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Metabolite Cross-Feeding Enhances Virulence in a Model Polymicrobial Infection


Microbes within polymicrobial infections often display synergistic interactions resulting in enhanced pathogenesis; however, the molecular mechanisms governing these interactions are not well understood. Development of model systems that allow detailed mechanistic studies of polymicrobial synergy is a critical step towards a comprehensive understanding of these infections in vivo. In this study, we used a model polymicrobial infection including the opportunistic pathogen Aggregatibacter actinomycetemcomitans and the commensal Streptococcus gordonii to examine the importance of metabolite cross-feeding for establishing co-culture infections. Our results reveal that co-culture with S. gordonii enhances the pathogenesis of A. actinomycetemcomitans in a murine abscess model of infection. Interestingly, the ability of A. actinomycetemcomitans to utilize L-lactate as an energy source is essential for these co-culture benefits. Surprisingly, inactivation of L-lactate catabolism had no impact on mono-culture growth in vitro and in vivo suggesting that A. actinomycetemcomitans L-lactate catabolism is only critical for establishing co-culture infections. These results demonstrate that metabolite cross-feeding is critical for A. actinomycetemcomitans to persist in a polymicrobial infection with S. gordonii supporting the idea that the metabolic properties of commensal bacteria alter the course of pathogenesis in polymicrobial communities.


Vyšlo v časopise: Metabolite Cross-Feeding Enhances Virulence in a Model Polymicrobial Infection. PLoS Pathog 7(3): e32767. doi:10.1371/journal.ppat.1002012
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002012

Souhrn

Microbes within polymicrobial infections often display synergistic interactions resulting in enhanced pathogenesis; however, the molecular mechanisms governing these interactions are not well understood. Development of model systems that allow detailed mechanistic studies of polymicrobial synergy is a critical step towards a comprehensive understanding of these infections in vivo. In this study, we used a model polymicrobial infection including the opportunistic pathogen Aggregatibacter actinomycetemcomitans and the commensal Streptococcus gordonii to examine the importance of metabolite cross-feeding for establishing co-culture infections. Our results reveal that co-culture with S. gordonii enhances the pathogenesis of A. actinomycetemcomitans in a murine abscess model of infection. Interestingly, the ability of A. actinomycetemcomitans to utilize L-lactate as an energy source is essential for these co-culture benefits. Surprisingly, inactivation of L-lactate catabolism had no impact on mono-culture growth in vitro and in vivo suggesting that A. actinomycetemcomitans L-lactate catabolism is only critical for establishing co-culture infections. These results demonstrate that metabolite cross-feeding is critical for A. actinomycetemcomitans to persist in a polymicrobial infection with S. gordonii supporting the idea that the metabolic properties of commensal bacteria alter the course of pathogenesis in polymicrobial communities.


Zdroje

1. BrownSAPalmerKLWhiteleyM 2008 Revisiting the host as a growth medium. Nat Rev Microbiol 6 657 666

2. BrouquiPRaoultD 2001 Endocarditis due to rare and fastidious bacteria. Clin Microbiol Rev 14 177 207

3. JenkinsonHFLamontRJ 2005 Oral microbial communities in sickness and in health. Trends Microbiol 13 589 595

4. KuramitsuHKHeXLuxRAndersonMHShiW 2007 Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71 653 670

5. BakaletzLO 2004 Developing animal models for polymicrobial diseases. Nat Rev Microbiol 2 552 568

6. BrownSAWhiteleyM 2007 A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol 189 6407 6414

7. RamseyMMWhiteleyM 2009 Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci U S A 106 1578 1583

8. DietrichLEPrice-WhelanAPetersenAWhiteleyMNewmanDK 2006 The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61 1308 1321

9. EbersoleJLCappelliDSandovalMN 1994 Subgingival distribution of A. actinomycetemcomitans in periodontitis. J Clin Periodontol 21 65 75

