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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2011, Vol. 6 Issue (6) : 435-445    https://doi.org/10.1007/s11515-011-1153-3
REVIEW
Population level virulence in polymicrobial communities associated with chronic disease
Jeff G. LEID(), Emily COPE
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA
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Abstract

Renewed studies of chronic infection have shifted the focus from single pathogens to multi-microbial communities as culture-independent techniques reveal complex consortia of microbes associated with chronic disease. Despite a general acceptance that some chronic diseases are caused by mixed microbial communities, areas of research exploring community interactions as they relate to the alteration of virulence are still in the early stages. Members of the NIH Human Microbiome Project have been actively characterizing the microbial communities of the skin, nasal, oral, gastrointestinal, and urogenital cavities of healthy adults. Concomitantly, several independent studies have begun to characterize the oral, nasal, sinus, upper and lower respiratory microbiomes in healthy and diseased human tissue. The interactions among the members of these polymicrobial communities have not been thoroughly explored and it is clear there is a need to identify the functional interactions that drive population-level virulence if new therapeutic approaches to chronic disease are to be developed. For example, multiple studies have examined the role of quorum sensing (QS) in microbial virulence, and QS antagonists are being developed and tested as novel therapeutics. Other potential targets include the Gram-negative type III signaling system (T3SS), type IV pili, and two component regulatory systems (TCRS). Initial results from these studies indicate limited efficacy in vivo, further suggesting that the interactions in a heterogeneous community are complex and poorly understood. If progress is to be made in the development of more effective treatments for chronic diseases, a better understanding of the composition and functional interactions that occur within multi-microbial communities must be developed.

Keywords polymicrobial      chronic infection      quorum sensing      therapeutics     
Corresponding Author(s): LEID Jeff G.,Email:Jeff.Leid@nau.edu   
Issue Date: 01 December 2011
 Cite this article:   
Jeff G. LEID,Emily COPE. Population level virulence in polymicrobial communities associated with chronic disease[J]. Front Biol, 2011, 6(6): 435-445.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1153-3
https://academic.hep.com.cn/fib/EN/Y2011/V6/I6/435
Fig.1  Fraction of bacterial taxa in CRS and non-CRS (control) sinus tissue determined by 454 pyrosequencing (Roche, Life Sciences). Actinobacteria, Alphaproteobacteria, and Clostridia are more abundant in CRS tissue. Bacteriodetes and Flavobacteria are more abundant in non-CRS control sinus tissue.
1 Anzaudo M M, Busquets N P, Ronchi S, Mayoral C (2005). Isolated pathogen microorganisms in respiratory samples from children with cystic fibrosis. Rev Argent Microbiol , 37(3): 129–134
pmid:16323660
2 Armbruster C E, Hong W, Pang B, Weimer K E, Juneau R A, Turner J, Swords W E (2010). Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio , 1(3): e00102-10–e00102-19
doi: 10.1128/mBio.00102-10 pmid:20802829
3 Arthur M, Molinas C, Courvalin P (1992). The VanS-VanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol , 174(8): 2582–2591
pmid:1556077
4 Baddour L M, Christensen G D (1987). Prosthetic valve endocarditis due to small-colony staphylococcal variants. Rev Infect Dis , 9(6): 1168–1174
doi: 10.1093/clinids/9.6.1168 pmid:3423588
5 Bader M S (2008). Diabetic foot infection. Am Fam Physician , 78(1): 71–79
pmid:18649613
6 Bakaletz L O (2010). Immunopathogenesis of polymicrobial otitis media. J Leukoc Biol, 87(2): 213–22
