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. 1993 Apr;175(8):2284–2291. doi: 10.1128/jb.175.8.2284-2291.1993

Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti.

J B Robinson 1, W D Bauer 1
PMCID: PMC204516  PMID: 8468289

Abstract

The relationship between chemotaxis and transport of C4 dicarboxylic acids was analyzed with Rhizobium meliloti dct mutants defective in one or all of the genes required for dicarboxylic acid transport. Succinate, malate, and fumarate were moderately potent chemoattractants for wild-type R. meliloti and appeared to share a common chemoreceptor. While dicarboxylate transport is inducible, taxis to succinate was shown to be constitutive. Mutations in the dctA and dctB genes both resulted in the reduction, but not elimination, of chemotactic responses to succinate, indicating that transport via DctA or chemosensing via DctB is not essential for C4 dicarboxylate taxis, although they appear to contribute to it. Mutations in dctD and rpoN genes did not affect taxis to succinate. Aspartate, which is also transported by the dicarboxylate transport system, elicited strong chemotactic responses via a chemoreceptor distinct from the succinate-malate-fumarate receptor. Taxis to aspartate was unaltered in dctA and dctB mutants but was considerably reduced in both dctD and rpoN mutants, indicating that aspartate taxis is strongly dependent on elements responsible for transcriptional activation of dctA. Methylation and methanol release experiments failed to show a significant increase in methyl esterification of R. meliloti proteins in response to any of the attractants tested.

