Proline utilization by Bacillus subtilis: Uptake and catabolism

Journal of Bacteriology

Volumn 194, Issue 4, 2012, Pages 745-758

  Moses, Susanne ^a   Sinner, Tatjana ^a   Zaprasis, Adrienne ^a   Stöveken, Nadine ^a   Hoffmann, Tamara ^a   Sonenshein, B R B ^b   Boris R Belitsky, ^b   Bremer, Erhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; PROLINE; PROLINE DEHYDROGENASE; PYRROLINE 5 CARBOXYLATE DEHYDROGENASE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; GENE EXPRESSION; GENE FUSION; GENE LOCUS; GENETIC TRANSCRIPTION; NONHUMAN; NORTHERN BLOTTING; OPERON; OSMOLARITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REPORTER GENE;

1-PYRROLINE-5-CARBOXYLATE DEHYDROGENASE; AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, REPORTER; GLUTAMIC ACID; OPERON; PROLINE; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 84857067830     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06380-11     Document Type: Article

References (72)

1. Alloing G, Travers I, Sagot B, Le Rudulier D, Dupont L. 2006. Proline betaine uptake in Sinorhizobium meliloti: characterization of Prb, an Opplike ABC transporter regulated by both proline betaine and salinity stress. J. Bacteriol. 188:6308-6317.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201.
4. Atkinson MR, Wray LV, Jr, Fisher SH. 1990. Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis. J. Bacteriol. 172:4758-4765.
5. Bates SL, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39:205-207.
6. Baumberg S, Harwood CR. 1979. Carbon and nitrogen repression of arginine catabolic enzymes in Bacillus subtilis. J. Bacteriol. 137:189-196.
7. Belitsky BR. 2011. Indirect repression by Bacillus subtilis CodY via displacement of the activator of the proline utilization operon. J. Mol. Biol. 413:321-336.
8. Belitsky BR, Sonenshein AL. 1998. Role and regulation of Bacillus subtilis glutamate dehydrogenase genes. J. Bacteriol. 180:6298-6305.
9. Bremer E. 2002. Adaptation to changing osmolarity, p 385-391. In Sonenshein AL, Hoch JA, and Losick R (ed), Bacillus subtilis and its closest relatives. ASM Press, Washington, DC.
10. Bremer E, Krämer R. 2000. Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes, p 79-97. In Storz G and Hengge-Aronis R (ed), Bacterial stress responses. ASM Press, Washington, DC.
11. Brill J, Hoffmann T, Bleisteiner M, Bremer E. 2011. Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity. J. Bacteriol. 193:5335-5346.
12. Brill J, Hoffmann T, Putzer H, Bremer E. 2011. T-box-mediated control of the anabolic proline biosynthetic genes of Bacillus subtilis. Microbiology 157:977-987.
13. Chen LM, Maloy S. 1991. Regulation of proline utilization in enteric bacteria: cloning and characterization of the Klebsiella put control region. J. Bacteriol. 173:783-790.
14. Commichau FM, Gunka K, Landmann JJ, Stülke J. 2008. Glutamate metabolism in Bacillus subtilis: gene expression and enzyme activities evolved to avoid futile cycles and to allow rapid responses to perturbations of the system. J. Bacteriol. 190:3557-3564.
15. Csonka LN. 1988. Regulation of cytoplasmic proline levels in Salmonella typhimurium: effect of osmotic stress on synthesis, degradation, and cellular retention of proline. J. Bacteriol. 170:2374-2378.
16. Csonka LN, Hanson AD. 1991. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45:569-606.
17. Dendinger S, Brill WJ. 1970. Regulation of proline degradation in Salmonella typhimurium. J. Bacteriol. 103:144-152.
18. Deutch CE. 2011. L-Proline nutrition and catabolism in Staphylococcus saprophyticus. Antonie Van Leeuwenhoek 99:781-793.
19. Deutch CE, Hasler JM, Houston RM, Sharma M, Stone VJ. 1989. Nonspecific inhibition of proline dehydrogenase synthesis in Escherichia coli during osmotic stress. Can. J. Microbiol. 35:779-785.
20. Earl AM, Losick R, Kolter R. 2008. Ecology and genomics of Bacillus subtilis. Trends Microbiol. 16:269-275.
21. Ekena K, Maloy S. 1990. Regulation of proline utilization in Salmonella typhimurium: how do cells avoid a futile cycle? Mol. Gen. Genet. 220: 492-494.
