Metabolite cross-feeding enhances virulence in a model polymicrobial infection

PLoS Pathogens

Volumn 7, Issue 3, 2011, Pages

  Ramsey, Matthew M ^a   Rumbaugh, Kendra P ^b   Whiteley, Marvin ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; LACTIC ACID;

ABSCESS; AEROBIC METABOLISM; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; CATABOLISM; COCULTURE; CONTROLLED STUDY; GLUCOSE METABOLISM; METABOLITE; METABOLITE CROSS FEEDING; MIXED INFECTION; MOUSE; NONHUMAN; PATHOGENESIS; STREPTOCOCCUS GORDONII; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; ORGANISMAL INTERACTION; PASTEURELLACEAE; PATHOGENICITY;

MURINAE; STREPTOCOCCUS GORDONII;

ABSCESS; ANIMALS; COCULTURE TECHNIQUES; COINFECTION; GLUCOSE; LACTIC ACID; MICE; MICROBIAL INTERACTIONS; MUTATION; PASTEURELLACEAE; STREPTOCOCCUS GORDONII;

EID: 79953284689     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002012     Document Type: Article

References (58)

1. Brown SA, Palmer KL, Whiteley M, (2008) Revisiting the host as a growth medium. Nat Rev Microbiol 6: 657-666.
2. Brouqui P, Raoult D, (2001) Endocarditis due to rare and fastidious bacteria. Clin Microbiol Rev 14: 177-207.
3. Jenkinson HF, Lamont RJ, (2005) Oral microbial communities in sickness and in health. Trends Microbiol 13: 589-595.
4. Kuramitsu HK, He X, Lux R, Anderson MH, Shi W, (2007) Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71: 653-670.
5. Bakaletz LO, (2004) Developing animal models for polymicrobial diseases. Nat Rev Microbiol 2: 552-568.
6. Brown SA, Whiteley M, (2007) A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol 189: 6407-6414.
7. Ramsey MM, Whiteley M, (2009) Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci U S A 106: 1578-1583.
8. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK, (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61: 1308-1321.
9. Ebersole JL, Cappelli D, Sandoval MN, (1994) Subgingival distribution of A. actinomycetemcomitans in periodontitis. J Clin Periodontol 21: 65-75.
10. Meyer DH, Fives-Taylor PM, (1998) Oral pathogens: from dental plaque to cardiac disease. Curr Opin Microbiol 1: 88-95.
11. Loesche WJ, Gusberti F, Mettraux G, Higgins T, Syed S, (1983) Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect Immun 42: 659-667.
12. Courts FJ, Boackle RJ, Fudenberg HH, Silverman MS, (1977) Detection of functional complement components in gingival crevicular fluid from humans with periodontal diseases. J Dent Res 56: 327-331.
13. Yamaguchi M, Kawabata Y, Kambe S, Wardell K, Nystrom FH, et al. (2004) Non-invasive monitoring of gingival crevicular fluid for estimation of blood glucose level. Med Biol Eng Comput 42: 322-327.
14. Ciantar M, Spratt DA, Newman HN, Wilson M, (2002) Development of an in vitro microassay for glucose quantification in submicrolitre volumes of biological fluid. J Periodontal Res 37: 79-85.
15. Serra E, Perinetti G, D'Attilio M, Cordella C, Paolantonio M, et al. (2003) Lactate dehydrogenase activity in gingival crevicular fluid during orthodontic treatment. Am J Orthod Dentofacial Orthop 124: 206-211.
16. Lamster IB, Hartley LJ, Oshrain RL, Gordon JM, (1985) Evaluation and modification of spectrophotometric procedures for analysis of lactate dehydrogenase, beta-glucuronidase and arylsulphatase in human gingival crevicular fluid collected with filter-paper strips. Arch Oral Biol 30: 235-242.
17. Bergey DH, (1994) Bergey's Manual of Determinitive Bacteriology. In: Holt JG, editors. Baltimore Williams & Wilkins.
18. Dzink JL, Tanner AC, Haffajee AD, Socransky SS, (1985) Gram negative species associated with active destructive periodontal lesions. J Clin Periodontol 12: 648-659.
19. Kreth J, Merritt J, Qi F, (2009) Bacterial and host interactions of oral streptococci. DNA Cell Biol 28: 397-403.
20. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, et al. (2002) Communication among oral bacteria. Microbiol Mol Biol Rev 66: 486-505.
21. Moore WE, Holdeman LV, Smibert RM, Hash DE, Burmeister JA, et al. (1982) Bacteriology of severe periodontitis in young adult humans. Infect Immun 38: 1137-1148.
22. Syed SA, Loesche WJ, (1978) Bacteriology of human experimental gingivitis: effect of plaque age. Infect Immun 21: 821-829.
23. Cook GS, Costerton JW, Lamont RJ, (1998) Biofilm formation by Porphyromonas gingivalis and Streptococcus gordonii. J Periodontal Res 33: 323-327.
24. Egland PG, Palmer RJ Jr, Kolenbrander PE, (2004) Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc Natl Acad Sci U S A 101: 16917-16922.
25. Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, et al. (2003) Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50: 1125-1139.
26. Kononen E, Paju S, Pussinen PJ, Hyvonen M, Di Tella P, et al. (2007) Population-based study of salivary carriage of periodontal pathogens in adults. J Clin Microbiol 45: 2446-2451.
27. Sirinian G, Shimizu T, Sugar C, Slots J, Chen C, (2002) Periodontopathic bacteria in young healthy subjects of different ethnic backgrounds in Los Angeles. J Periodontol 73: 283-288.