10. MeyerDHFives-TaylorPM 1998 Oral pathogens: from dental plaque to cardiac disease. Curr Opin Microbiol 1 88 95

11. LoescheWJGusbertiFMettrauxGHigginsTSyedS 1983 Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect Immun 42 659 667

12. CourtsFJBoackleRJFudenbergHHSilvermanMS 1977 Detection of functional complement components in gingival crevicular fluid from humans with periodontal diseases. J Dent Res 56 327 331

13. YamaguchiMKawabataYKambeSWardellKNystromFH 2004 Non-invasive monitoring of gingival crevicular fluid for estimation of blood glucose level. Med Biol Eng Comput 42 322 327

14. CiantarMSprattDANewmanHNWilsonM 2002 Development of an in vitro microassay for glucose quantification in submicrolitre volumes of biological fluid. J Periodontal Res 37 79 85

15. SerraEPerinettiGD'AttilioMCordellaCPaolantonioM 2003 Lactate dehydrogenase activity in gingival crevicular fluid during orthodontic treatment. Am J Orthod Dentofacial Orthop 124 206 211

16. LamsterIBHartleyLJOshrainRLGordonJM 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. BergeyDH 1994 Bergey's Manual of Determinitive Bacteriology. HoltJG Baltimore Williams & Wilkins

18. DzinkJLTannerACHaffajeeADSocranskySS 1985 Gram negative species associated with active destructive periodontal lesions. J Clin Periodontol 12 648 659

19. KrethJMerrittJQiF 2009 Bacterial and host interactions of oral streptococci. DNA Cell Biol 28 397 403

20. KolenbranderPEAndersenRNBlehertDSEglandPGFosterJS 2002 Communication among oral bacteria. Microbiol Mol Biol Rev 66 486 505

21. MooreWEHoldemanLVSmibertRMHashDEBurmeisterJA 1982 Bacteriology of severe periodontitis in young adult humans. Infect Immun 38 1137 1148

22. SyedSALoescheWJ 1978 Bacteriology of human experimental gingivitis: effect of plaque age. Infect Immun 21 821 829

23. CookGSCostertonJWLamontRJ 1998 Biofilm formation by Porphyromonas gingivalis and Streptococcus gordonii. J Periodontal Res 33 323 327

24. EglandPGPalmerRJJrKolenbranderPE 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. AsakawaRKomatsuzawaHKawaiTYamadaSGoncalvesRB 2003 Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50 1125 1139

26. KononenEPajuSPussinenPJHyvonenMDi TellaP 2007 Population-based study of salivary carriage of periodontal pathogens in adults. J Clin Microbiol 45 2446 2451

27. SirinianGShimizuTSugarCSlotsJChenC 2002 Periodontopathic bacteria in young healthy subjects of different ethnic backgrounds in Los Angeles. J Periodontol 73 283 288

28. NuttallFQKhanMAGannonMC 2000 Peripheral glucose appearance rate following fructose ingestion in normal subjects. Metabolism 49 1565 1571

29. BrownSAWhiteleyM 2009 Characterization of the L-lactate dehydrogenase from Aggregatibacter actinomycetemcomitans. PLoS One 4 e7864

30. TalasniemiJPPennanenSSavolainenHNiskanenLLiesivuoriJ 2008 Analytical investigation: assay of D-lactate in diabetic plasma and urine. Clin Biochem 41 1099 1103

31. KolenbranderP 2006 The genus Veillonella. DworkinM The Prokaryotes.Third ed New York Springer 1022 1040

32. ChenCKittichotiratWSiYBumgarnerR 2009 Genome sequence of Aggregatibacter actinomycetemcomitans serotype c strain D11S-1. J Bacteriol 191 7378 7379

33. ChenCKittichotiratWChenWDowneyJSSiY 2010 Genome sequence of naturally competent Aggregatibacter actinomycetemcomitans serotype a strain D7S-1. J Bacteriol 192 2643 2644

