Langford, M. L.,, S. Hasim,, K. W. Nickerson, and, A. L. Atkin. 2010. Activity and toxicity of farnesol towards Candida albicans are dependent on growth conditions. Antimicrob. Agents Chemother. 54: 940942.
107. Leberer, E.,, D. Harcus,, D. Dignard,, L. Johnson,, S. Ushinsky,, D. Y. Thomas, and, K. Schroppel. 2001. Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol. Microbiol. 42: 673687.
108. Leunisse, C.,, R. van Weissenbruch,, H. J. Busscher,, H. C. van der Mei, and, F. W. Albers. 1999. The artificial throat: a new method for standardization of in vitro experiments with tracheo-oesophageal voice prostheses. Acta Otolaryngol. 119: 604608.
109. Li, D.,, D. Williams,, D. Lowman,, M. A. Monteiro,, X. Tan,, M. Kruppa,, W. Fonzi,, E. Roman,, J. Pla, and, R. Calderone. 2009. The Candida albicans histidine kinase Chk1p: signaling and cell wall mannan. Fungal Genet. Biol. 46: 731741.
110. Lo, H. J.,, J. R. Kohler,, B. DiDomenico,, D. Loebenberg,, A. Cacciapuoti, and, G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939949.
111. Lorenz, M. C.,, J. A. Bender, and, G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3: 10761087.
112. Machida, K., and, T. Tanaka. 1999. Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F0F1-ATPase in yeast. FEBS Lett. 462: 108112.
113. Machida, K.,, T. Tanaka,, K.-I. Fujita, and, M. Taniguchi. 1998. Farnesol-induced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae. J. Bacteriol. 180: 44604465.
114. Maidan, M. M.,, L. De Rop,, J. Serneels,, S. Exler,, S. Rupp,, H. Tournu,, J. M. Thevelein, and, P. Van Dijck. 2005. The G protein-coupled receptor Gpr1 and the Ga protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16: 19711986.
115. Makoto, K.,, N. Sanae,, I. Ryuta, and, O. Toshiko. 2007. Sesquiterpene farnesol as a competitive inhibitor of lipase activity of Staphylococcus aureus. FEMS Microbiol. Lett. 273: 2834.
116. Martins, M.,, M. Henriques,, J. Azeredo,, S. M. Rocha,, M. A. Coimbra, and, R. Oliveira. 2007. Morphogenesis control in Candida albicans and Candida dubliniensis through signaling molecules produced by planktonic and biofilm cells. Eukaryot. Cell 6: 24292436.
117. McAlester, G.,, F. O’Gara, and, J. P. Morrissey. 2008. Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. J. Med. Microbiol. 57: 563569.
118. McNab, R.,, A. R. Holmes,, J. M. Clarke,, G. W. Tannock, and, H. F. Jenkinson. 1996. Cell surface polypep-tide CshA mediates binding of Streptococcus gordonii to other oral bacteria and to immobilized fibronectin. Infect. Immun. 64: 42044210.
119. Mitchell, A. P. 1998. Dimorphism and virulence in Candida albicans. Curr. Opin. Microbiol. 1: 687692.
120. Morales, D. K.,, N. J. Jacobs,, S. Rajamani,, M. Krishnamurthy,, J. C. Cubillos-Ruiz, and, D. A. Hogan. 2010. Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol. Microbiol. 78: 13791392.
121. Moran, G. P.,, D. J. Sullivan,, M. C. Henman,, C. E. McCreary,, B. J. Harrington,, D. B. Shanley, and, D. C. Coleman. 1997. Antifungal drug susceptibilities of oral Candida dubliniensis isolates from human immunodeficiency virus (HIV)-infected and non-HIV-infected subjects and generation of stable fluconazole-resistant derivatives in vitro. Antimicrob. Agents Chemother. 41: 617623.
122. Morris, A.,, K. Wei,, K. Afshar, and, L. Huang. 2008. Epidemiology and clinical significance of Pneumocystis colonization. J. Infect. Dis. 197: 1017.
