Use of mCherry red fluorescent protein for studies of protein localization and gene expression in Clostridium difficile

Applied and Environmental Microbiology

Volumn 81, Issue 5, 2015, Pages 1652-1660

  Ransom, Eric M ^a   Ellermeier, Craig D ^a   Weiss, David S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL PROLIFERATION; CHROMOPHORES; CLOSTRIDIUM; DNA; ENZYMES; FLUORESCENCE; GENES; PROTEINS; SIGNAL TO NOISE RATIO;

ANAEROBIC BACTERIUM; CLOSTRIDIUM DIFFICILE; CYAN FLUORESCENT PROTEIN; DEVELOPED COUNTRIES; LYSOZYME RESISTANCE; PROOF OF PRINCIPLES; PROTEIN LOCALIZATION; RED FLUORESCENT PROTEINS;

GENE EXPRESSION;

BACTERIUM; ENZYME; GENE EXPRESSION; GENOMICS; MATURATION; PLASMID;

CLOSTRIDIUM DIFFICILE;

BACTERIAL DNA; PHOTOPROTEIN; RECOMBINANT PROTEIN; RED FLUORESCENT PROTEIN;

CHEMISTRY; DNA SEQUENCE; GENE VECTOR; GENETICS; METABOLISM; MICROBIAL GENETICS; MOLECULAR BIOLOGY; MOLECULAR GENETICS; PEPTOCLOSTRIDIUM DIFFICILE; PLASMID; PROCEDURES; REPORTER GENE;

CLOSTRIDIUM DIFFICILE; DNA, BACTERIAL; GENES, REPORTER; GENETIC VECTORS; GENETICS, MICROBIAL; LUMINESCENT PROTEINS; MOLECULAR BIOLOGY; MOLECULAR SEQUENCE DATA; PLASMIDS; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84922895002     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03446-14     Document Type: Article

References (47)

1. Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention, Atlanta, GA.
2. Rupnik M, Wilcox MH, Gerding DN. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7:526-536. http://dx.doi.org/10.1038/nrmicro2164.
3. Jones AM, Kuijper EJ, Wilcox MH. 2013. Clostridium difficile: a European perspective. J Infect 66:115-128. http://dx.doi.org/10.1016/j.jinf.2012.10.019.
4. Heim R, Prasher DC, Tsien RY. 1994. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci USA 91:12501-12504. http://dx.doi.org/10.1073/pnas.91.26.12501.
5. Zhang C, Xing XH, Lou K. 2005. Rapid detection of a gfp-marked Enterobacter aerogenes under anaerobic conditions by aerobic fluorescence recovery. FEMS Microbiol Lett 249:211-218. http://dx.doi.org/10.1016/j.femsle.2005.05.051.
6. Ransom EM, Williams KB, Weiss DS, Ellermeier CD. 2014. Identification and characterization of a gene cluster required for proper rod shape, cell division, and pathogenesis in Clostridium difficile. J Bacteriol 196: 2290-2300. http://dx.doi.org/10.1128/JB.00038-14.
7. Rueda S, Vicente M, Mingorance J. 2003. Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J Bacteriol 185:3344-3351. http://dx.doi.org/10.1128/JB.185.11.3344-3351.2003.
8. Anderson DE, Gueiros-Filho FJ, Erickson HP. 2004. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZregulating proteins. J Bacteriol 186:5775-5781. http://dx.doi.org/10.1128/JB.186.17.5775-5781.2004.
9. Strahl H, Hamoen LW. 2010. Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 107:12281-12286. http://dx.doi.org/10.1073/pnas.1005485107.
10. Barra-Carrasco J, Olguin-Araneda V, Plaza-Garrido A, Miranda-Cardenas C, Cofre-Araneda G, Pizarro-Guajardo M, Sarker MR, Paredes-Sabja D. 2013. The Clostridium difficile exosporium cysteine (CdeC)-rich protein is required for exosporium morphogenesis and coat assembly. J Bacteriol 195:3863-3875. http://dx.doi.org/10.1128/JB.00369-13.
11. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567-1572. http://dx.doi.org/10.1038/nbt1037.
12. O'Connor JR, Lyras D, Farrow KA, Adams V, Powell DR, Hinds J, Cheung JK, Rood JI. 2006. Construction and analysis of chromosomal Clostridium difficile mutants. Mol Microbiol 61:1335-1351. http://dx.doi.org/10.1111/j.1365-2958.2006.05315.x.
13. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeno-Tarraga AM, Wang H, Holden MT, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38:779-786. http://dx.doi.org/10.1038/ng1830.
14. Fagan RP, Fairweather NF. 2011. Clostridium difficile has two parallel and essential Sec secretion systems. J Biol Chem 286:27483-27493. http://dx.doi.org/10.1074/jbc.M111.263889.
15. Cormack BP, Valdivia RH, Falkow S. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38. http://dx.doi.org/10.1016/0378-1119(95)00685-0.
16. Heap JT, Kuehne SA, Ehsaan M, Cartman ST, Cooksley CM, Scott JC, Minton NP. 2010. The ClosTron: mutagenesis in Clostridium refined and streamlined. J Microbiol Methods 80:49-55. http://dx.doi.org/10.1016/j.mimet.2009.10.018.
17. Ho TD, Ellermeier CD. 2011. PrsW is required for colonization, resistance to antimicrobial peptides, and expression of extracytoplasmic function sigma factors in Clostridium difficile. Infect Immun 79:3229-3238. http://dx.doi.org/10.1128/IAI.00019-11.
18. Nakamura Y, Gojobori T, Ikemura T. 2000. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 28:292. http://dx.doi.org/10.1093/nar/28.1.292.
19. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. http://dx.doi.org/10.1038/msb.2011.75.
20. Pogliano K, Harry E, Losick R. 1995. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol Microbiol 18:459-470. http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_18030459.x.
21. Bouillaut L, McBride SM, Sorg JA. 2011. Genetic manipulation of Clostridium difficile. Curr Protoc Microbiol Chapter 9:Unit 9A.2. http://dx.doi.org/10.1002/9780471729259.mc09a02s20.
22. Heap JT, Pennington OJ, Cartman ST, Minton NP. 2009. A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78:79-85. http://dx.doi.org/10.1016/j.mimet.2009.05.004.
23. Shaner NC, Steinbach PA, Tsien RY. 2005. A guide to choosing fluorescent proteins. Nat Methods 2:905-909. http://dx.doi.org/10.1038/nmeth819.
24. Sastalla I, Chim K, Cheung GY, Pomerantsev AP, Leppla SH. 2009. Codon-optimized fluorescent proteins designed for expression in low-GC gram-positive bacteria. Appl Environ Microbiol 75:2099-2110. http://dx.doi.org/10.1128/AEM.02066-08.