7 Bala A, Kumar R, Harjai K(2011). Inhibition of quorum sensing in Pseudomonas aeruginosaby azithromycin and its effectiveness in urinary tract infections. J Med Microbiol, 60(Pt 3): 300–306
8 Bassler B L (1999). How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol, 2(6): 582–587
9 Bassler B L, Wright M, Silverman M R (1994). Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol , 13(2): 273–286
doi: 10.1111/j.1365-2958.1994.tb00422.x pmid:7984107
10 Bjarnsholt T, Givskov M (2007). Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Philos Trans R Soc Lond B Biol Sci, 362(1483): 1213–22
11 Bjarnsholt T, Jensen P O, Jakobsen T H, Phipps R, Nielsen A K, Rybtke M T, Tolker-Nielsen T, Givskov M, H?iby N, Ciofu O, the Scandinavian Cystic Fibrosis Study Consortium (2010). Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS One , 5(4): e10115
doi: 10.1371/journal.pone.0010115 pmid:20404933
12 Boles B R , Thoendel M, Singh P K(2005). Genetic variation in biofilms and the insurance effects of diversity. Microbiology , 151(Pt 9: 2816–2818
13 Brown S M (2010). Multiple strains of non-tuberculous mycobacteria in a patient with cystic fibrosis. J R Soc Med, 103(Suppl 1): 34–43
14 Burmolle M, Thomsen T R, Fazli M, Dige I, Christensen L, Homoe P, Tvede M, Nyvad B, Tolker-Nielsen T, Givskov M, Moser C, Kirketerp-Moller K, Johansen H K , Hoiby N, Jensen P O, Sorensen S J, Bjarnsholt T (2010). Biofilms in chronic infections — a matter of opportunity — monospecies biofilms in multispecies infections. FEMS Immunol Med Microbiol, 59(3), 324–336
15 Burns J L, Emerson J, Stapp J R, Yim D L, Krzewinski J, Louden L, Ramsey B W, Clausen C R (1998). Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis , 27(1): 158–163
doi: 10.1086/514631 pmid:9675470
16 Chan J, Hadley J (2001). The microbiology of chronic rhinosinusitis: results of a community surveillance study. Ear Nose Throat J , 80(3): 143–145
pmid:11269215
17 Charlson E S, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, Hwang J, Bushman F D, Collman R G (2010). Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS ONE , 5(12): e15216
doi: 10.1371/journal.pone.0015216 pmid:21188149
18 Chen P B, Davern L B, Katz J, Eldridge J H, Michalek S M (1996). Host responses induced by co-infection with Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in a murine model. Oral Microbiol Immunol , 11(4): 274–281
doi: 10.1111/j.1399-302X.1996.tb00181.x pmid:9002881
19 Cherry D K, Woodwell D A (2002). National Ambulatory Medical Care Survey: 2000 summary. Adv Data , 328: 1–32
20 Deng D M, Liu M J, ten Cate J M, Crielaard W (2007). The VicRK system of Streptococcus mutans responds to oxidative stress. J Dent Res , 86(7): 606–610
21 Dewhirst F E, Chen T, Izard J, Paster B J, Tanner A C, Yu W H, Lakshmanan A, Wade W G (2010). The human oral microbiome. J Bacteriol , 192(19): 5002–5017
22 Duque C, Stipp R N, Wang B, Smith D J, Hofling J F, Kuramitsu H K, Duncan M J, Mattos-Graner R O (2011). Downregulation of GbpB, a component of the VicRK regulon, affects biofilm formation and cell surface characteristics of Streptococcus mutans. Infect Immun, 79(2): 786–796
23 Ebersole J L, Feuille F, Kesavalu L, Holt S C (1997). Host modulation of tissue destruction caused by periodontopathogens: effects on a mixed microbial infection composed of Porphyromonas gingivalis and Fusobacterium nucleatum. Microb Pathog, 23(1): 23–32
24 Ehrlich G D, Ahmed A, Earl J, Hiller N L, Costerton J W, Stoodley P, Post J C, Demeo P, Hu F Z (2010). The distributed genome hypothesis as a rubric for understanding evolution in situ during chronic bacterial biofilm infectious processes. FEMS Immunol Med Microbiol , 59(3): 269–279
25 Ehrlich G D, Hiller N L, Hu F Z (2008). What makes pathogens pathogenic. Genome Biol , 9(6): 225
26 Ehrlich G D, Hu F Z, Shen K, Stoodley P, Post J C (2005). Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin Orthop Relat Res , (437):20–24
27 Evers S, Courvalin P (1996). Regulation of VanB-type vancomycin resistance gene expression by the VanS(B)-VanR (B) two-component regulatory system in Enterococcus faecalis V583. J Bacteriol , 178(5): 1302–1309