123. Navarathna, D. H. M. L. P.,, J. M. Hornby,, N. Krishnan,, A. Parkhurst,, G. E. Duhamel, and, K. W. Nickerson. 2007. Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a dpp3 knockout mutant of Candida albicans. Infect. Immun. 75: 16091618.
124. Nobbs, A. H.,, B. H. Shearer,, M. Drobni,, M. A. Jepson, and, H. F. Jenkinson. 2007. Adherence and internalization of Streptococcus gordonii by epithelial cells involves beta1 integrin recognition by SspA and SspB (antigen I/ II family) polypeptides. Cell. Microbiol. 9: 6583.
125. Noverr, M. C., and, G. B. Huffnagle. 2004. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect. Immun. 72: 62066210.
126. Nseir, S.,, E. Jozefowicz,, B. Cavestri,, B. Sendid,, C. Di Pompeo,, F. Dewavrin,, R. Favory,, M. Roussel-Delvallez, and, A. Durocher. 2007. Impact of antifungal treatment on Candida-Pseudomonas interaction: a preliminary retrospective case-control study. Intensive Care Med. 33: 137142.
127. Nuzzo, I.,, M. R. Sanges,, A. Folgore, and, C. R. Carratelli. 2000. Apoptosis of human keratinocytes after bacterial invasion. FEMS Immunol. Med. Microbiol. 27: 235240.
128. Oh, K.-B.,, H. Miyazawa,, T. Naito, and, H. Matsuoka. 2001. Purification and characterization of an autoregulatory substance capable of regulating the morphological transition in Candida albicans. Proc. Natl. Acad. Sci. USA 98: 46644668.
129. O’Sullivan, J. M.,, R. D. Cannon,, P. A. Sullivan, and, H. F. Jenkinson. 1997. Identification of salivary basic proline-rich proteins as receptors for Candida albicans adhesion. Microbiology 143: 341348.
130. O’Sullivan, J. M.,, H. F. Jenkinson, and, R. D. Cannon. 2000. Adhesion of Candida albicans to oral streptococci is promoted by selective adsorption of salivary proteins to the streptococcal cell surface. Microbiology 146: 4148.
131. Paster, B. J.,, S. K. Boches,, J. L. Galvin,, R. E. Ericson,, C. N. Lau,, V. A. Levanos,, A. Sahasrabudhe, and, F. E. Dewhirst. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183: 37703783.
132. Paulitsch, A.,, W. Weger,, G. Ginter-Hanselmayer,, E. Marth, and, W. Buzina. 2006. A 5-year (2000–2004) epidemiological survey of Candida and non-Candida yeast species causing vulvovaginal candidiasis in Graz, Austria. Mycoses 49: 471475.
133. Peleg, A. Y.,, D. A. Hogan, and, E. Mylonakis. 2010. Medically important bacterial-fungal interactions. Nat. Rev. Microbiol. 8: 340349.
134. Peleg, A. Y.,, E. Tampakakis,, B. B. Fuchs,, G. M. Eliopoulos,, R. C. Moellering, and, E. Mylonakis. 2008. Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105: 1458514590.
135. Pereira-Cenci, T.,, D. M. Deng,, E. A. Kraneveld,, E. M. M. Manders,, A. A. Del Bel Cury,, J. M. ten Cate, and, W. Crielaard. 2008. The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch. Oral Biol. 53: 755764.
136. Peres-Bota, D.,, H. Rodriguez-Villalobos,, G. Dimopoulos,, C. Melot, and, J. L. Vincent. 2004. Potential risk factors for infection with Candida spp. in critically ill patients. Clin. Microbiol. Infect. 10: 550555.
137. Pfaller, M. A. 1996. Nosocomial candidiasis: emerging species, reservoirs, and modes of transmission. Clin. Infect. Dis. 22 (Suppl. 2): S89S94.
138. Pfaller, M. A., and, D. J. Diekema. 2010. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36: 153.
139. Ponniah, G.,, C. Rollenhagen,, Y. S. Bahn,, J. F. Staab, and, P. Sundstrom. 2007. State of differentiation defines buccal epithelial cell affinity for cross-linking to Candida albicans Hwp1. J. Oral Pathol. Med. 36: 456467.
