1887

Abstract

is the major aetiological agent of chronic pulmonary infections in cystic fibrosis (CF) patients. However, recent evidence suggests that the polymicrobial community of the CF lung may also harbour oral streptococci, and colonization by these micro-organisms may have a negative impact on within the CF lung. Our previous studies demonstrated that nitrite abundance plays an important role in survival during co-infection with oral streptococci. Nitrite reductase is a key enzyme involved in nitrite metabolism. Therefore, the objective of this study was to examine the role nitrite reductase (gene ) plays in survival during co-infection with an oral streptococcus, . Inactivation of in both the chronic CF isolate FRD1 and acute wound isolate PAO1 reduced the survival rate of when co-cultured with . Growth of both mutants was restored when co-cultured with that was defective for HO production. Furthermore, the nitrite reductase mutant was unable to kill during co-infection with . Taken together, these results suggest that nitrite reductase plays an important role for survival of during co-infection with .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000226
2016-02-01
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/2/376.html?itemId=/content/journal/micro/10.1099/mic.0.000226&mimeType=html&fmt=ahah

References

  1. Akhtar S., Khan A., Sohaskey C. D., Jagannath C., Sarkar D. 2013; Nitrite reductase NirBD is induced and plays an important role during in vitro dormancy of Mycobacterium tuberculosis . J Bacteriol 195:4592–4599 [View Article][PubMed]
    [Google Scholar]
  2. Carmeli Y., Troillet N., Eliopoulos G. M., Samore M. H. 1999; Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different antipseudomonal agents. Antimicrob Agents Chemother 43:1379–1382[PubMed]
    [Google Scholar]
  3. Cole R. M., Calandra G. B., Huff E., Nugent K. M. 1976; Attributes of potential utility in differentiating among “group H” streptococci or Streptococcus sanguis . J Dent Res 55:(Suppl.)A142–A153 [View Article][PubMed]
    [Google Scholar]
  4. de la Fuente-Núñez C., Reffuveille F., Fairfull-Smith K. E., Hancock R. E. 2013; Effect of nitroxides on swarming motility and biofilm formation, multicellular behaviors in Pseudomonas aeruginosa . Antimicrob Agents Chemother 57:4877–4881 [View Article][PubMed]
    [Google Scholar]
  5. Doel J. J., Hector M. P., Amirtham C. V., Al-Anzan L. A., Benjamin N., Allaker R. P. 2004; Protective effect of salivary nitrate and microbial nitrate reductase activity against caries. Eur J Oral Sci 112:424–428 [View Article][PubMed]
    [Google Scholar]
  6. Filkins L. M., Hampton T. H., Gifford A. H., Gross M. J., Hogan D. A., Sogin M. L., Morrison H. G., Paster B. J., O'Toole G. A. 2012; Prevalence of streptococci and increased polymicrobial diversity associated with cystic fibrosis patient stability. J Bacteriol 194:4709–4717 [View Article][PubMed]
    [Google Scholar]
  7. Grasemann H., Ioannidis I., Tomkiewicz R. P., de Groot H., Rubin B. K., Ratjen F. 1998; Nitric oxide metabolites in cystic fibrosis lung disease. Arch Dis Child 78:49–53 [View Article][PubMed]
    [Google Scholar]
  8. Hezel M. P., Weitzberg E. 2015; The oral microbiome and nitric oxide homoeostasis. Oral Dis 21:7–16 [View Article][PubMed]
    [Google Scholar]
  9. Holloway B. W., Krishnapillai V., Morgan A. F. 1979; Chromosomal genetics of Pseudomonas . Microbiol Rev 43:73–102[PubMed]
    [Google Scholar]
  10. Hyde E. R., Andrade F., Vaksman Z., Parthasarathy K., Jiang H., Parthasarathy D. K., Torregrossa A. C., Tribble G., Kaplan H. B., other authors. 2014; Metagenomic analysis of nitrate-reducing bacteria in the oral cavity: implications for nitric oxide homeostasis. PLoS One 9:e88645 [View Article][PubMed]
    [Google Scholar]
  11. Kolenbrander P. E., London J. 1993; Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175:3247–3252[PubMed]
    [Google Scholar]
  12. Kreth J., Zhang Y., Herzberg M. C. 2008; Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans . J Bacteriol 190:4632–4640 [View Article][PubMed]
    [Google Scholar]
  13. Lewis J. P., Yanamandra S. S., Anaya-Bergman C. 2012; HcpR of Porphyromonas gingivalis is required for growth under nitrosative stress and survival within host cells. Infect Immun 80:3319–3331 [View Article][PubMed]
    [Google Scholar]