22. Fisher SH. 1993. Utilization of amino acids and other nitrogencontaining compounds, p 221-235. In Sonenshein AL, Hoch JA, and Losick R (ed), Bacillus subtilis and other Gram-positive bacteria. ASM Press, Washington, DC.
23. Gotsche S, Dahl MK. 1995. Purification and characterization of the phospho-alpha(1,1)glucosidase (TreA) of Bacillus subtilis 168. J. Bacteriol. 177:2721-2726.
24. Hahne H, et al. 2010. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J. Bacteriol. 192:870-882.
25. Hanson AD, et al. 1994. Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc. Natl. Acad. Sci. U. S. A. 91:306-310.
26. Harwood CR, Archibald AR. 1990. Growth, maintenance and general techniques, p 1-26. In Harwood CR and Cutting SM (ed), Molecular biological methods for Bacillus. John Wiley & Sons, Chichester, United Kingdom.
27. Harwood CR, Crawshaw SG, Wipat A. 2001. From genome to function: systematic analysis of the soil bacterium Bacillus subtilis. Comp. Funct. Genomics 2:22-24.
28. Harwood CR, Cutting SM. 1990. Molecular biological methods for Bacillus. John Wiley & Sons, Chichester, United Kingdom.
29. Helmann JD. 1995. Compilation and analysis of Bacillus subtilis sigma A-dependent promoter sequences: evidence for extended contact between RNA polymerase and upstream promoter DNA. Nucleic Acids Res. 23: 2351-2360.
30. Holtmann G, Bremer E. 2004. Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J. Bacteriol. 186:1683-1693.
31. Huang SC, Lin TH, Shaw GC. 2011. PrcR, a PucR-type transcriptional activator, is essential for proline utilization and mediates prolineresponsive expression of the proline utilization operon putBCP in Bacillus subtilis. Microbiology 157:3370-3377.
32. 1-pyrroline-5-carboxylate dehydrogenase. J. Mol. Biol. 362:490-501.
33. Jafri S, Evoy S, Cho K, Craighead HG, Winans SC. 1999. An Lrp-type transcriptional regulator from Agrobacterium tumefaciens condenses more than 100 nucleotides of DNA into globular nucleoprotein complexes. J. Mol. Biol. 288:811-824.
34. Kappes RM, Kempf B, Bremer E. 1996. Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J. Bacteriol. 178:5071-5079.
35. Köcher S, Tausendschön M, Thompson M, Saum SH, Müller V. 2011. Proline metabolism in the moderate halophilic bacterium Halobacillus halophilus: differential regulation of isogenes in proline utilization. Environ. Microbiol. Rep. 3:443-448.
36. Lee JH, Park NY, Lee MH, Choi SH. 2003. Characterization of the Vibrio vulnificus putAP operon, encoding proline dehydrogenase and proline permease, and its differential expression in response to osmotic stress. J. Bacteriol. 185:3842-3852.
37. 1-pyrroline-5-carboxylate dehydrogenase domains of the multifunctional Escherichia coli PutA protein. J. Mol. Biol. 243:950-956.
38. Lucht JM, Bremer E. 1994. Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-affinity glycine betaine transport system ProU. FEMS Microbiol. Rev. 14:3-20.
39. May G, Faatz E, Villarejo M, Bremer E. 1986. Binding protein dependent transport of glycine betaine and its osmotic regulation in Escherichia coli K12. Mol. Gen. Genet. 205:225-233.
40. +-coupled substrate co-transport. J. Biol. Chem. 286:29347-29355.
41. Menzel R, Roth J. 1981. Regulation of the genes for proline utilization in Salmonella typhimurium: autogenous repression by the putA gene product. J. Mol. Biol. 148:21-44.
42. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
43. Milner JL, McClellan DJ, Wood JM. 1987. Factors reducing and promoting the effectiveness of proline as an osmoprotectant in Escherichia coli K12. J. Gen. Microbiol. 133:1851-1860.
44. Molle V, et al. 2003. Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J. Bacteriol. 185:1911-1922.
45. Müller J, Schiel S, Ordal GW, Saxild HH. 1997. Functional and genetic characterization of mcpC, which encodes a third methyl-accepting chemotaxis protein in Bacillus subtilis. Microbiology 143:3231-3240.
46. Muro-Pastor AM, Ostrovsky P, Maloy S. 1997. Regulation of gene expression by repressor localization: biochemical evidence that membrane and DNA binding by the PutA protein are mutually exclusive. J. Bacteriol. 179:2788-2791.