140. Pulimood, S.,, L. Ganesan,, G. Alangaden, and, P. Chandrasekar. 2002. Polymicrobial candidemia. Diagn. Microbiol. Infect. Dis. 44: 353357.
141. Raad, I. I., and, H. A. Hanna. 2002. Intravascular catheter-related infections: new horizons and recent advances. Arch. Intern. Med. 162: 871878.
142. Ramage, G.,, S. P. Saville,, B. L. Wickes, and, J. L. Lopez-Ribot. 2002. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl. Environ. Microbiol. 68: 54595463.
143. Ramage, G.,, K. Vande-Walle,, J. L. Lopez-Ribot, and, B. L. Wickes. 2002. The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol. Lett. 214: 95100.
144. Rauceo, J. M.,, R. De Armond,, H. Otoo,, P. C. Kahn,, S. A. Klotz,, N. K. Gaur, and, P. N. Lipke. 2006.Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot. Cell 5: 16641673.
145. Reeves, E. P.,, H. Lu,, H. L. Jacobs,, C. G. M. Messina,, S. Bolsover,, G. Gabella,, E. O. Potma,, A. Warley,, J. Roes, and, A. W. Segal. 2002. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416: 291297.
146. Richards, M. J.,, J. R. Edwards,, D. H. Culver, and, R. P. Gaynes. 1999. Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit. Care Med. 27: 887892.
147. Román, E.,, R. Alonso-Monge,, Q. Gong,, D. Li,, R. Calderone, and, J. Pla. 2009. The cek1 MAPK is a short-lived protein regulated by quorum sensing in the fungal pathogen Candida albicans. FEMS Yeast Res. 9: 942955.
148. Ronnqvist, D.,, U. Forsgren-Brusk,, U. Husmark, and, E. Grahn-Hakansson. 2007. Lactobacillus fermentum Ess-1 with unique growth inhibition of vulvo-vaginal candidiasis pathogens. J. Med. Microbiol. 56: 15001504.
149. Rosenthal, V. D.,, D. G. Maki,, R. Salomao,, C. A. Moreno,, Y. Mehta,, F. Higuera,, L. E. Cuellar,, O. A. Arikan,, R. Abouqal, and, H. Leblebicioglu. 2006. Device-associated nosocomial infections in 55 intensive care units of 8 developing countries. Ann. Intern. Med. 145: 582591.
150. Rossignol, T.,, M. E. Logue,, K. Reynolds,, M. Grenon,, N. F. Lowndes, and, G. Butler. 2007. Transcriptional response of Candida parapsilosis following exposure to farnesol. Antimicrob. Agents Chemother. 51: 23042312.
151. Roux, D.,, S. Gaudry,, D. Dreyfuss,, J. El-Benna,, N. de Prost,, E. Denamur,, G. Saumon, and, J.-D. Ricard. 2009. Candida albicans impairs macrophage function and facilitates Pseudomonas aeruginosa pneumonia in rat. Crit. Care Med. 37: 10621067.
152. Saville, S. P.,, A. L. Lazzell,, C. Monteagudo, and, J. L. Lopez-Ribot. 2003. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2: 10531060.
153. Semighini, C. P.,, J. M. Hornby,, R. Dumitru,, K. W. Nickerson, and, S. D. Harris. 2006. Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol. Microbiol. 59: 753764.
154. Shirtliff, M. E.,, B. P. Krom,, R. A. M. Meijering,, B. M. Peters,, J. Zhu,, M. A. Scheper,, M. L. Harris, and, M. A. Jabra-Rizk. 2009. Farnesol-induced apoptosis in Candida albicans. Antimicrob. Agents Chemother. 53: 23922401.
155. Smith, D. A.,, S. Nicholls,, B. A. Morgan,, A. J. P. Brown, and, J. Quinn. 2004. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol. Biol. Cell 15: 41794190.
