Mutation of a broadly conserved operon (RL3499-RL3502) from Rhizobium leguminosarum biovar viciae causes defects in cell morphology and envelope integrity

Journal of Bacteriology

Volumn 193, Issue 11, 2011, Pages 2684-2694

  Vanderlinde, Elizabeth M ^a   Magnus, Samantha A ^a   Tambalo, Dinah D ^b   Koval, Susan F ^c   Yost, Christopher K ^a  

^a UNIVERSITY OF REGINA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; DETERGENT; GLYCINE; MEMBRANE PROTEIN;

ALKALINITY; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTERIUM MUTANT; CELL SURVIVAL; CHEMOSENSITIVITY; CONSERVATION GENETICS; CULTURE MEDIUM; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; GROWTH CURVE; MUTAGENESIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RHIZOBIUM LEGUMINOSARUM; TRANSPOSON; WILD TYPE; YEAST;

ADENOSINE TRIPHOSPHATASES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL MEMBRANE; CELL WALL; CULTURE MEDIA; DETERGENTS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION PROFILING; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS, INSERTIONAL; MUTATION; OPERON; RHIZOBIUM LEGUMINOSARUM;

ALPHAPROTEOBACTERIA; ANIMALIA; BACTERIA (MICROORGANISMS); BRUCELLA; RHIZOBIUM LEGUMINOSARUM;

EID: 79958122911     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01456-10     Document Type: Article

References (66)

