Deletion mutant library for investigation of functional outputs of cyclic diguanylate metabolism in Pseudomonas aeruginosa PA14

Applied and Environmental Microbiology

Volumn 80, Issue 11, 2014, Pages 3384-3393

  Ha, Dae Gon ^a   Richman, Megan E ^b   O'Toolea, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b CLAREMONT MCKENNA COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; METABOLISM; PHYSIOLOGY;

BIOFILM FORMATION; DELETION MUTANTS; EXOPOLYSACCHARIDES; FUNCTIONAL OUTPUTS; POTENTIAL UTILITY; PSEUDOMONAS AERUGINOSA; SWIMMING MOTILITY;

MOLECULAR BIOLOGY;

BACTERIAL POLYSACCHARIDE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP;

ANALOGS AND DERIVATIVES; BIOFILM; BIOTRANSFORMATION; GENE DELETION; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; METABOLISM; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA;

BIOFILMS; BIOTRANSFORMATION; CYCLIC GMP; GENE DELETION; GENE LIBRARY; LOCOMOTION; METABOLIC NETWORKS AND PATHWAYS; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA;

EID: 84899869588     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00299-14     Document Type: Article

References (65)

1. Gaspar MC, Couet W, Olivier JC, Pais AA, Sousa JJ. 2013. Pseudomonas aeruginosa infection in cystic fibrosis lung disease and new perspectives of treatment: a review. Eur. J. Clin. Microbiol. Infect. Dis. 32:1231-1252. http://dx.doi.org/10.1007/s10096-013-1876-y.
2. Hogardt M, Heesemann J. 2013. Microevolution of Pseudomonas aeruginosa to a chronic pathogen of the cystic fibrosis lung. Curr. Top. Microbiol. Immunol. 358:91-118. http://dx.doi.org/10.1007/82_2011_199.
3. Wu DC, Chan WW, Metelitsa AI, Fiorillo L, Lin AN. 2011. Pseudomonas skin infection: clinical features, epidemiology, and management. Am. J. Clin. Dermatol. 12:157-169. http://dx.doi.org/10.2165/11539770-000000000-00000.
4. Mah TF, O'Toole GA. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39. http://dx.doi.org/10.1016/S0966-842X(00)01913-2.
5. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306-310. http://dx.doi.org/10.1038/nature02122.
6. Quinn JP. 2003. Pseudomonas aeruginosa infections in the intensive care unit. Semin. Respir. Crit. Care Med. 24:61-68. http://dx.doi.org/10.1055/s-2003-37917.
7. Parsek MR, Singh PK. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701. http://dx.doi.org/10.1146/annurev.micro.57.030502.090720.
8. O'Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79. http://dx.doi.org/10.1146/annurev.micro.54.1.49.
9. Jain R, Behrens AJ, Kaever V, Kazmierczak BI. 2012. Type IV pilus assembly in Pseudomonas aeruginosa over a broad range of cyclic di-GMP concentrations. J. Bacteriol. 194:4285-4294. http://dx.doi.org/10.1128/JB.00803-12.
10. Baraquet C, Murakami K, Parsek MR, Harwood CS. 2012. The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res. 40:7207-7218. http://dx.doi.org/10.1093/nar/gks384.
11. Malone JG, Jaeger T, Spangler C, Ritz D, Spang A, Arrieumerlou C, Kaever V, Landmann R, Jenal U. 2010. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog. 6:e1000804. http://dx.doi.org/10.1371/journal.ppat.1000804.
12. Hay ID, Remminghorst U, Rehm BH. 2009. MucR, a novel membraneassociated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75:1110-1120. http://dx.doi.org/10.1128/AEM.02416-08.
13. Kazmierczak BI, Lebron MB, Murray TS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60:1026-1043. http://dx.doi.org/10.1111/j.1365-2958.2006.05156.x.
14. Meissner A, Wild V, Simm R, Rohde M, Erck C, Bredenbruch F, Morr M, Romling U, Haussler S. 2007. Pseudomonas aeruginosa cupAencoded fimbriae expression is regulated by a GGDEF and EAL domaindependent modulation of the intracellular level of cyclic diguanylate. Environ. Microbiol. 9:2475-2485. http://dx.doi.org/10.1111/j.1462-2920.2007.01366.x.
15. Kuchma SL, Ballok AE, Merritt JH, Hammond JH, Lu W, Rabinowitz JD, O'Toole GA. 2010. Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J. Bacteriol. 192:2950-2964. http://dx.doi.org/10.1128/JB.01642-09.
16. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, O'Toole GA. 2007. BifA, a cyclic-Di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:8165-8178. http://dx.doi.org/10.1128/JB.00586-07.
