Pseudomonas aeruginosa exhibits deficient biofilm formation in the absence of class II and III ribonucleotide reductases due to hindered anaerobic growth

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Crespo, Anna ^a   Pedraz, Lucas ^a   Astola, Josep ^a   Torrents, Eduard ^a  

^a INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

Author keywords

Anaerobic metabolism; Biofilm formation; DNA synthesis; Nrd genes; Oxygen diffusion; Pseudomonas aeruginosa; Ribonucleotide reductases; Vitamin B12

Indexed keywords

DNA FRAGMENT; GREEN FLUORESCENT PROTEIN; POTASSIUM NITRATE; RIBONUCLEOTIDE REDUCTASE; S NITROSOGLUTATHIONE; TRANSCRIPTION FACTOR;

ANAEROBIC GROWTH; ANAEROBIC METABOLISM; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL STRAIN; BIOFILM; CELL COMMUNICATION; CELL DIVISION; CELL ELONGATION; CELL MATURATION; CELL STRUCTURE; CONFOCAL LASER MICROSCOPY; DNA REPAIR; DNA SYNTHESIS; ESCHERICHIA COLI; GENE; GENE EXPRESSION; GENETIC REGULATION; NRDD GENE; NRDJ GENE; PHYSICAL STRESS; PLASMID; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; RECOMBINANT DNA TECHNOLOGY; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION; WESTERN BLOTTING;

EID: 84973449220     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00688     Document Type: Article

References (49)