pmid:8631706
28 Falleiros de Padua R A, Norman Negri M F, Svidzinski A E, Nakamura C V, Svidzinski T I (2008). Adherence of Pseudomonas aeruginosa and Candida albicans to urinary catheters. Rev Iberoam Micol, 25(3): 173–175
29 Feuille F, Ebersole J L, Kesavalu L, Stepfen M J, Holt S C (1996). Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun , 64(6): 2094–2100
pmid:8675312
30 Foreman A, Psaltis A J, Tan L W, Wormald P J (2009). Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy , 23(6): 556–561
doi: 10.2500/ajra.2009.23.3413 pmid:19958600
31 Foreman A, Wormald P J (2010). Different biofilms, different disease? A clinical outcomes study. Laryngoscope , 120(8): 1701–1706
doi: 10.1002/lary.21024 pmid:20641074
32 Galperin M Y(2006). Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol, 188(12): 4169–4182
33 Geske G D, O’Neill J C, Blackwell H E (2007). N-phenylacetanoyl-L-homoserine lactones can strongly antagonize or superagonize quorum sensing in Vibrio fischeri. ACS Chem Biol , 2(5): 315–319
doi: 10.1021/cb700036x pmid:17480049
34 Geske G D, O’Neill J C, Miller D M, Mattmann M E, Blackwell H E (2007). Modulation of bacterial quorum sensing with synthetic ligands: systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action. J Am Chem Soc , 129(44): 13613–13625
doi: 10.1021/ja074135h pmid:17927181
35 Gotoh Y, Doi A, Furuta E, Dubrac S, Ishizaki Y, Okada M, Igarashi M, Misawa N, Yoshikawa H, Okajima T, Msadek T, Utsumi R(2010). Novel antibacterial compounds specifically targeting the essential WalR response regulator. J Antibiot (Tokyo), 63(3): 127–134
36 Guggenheim B, Gmur R, Galicia J C, Stathopoulou P G, Benakanakere M R, Meier A, Thurnheer T, Kinane D F(2009). In vitro modeling of host-parasite interactions: the ‘subgingival’ biofilm challenge of primary human epithelial cells. BMC Microbiol , 9: 280
37 Hall-Stoodley L, Hu F Z, Gieseke A, Nistico L, Nguyen D, Hayes J, Forbes M, Greenberg D P, Dice B, Burrows A, Wackym P A, Stoodley P, Post J C, Ehrlich G D, Kerschner J E(2006). Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA, 296(2): 202–211
38 Healy D Y, Leid J G, Sanderson A R, Hunsaker D H(2008). Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg , 138(5): 641–647
39 Hemady R K (1995). Microbial keratitis in patients infected with the human immunodeficiency virus. Ophthalmology , 102(7): 1026–1030
pmid:9121747
40 Hentzer M, Eberl L, Nielsen J, Givskov M(2003). Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs , 17(4): 241–250
41 Hentzer M, Wu H, Andersen J B, Riedel K, Rasmussen T B, Bagge N, Kumar N, Schembri M A, Song Z, Kristoffersen P, Manefield M, Costerton J W, Molin S, Eberl L, Steinberg P, Kjelleberg S, H?iby N, Givskov M (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J , 22(15): 3803–3815
doi: 10.1093/emboj/cdg366 pmid:12881415
42 Hermann C, Hermann J, Munzel U, R?chel R (1999). Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses , 42(11-12): 619–627
doi: 10.1046/j.1439-0507.1999.00519.x pmid:10680438
43 Higgins D A, Pomianek M E, Kraml C M, Taylor R K, Semmelhack M F, Bassler B L(2007). The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature , 450(7171): 883–886
44 HoffmanL R, Deziel E, D'Argenio D A, Lepine F, Emerson J, McNamara S, Gibson R L, Ramsey B W, Miller S I(2006). Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A, 103(52): 19890–19895
45 Hogan D A, Kolter R (2002). Pseudomonas-Candida interactions: an ecological role for virulence factors. Science, 296(5576): 2229–22232
46 Hoiby N (1974). Epidemiological investigations of the respiratory tract bacteriology in patients with cystic fibrosis. Acta Pathol Microbiol Scand B Microbiol Immunol , 82(4): 541–550
pmid:4153350
47 H?iby N, Ciofu O, Bjarnsholt T (2010). Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol , 5(11): 1663–1674
doi: 10.2217/fmb.10.125 pmid:21133688
48 Holcombe L J, McAlester G, Munro C A, Enjalbert B, Brown A J, Gow N A, Ding C, Butle G R, O’Gara F, Morrissey J P(2010). Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans . Microbiology, 156(Pt 5): 1476–1486
