Optogenetics Manipulation Enables Prevention of Biofilm Formation of Engineered Pseudomonas aeruginosa on Surfaces

ACS Synthetic Biology

Volumn 7, Issue 1, 2018, Pages 200-208

  Pu, Lu ^a   Yang, Shuai ^a   Xia, Aiguo ^a   Jin, Fan ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

biofilms; c di GMP; light sensing; optogenetic; Pseudomonas aeruginosa

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL CHROMOSOME; BIOFILM; BLUE LIGHT; CELL DIVISION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DARKNESS; DISPERSION; FLUORESCENCE; GENE EXPRESSION; ILLUMINATION; LIGHT ABSORPTION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PSEUDOMONAS AERUGINOSA; WHITE LIGHT; ANALOGS AND DERIVATIVES; FLUORESCENCE MICROSCOPY; GENETICS; LIGHT; METABOLISM; PHYSIOLOGY; PLASMID; PROCEDURES; RADIATION RESPONSE; TIME LAPSE IMAGING;

BACTERIAL PROTEIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; FIXJ PROTEIN, BACTERIA; GREEN FLUORESCENT PROTEIN; PROTEIN HISTIDINE KINASE;

BACTERIAL PROTEINS; BIOFILMS; CYCLIC GMP; GREEN FLUORESCENT PROTEINS; HISTIDINE KINASE; LIGHT; MICROSCOPY, FLUORESCENCE; OPTOGENETICS; PLASMIDS; PSEUDOMONAS AERUGINOSA; TIME-LAPSE IMAGING;

EID: 85040862672     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.7b00273     Document Type: Article

References (54)