47. Nakada Y, Nishijyo T, Itoh Y. 2002. Divergent structure and regulatory mechanism of proline catabolic systems: characterization of the putAP proline catabolic operon of Pseudomonas aeruginosa PAO1 and its regulation by PruR, an AraC/XylS family protein. J. Bacteriol. 184:5633-5640.
48. +/proline transporter PutP of Escherichia coli and its functional implications. J. Mol. Biol. 406:59-74.
49. Ordal GW, Marquez-Magana L, Chamberlin MJ. 1993. Motility and chemotaxis, p 765-784. In Sonenshein AL, Hoch JA, and Losick R (ed), Bacillus subtilis and other Gram-positive bacteria. ASM Press, Washington, DC.
50. Ordal GW, Villani DP, Gibson KJ. 1977. Amino acid chemoreceptors of Bacillus subtilis. J. Bacteriol. 129:156-165.
51. Ordal GW, Villani DP, Nicholas RA, Hamel FG. 1978. Independence of proline chemotaxis and transport in Bacillus subtilis. J. Biol. Chem. 253: 4916-4919.
52. Ostrovsky de Spicer P, Maloy S. 1993. PutA protein, a membraneassociated flavin dehydrogenase, acts as a redox-dependent transcriptional regulator. Proc. Natl. Acad. Sci. U. S. A. 90:4295-4298.
53. Smits SH, et al. 2008. The compatible-solute-binding protein OpuAC from Bacillus subtilis: ligand binding, site-directed mutagenesis, and crystallographic studies. J. Bacteriol. 190:5663-5671.
54. Sonenshein AL. 2005. CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8:203-207.
55. Sonenshein AL. 2007. Control of key metabolic intersections in Bacillus subtilis. Nat. Rev. Microbiol. 5:917-927.
56. Sonenshein AL. 2000. Control of sporulation initiation in Bacillus subtilis. Curr. Opin. Microbiol. 3:561-566.
57. Soto MJ, Jimenez-Zurdo JI, van Dillewijn P, Toro N. 2000. Sinorhizobium meliloti putA gene regulation: a new model within the family Rhizobiaceae. J. Bacteriol. 182:1935-1941.
58. Spiegelhalter F, Bremer E. 1998. Osmoregulation of the opuE proline transport gene from Bacillus subtilis: contributions of the sigma A- and sigma B-dependent stress-responsive promoters. Mol. Microbiol. 29:285-296.
59. Srivastava D, et al. 2010. Crystal structure of the bifunctional proline utilization A flavoenzyme from Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U. S. A. 107:2878-2883.
60. Steil L, Hoffmann T, Budde I, Völker U, Bremer E. 2003. Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. J. Bacteriol. 185:6358-6370.
61. Tanner JJ. 2008. Structural biology of proline catabolism. Amino Acids 35:719-730.
62. Tetsch L, Koller C, Haneburger I, Jung K. 2008. The membraneintegrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol. Microbiol. 67:570-583.
63. Thompson JD, Plewniak F, Thierry JC, Poch O. 2000. DbClustal: rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acids Res. 28:2919-2926.
64. Vilchez S, Molina L, Ramos C, Ramos JL. 2000. Proline catabolism by Pseudomonas putida: cloning, characterization, and expression of the put genes in the presence of root exudates. J. Bacteriol. 182:91-99.
65. von Blohn C, Kempf B, Kappes RM, Bremer E. 1997. Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Mol. Microbiol. 25:175-187.
66. Welsh DT. 2000. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 24:263-290.
67. Whatmore AM, Chudek JA, Reed RH. 1990. The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J. Gen. Microbiol. 136:2527-2535.
68. White TA, Krishnan N, Becker DF, Tanner JJ. 2007. Structure andkinetics of monofunctional proline dehydrogenase from Thermus thermophilus. J. Biol. Chem. 282:14316-14327
69. Wood JM. 1981. Genetics of L-proline utilization in Escherichia coli. J. Bacteriol. 146:895-901.
70. Wood JM. 1987. Membrane association of proline dehydrogenase in Escherichia coli is redox dependent. Proc. Natl. Acad. Sci. U. S. A. 84:373-377.
71. Zhou Y, et al. 2008. Structural basis of the transcriptional regulation of the proline utilization regulon by multifunctional PutA. J. Mol. Biol. 381: 174-188.
72. Zhou Y, Zhu W, Bellur PS, Rewinkel D, Becker DF. 2008. Direct linking of metabolism and gene expression in the proline utilization A protein from Escherichia coli. Amino Acids 35:711-718.