49 Hong H J, Hutchings M I, Buttner M J, the Biotechnology and Biological Sciences Research Council, U K (2008). Vancomycin resistance VanS/VanR two-component systems. Adv Exp Med Biol , 631: 200–213
doi: 10.1007/978-0-387-78885-2_14 pmid:18792691
50 Hu F Z, Ehrlich G D (2008). Population-level virulence factors amongst pathogenic bacteria: relation to infection outcome. Future Microbiol , 3(1): 31–42
doi: 10.2217/17460913.3.1.31 pmid:18230032
51 Ito R, Ishihara K, Shoji M, Nakayama K, Okuda K (2010). Hemagglutinin/adhesin domains of Porphyromonas gingivalis play key roles in coaggregation with Treponema denticola. FEMS Immunol Med Microbiol , 60(3): 251–260
doi: 10.1111/j.1574-695X.2010.00737.x pmid:21039921
52 Jakubovics N S, Kolenbrander P E(2010). The road to ruin: the formation of disease-associated oral biofilms. Oral Dis , 16(8): 729–739
53 Jenkinson H F, Lamont R J(2005). Oral microbial communities in sickness and in health. Trends Microbiol, 13(12): 589–595
54 Jesaitis A J, Franklin M J, Berglund D, Sasaki M, Lord C I, Bleazard J B, Duffy J E, Beyenal H, Lewandowski Z (2003). Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol , 171(8): 4329–4339
pmid:14530358
55 Jones M B, Peterson S N, Benn R, Braisted J C, Jarrahi B, Shatzkes K, Ren D, Wood T K, Blaser M J(2010). Role of luxS in Bacillus anthracis growth and virulence factor expression. Virulence, 1(2): 72–83
56 Kahl B, Herrmann M, Everding A S, Koch H G, Becker K, Harms E, Proctor R A, Peters G (1998). Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J Infect Dis , 177(4): 1023–1029
pmid:9534977
57 Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K(2004a). Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett , 230(1): 13–18
58 Keren I, Shah D, Spoering A, Kaldalu N, Lewis K (2004b). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol, 186(24): 8172–8180
59 Kesavalu L, Holt S C, Ebersole J L (1998). Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol , 13(6): 373–377
doi: 10.1111/j.1399-302X.1998.tb00694.x pmid:9872114
60 Klinger J D, Thomassen M J(1985). Occurrence and antimicrobial susceptibility of Gram-negative nonfermentative bacilli in cystic fibrosis patients. Diagn Microbiol Infect Dis, 3(2): 149–158
61 Kolenbrander P E(2000). Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol, 54: 413–437
62 Kolenbrander P E, Andersen R N, Blehert D S, Egland P G, Foster J S, Palmer R J Jr(2002). Communication among oral bacteria. Microbiol Mol Biol Rev , 66(3): 486–505
63 Kolenbrander P E, Palmer R J Jr, Rickard A H, Jakubovics N S, Chalmers N I, Diaz P I(2006). Bacterial interactions and successions during plaque development. Periodontol 2000 , 42: 47–79
64 Krishnamurthy A, McGrath J, Cripps A W, Kyd J M (2009). The incidence of Streptococcus pneumoniae otitis media is affected by the polymicrobial environment particularly Moraxella catarrhalis in a mouse nasal colonisation model. Microbes Infect, 11(5): 545–553
65 Lambiase A, Catania M R, Del Pezzo M, Rossano F, Terlizzi V, Sepe A, Raia V (2011). Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis ,
doi: 10.1007/s10096-011-1182-5 pmid:21279730
66 Lanza D C, Kennedy D W(1997). Adult rhinosinusitis defined. Otolaryngol Head Neck Surg, 117(Suppl 3): 1–7
67 Lattar S M, Tuchscherr L P, Caccuri R L, Centron D, Becker K, Alonso C A, Barberis C, Miranda G, Buzzola F R, von Eiff C, Sordelli D O(2009). Capsule expression and genotypic differences among Staphylococcus aureus isolates from patients with chronic or acute osteomyelitis. Infect Immun , 77(5): 1968–1975
68 Lee B, Haagensen J A, Ciofu O, Andersen J B, Hoiby N, Molin S(2005). Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J Clin Microbiol , 43(10): 5247–5255
69 Leid J G, Costerton J W, Shirtliff M E, Gilmore M S, Engelbert M (2002). Immunology of Staphylococcal biofilm infections in the eye: new tools to study biofilm endophthalmitis. DNA Cell Biol , 21(5-6): 405–413
doi: 10.1089/10445490260099692 pmid:12167243