25. Gueiros-Filho FJ, Losick R. 2002. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16:2544-2556. http://dx.doi.org/10.1101/gad.1014102.
26. DMinC/MinD, complexes to septal ring assemblies in Escherichia coli. J Bacteriol 186:2418-2429. http://dx.doi.org/10.1128/JB.186.8.2418-2429.2004.
27. Small E, Marrington R, Rodger A, Scott DJ, Sloan K, Roper D, Dafforn TR, Addinall SG. 2007. FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J Mol Biol 369:210-221. http://dx.doi.org/10.1016/j.jmb.2007.03.025.
28. Scheffers DJ. 2008. The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett 582:2601-2608. http://dx.doi.org/10.1016/j.febslet.2008.06.038.
29. Galli E, Gerdes K. 2010. Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol 76:1514-1526. http://dx.doi.org/10.1111/j.1365-2958.2010.07183.x.
30. Buss J, Coltharp C, Huang T, Pohlmeyer C, Wang SC, Hatem C, Xiao J. 2013. In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol Microbiol 89:1099-1120. http://dx.doi.org/10.1111/mmi.12331.
31. Low HH, Moncrieffe MC, Lowe J. 2004. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J Mol Biol 341:839-852. http://dx.doi.org/10.1016/j.jmb.2004.05.031.
32. Roach EJ, Kimber MS, Khursigara CM. 2014. Crystal structure and site-directed mutational analysis reveals key residues involved in Escherichia coli ZapA function. J Biol Chem 289:23276-23286. http://dx.doi.org/10.1074/jbc.M114.561928.
33. Monot M, Boursaux-Eude C, Thibonnier M, Vallenet D, Moszer I, Medigue C, Martin-Verstraete I, Dupuy B. 2011. Reannotation of the genome sequence of Clostridium difficile strain 630. J Med Microbiol 60: 1193-1199. http://dx.doi.org/10.1099/jmm.0.030452-0.
34. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 2014. Pfam: the protein families database. Nucleic Acids Res 42:D222-D230. http://dx.doi.org/10.1093/nar/gkt1223.
35. Ho TD, Williams KB, Chen Y, Helm RF, Popham DL, Ellermeier CD. 2014. Clostridium difficile extracytoplasmic function sigma factor sigmaV regulates lysozyme resistance and is necessary for pathogenesis in the hamster model of infection. Infect Immun 82:2345-2355. http://dx.doi.org/10.1128/IAI.01483-13.
36. Cartman ST, Minton NP. 2010. A mariner-based transposon system for in vivo random mutagenesis of Clostridium difficile. Appl Environ Microbiol 76:1103-1109. http://dx.doi.org/10.1128/AEM.02525-09.
37. Purdy D, O'Keeffe TA, Elmore M, Herbert M, McLeod A, Bokori-Brown M, Ostrowski A, Minton NP. 2002. Conjugative transfer of clostridial shuttle vectors from Escherichia coli to Clostridium difficile through circumvention of the restriction barrier. Mol Microbiol 46:439-452. http://dx.doi.org/10.1046/j.1365-2958.2002.03134.x.
38. Dubnau D, Losick R. 2006. Bistability in bacteria. Mol Microbiol 61:564-572. http://dx.doi.org/10.1111/j.1365-2958.2006.05249.x.
39. Maamar H, Raj A, Dubnau D. 2007. Noise in gene expression determines cell fate in Bacillus subtilis. Science 317:526-529. http://dx.doi.org/10.1126/science.1140818.
40. Lequette Y, Greenberg EP. 2005. Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37-44. http://dx.doi.org/10.1128/JB.187.1.37-44.2005.
41. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199-210. http://dx.doi.org/10.1038/nrmicro1838.
42. Andersen JB, Sternberg C, Poulsen LK, Bjorn SP, Givskov M, Molin S. 1998. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64:2240-2246.
43. Margolin W. 2012. The price of tags in protein localization studies. J Bacteriol 194:6369-6371. http://dx.doi.org/10.1128/JB.01640-12.
44. Hartman AH, Liu H, Melville SB. 2011. Construction and characterization of a lactose-inducible promoter system for controlled gene expression in Clostridium perfringens. Appl Environ Microbiol 77:471-478. http://dx.doi.org/10.1128/AEM.01536-10.
45. Mukherjee A, Schroeder CM. 2014. Flavin-based fluorescent proteins: emerging paradigms in biological imaging. Curr Opin Biotechnol 31C: 16-23. http://dx.doi.org/10.1016/j.copbio.2014.07.010.
46. Hinner MJ, Johnsson K. 2010. How to obtain labeled proteins and what to do with them. Curr Opin Biotechnol 21:766-776. http://dx.doi.org/10.1016/j.copbio.2010.09.011.
47. Trieu-Cuot P, Arthur M, Courvalin P. 1987. Origin, evolution and dissemination of antibiotic resistance genes. Microbiol Sci 4:263-266.