Mutagenesis of the carboxy terminal protease CtpA decreases desiccation tolerance in Rhizobium leguminosarum

FEMS Microbiology Letters

Volumn 272, Issue 1, 2007, Pages 65-74

  Gilbert, Kerrigan B ^b,c   Vanderlinde, Elizabeth M ^c   Yost, Christopher K ^a,c  

^a Oregon State University ^*  (Canada)

^b OREGON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF REGINA   (Canada)

Author keywords

Cell envelope; Cell morphology; Mutagenesis; Rhizobia

Indexed keywords

CARBOXY TERMINAL PROTEASE A; ISOENZYME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DESICCATION; GRAM NEGATIVE BACTERIUM; MEMBRANE PERMEABILITY; MOLECULAR CLONING; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; RHIZOBIUM LEGUMINOSARUM;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; CARBOXYPEPTIDASES; CELL MEMBRANE; DEHYDRATION; DETERGENTS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, ESSENTIAL; GENES, REPORTER; GLUCURONIDASE; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PERMEABILITY; PROPROTEIN CONVERTASES; RHIZOBIUM LEGUMINOSARUM;

RHIZOBIACEAE; RHIZOBIUM LEGUMINOSARUM;

EID: 34250630580     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2007.00735.x     Document Type: Article

References (45)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 : 3389 3402.
2. Bandara AB, Sriranganathan N, Schurig GG Boyle SM (2005) Carboxyl-terminal protease regulates Brucella suis morphology in culture and persistence in macrophages and mice. J Bacteriol 187 : 5767 5775.
3. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84 : 188 198.
4. Charles TC Nester EW (1993) A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J Bacteriol 175 : 6614 6625.
5. Cheng H-P Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180 : 5183 5191.
6. de Pedro MA, Quintela JC, Holtje JV Schwarz H (1997) Murein segregation in Escherichia coli. J Bacteriol 179 : 2823 2834.
7. Fellay R, Frey J Krisch H (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52 : 147 154.
8. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68 : 280 300.
9. Galibert F, Finan TM, Long SR et al 2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293 : 668 672.
10. Glenn AR, Poole PS Hudman JF (1980) Succinate uptake by free-living and bacteroid forms of Rhizobium leguminosarum. J Gen Microbiol 119 : 267 271.
11. Hancock REW (1984) Alterations in outer membrane permeability. Annu Rev Microbiol 38 : 237 264.
12. Hara H, Nishimura Y, Kato J, Suzuki H, Nagasawa H, Suzuki A Hirota Y (1989) Genetic analyses of processing involving C-terminal cleavage in penicillin-binding protein 3 of Escherichia coli. J Bacteriol 171 : 5882 5889.
13. Hara H, Yamamoto Y, Higashitani A, Suzuki H Nishimura Y (1991) Cloning, mapping, and characterization of the Escherichia coli prc gene, which is involved in C-terminal processing of penicillin-binding protein 3. J Bacteriol 173 : 4799 4813.
14. Hengge R Bukau B (2003) Proteolysis in prokaryotes: protein quality control and regulatory principles. Mol Microbiol 49 : 1451 1462.
15. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
16. Holtje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62 : 181 203.
17. Jenal U Hengge-Aronis R (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6 : 163 172.
18. Johnston AWB Beringer JE (1975) Identification of the Rhizobium strains in pea root nodules using genetic markers. J Gen Microbiol 87 : 343 350.
19. Keiler KC Sauer RT (1995) Identification of active site residues of the Tsp protease. J Biol Chem 270 : 28864 28868.
20. Kumamoto CA Beckwith J (1985) Evidence for specificity at an early step in protein export in Escherichia coli. J Bacteriol 163 : 267 274.
21. Mitchell SJ Minnick MF (1997) A carboxy-terminal processing protease gene is located immediately upstream of the invasion-associated locus from Bartonella bacilliformis. Microbiology 143 : 1221 1233.
22. Nagasawa H, Sakagami Y, Suzuki A, Suzuki H, Hara H Hirota Y (1989) Determination of the cleavage site involved in C-terminal processing of penicillin-binding protein 3 of Escherichia coli. J Bacteriol 171 : 5890 5893.
23. Nanninga N (1998) Morphogenesis of Escherichia coli. Microbiol Mol Biol Rev 62 : 110 129.
24. Nielsen H, Engelbrecht J, Brunak S von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10 : 1 6.
25. Oke V Long SR (1999) Bacteroid formation in the Rhizobium-legume symbiosis. Curr Opin Microbiol 2 : 641 646.
26. Ophir T Gutnick D (1994) A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol 60 : 740 745.
27. Östberg Y, Carroll JA, Pinne M, Krum JG, Rosa P Bergstrom S (2004) Pleiotropic effects of inactivating a carboxyl-terminal protease, CtpA, in Borrelia burgdorferi. J Bacteriol 186 : 2074 2084.
28. Pinne M, Denker K, Nilsson E, Benz R Bergström S (2006) The BBA01 protein, a member of paralog family 48 from Borrelia burgdorferi is potentially interchangeable with the channel-forming protein P13. J Bacteriol 188 : 4207 4217.
29. Popham DL Young KD (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6 : 594 599.
30. Quandt J Hynes MF (1993) Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127 : 15 21.
31. Raivio TL (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56 : 1119 1128.
32. Reeve WG, Tiwari RP, Worsley PS, Dilworth MJ, Glenn AR Howieson JG (1999) Constructs for insertional mutagenesis, transcriptional signal localization and gene regulation studies in root nodule and other bacteria. Microbiology 145 : 1307 1316.
33. Reiling SA, Jansen JA, Henley BJ, Singh S, Chattin C, Chandler M Rowen DW (2005) Prc protease promotes mucoidy in mucA mutants of Pseudomonas aeruginosa. Microbiology 151 : 2251 2261.
34. Roberson EB Firestone MK (1992) Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl Environ Microbiol 58 : 1284 1291.
35. Sambrook J, Fritsch EF Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Schnider-Keel U, Lejbølle KB, Baehler E, Haas D Keel C (2001) The sigma factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHAO. Appl Environ Microbiol 67 : 5683 5693.
37. Shestakov SV, Anbudurai PR, Stanbekova GE, Gadzhiev A, Lind LK Pakrasi HB (1994) Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 269 : 19354 19359.
38. Simon R, Priefer U Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology 1 : 784 791.
39. Stougaard J (2001) Genetics and genomics of root symbiosis. Curr Opin Plant Biol 4 : 328 335.
40. Summers ML, Botero LM, Busse SC McDermott TR (2000) The Sinorhizobium meliloti lon protease is involved in regulating exopolysaccharide synthesis and is required for nodulation of alfalfa. J Bacteriol 182 : 2551 2558.
41. van de Mortel M Halverson LJ (2004) Cell envelope components contributing to biofilm growth and survival of Pseudomonas putida in low-water-content habitats. Mol Microbiol 52 : 735 750.
42. Vincent VM (1970) A Manual for the Practical Study of Root-nodule Bacteria (IBP Handbook no. 15), Blackwell Scientific Publications, Oxford.
43. Wilson KJ, Jefferson RA Hughes SG (1992) The Escherichia coli gus operon: induction and expression of the gus operon in E. coli and the occurrence and use of Gus in other bacteria. Gus Protocols (Gallagher SR, ed), pp 7 22. Academic Press Inc., San Diego, CA.
44. Young JP, Crossman LC, Johnston AW et al 2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7 : R34.
45. Yost CK, Rath AM, Noel TC Hynes MF (2006) Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae. Microbiology 152 : 2061 2074.