70 Leid J G, Kerr M, Selgado C, Johnson C, Moreno G, Smith A, Shirtliff M E, O'Toole G A,Cope E K(2009). Flagellar-mediated biofilm defense mechanisms of Pseudomonas aeruginosa against host derived lactoferrin. Infect Immun, 77(10): 4559–4566
doi: 10.1128/IAI.00075-09
71 Leid J G, Willson C J, Shirtliff M E, Hassett D J, Parsek M R,Jeffers A K(2005). The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol, 175(11): 7512–7518
72 Li J, Helmerhorst E J, Leone C W, Troxler R F, Yaskell T, Haffajee A D, Socransky S S,Oppenheim F G(2004). Identification of early microbial colonizers in human dental biofilm. J Appl Microbiol, 97(6): 1311–1318
73 Li M, Villaruz A E, Vadyvaloo V, Sturdevant D E,Otto M (2008). AI-2-dependent gene regulation in Staphylococcus epidermidis . BMC Microbiol, 8: 4
74 Ly N,McCaig L F(2002). National Hospital Ambulatory Medical Care Survey: 2000 outpatient department summary. Adv Data, (327): 1–27
75 Maeda S, Ito M, Ando T, Ishimoto Y, Fujisawa Y, Takahashi H, Matsuda A, Sawamura A, Kato S(2006). Horizontal transfer of nonconjugative plasmids in a colony biofilm of Escherichia coli. FEMS Microbiol Lett, 255(1): 115–120
76 Moore J E, Reid A, Millar B C, Jiru X, Mccaughan J, Goldsmith C E, Collins J, Murphy P G, Elborn J S (2002). Pandoraea apista isolated from a patient with cystic fibrosis: problems associated with laboratory identification. Br J Biomed Sci , 59(3): 164–166
pmid:12371061
77 Nadel D M, Lanza D C, Kennedy D W (1999). Endoscopically guided sinus cultures in normal subjects. Am J Rhinol , 13(2): 87–90
doi: 10.2500/105065899782106742 pmid:10219435
78 Nyvad B, Kilian M (1987). Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res , 95(5): 369–380
pmid:3477852
79 Palmer R J Jr, Gordon S M, Cisar J O, Kolenbrander P E (2003). Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J Bacteriol , 185(11): 3400–3409
doi: 10.1128/JB.185.11.3400-3409.2003 pmid:12754239
80 Palmer R J Jr, Kazmerzak K, Hansen M C, Kolenbrander P E (2001). Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect Immun , 69(9): 5794–5804
doi: 10.1128/IAI.69.9.5794-5804.2001 pmid:11500457
81 Park J E, Yung R, Stefanowicz D, Shumansky K, Akhabir L, Durie P R, Corey M, Zielenski J, Dorfman R, Daley D, Sandford A J(2011). Cystic fibrosis modifier genes related to Pseudomonas aeruginosa infection. Genes Immun,
doi: 10.1038/gene.2011.5
82 Periasamy S, Kolenbrander P E (2009). Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol, 191(22): 6804–6411
83 Perloff J R, Palmer J N (2004). Evidence of bacterial biofilms on frontal recess stents in patients with chronic rhinosinusitis. Am J Rhinol , 18(6): 377–380
pmid:15706985
84 Peters B M, Jabra-Rizk M A, Scheper M A, Leid J G, Costerton J W, Shirtliff M E(2010). Microbial interactions and differential protein expre ssion in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol, 59(3): 493–503
85 Prince A A, Steiger J D, Khalid A N, Dogrhamji L, Reger C, Eau Claire S, Chiu A G, Kennedy D W, Palmer J N, Cohen N A (2008). Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol , 22(3): 239–245
doi: 10.2500/ajr.2008.22.3180 pmid:18588755
86 Proctor R A, Von Eiff C, Kahl B C, Becker K, McNamara P, Herrmann M,Peters G(2006). Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol , 4(4): 295–305
87 Ramsey M M, Whiteley M(2009). Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci U S A, 106(5): 1578–1583
88 Rickard A H, Palmer R J Jr, Blehert D S, Campagna S R, Semmelhack M F, Egland P G, Bassler B L,Kolenbrander P E(2006). Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol, 60(6): 1446–1456
89 Roberts M E, Stewart P S (2004). Modeling antibiotic tolerance in biofilms by accounting for nutrient limitation. Antimicrob Agents Chemother , 48(1): 48–52
doi: 10.1128/AAC.48.1.48-52.2004 pmid:14693517
90 Rolauffs B, Bernhardt T M, von Eiff C, Hart M L, Bettin D (2002). Osteopetrosis, femoral fracture, and chronic osteomyelitis caused by Staphylococcus aureus small colony variants (SCV) treated by girdlestone resection—6-year follow-up. Arch Orthop Trauma Surg , 122(9-10): 547–550