156. Spear, G. T.,, M. R. Zariffard,, M. H. Cohen, and, B. E. Sha. 2008. Vaginal IL-8 levels are positively associated with Candida albicans and inversely with lactobacilli in HIV-infected women. J. Reprod. Immunol. 78: 7679.
157. Staab, J. F.,, S. D. Bradway,, P. L. Fidel, and, P. Sund-strom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 15351538.
158. Sullivan, D. J.,, G. P. Moran,, E. Pinjon,, A. Al-Mosaid,, C. Stokes,, C. Vaughan, and, D. C. Coleman. 2004. Comparison of the epidemiology, drug resistance mechanisms, and virulence of Candida dubliniensis and Candida albicans. FEMS Yeast Res. 4: 369376.
159. Tampakakis, E.,, A. Y. Peleg, and, E. Mylonakis. 2009. Interaction of Candida albicans with an intestinal pathogen, Salmonella enterica serovar Typhimurium. Eukaryot. Cell 8: 732737.
160. Thein, Z. M.,, Y. H. Samaranayake, and, L. P. Samaranayake. 2006. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch. Oral Biol. 51: 672680.
161. Uppuluri, P.,, A. K. Chaturvedi,, A. Srinivasan,, M. Banerjee,, A. K. Ramasubramaniam,, J. R. Köhler,, D. Kadosh, and, J. L. Lopez-Ribot. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6: e1000828.
162. Uppuluri, P.,, S. Mekala, and, W. L. Chaffin. 2007. Farnesol-mediated inhibition of Candida albicans yeast growth and rescue by a diacylglycerol analogue. Yeast 24: 681693.
163. Verghese, A.,, K. Prabhu,, D. R. Diamond, and, A. Sugar. 1988. Synchronous bacterial and fungal septicemia: a marker for the critically ill surgical patient. Am. Surg. 54: 276283.
164. Wagner, R. D.,, C. Pierson,, T. Warner,, M. Dohnalek,, J. Farmer,, L. Roberts,, M. Hilty, and, E. Balish. 1997. Bio-therapeutic effects of probiotic bacteria on candidiasis in immunodeficient mice. Infect. Immun. 65: 41654172.
165. Wang, L.-H.,, Y. He,, Y. Gao,, J. E. Wu,, Y.-H. Dong,, C. He,, S. X. Wang,, L.-X. Weng,, J.-L. Xu,, L. Tay,, R. X. Fang, and, L.-H. Zhang. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51: 903912.
166. Weber, K.,, R. Sohr,, B. Schulz,, M. Fleischhacker, and, M. Ruhnke. 2008. Secretion of E,E-farnesol and biofilm formation in eight different Candida species. Antimicrob. Agents Chemother. 52: 18591861. (Erratum, 53: 848, 2009.)
167. Westwater, C.,, E. Balish, and, D. A. Schofield. 2005. Candida albicans-conditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot. Cell 4: 16541661.
168. Wilson, D.,, A. Tutulan-Cunita,, W. Jung,, N. C. Hauser,, R. Hernandez,, T. Williamson,, K. Piekarska,, S. Rupp,, T. Young, and, L. Stateva. 2007. Deletion of the high-affinity cAMP phosphodiesterase encoded by PDE2 affects stress responses and virulence in Candida albicans. Mol. Microbiol. 65: 841856.
169. Wisplinghoff, H.,, T. Bischoff,, S. M. Tallent,, H. Seifert,, R. P. Wenzel, and, M. B. Edmond. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39: 309317. (Erratum, 39: 1093; erratum, 40: 1077, 2005.)
170. Xu, X.-L.,, R. T. H. Lee,, H.-M. Fang,, Y.-M. Wang,, R. Li,, H. Zou,, Y. Zhu, and, Y. Wang. 2008. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 4: 2839.
171. Zheng, X.,, Y. Wang, and, Y. Wang. 2004. Hgc1, a novel hypha-specific G1 cyclin-related protein, regulates Candida albicans hyphal morphogenesis. EMBO J. 23: 18451856.

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