1. Alvarez-Ortega, C., and Harwood, C. S. (2007). Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol. Microbiol. 65, 153-165. doi: 10.1111/j.1365-2958.2007.05772.x
2. Arai, H. (2003). Transcriptional regulation of the nos genes for nitrous oxide reductase in Pseudomonas aeruginosa. Microbiology 149, 29-36. doi: 10.1099/mic.0.25936-0
3. Arai, H. (2011). Regulation and function of versatile aerobic and anaerobic respiratory metabolism in Pseudomonas aeruginosa. Front. Microbiol. 2:103. doi: 10.3389/fmicb.2011.00103
4. Arat, S., Bullerjahn, G. S., and Laubenbacher, R. (2015). A network biology approach to denitrification in Pseudomonas aeruginosa. PLoS ONE 10:e0118235. doi: 10.1371/journal.pone.0118235
5. Baelo, A., Levato, R., Julian, E., Crespo, A., Astola, J., Gavalda, J., et al. (2015). Disassembling bacterial extracellular matrix with DNase-coated nanoparticles to enhance antibiotic delivery in biofilm infections. J. Control. Release 209, 150-158. doi: 10.1016/j.jconrel.2015.04.028
6. Benkert, B., Quack, N., Schreiber, K., Jaensch, L., Jahn, D., and Schobert, M. (2008). Nitrate-responsive NarX-NarL represses arginine-mediated induction of the Pseudomonas aeruginosa arginine fermentation arcDABC operon. Microbiology 154, 3053-3060. doi: 10.1099/mic.0.2008/018929-0
7. Borriello, G., Richards, L., Ehrlich, G. D., and Stewart, P. S. (2006). Arginine or nitrate enhances antibiotic susceptibility of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 50, 382-384. doi: 10.1128/AAC.50.1.382-384.2006
8. Castiglione, N., Rinaldo, S., Giardina, G., and Cutruzzola, F. (2009). The transcription factor DNR from Pseudomonas aeruginosa specifically requires nitric oxide and haem for the activation of a target promoter in Escherichia coli. Microbiology 155, 2838-2844. doi: 10.1099/mic.0.028027-0
9. Cendra Mdel, M., Juarez, A., and Torrents, E. (2012). Biofilm modifies expression of ribonucleotide reductase genes in Escherichia coli. PLoS ONE 7:e46350. doi: 10.1371/journal.pone.0046350
10. Christensen, B. B., Sternberg, C., Andersen, J. B., Palmer, R. J. Jr., Nielsen, A. T., Givskov, M., et al. (1999). Molecular tools for study of biofilm physiology. Methods Enzymol. 310, 20-42. doi: 10.1016/S0076-6879(99)10004-1
11. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322. doi: 10.1126/science.284.5418.1318
12. Cotruvo, J. A., and Stubbe, J. (2011). Class I ribonucleotide reductases: metallocofactor assembly and repair in vitro and in vivo. Annu. Rev. Biochem. 80, 733-767. doi: 10.1146/annurev-biochem-061408-095817
13. Crespo, A., Pedraz, L., and Torrents, E. (2015). Function of the Pseudomonas aeruginosa NrdR transcription factor: global transcriptomic analysis and its role on ribonucleotide reductase gene expression. PLoS ONE 10:e0123571. doi: 10.1371/journal.pone.0123571
14. Crona, M., Hofer, A., Astorga-Wells, J., Sjoberg, B. M., and Tholander, F. (2015). Biochemical Characterization of the Split Class II Ribonucleotide Reductase from Pseudomonas aeruginosa. PLoS ONE 10:e0134293. doi: 10.1371/journal.pone.0134293
15. Davies, J. C., Alton, E. W., and Bush, A. (2007). Cystic fibrosis. BMJ 335, 1255-1259. doi: 10.1136/bmj.39391.713229.AD
16. Dietrich, L. E., Okegbe, C., Price-Whelan, A., Sakhtah, H., Hunter, R. C., and Newman, D. K. (2013). Bacterial community morphogenesis is intimately linked to the intracellular redox state. J. Bacteriol. 195, 1371-1380. doi: 10.1128/JB.02273-12
17. Eichner, A., Gunther, N., Arnold, M., Schobert, M., Heesemann, J., and Hogardt, M. (2014). Marker genes for the metabolic adaptation of Pseudomonas aeruginosa to the hypoxic cystic fibrosis lung environment. Int. J. Med. Microbiol. 304, 1050-1061. doi: 10.1016/j.ijmm.2014.07.014
18. Filiatrault, M. J., Wagner, V. E., Bushnell, D., Haidaris, C. G., Iglewski, B. H., and Passador, L. (2005). Effect of anaerobiosis and nitrate on gene expression in Pseudomonas aeruginosa. Infect. Immun. 73, 3764-3772. doi: 10.1128/IAI.73.6.3764-3772.2005
19. Garriga, X., Eliasson, R., Torrents, E., Jordan, A., Barbe, J., Gibert, I., et al. (1996). nrdD and nrdG genes are essential for strict anaerobic growth of Escherichia coli. Biochem. Biophys. Res. Commun. 229, 189-192. doi: 10.1006/bbrc.1996.1778
20. Hassett, D. J., Sutton, M. D., Schurr, M. J., Herr, A. B., Caldwell, C. C., and Matu, J. O. (2009). Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 17, 130-138. doi: 10.1016/j.tim.2008.12.003
21. Hofer, A., Crona, M., Logan, D. T., and Sjoberg, B. M. (2012). DNA building blocks: keeping control of manufacture. Crit. Rev. Biochem. Mol. Biol. 47, 50-63. doi: 10.3109/10409238.2011.630372
22. Ito, K., and Barnes, P. J. (2009). COPD as a disease of accelerated lung aging. Chest 135, 173-180. doi: 10.1378/chest.08-1419
23. Kempes, C. P., Okegbe, C., Mears-Clarke, Z., Follows, M. J., and Dietrich, L. E. (2014). Morphological optimization for access to dual oxidants in biofilms. Proc. Natl. Acad. Sci. U.S.A. 111, 208-213. doi: 10.1073/pnas.1315521110