1. Costerton, J. W., Geesey, G., and Cheng, K.-J. (1978) How bacteria stick Sci. Am. 238, 86-95 10.1038/scientificamerican0178-86
2. Kolter, R. and Greenberg, E. P. (2006) Microbial sciences: the superficial life of microbes Nature 441, 300-302 10.1038/441300a
3. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial Biofilms: A Common Cause of Persistent Infections Science 284, 1318-1322 10.1126/science.284.5418.1318
4. Beech, I. B. and Sunner, J. (2004) Biocorrosion: towards understanding interactions between biofilms and metals Curr. Opin. Biotechnol. 15, 181-186 10.1016/j.copbio.2004.05.001
5. Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., Olakanmi, O., Beer, K., McKay, G., Siehnel, R., Schafhauser, J., Wang, Y., Britigan, B. E., and Singh, P. K. (2011) Active Starvation Responses Mediate Antibiotic Tolerance in Biofilms and Nutrient-Limited Bacteria Science 334, 982-986 10.1126/science.1211037
6. Karatan, E. and Watnick, P. (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms Microbiol. Mol. Biol. Rev. 73, 310-347 10.1128/MMBR.00041-08
7. Simm, R., Morr, M., Kader, A., Nimtz, M., and Römling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility Mol. Microbiol. 53, 1123-1134 10.1111/j.1365-2958.2004.04206.x
8. Flemming, H.-C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S. A., and Kjelleberg, S. (2016) Biofilms: an emergent form of bacterial life Nat. Rev. Microbiol. 14, 563-575 10.1038/nrmicro.2016.94
9. Merighi, M., Lee, V. T., Hyodo, M., Hayakawa, Y., and Lory, S. (2007) The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa, Mol Mol. Microbiol. 65, 876-895 10.1111/j.1365-2958.2007.05817.x
10. Baraquet, C., Murakami, K., Parsek, M. R., and Harwood, C. S. (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 10.1093/nar/gks384
11. Hickman, J. W. and Harwood, C. S. (2008) Identification of FleQ from Pseudomonas aeruginosa as ac-di-GMP-responsive transcription factor Mol. Microbiol. 69, 376-389 10.1111/j.1365-2958.2008.06281.x
12. Borlee, B. R., Goldman, A. D., Murakami, K., Samudrala, R., Wozniak, D. J., and Parsek, M. R. (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix, Mol Mol. Microbiol. 75, 827-842 10.1111/j.1365-2958.2009.06991.x
13. Hickman, J. W., Tifrea, D. F., and Harwood, C. S. (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels Proc. Natl. Acad. Sci. U. S. A. 102, 14422-14427 10.1073/pnas.0507170102
14. Ueda, A. and Wood, T. K. (2009) Connecting Quorum Sensing, c-di-GMP, Pel Polysaccharide, and Biofilm Formation in Pseudomonas aeruginosa through Tyrosine Phosphatase TpbA (PA3885) PLoS Pathog. 5, e1000483 10.1371/journal.ppat.1000483
15. Odessart, N., Muñoa, F. J., Regue, M., and Juærez, A. (1988) Chromosomal Mutations That Increase the Production of a Plasmid-encoded Haemolysin in Escherichia coli Microbiology 134, 2779-2787 10.1099/00221287-134-10-2779
16. Lu, T. K. and Collins, J. J. (2007) Dispersing biofilms with engineered enzymatic bacteriophage Proc. Natl. Acad. Sci. U. S. A. 104, 11197-11202 10.1073/pnas.0704624104
17. Ma, Q., Yang, Z., Pu, M., Peti, W., and Wood, T. K. (2011) Engineering a novel c-di-GMP-binding protein for biofilm dispersal Environ. Microbiol. 13, 631-642 10.1111/j.1462-2920.2010.02368.x
18. Seok Hoon, H. O. N. G., Hegde, M., Kim, J., Wang, X., Jayaraman, A., and Wood, T. K. (2012) Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device Nat. Commun. 3, 613 10.1038/ncomms1616
19. Cameron, D. E., Bashor, C. J., and Collins, J. J. (2014) A brief history of synthetic biology Nat. Rev. Microbiol. 12, 381-390 10.1038/nrmicro3239
20. Gardner, T. S., Cantor, C. R., and Collins, J. J. (2000) Construction of a genetic toggle switch in Escherichia coli Nature 403, 339-342 10.1038/35002131
21. Moon, T. S., Lou, C., Tamsir, A., Stanton, B. C., and Voigt, C. A. (2012) Genetic programs constructed from layered logic gates in single cells Nature 491, 249-253 10.1038/nature11516
22. Elowitz, M. B. and Leibler, S. (2000) A synthetic oscillatory network of transcriptional regulators Nature 403, 335-338 10.1038/35002125
23. Becskei, A. and Serrano, L. (2000) Engineering stability in gene networks by autoregulation Nature 405, 590-593 10.1038/35014651
24. Levskaya, A., Chevalier, A. A., Tabor, J. J., Simpson, Z. B., Lavery, L. A., Levy, M., Davidson, E. A., Scouras, A., Ellington, A. D., and Marcotte, E. M. et al. 2005, Synthetic biology: engineering Escherichia coli to see light Nature 438, 441-442 10.1038/nature04405
25. Pathak, G. P., Vrana, J. D., and Tucker, C. L. (2013) Optogenetic control of cell function using engineered photoreceptors Biol. Cell 105, 59-72 10.1111/boc.201200056
26. Ziegler, T. and Möglich, A. (2015) Photoreceptor engineering Front. Mol. Biosci. 2, 30-55 10.3389/fmolb.2015.00030
27. Wang, X., Chen, X., and Yang, Y. (2012) Spatiotemporal control of gene expression by a light-switchable transgene system Nat. Methods 9, 266-269 10.1038/nmeth.1892
28. Olson, E. J., Hartsough, L. A., Landry, B. P., Shroff, R., and Tabor, J. J. (2014) Characterizing bacterial gene circuit dynamics with optically programmed gene expression signals Nat. Methods 11, 449-455 10.1038/nmeth.2884