17. Merritt JH, Brothers KM, Kuchma SL, O'Toole GA. 2007. SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J. Bacteriol. 189:8154-8164. http://dx.doi.org/10.1128/JB.00585-07.
18. Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, Rabinowitz J, Gitai Z, O'Toole GA. 2010. Specific control of Pseudomonas aeruginosa surfaceassociated behaviors by two c-di-GMP diguanylate cyclases. mBio 1(4): e00183-10. http://dx.doi.org/10.1128/mBio.e00183-10.
19. Irie Y, Borlee BR, O'Connor JR, Hill PJ, Harwood CS, Wozniak DJ, Parsek MR. 2012. Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 109:20632-20636. http://dx.doi.org/10.1073/pnas.1217993109.
20. Morgan R, Kohn S, Hwang SH, Hassett DJ, Sauer K. 2006. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J. Bacteriol. 188:7335-7343. http://dx.doi.org/10.1128/JB.00599-06.
21. Ryan RP, Lucey J, O'Donovan K, McCarthy Y, Yang L, Tolker-Nielsen T, Dow JM. 2009. HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environ. Microbiol. 11:1126-1136. http://dx.doi.org/10.1111/j.1462-2920.2008.01842.x.
22. Moscoso JA, Mikkelsen H, Heeb S, Williams P, Filloux A. 2011. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ. Microbiol. 13:3128-3138. http://dx.doi.org/10.1111/j.1462-2920.2011.02595.x.
23. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, Jenal U. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727. http://dx.doi.org/10.1101/gad.289504.
24. Simm R, Morr M, Kader A, Nimtz M, Romling U. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53:1123-1134. http://dx.doi.org/10.1111/j.1365-2958.2004.04206.x.
25. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Camara M, Williams P, Dow JM. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. U. S. A. 103:6712-6717. http://dx.doi.org/10.1073/pnas.0600345103.
26. Roy AB, Petrova OE, Sauer K. 2012. The phosphodiesterase DipA (PA5017) is essential for Pseudomonas aeruginosa biofilm dispersion. J. Bacteriol. 194:2904-2915. http://dx.doi.org/10.1128/JB.05346-11.
27. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S. 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol. 191:7333-7342. http://dx.doi.org/10.1128/JB.00975-09
28. An S, Wu J, Zhang LH. 2010. Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl. Environ. Microbiol. 76:8160-8173. http://dx.doi.org/10.1128/AEM.01233-10.
29. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838. http://dx.doi.org/10.1073/pnas.0511100103.
30. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3=-5=)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 103:2839-2844. http://dx.doi.org/10.1073/pnas.0511090103.
31. Bertani G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186:595-600. http://dx.doi.org/10.1128/JB.186.3.595-600.2004.
32. Pardee AB, Jacob F, Monod J. 1959. The genetic control and cytoplasmic expression of "inducibility" in the synthesis of beta-galactosidase by E. coli. J. Mol. Biol. 1:165-178. http://dx.doi.org/10.1016/S0022-2836(59) 80045-0.
33. Kohler T, Curty LK, Barja F, van Delden C, Pechere JC. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996. http://dx.doi.org/10.1128/JB.182.21.5990-5996.2000.
34. Romling U, Sierralta WD, Eriksson K, Normark S. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249-264. http://dx.doi.org/10.1046/j.1365-2958.1998.00791.x.
35. Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O'Toole GA. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl. Environ. Microbiol. 72:5027-5036. http://dx.doi.org/10.1128/AEM.00682-06.
36. Burke D, Dawson D, Stearns T. 2000. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
37. Woodman ME. 2008. Direct PCR of intact bacteria (colony PCR). Curr. Protoc. Microbiol. Appendix 3:Appendix 3D. http://dx.doi.org/10.1002/9780471729259.mca03ds9.
38. O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461. http://dx.doi.org/10.1046/j.1365-2958.1998.00797.x.
39. Friedman L, Kolter R. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51:675-690. http://dx.doi.org/10.1046/j.1365-2958.2003.03877.x.
40. Caiazza NC, Shanks RM, O'Toole GA. 2005. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J. Bacteriol. 187: 7351-7361. http://dx.doi.org/10.1128/JB.187.21.7351-7361.2005.