  14. Liu J., Wu C., Huang I. H., Merritt J., Qi F. 2011; Differential response of Streptococcus mutans towards friend and foe in mixed-species cultures. Microbiology 157:2433–2444 [View Article][PubMed]
    [Google Scholar]
  15. Maeda Y., Elborn J. S., Parkins M. D., Reihill J., Goldsmith C. E., Coulter W. A., Mason C., Millar B. C., Dooley J. S. G., other authors. 2011; Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). J Cyst Fibros 10:133–139 [View Article][PubMed]
    [Google Scholar]
  16. Majorana A., Notarangelo L. D., Savoldi E., Gastaldi G., Lozada-Nur F. 1999; Leukocyte adhesion deficiency in a child with severe oral involvement. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 87:691–694 [View Article][PubMed]
    [Google Scholar]
  17. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  18. Nobbs A. H., Lamont R. J., Jenkinson H. F. 2009; Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73:407–450 [View Article][PubMed]
    [Google Scholar]
  19. Ohman D. E., Chakrabarty A. M. 1981; Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect Immun 33:142–148[PubMed]
    [Google Scholar]
  20. Parkins M. D., Sibley C. D., Surette M. G., Rabin H. R. 2008; The Streptococcus milleri group—an unrecognized cause of disease in cystic fibrosis: a case series and literature review. Pediatr Pulmonol 43:490–497 [View Article][PubMed]
    [Google Scholar]
  21. Peters B. M., Jabra-Rizk M. A., O'May G. A., Costerton J. W., Shirtliff M. E. 2012; Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25:193–213 [View Article][PubMed]
    [Google Scholar]
  22. Ramsey M. M., Whiteley M. 2009; Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci U S A 106:1578–1583 [View Article][PubMed]
    [Google Scholar]
  23. Schweizer H. D. 1993; Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. Biotechniques 15:831–834[PubMed]
    [Google Scholar]
  24. Scoffield J. A., Wu H. 2015; Oral streptococci and nitrite-mediated interference of Pseudomonas aeruginosa . Infect Immun 83:101–107 [View Article][PubMed]
    [Google Scholar]
  25. Sibley C. D., Parkins M. D., Rabin H. R., Duan K., Norgaard J. C., Surette M. G. 2008; A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A 105:15070–15075 [View Article][PubMed]
    [Google Scholar]
  26. Smith E. E., Buckley D. G., Wu Z., Saenphimmachak C., Hoffman L. R., D'Argenio D. A., Miller S. I., Ramsey B. W., Speert D. P., other authors. 2006; Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103:8487–8492 [View Article][PubMed]
    [Google Scholar]
  27. Stacy A., Everett J., Jorth P., Trivedi U., Rumbaugh K. P., Whiteley M. 2014; Bacterial fight-and-flight responses enhance virulence in a polymicrobial infection. Proc Natl Acad Sci U S A 111:7819–7824 [View Article][PubMed]
    [Google Scholar]
  28. Su S., Panmanee W., Wilson J. J., Mahtani H. K., Li Q., Vanderwielen B. D., Makris T. M., Rogers M., McDaniel C., other authors. 2014; Catalase (KatA) plays a role in protection against anaerobic nitric oxide in Pseudomonas aeruginosa . PLoS One 9:e91813 [View Article][PubMed]
    [Google Scholar]
  29. Suh S. J., Silo-Suh L. A., Ohman D. E. 2004; Development of tools for the genetic manipulation of Pseudomonas aeruginosa . J Microbiol Methods 58:203–212 [View Article][PubMed]
    [Google Scholar]
  30. Van Alst N. E., Wellington M., Clark V. L., Haidaris C. G., Iglewski B. H. 2009; Nitrite reductase NirS is required for type III secretion system expression and virulence in the human monocyte cell line THP-1 by Pseudomonas aeruginosa . Infect Immun 77:4446–4454 [View Article][PubMed]
    [Google Scholar]
  31. Whiley R. A., Sheikh N. P., Mushtaq N., Hagi-Pavli E., Personne Y., Javaid D., Waite R. D. 2014; Differential potentiation of the virulence of the Pseudomonas aeruginosa cystic fibrosis Liverpool epidemic strain by oral commensal streptococci. J Infect Dis 209:769–780 [View Article][PubMed]
    [Google Scholar]
  32. Whiley R. A., Fleming E. V., Makhija R., Waite R. D. 2015; Environment and colonisation sequence are key parameters driving cooperation and competition between Pseudomonas aeruginosa cystic fibrosis strains and oral commensal streptococci. PLoS One 10:e0115513 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.000226
Loading
/content/journal/micro/10.1099/mic.0.000226
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error