24. Lebeaux, D., Chauhan, A., Rendueles, O., and Beloin, C. (2013). From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens 2, 288-356. doi: 10.3390/pathogens2020288
25. Lee, K. M., Go, J., Yoon, M. Y., Park, Y., Kim, S. C., Yong, D. E., et al. (2012). Vitamin B12-mediated restoration of defective anaerobic growth leads to reduced biofilm formation in Pseudomonas aeruginosa. Infect. Immun. 80, 1639-1649. doi: 10.1128/IAI.06161-11
26. Lundin, D., Berggren, G., Logan, D. T., and Sjoberg, B. M. (2015). The origin and evolution of ribonucleotide reduction. Life (Basel) 5, 604-636. doi: 10.3390/life5010604
27. Lyczak, J. B., Cannon, C. L., and Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15, 194-222. doi: 10.1128/CMR.15.2.194-222.2002
28. Okegbe, C., Price-Whelan, A., and Dietrich, L. E. (2014). Redox-driven regulation of microbial community morphogenesis. Curr. Opin. Microbiol. 18, 39-45. doi: 10.1016/j.mib.2014.01.006
29. Palmer, K. L., Brown, S. A., and Whiteley, M. (2007). Membrane-bound nitrate reductase is required for anaerobic growth in cystic fibrosis sputum. J. Bacteriol. 189, 4449-4455. doi: 10.1128/JB.00162-07
30. Quenee, L., Lamotte, D., and Polack, B. (2005). Combined sacB-based negative selection and cre-lox antibiotic marker recycling for efficient gene deletion in Pseudomonas aeruginosa. Biotechniques 38, 63-67. doi: 10.2144/05381ST01
31. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
32. Schobert, M., and Jahn, D. (2010). Anaerobic physiology of Pseudomonas aeruginosa in the cystic fibrosis lung. Int. J. Med. Microbiol. 300, 549-556. doi: 10.1016/j.ijmm.2010.08.007
33. Schreiber, K., Krieger, R., Benkert, B., Eschbach, M., Arai, H., Schobert, M., et al. (2007). The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration. J. Bacteriol. 189, 4310-4314. doi: 10.1128/JB.00240-07
34. Sjoberg, B. M., and Torrents, E. (2011). Shift in ribonucleotide reductase gene expression in Pseudomonas aeruginosa during infection. Infect. Immun. 79, 2663-2669. doi: 10.1128/IAI.01212-10
35. Stewart, P. S. (2003). Diffusion in biofilms. J. Bacteriol. 185, 1485-1491. doi: 10.1128/JB.185.5.1485-1491.2003
36. Stewart, P. S., and Franklin, M. J. (2008). Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199-210. doi: 10.1038/nrmicro1838
37. Torrents, E. (2014). Ribonucleotide reductases: essential Enzymes for bacterial life. Front. Cell. Infect. Microbiol. 4:52. doi: 10.3389/fcimb.2014.00052
38. Torrents, E., Poplawski, A., and Sjoberg, B. M. (2005). Two proteins mediate class II ribonucleotide reductase activity in Pseudomonas aeruginosa: expression and transcriptional analysis of the aerobic enzymes. J. Biol. Chem. 280, 16571-16578. doi: 10.1074/jbc.M501322200
39. Trunk, K., Benkert, B., Quack, N., Munch, R., Scheer, M., Garbe, J., et al. (2010). Anaerobic adaptation in Pseudomonas aeruginosa: definition of the Anr and Dnr regulons. Environ. Microbiol. 12, 1719-1733. doi: 10.1111/j.1462-2920.2010.02252.x
40. Urban, A., Neukirchen, S., and Jaeger, K. E. (1997). A rapid and efficient method for site-directed mutagenesis using one-step overlap extension PCR. Nucleic Acids Res. 25, 2227-2228. doi: 10.1093/nar/25.11.2227
41. Van Alst, N. E., Picardo, K. F., Iglewski, B. H., and Haidaris, C. G. (2007). Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect. Immun. 75, 3780-3790. doi: 10.1128/IAI.00201-07
42. Waite, R. D., Paccanaro, A., Papakonstantinopoulou, A., Hurst, J. M., Saqi, M., Littler, E., et al. (2006). Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genomics 7:162. doi: 10.1186/1471-2164-7-162
43. Weiss Nielsen, M., Sternberg, C., Molin, S., and Regenberg, B. (2011). Pseudomonas aeruginosa and Saccharomyces cerevisiae biofilm in flow cells. J. Vis. Exp. 15:2383. doi: 10.3791/2383
44. Werner, E., Roe, F., Bugnicourt, A., Franklin, M. J., Heydorn, A., Molin, S., et al. (2004). Stratified growth in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 70, 6188-6196. doi: 10.1128/AEM.70.10.6188-6196.2004
45. Wu, M., Guina, T., Brittnacher, M., Nguyen, H., Eng, J., and Miller, S. I. (2005). The Pseudomonas aeruginosa proteome during anaerobic growth. J. Bacteriol. 187, 8185-8190. doi: 10.1128/JB.187.23.8185-8190.2005
46. Xu, K. D., Stewart, P. S., Xia, F., Huang, C. T., and Mcfeters, G. A. (1998). Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64, 4035-4039.
47. Ye, R. W., Averill, B. A., and Tiedje, J. M. (1994). Denitrification: production and consumption of nitric oxide. Appl. Environ. Microbiol. 60, k1053-1058.
48. Yoon, M. Y., Lee, K. M., Park, Y., and Yoon, S. S. (2011). Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. PLoS ONE 6:e16105. doi: 10.1371/journal.pone.0016105
49. Yoon, S. S., Hennigan, R. F., Hilliard, G. M., Ochsner, U. A., Parvatiyar, K., Kamani, M. C., et al. (2002). Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3, 593-603. doi: 10.1016/S1534-5807(02)00295-2