41. Whitchurch CB, Hobbs M, Livingston SP, Krishnapillai V, Mattick JS. 1991. Characterization of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialized protein export system widespread in eubacteria. Gene 101:33-44.
42. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:D302-D305. http://dx.doi.org/10.1093/nar/gkr931.
43. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95:5857-5864. http://dx.doi.org/10.1073/pnas.95.11.5857.
44. Zhulin IB, Taylor BL, Dixon R. 1997. PAS domain S-boxes in archaea, bacteria and sensors for oxygen and redox. Trends Biochem. Sci. 22:331-333. http://dx.doi.org/10.1016/S0968-0004(97)01110-9.
45. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
46. Huang ZJ, Edery I, Rosbash M. 1993. PAS is a dimerization domain common to Drosophila Period and several transcription factors. Nature 364:259-262. http://dx.doi.org/10.1038/364259a0.
47. Kay SA. 1997. PAS, present, and future: clues to the origins of circadian clocks. Science 276:753-754. http://dx.doi.org/10.1126/science.276.5313.753.
48. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304. http://dx.doi.org/10.1046/j.1365-2958.1998.01062.x.
49. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
50. Top J, Paganelli FL, Zhang X, van Schaik W, Leavis HL, van Luit-Asbroek M, van der Poll T, Leendertse M, Bonten MJ, Willems RJ. 2013. The Enterococcus faecium enterococcal biofilm regulator, EbrB, regulates the esp operon and is implicated in biofilm formation and intestinal colonization. PLoS One 8:e65224. http://dx.doi.org/10.1371/journal.pone.0065224.
51. Gomes LC, Moreira JM, Miranda JM, Simoes M, Melo LF, Mergulhao FJ. 2013. Macroscale versus microscale methods for physiological analysis of biofilms formed in 96-well microtiter plates. J. Microbiol. Methods 95:342-349. http://dx.doi.org/10.1016/j.mimet.2013.10.002.
52. Bernier SP, Ha DG, Khan W, Merritt JH, O'Toole GA. 2011. Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Res. Microbiol. 162: 680-688. http://dx.doi.org/10.1016/j.resmic.2011.04.014.
53. Franklin MJ, Nivens DE, Weadge JT, Howell PL. 2011. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol. 2:167. http://dx.doi.org/10.3389/fmicb.2011.00167.
54. Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. 2005. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151:985-997. http://dx.doi.org/10.1099/mic.0.27410-0.
55. Slifkin M, Cumbie R. 1988. Congo red as a fluorochrome for the rapid detection of fungi. J. Clin. Microbiol. 26:827-830.
56. Wood PJ, Fulcher RG. 1978. Interaction of some dyes with cereal betaglucans. Cereal Chem. 55:952-966.
57. Ruinen L, Smit-van Dijk W, Pros M, Scholten JH, Mandema E. 1972. The binding of Congo red and toluidine blue to isolated amyloid. Acta Pathol. Microbiol. Scand. Suppl. 233:122-127.
58. Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC, Ryder C, Howell PL, Wozniak DJ, Parsek MR. 2012. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol. 14:1913-1928. http://dx.doi.org/10.1111/j.1462-2920.2011.02657.x.
59. D'Argenio DA, Calfee MW, Rainey PB, Pesci EC. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184:6481-6489. http://dx.doi.org/10.1128/JB.184.23.6481-6489.2002.
60. Romling U, Galperin MY, Gomelsky M. 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 77:1-52. http://dx.doi.org/10.1128/MMBR.00043-12.
61. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA. 2007. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:3603-3612. http://dx.doi.org/10.1128/JB.01685-06.
62. Kulasekara HD, Ventre I, Kulasekara BR, Lazdunski A, Filloux A, Lory S. 2005. A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol. Microbiol. 55:368-380. http://dx.doi.org/10.1111/j.1365-2958.2004.04402.x.
63. Kuchma SL, Connolly JP, O'Toole GA. 2005. A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J. Bacteriol. 187:1441-1454. http://dx.doi.org/10.1128/JB.187.4.1441-1454.2005.
64. Mattick JS, Whitchurch CB, Alm RA. 1996. The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa-a review. Gene 179:147-155. http://dx.doi.org/10.1016/S0378-1119(96)00441-6.
65. Strom MS, Lory S. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596. http://dx.doi.org/10.1146/annurev.mi.47.100193.003025.