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Selected References

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  1. Adler J. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol. 1973 Jan;74(1):77–91. doi: 10.1099/00221287-74-1-77. [DOI] [PubMed] [Google Scholar]
  2. Armitage J. P., Gallagher A., Johnston A. W. Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid. Mol Microbiol. 1988 Nov;2(6):743–748. doi: 10.1111/j.1365-2958.1988.tb00085.x. [DOI] [PubMed] [Google Scholar]
  3. Aswad D. W., Koshland D. E., Jr Evidence for an S-adenosylmethionine requirement in the chemotactic behavior of Salmonella typhimurium. J Mol Biol. 1975 Sep 15;97(2):207–223. doi: 10.1016/s0022-2836(75)80035-0. [DOI] [PubMed] [Google Scholar]
  4. Caetano-Anollés G., Crist-Estes D. K., Bauer W. D. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol. 1988 Jul;170(7):3164–3169. doi: 10.1128/jb.170.7.3164-3169.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chelsky D., Dahlquist F. W. Structural studies of methyl-accepting chemotaxis proteins of Escherichia coli: evidence for multiple methylation sites. Proc Natl Acad Sci U S A. 1980 May;77(5):2434–2438. doi: 10.1073/pnas.77.5.2434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Engelke T., Jording D., Kapp D., Pühler A. Identification and sequence analysis of the Rhizobium meliloti dctA gene encoding the C4-dicarboxylate carrier. J Bacteriol. 1989 Oct;171(10):5551–5560. doi: 10.1128/jb.171.10.5551-5560.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engström P., Hazelbauer G. L. Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli to chemical stimuli. Cell. 1980 May;20(1):165–171. doi: 10.1016/0092-8674(80)90244-5. [DOI] [PubMed] [Google Scholar]
  8. Finan T. M., Oresnik I., Bottacin A. Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol. 1988 Aug;170(8):3396–3403. doi: 10.1128/jb.170.8.3396-3403.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finan T. M., Wood J. M., Jordan D. C. Succinate transport in Rhizobium leguminosarum. J Bacteriol. 1981 Oct;148(1):193–202. doi: 10.1128/jb.148.1.193-202.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finan T. M., Wood J. M., Jordan D. C. Symbiotic properties of C4-dicarboxylic acid transport mutants of Rhizobium leguminosarum. J Bacteriol. 1983 Jun;154(3):1403–1413. doi: 10.1128/jb.154.3.1403-1413.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gardiol A. E., Truchet G. L., Dazzo F. B. Requirement of succinate dehydrogenase activity for symbiotic bacteroid differentiation of Rhizobium meliloti in alfalfa nodules. Appl Environ Microbiol. 1987 Aug;53(8):1947–1950. doi: 10.1128/aem.53.8.1947-1950.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanlon D. W., Carpenter P. B., Ordal G. W. Influence of attractants and repellents on methyl group turnover on methyl-accepting chemotaxis proteins of Bacillus subtilis and role of CheW. J Bacteriol. 1992 Jul;174(13):4218–4222. doi: 10.1128/jb.174.13.4218-4222.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harwood C. S. A methyl-accepting protein is involved in benzoate taxis in Pseudomonas putida. J Bacteriol. 1989 Sep;171(9):4603–4608. doi: 10.1128/jb.171.9.4603-4608.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harwood C. S., Rivelli M., Ornston L. N. Aromatic acids are chemoattractants for Pseudomonas putida. J Bacteriol. 1984 Nov;160(2):622–628. doi: 10.1128/jb.160.2.622-628.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ingham C. J., Armitage J. P. Involvement of transport in Rhodobacter sphaeroides chemotaxis. J Bacteriol. 1987 Dec;169(12):5801–5807. doi: 10.1128/jb.169.12.5801-5807.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Karimian M., Ornston L. N. Participation of the beta-ketoadipate transport system in chemotaxis. J Gen Microbiol. 1981 May;124(1):25–28. doi: 10.1099/00221287-124-1-25. [DOI] [PubMed] [Google Scholar]
  17. Kleene S. J., Hobson A. C., Adler J. Attractants and repellents influence methylation and demethylation of methyl-accepting chemotaxis proteins in an extract of Escherichia coli. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6309–6313. doi: 10.1073/pnas.76.12.6309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kort E. N., Goy M. F., Larsen S. H., Adler J. Methylation of a membrane protein involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3939–3943. doi: 10.1073/pnas.72.10.3939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McAllister C. F., Lepo J. E. Succinate transport by free-living forms of Rhizobium japonicum. J Bacteriol. 1983 Mar;153(3):1155–1162. doi: 10.1128/jb.153.3.1155-1162.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Melton T., Hartman P. E., Stratis J. P., Lee T. L., Davis A. T. Chemotaxis of Salmonella typhimurium to amino acids and some sugars. J Bacteriol. 1978 Feb;133(2):708–716. doi: 10.1128/jb.133.2.708-716.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mesibov R., Adler J. Chemotaxis toward amino acids in Escherichia coli. J Bacteriol. 1972 Oct;112(1):315–326. doi: 10.1128/jb.112.1.315-326.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nowlin D. M., Nettleton D. O., Ordal G. W., Hazelbauer G. L. Chemotactic transducer proteins of Escherichia coli exhibit homology with methyl-accepting proteins from distantly related bacteria. J Bacteriol. 1985 Jul;163(1):262–266. doi: 10.1128/jb.163.1.262-266.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ordal G. W. Bacterial chemotaxis: biochemistry of behavior in a single cell. Crit Rev Microbiol. 1985;12(2):95–130. doi: 10.3109/10408418509104426. [DOI] [PubMed] [Google Scholar]
  24. Palleroni N. J. Chamber for bacterial chemotaxis experiments. Appl Environ Microbiol. 1976 Nov;32(5):729–730. doi: 10.1128/aem.32.5.729-730.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Parke D., Rivelli M., Ornston L. N. Chemotaxis to aromatic and hydroaromatic acids: comparison of Bradyrhizobium japonicum and Rhizobium trifolii. J Bacteriol. 1985 Aug;163(2):417–422. doi: 10.1128/jb.163.2.417-422.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reding H. K., Lepo J. E. Physiological Characterization of Dicarboxylate-Induced Pleomorphic Forms of Bradyrhizobium japonicum. Appl Environ Microbiol. 1989 Mar;55(3):666–671. doi: 10.1128/aem.55.3.666-671.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robinson J. B., Tuovinen O. H., Bauer W. D. Role of divalent cations in the subunit associations of complex flagella from Rhizobium meliloti. J Bacteriol. 1992 Jun;174(12):3896–3902. doi: 10.1128/jb.174.12.3896-3902.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ronson C. W., Astwood P. M., Downie J. A. Molecular cloning and genetic organization of C4-dicarboxylate transport genes from Rhizobium leguminosarum. J Bacteriol. 1984 Dec;160(3):903–909. doi: 10.1128/jb.160.3.903-909.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ronson C. W., Astwood P. M., Nixon B. T., Ausubel F. M. Deduced products of C4-dicarboxylate transport regulatory genes of Rhizobium leguminosarum are homologous to nitrogen regulatory gene products. Nucleic Acids Res. 1987 Oct 12;15(19):7921–7934. doi: 10.1093/nar/15.19.7921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ronson C. W., Nixon B. T., Albright L. M., Ausubel F. M. Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions. J Bacteriol. 1987 Jun;169(6):2424–2431. doi: 10.1128/jb.169.6.2424-2431.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ronson C. W., Nixon B. T., Ausubel F. M. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell. 1987 Jun 5;49(5):579–581. doi: 10.1016/0092-8674(87)90530-7. [DOI] [PubMed] [Google Scholar]
  33. Russo A. F., Koshland D. E., Jr Separation of signal transduction and adaptation functions of the aspartate receptor in bacterial sensing. Science. 1983 Jun 3;220(4601):1016–1020. doi: 10.1126/science.6302843. [DOI] [PubMed] [Google Scholar]
  34. Sockett R. E., Armitage J. P., Evans M. C. Methylation-independent and methylation-dependent chemotaxis in Rhodobacter sphaeroides and Rhodospirillum rubrum. J Bacteriol. 1987 Dec;169(12):5808–5814. doi: 10.1128/jb.169.12.5808-5814.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Springer M. S., Goy M. F., Adler J. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3312–3316. doi: 10.1073/pnas.74.8.3312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Springer W. R., Koshland D. E., Jr Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci U S A. 1977 Feb;74(2):533–537. doi: 10.1073/pnas.74.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stowers M. D. Carbon metabolism in Rhizobium species. Annu Rev Microbiol. 1985;39:89–108. doi: 10.1146/annurev.mi.39.100185.000513. [DOI] [PubMed] [Google Scholar]
  39. Urban J. E., Dazzo F. B. Succinate-Induced Morphology of Rhizobium trifolii 0403 Resembles That of Bacteroids in Clover Nodules. Appl Environ Microbiol. 1982 Jul;44(1):219–226. doi: 10.1128/aem.44.1.219-226.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Watson R. J., Chan Y. K., Wheatcroft R., Yang A. F., Han S. H. Rhizobium meliloti genes required for C4-dicarboxylate transport and symbiotic nitrogen fixation are located on a megaplasmid. J Bacteriol. 1988 Feb;170(2):927–934. doi: 10.1128/jb.170.2.927-934.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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