doi: 10.1007/s00402-002-0435-2 pmid:12483342
91 Romano J D,Kolter R(2005). Pseudomonas-Saccharomyces interactions: influence of fungal metabolism on bacterial physiology and survival. J Bacteriol, 187(3): 940–948
92 Ryan R P,Dow J M(2008). Diffusible signals and interspecies communication in bacteria. Microbiology, 154(7): 1845–1858
93 Sanderson A R, Leid J G, Hunsaker D(2006). Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope, 116(7): 1121–1126
94 Schauder S, Shokat K, Surette M G, Bassler B L(2001). The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol , 41(2): 463–476
95 Shirtliff M E, Peters B M, Jabra-Rizk M A(2009). Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett , 299(1): 1–8
96 Soni K A, Lu L, Jesudhasan P R, Hume M E,Pillai S D(2008). Influence of autoinducer-2 (AI-2) and beef sample extracts on E. coli O157:H7 survival and gene expression of virulence genes yadK and hhA. J Food Sci, 73(3): M135–M139
97 Soni K, Jesudhasan P, Cepeda M, Williams B, Hume M, Russell W K, Jayaraman A, Pillai S D (2007). Proteomic analysis to identify the role of LuxS/AI-2 mediated protein expression in Escherichia coli O157:H7. Foodborne Pathog Dis , 4(4): 463–471
doi: 10.1089/fpd.2007.0034 pmid:18041955
98 Stelzmueller I, Biebl M, Wiesmayr S, Eller M, Hoeller E, Fille M, Weiss G, Lass-Floerl C, Bonatti H(2006). Ralstonia pickettii —innocent bystander or a potential threat? Clin Microbiol Infect, 12(2): 99–101
99 Stephenson M F, Mfuna L, Dowd S E, Wolcott R D, Barbeau J, Poisson M, James G, Desrosiers M (2010). Molecular characterization of the polymicrobial flora in chronic rhinosinusitis. J Otolaryngol Head Neck Surg , 39(2): 182–187
pmid:20211106
100 Stone A, Saiman L(2007). Update on the epidemiology and management of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, in patients with cystic fibrosis. Curr Opin Pulm Med, 13(6): 515–521
101 Surette M G, Miller M B, Bassler B L (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(4): 1639–1644
doi: 10.1073/pnas.96.4.1639 pmid:9990077
102 Swem L R, Swem D L, O’Loughlin C T, Gatmaitan R, Zhao B, Ulrich S M, Bassler B L(2009). A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell, 35(2): 143–153
103 Taga M E, Semmelhack J L, Bassler B L(2001). The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol Microbiol, 42(3): 777–793
104 Tribble G D, Lamont G J, Progulske-Fox A, Lamont R J(2007). Conjugal transfer of chromosomal DNA contributes to genetic variation in the oral pathogen Porphyromonas gingivalis. J Bacteriol, 189(17): 6382–6388
105 Ulrich L E,Zhulin I B(2007). MiST: a microbial signal transduction database. Nucleic Acids Res, 35(Database issue): D386–D390
106 Waters C M, Bassler B L (2005). Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol , 21(1): 319–346
doi: 10.1146/annurev.cellbio.21.012704.131001 pmid:16212498
107 Weimer K E, Armbruster C E, Juneau R A, Hong W, Pang B, Swords W E (2010). Coinfection with Haemophilus influenzae promotes pneumococcal biofilm formation during experimental otitis media and impedes the progression of pneumococcal disease. J Infect Dis , 202(7): 1068–1075
doi: 10.1086/656046 pmid:20715928
108 Wellinghausen N, Essig A, Sommerburg O (2005). Inquilinus limosus in patients with cystic fibrosis, Germany. Emerg Infect Dis , 11(3): 457–459
pmid:15757565
109 Wolcott R, Dowd S(2011). The role of biofilms: are we hitting the right target? Plast Reconstr Surg, 127 (Suppl 1): 28–35
110 Xavier K B,Bassler B L(2005). Interference with AI-2-mediated bacterial cell-cell communication. Nature, 437(7059): 750–753
111 Xu K D, Stewart P S, Xia F, Huang C T, McFeters G A (1998). Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol , 64(10): 4035–4039
pmid:9758837
112 Zhao L, Xue T, Shang F, Sun H,Sun B(2010). Staphylococcus aureus AI-2 quorum sensing associates with the KdpDE two-component system to regulate capsular polysaccharide synthesis and virulence. Infect Immun, 78(8): 3506–3815
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