29. Chen, X., Liu, R., Ma, Z., Xu, X., Zhang, H., Xu, J., Ouyang, Q., and Yang, Y. (2016) An extraordinary stringent and sensitive light-switchable gene expression system for bacterial cells Cell Res. 26, 854-857 10.1038/cr.2016.74
30. Kaberniuk, A. A., Shemetov, A. A., and Verkhusha, V. V. (2016) A bacterial phytochrome-based optogenetic system controllable with near-infrared light Nat. Methods 13, 591-597 10.1038/nmeth.3864
31. Ohlendorf, R., Vidavski, R. R., Eldar, A., Moffat, K., and Möglich, A. (2012) From Dusk till Dawn: One-Plasmid Systems for Light-Regulated Gene Expression J. Mol. Biol. 416, 534-542 10.1016/j.jmb.2012.01.001
32. Kulesekara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S., Lee, D. G., Neely, A. N., Hyodo, M., Hayakawa, Y., Ausubel, F. M., and 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 10.1073/pnas.0511090103
33. Choi, K.-H., Gaynor, J. B., White, K. G., Lopez, C., Bosio, C. M., Karkhoff-Schweizer, R. R., and Schweizer, H. P. (2005) A Tn7-based broad-range bacterial cloning and expression system Nat. Methods 2, 443-448 10.1038/nmeth765
34. Möglich, A., Ayers, R. A., and Moffat, K. (2009) Design and Signaling Mechanism of Light-Regulated Histidine Kinases J. Mol. Biol. 385, 1433-1444 10.1016/j.jmb.2008.12.017
35. Crosson, S., Rajagopal, S., and Moffat, K. (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains Biochemistry 42, 2-10 10.1021/bi026978l
36. Zhang, R., Ni, L., Jin, Z., Li, J., and Jin, F. (2014) Bacteria slingshot more on soft surfaces Nat. Commun. 5, 5541 10.1038/ncomms6541
37. Ni, L., Yang, S., Zhang, R., Jin, Z., Chen, H., Conrad, J. C., and Jin, F. (2016) Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability NPJ. Biofilms Microbiomes 2, 15029 10.1038/npjbiofilms.2015.29
38. Golding, I., Paulsson, J., Zawilski, S. M., and Cox, E. C. (2005) Real-Time Kinetics of Gene Activity in Individual Bacteria Cell 123, 1025-1036 10.1016/j.cell.2005.09.031
39. Kennedy, M. J., Hughes, R. M., Peteya, L. A., Schwartz, J. W., Ehlers, M. D., and Tucker, C. L. (2010) Rapid blue-light-mediated induction of protein interactions in living cells Nat. Methods 7, 973-975 10.1038/nmeth.1524
40. Rybtke, M. T., Borlee, B. R., Murakami, K., Irie, Y., Hentzer, M., Nielsen, T. E., Givskov, M., Parsek, M. R., and Tolker-Nielsen, T. (2012) Fluorescence-based reporter for gauging cyclic di-GMP levels in Pseudomonas aeruginosa Appl. Environ. Microbiol. 78, 5060-5069 10.1128/AEM.00414-12
41. Bindels, D. S., Haarbosch, L., Van Weeren, L., Postma, M., Wiese, K. E., Mastop, M., Aumonier, S., Gotthard, G., Royant, A., and Hink, M. A. et al. 2017, mScarlet: a bright monomeric red fluorescent protein for cellular imaging Nat. Methods 14, 53-56 10.1038/nmeth.4074
42. Saeidi, N., Wong, C. K., Lo, T.-M., Nguyen, H. X., Ling, H., Leong, S. S. J., Poh, C. L., and Chang, M. W. (2011) Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen Mol. Syst. Biol. 7, 521 10.1038/msb.2011.55
43. Heydorn, A., Nielsen, A. T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B. K., and Molin, S. (2000) Quantification of biofilm structures by the novel computer program comstat Microbiology 146, 2395-2407 10.1099/00221287-146-10-2395
44. Choi, K.-H. and Schweizer, H. P. (2006) mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa Nat. Protoc. 1, 153-161 10.1038/nprot.2006.24
45. Friedland, A. E., Lu, T. K., Wang, X., Shi, D., Church, G., and Collins, J. J. (2009) Synthetic gene networks that count Science 324, 1199-1202 10.1126/science.1172005
46. Gottesman, S., Roche, E., Zhou, Y., and Sauer, R. T. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system Genes Dev. 12, 1338-1347 10.1101/gad.12.9.1338
47. McGinness, K. E., Baker, T. A., and Sauer, R. T. (2006) Engineering Controllable Protein Degradation Mol. Cell 22, 701-707 10.1016/j.molcel.2006.04.027
48. Choi, K.-H., Kumar, A., and Schweizer, H. P. (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation J. Microbiol. Methods 64, 391-397 10.1016/j.mimet.2005.06.001
49. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J., and Schweizer, H. P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants Gene 212, 77-86 10.1016/S0378-1119(98)00130-9
50. Nieto, C., Giraldo, R., Fernández-Tresguerres, E., and Díaz, R. (1992) Genetic and functional analysis of the basic replicon of pPS10, a plasmid specific for Pseudomonas isolated from Pseudomonas syringae patovar savastanoi J. Mol. Biol. 223, 415-426 10.1016/0022-2836(92)90661-3
51. Flynn, J. M., Neher, S. B., Kim, Y.-I., Sauer, R. T., and Baker, T. A. (2003) Proteomic Discovery of Cellular Substrates of the ClpXP Protease Reveals Five Classes of ClpX-Recognition Signals Mol. Cell 11, 671-683 10.1016/S1097-2765(03)00060-1
52. Flynn, J. M., Levchenko, I., Seidel, M., Wickner, S. H., Sauer, R. T., and Baker, T. A. (2001) Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis Proc. Natl. Acad. Sci. U. S. A. 98, 10584-10589 10.1073/pnas.191375298
53. Andersen, J. B., Sternberg, C., Poulsen, L. K., Bjørn, S. P., Givskov, M., and Molin, S. (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria Appl. Environ. Microbiol. 64, 2240-2246
54. Christensen, B. B., Sternberg, C., Andersen, J. B., Palmer, R. J., Nielsen, A. T., Givskov, M., and Molin, S. (1999) Molecular tools for study of biofilm physiology Methods Enzymol. 310, 20-42 10.1016/S0076-6879(99)10004-1