1. Altschul, S. F., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Aono, R., and T. Sanada. 1994. Hyper-autolysis of the facultative alkaliphile Bacillus sp. C-125 cells grown at neutral pH: culture-pH dpendent crosslinking of the peptide moieties of the peptidoglycan. Biosci. Biotechnol. Biochem. 58:2015-2019.
3. Arai, M., et al. 2004. ConPred II: a consensus prediction method for obtaining transmembrane topology models with high reliability. Nucleic Acids Res. 32:W390-W393.
4. Bélanger, L., K. Dimmick, J. Fleming, and T. Charles. 2009. Null mutations in Sinorhizobium meliloti exoS and chvI demonstrate the importance of this two-component regulatory system for symbiosis. Mol. Microbiol. 74:1223- 1237.
5. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
6. Beringer, J. E. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:189-198.
7. Campbell, G. R. O., B. L. Reuhst, and G. C. Walker. 2002. Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc. Natl. Acad. Sci. U. S. A. 99:3938-3943.
8. Chen, E. J., R. F. Fisher, V. M. Perovich, E. A. Sabio, and S. R. Long. 2009. Identification of direct transcriptional target genes of ExoS/ChvI two-component signaling in Sinorhizobium meliloti. J. Bacteriol. 191:6833-6842.
9. Darling, A. C., B. Mau, F. R. Blattner, and N. T. Perna. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394-1403. 10.
10. Dominguez, D. C. 2004. Calcium signaling in bacteria. Mol. Microbiol. 54: 291-297.
11. Dylan, T., D. R. Helinski, and G. S. Ditta. 1990. Hypoosmotic adaptation in Rhizobium meliloti requires β-(1→2)-glucan. J. Bacteriol. 172:1400-1408.
12. Eisenhut, M., H. Bauwe, and M. Hagemann. 2007. Glycine accumulation is toxic for the cyanobacterium Synechocystis sp. strain PCC 6803, but can be compensated by supplementation with magnesium ions. FEMS Microbiol. Lett. 277:232-237.
13. Eisenschenk, L., et al. 1994. Inhibition of Rhizobium etli polysaccharide mutants by Phaseolus vulgaris root compounds. Appl. Environ. Microbiol. 60:3315-3322.
14. Ferguson, B. J., et al. 2010. Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52:61-76.
15. Ferguson, G. P., A. Datta, R. W. Carlson, and G. C. Walker. 2005. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol. Microbiol. 56:68-80.
16. Ferguson, G. P., R. M. I. I. Roop, and G. C. Walker. 2002. Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope. J. Bacteriol. 184:5625-5632.
17. Foreman, D. L., E. M. Vanderlinde, D. C. Bay, and C. K. Yost. 2010. Characterization of a gene family of outer membrane proteins (ropB) in Rhizobium leguminosarum bv. viciae VF39SM and the role of the sensor kinase ChvG in their regulation. J. Bacteriol. 192:975-983.
18. Gage, D. J. 2002. Analysis of infection thread development using gfp- and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184:7042-7046.
19. Galperin, M. Y., and E. V. Koonin. 2010. From complete genome sequence to 'complete' understanding? Trends Biotechnol. 28:398-406.
20. Gaudy, A. F. Jr., F. Abu-Niajj, and E. T. Gaudy. 1963. Statistical study of the spot-plate technique for viable-cell counts. Appl. Microbiol. 11:305-309.
21. Gibson, K. E., H. Kobayashi, and G. C. Walker. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441.
22. Gilbert, K. B., E. M. Vanderlinde, and C. K. Yost. 2007. Mutagenesis of the carboxy terminal protease CtpA decreases desiccation tolerance in Rhizobium leguminosarum. FEMS Microbiol. Lett. 272:65-74.
23. Goley, E. D., L. R. Comolli, K. E. Fero, K. H. Downing, and L. Shapiro. 24 May 2010. DipM links peptidoglycan remodeling to outer membrane organization in Caulobacter. Mol. Microbiol. doi:10.1111/j.1365-2958.2010.07222.x.
24. Griffitts, J. S., and S. R. Long. 2008. A symbiotic mutant of Sinorhizobium meliloti reveals a novel genetic pathway involving succinoglycan biosynthetic functions. Mol. Microbiol. 67:1292-1306.
25. Haag, A. F., et al. 2009. The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J. Bacteriol. 191:4681-4686.
26. Hammes, W., K. H. Schleifer, and O. Kandler. 1973. Mode of action of glycine on the biosynthesis of peptidoglycan. J. Bacteriol. 116:1029-1053.
27. Hartmann, R., S. B. Bock-Hennig, U. Schwarz. 1974. Murein hydrolases in the envelope of Escherichia coli. Properties in situ and solubilization from the envelope. Eur. J. Biochem. 41:203-208.
28. Johnston, A. W., and J. E. Beringer. 1975. Identification of the rhizobium strains in pea root nodules using genetic markers. J. Gen. Microbiol. 87:343- 350.
29. Kumar, S., M. Nei, J. Dudley, and K. Tamura. 2008. MEGA: a biologistcentric software for evolutionary analysis of DNA and protein sequences. Brief Bioinformatics 9:299-306.
30. Leduc, M., R. Kasra, and J. van Heijenoort. 1982. Induction and control of the autolytic system of Escherichia coli. J. Bacteriol. 152:26-34.
31. Leduc, M., and J. van Heijenoort. 1980. Autolysis of Escherichia coli. J. Bacteriol. 142:52-59.