28. Nuttall FQ, Khan MA, Gannon MC, (2000) Peripheral glucose appearance rate following fructose ingestion in normal subjects. Metabolism 49: 1565-1571.
29. Brown SA, Whiteley M, (2009) Characterization of the L-lactate dehydrogenase from Aggregatibacter actinomycetemcomitans. PLoS One 4: e7864.
30. Talasniemi JP, Pennanen S, Savolainen H, Niskanen L, Liesivuori J, (2008) Analytical investigation: assay of D-lactate in diabetic plasma and urine. Clin Biochem 41: 1099-1103.
31. Kolenbrander P, (2006) The genus Veillonella. In: Dworkin M, editors. The Prokaryotes.Third ed New York Springer pp. 1022-1040.
32. Chen C, Kittichotirat W, Si Y, Bumgarner R, (2009) Genome sequence of Aggregatibacter actinomycetemcomitans serotype c strain D11S-1. J Bacteriol 191: 7378-7379.
33. Chen C, Kittichotirat W, Chen W, Downey JS, Si Y, et al. (2010) Genome sequence of naturally competent Aggregatibacter actinomycetemcomitans serotype a strain D7S-1. J Bacteriol 192: 2643-2644.
34. Kaplan AH, Weber DJ, Oddone EZ, Perfect JR, (1989) Infection due to Actinobacillus actinomycetemcomitans: 15 cases and review. Rev Infect Dis 11: 46-63.
35. Ebersole JL, Kesavalu L, Schneider SL, Machen RL, Holt SC, (1995) Comparative virulence of periodontopathogens in a mouse abscess model. Oral Dis 1: 115-128.
36. Kesavalu L, Holt SC, Ebersole JL, (1998) Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol 13: 373-377.
37. Mastropaolo MD, Evans NP, Byrnes MK, Stevens AM, Robertson JL, et al. (2005) Synergy in polymicrobial infections in a mouse model of type 2 diabetes. Infect Immun 73: 6055-6063.
38. Kozarov EV, Dorn BR, Shelburne CE, Dunn WA Jr, Progulske-Fox A, (2005) Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 25: e17-18.
39. Nagashima H, Takao A, Maeda N, (1999) Abscess forming ability of streptococcus milleri group: synergistic effect with Fusobacterium nucleatum. Microbiol Immunol 43: 207-216.
40. Chen PB, Davern LB, Katz J, Eldridge JH, Michalek SM, (1996) Host responses induced by co-infection with Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in a murine model. Oral Microbiol Immunol 11: 274-281.
41. Periasamy S, Kolenbrander PE, (2009) Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva. Infect Immun 77: 3542-3551.
42. Schultz JE, Breznak JA, (1979) Cross-Feeding of Lactate Between Streptococcus lactis and Bacteroides sp. Isolated from Termite Hindguts. Appl Environ Microbiol 37: 1206-1210.
43. Kesavalu L, Sathishkumar S, Bakthavatchalu V, Matthews C, Dawson D, et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704-1712.
44. Fine DH, Goncharoff P, Schreiner H, Chang KM, Furgang D, et al. (2001) Colonization and persistence of rough and smooth colony variants of Actinobacillus actinomycetemcomitans in the mouths of rats. Arch Oral Biol 46: 1065-1078.
45. Fine DH, Furgang D, Kaplan J, Charlesworth J, Figurski DH, (1999) Tenacious adhesion of Actinobacillus actinomycetemcomitans strain CU1000 to salivary-coated hydroxyapatite. Arch Oral Biol 44: 1063-1076.
46. Fine DH, Furgang D, Schreiner HC, Goncharoff P, Charlesworth J, et al. (1999) Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 145 (Pt 6): 1335-1347.
47. Han G, Martinez LR, Mihu MR, Friedman AJ, Friedman JM, et al. (2009) Nitric oxide releasing nanoparticles are therapeutic for Staphylococcus aureus abscesses in a murine model of infection. PLoS One 4: e7804.
48. Fetiye K, Karadenizli A, Okay E, Oz S, Budak F, et al. (2004) Comparison in a rat thigh abscess model of imipenem, meropenem and cefoperazone-sulbactam against Acinetobacter baumannii strains in terms of bactericidal efficacy and resistance selection. Ann Clin Microbiol Antimicrob 3: 2.
49. Dworkin M, Falkow S, (2006) The prokaryotes: a handbook on the biology of bacteria. New York; [London] Springer pp. v.1-6.
50. Kreth J, Zhang Y, Herzberg MC, (2008) Streptococcal Antagonism In Oral Biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 190: 4632-4640.
51. Slots J, Reynolds HS, Genco RJ, (1980) Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun 29: 1013-1020.
52. Yamada H, Takashima E, Konishi K, (2007) Molecular characterization of the membrane-bound quinol peroxidase functionally connected to the respiratory chain. FEBS J 274: 853-866.
53. Mintz KP, Fives-Taylor PM, (2000) impA, a gene coding for an inner membrane protein, influences colonial morphology of Actinobacillus actinomycetemcomitans. Infect Immun 68: 6580-6586.
54. Ausubel FM, (2002) Short protocols in molecular biology: a compendium of methods from Current protocols in molecular biology. 2 v New York Wiley.
55. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
56. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
57. Mintz KP, Brissette C, Fives-Taylor PM, (2002) A recombinase A-deficient strain of Actinobacillus actinomycetemcomitans constructed by insertional mutagenesis using a mobilizable plasmid. FEMS Microbiol Lett 206: 87-92.
58. Galli DM, Polan-Curtain JL, LeBlanc DJ, (1996) Structural and segregational stability of various replicons in Actinobacillus actinomycetemcomitans. Plasmid 36: 42-48.