34. KaplanAHWeberDJOddoneEZPerfectJR 1989 Infection due to Actinobacillus actinomycetemcomitans: 15 cases and review. Rev Infect Dis 11 46 63

35. EbersoleJLKesavaluLSchneiderSLMachenRLHoltSC 1995 Comparative virulence of periodontopathogens in a mouse abscess model. Oral Dis 1 115 128

36. KesavaluLHoltSCEbersoleJL 1998 Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol 13 373 377

37. MastropaoloMDEvansNPByrnesMKStevensAMRobertsonJL 2005 Synergy in polymicrobial infections in a mouse model of type 2 diabetes. Infect Immun 73 6055 6063

38. KozarovEVDornBRShelburneCEDunnWAJrProgulske-FoxA 2005 Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 25 e17 18

39. NagashimaHTakaoAMaedaN 1999 Abscess forming ability of streptococcus milleri group: synergistic effect with Fusobacterium nucleatum. Microbiol Immunol 43 207 216

40. ChenPBDavernLBKatzJEldridgeJHMichalekSM 1996 Host responses induced by co-infection with Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in a murine model. Oral Microbiol Immunol 11 274 281

41. PeriasamySKolenbranderPE 2009 Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva. Infect Immun 77 3542 3551

42. SchultzJEBreznakJA 1979 Cross-Feeding of Lactate Between Streptococcus lactis and Bacteroides sp. Isolated from Termite Hindguts. Appl Environ Microbiol 37 1206 1210

43. KesavaluLSathishkumarSBakthavatchaluVMatthewsCDawsonD 2007 Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75 1704 1712

44. FineDHGoncharoffPSchreinerHChangKMFurgangD 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. FineDHFurgangDKaplanJCharlesworthJFigurskiDH 1999 Tenacious adhesion of Actinobacillus actinomycetemcomitans strain CU1000 to salivary-coated hydroxyapatite. Arch Oral Biol 44 1063 1076

46. FineDHFurgangDSchreinerHCGoncharoffPCharlesworthJ 1999 Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 145 Pt 6 1335 1347

47. HanGMartinezLRMihuMRFriedmanAJFriedmanJM 2009 Nitric oxide releasing nanoparticles are therapeutic for Staphylococcus aureus abscesses in a murine model of infection. PLoS One 4 e7804

48. FetiyeKKaradenizliAOkayEOzSBudakF 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. DworkinMFalkowS 2006 The prokaryotes : a handbook on the biology of bacteria. New York ;[London] Springer v.1 6

50. KrethJZhangYHerzbergMC 2008 Streptococcal Antagonism In Oral Biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 190 4632 4640

51. SlotsJReynoldsHSGencoRJ 1980 Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun 29 1013 1020

52. YamadaHTakashimaEKonishiK 2007 Molecular characterization of the membrane-bound quinol peroxidase functionally connected to the respiratory chain. FEBS J 274 853 866

53. MintzKPFives-TaylorPM 2000 impA, a gene coding for an inner membrane protein, influences colonial morphology of Actinobacillus actinomycetemcomitans. Infect Immun 68 6580 6586

54. AusubelFM 2002 Short protocols in molecular biology : a compendium of methods from Current protocols in molecular biology. 2 v New York Wiley

55. KovachMEElzerPHHillDSRobertsonGTFarrisMA 1995 Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166 175 176

56. HoSNHuntHDHortonRMPullenJKPeaseLR 1989 Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77 51 59

57. MintzKPBrissetteCFives-TaylorPM 2002 A recombinase A-deficient strain of Actinobacillus actinomycetemcomitans constructed by insertional mutagenesis using a mobilizable plasmid. FEMS Microbiol Lett 206 87 92

58. GalliDMPolan-CurtainJLLeBlancDJ 1996 Structural and segregational stability of various replicons in Actinobacillus actinomycetemcomitans. Plasmid 36 42 48

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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