32. Li, L., et al. 2002. A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc. Natl. Acad. Sci. U. S. A. 99:12369-12374.
33. Li, Z., et al. 2009. Calcium leads to further increase in glycine-enhanced extracellular secretion of recombinant alpha-cyclodextrin glycosyltransferase in Escherichia coli. J. Agric. Food Chem. 57:6231-6237.
34. Manzon, R. G., T. M. Neuls, and L. A. Manzon. 2007. Molecular cloning, tissue distribution, and developmental expression of lamprey transthyretins. Gen. Comp. Endocrinol. 151:55-65.
35. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
36. Miller, L. D., C. K. Yost, M. F. Hynes, and G. Alexandre. 2007. The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol. Microbiol. 63:348-362.
37. Miller-Williams, M., P. C. Loewen, and I. J. Oresnik. 2006. Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiology 152:2049-2059.
38. Nagarajan, T., J. Vanderleyden, and A. K. Tripathi. 2007. Identification of salt stress inducible genes that control cell envelope related functions in Azospirillum brasilense Sp7. Mol. Genet. Genomics 278:43-51.
39. Norris, V., et al. 1991. Calcium in bacteria: a solution to which problem? Mol. Microbiol. 5:775-778.
40. Onoda, T., et al. 2000. Effects of calcium and calcium chelators on growth and morphology of Escherichia coli L-form NC-7. J. Bacteriol. 182:1419-1422.
41. Parada, M., et al. 2006. Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol. Plant Microbe Interact. 19:43-52.
42. Priefer, U. 1989. Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39. J. Bacteriol. 171:6161-6168.
43. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127: 15-21.
44. Reeve, W. G., et al. 1999. Constructs for insertional mutagenesis, transcriptional signal localization and gene regulation studies in root nodule and other bacteria. Microbiology 145:1307-1316.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
46. Sherwood, M. 1972. Inhibition of Rhizobium trifolii by yeast extracts or glycine is prevented by calcium. Microbiology 71:351.
47. Skinner, F. A., R. J. Roughley, and M. R. Chandler. 1977. Effects of yeast extraction concentration on viability and cell distortion in Rhizobium spp. J. Appl. Bacteriol. 43:287-297.
48. Skorupska, A., M. Janczarik, M. Marczak, A. Mazur, and J. Król. 2006. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5:7.
49. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering-transposon mutagenesis in Gram negative bacteria. Biotechnology 1:784-791.
50. Smith, R. J. 1995. Calcium signaling in bacteria. Adv. Microb. Physiol. 37:83-133.
51. Snider, J., and W. A. Houry. 2006. MoxR AAA+ ATPases: a novel family of molecular chaperones? J. Struct. Biol. 156:200-209.
52. Stougaard, J. 2000. Regulators and regulation of legume root nodule development. Plant Physiol. 124:531-540.
53. Sukdeo, N., and T. C. Charles. 2003. Application of crossover-PCR-mediated deletion-insertion mutagenesis to analysis of the bdhA-xdhA2-xdhB2 mixed-function operon of Sinorhizobium meliloti. Arch. Microbiol. 179:301-304.
54. Tambalo, D. D., et al. 2010. Regulation of flagellar, motility and chemotaxis genes in Rhizobium leguminosarum by the VisN/R-Rem cascade. Microbiology 156:1673-1685.
55. Tang, X., B. F. Lu, and S. Q. Pan. 1999. A bifunctional transposon mini-Tn5gfp-km which can be used to select for promoter fusions and report gene expression levels in Agrobacterium tumefaciens. FEMS Microbiol. Lett. 179: 37-42.
56. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 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.
57. Vanderlinde, E. M., et al. 2010. Identification of a novel ABC transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol. Ecol. 71:327-340.
58. Vanderlinde, E. M., et al. 2009. Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155:3055-3069.
59. Vedam, V., J. G. Haynes, E. L. Kannenberg, R. W. Carlson, and D. J. Sherrier. 2004. A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol. Plant Microbe Interact. 17:283-291.
60. Vincent, V. M. 1970. A manual for the practical study of root-nodule bacteria. Lippincott Williams & Wilkins, Hagerstown, MD.
61. Vriezen, J. A. C., F. J. de Bruijn, and K. Nüsslein. 2007. Responses of rhizobia to desiccation in relation to osmotic stress, oxygen and temperature. Appl. Environ. Microbiol. 73:3451-3459.
62. Williams, K. P., B. W. Sobral, and A. W. Dickerman. 2007. A robust species tree for the Alphaproteobacteria. J. Bacteriol. 189:4578-4586.
63. Yost, C. K., A. M. Rath, T. C. Noel, and M. F. Hynes. 2006. Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae. Microbiology 152:2061-2074.
64. Yost, C. K., K. L. Del Bel, J. Quandt, and M. F. Hynes. 2004. Rhizobium leguminosarum methyl-accepting chemotaxis protein genes are down-regulated in the pea nodule. Arch. Microbiol. 182:505-513.
65. Yost, C. K., P. Rochepeau, and M. F. Hynes. 1998. Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144:1945-1956.
66. Young, J. P., et al. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7:R34.