Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Salmonella enterica forms polyhedral organelles involved in coenzyme B 12 -dependent 1,2-propanediol degradation. These organelles are thought to consist of a proteinaceous shell that encases coenzyme B 12 -dependent diol dehydratase and perhaps other enzymes involved in 1,2-propanediol degradation. The function of these organelles is unknown, and no detailed studies of their structure have been reported. Genes needed for organelle formation and for 1,2-propanediol degradation are located at the 1,2-propanediol utilization ( pdu ) locus, but the specific genes involved in organelle formation have not been identified. Here, we show that the pduA gene encodes a shell protein required for the formation of polyhedral organelles involved in coenzyme B 12 -dependent 1,2-propanediol degradation. A His 6 -PduA fusion protein was purified from a recombinant Escherichia coli strain and used for the preparation of polyclonal antibodies. The anti-PduA antibodies obtained were partially purified by a subtraction procedure and used to demonstrate that the PduA protein localized to the shell of the polyhedral organelles. In addition, electron microscopy studies established that strains with nonpolar pduA mutations were unable to form organelles. These results show that the pduA gene is essential for organelle formation and indicate that the PduA protein is a structural component of the shell of these organelles. Physiological studies of nonpolar pduA mutants were also conducted. Such mutants grew similarly to the wild-type strain at low concentrations of 1,2-propanediol but exhibited a period of interrupted growth in the presence of higher concentrations of this growth substrate. Growth tests also showed that a nonpolar pduA deletion mutant grew faster than the wild-type strain at low vitamin B 12 concentrations. These results suggest that the polyhedral organelles formed by S. enterica during growth on 1,2-propanediol are not involved in the concentration of 1,2-propanediol or coenzyme B 12 , but are consistent with the hypothesis that these organelles moderate aldehyde production to minimize toxicity.

Bibliography

Havemann, G. D., Sampson, E. M., & Bobik, T. A. (2002). PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B 12 -Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2. Journal of Bacteriology, 184(5), 1253–1261.

Authors 3
  1. Gregory D. Havemann (first)
  2. Edith M. Sampson (additional)
  3. Thomas A. Bobik (additional)
References 39 Referenced 132
  1. 10.1016/S0022-2836(05)80360-2
  2. Baker, S. H., S. C. Lorbach, M. Rodriguez-Buey, D. S. Williams, H. C. Aldrich, and J. M. Shively. 1999. The correlation of the gene csoS2 of the carboxysome operon with two polypeptides of the carboxysome in Thiobacillus neapolitanus. Arch. Microbiol.172:233-239. (10.1007/s002030050765) / Arch. Microbiol. (1999)
  3. Baker, S. H., D. S. Williams, H. C. Aldrich, A. C. Gambrell, and J. M. Shively. 2000. Identification and localization of the carboxysome peptide Csos3 and its corresponding gene in Thiobacillus neapolitanus. Arch. Microbiol.173:278-283. (10.1007/s002030000141) / Arch. Microbiol. (2000)
  4. 10.1128/jb.96.1.215-220.1968
  5. 10.1128/jb.174.7.2253-2266.1992
  6. 10.1128/JB.181.19.5967-5975.1999
  7. Conner, C. P., D. M. Heithoff, S. M. Julio, R. L. Sinsheimer, and M. J. Mahan. 1998. Differential patterns of acquired virulence genes distinguish Salmonella strains. Proc. Natl. Acad. Sci. USA95:4641-4645. (10.1073/pnas.95.8.4641) / Proc. Natl. Acad. Sci. USA (1998)
  8. 10.1073/pnas.120163297
  9. Davis R. W. D. Botstein J. R. Roth and Cold Spring Harbor Laboratory. 1980. Advanced bacterial genetics: a manual for genetic engineering. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  10. Harlow E. and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  11. 10.1128/JB.181.3.799-807.1999
  12. 10.1128/jb.179.3.928-940.1997
  13. Jeter, R. M. 1990. Cobalamin-dependent 1,2-propanediol utilization by Salmonella typhimurium. J. Gen. Microbiol.136:887-896. (10.1099/00221287-136-5-887) / J. Gen. Microbiol. (1990)
  14. 10.1128/JB.183.5.1577-1584.2001
  15. Kaplan, A., and L. Reinhold. 1999. CO2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol.50:539-570. (10.1146/annurev.arplant.50.1.539) / Annu. Rev. Plant Physiol. Plant Mol. Biol. (1999)
  16. Lawrence, J. G., and J. R. Roth. 1996. Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and reacquisition of a multigene complex. Genetics142:11-24. (10.1093/genetics/142.1.11) / Genetics (1996)
  17. Ludwig, M., D. Sultemeyer, and G. D. Price. 2000. Isolation of ccmKLMN genes from the marine cyanobacterium, Synechococcus sp. PCC7002 (Cyanophyceae), and evidence that CcmM is essential for carboxysome assembly. J. Phycol.36:1109-1118. (10.1046/j.1529-8817.2000.00028.x) / J. Phycol. (2000)
  18. 10.1128/aem.60.3.1018-1020.1994
  19. Marco, E., and M. I. Orus. 1993. Trichlorfon-induced inhibition of nitrate and ammonium uptake in cyanobacteria. J. Exp. Bot.44:501-508. (10.1093/jxb/44.2.501) / J. Exp. Bot. (1993)
  20. Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  21. 10.1128/jb.170.5.2159-2162.1988
  22. Ogawa, T., D. Amichay, and M. Gurevitz. 1994. Isolation and characterization of the ccmM gene required by the cyanobacterium Synechocystis PCC6803 for inorganic carbon utilization. Photosynth. Res.39:183-190. (10.1007/BF00029385) / Photosynth. Res. (1994)
  23. Price, G. D., and M. R. Badger. 1991. Evidence for the role of carboxysomes in the cyanobacterial CO2-concentrating mechanism. Can. J. Bot.69:963-973. (10.1139/b91-124) / Can. J. Bot. (1991)
  24. 10.1128/jb.175.10.2871-2879.1993
  25. Price, G. D., D. Sultemeyer, B. Klughammer, M. Ludwig, and R. Badger Murray. 1998. The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can. J. Bot.76:973-1002. / Can. J. Bot. (1998)
  26. 10.1128/JB.183.8.2463-2475.2001
  27. 10.1128/jb.179.18.5827-5834.1997
  28. 10.1128/jb.170.9.3855-3863.1988
  29. Roth, J. R., J. G. Lawrence, and T. A. Bobik. 1996. Cobalamin (coenzyme B12): synthesis and biological significance. Annu. Rev. Microbiol.50:137-181. (10.1146/annurev.micro.50.1.137) / Annu. Rev. Microbiol. (1996)
  30. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  31. Schmieger H. 1971. Method for detection of phage mutants with altered transducing ability. Mol. Gen. Genet.110:378-381. (10.1007/BF00438281) / Mol. Gen. Genet. (1971)
  32. 10.1128/jb.116.3.1405-1411.1973
  33. Shively, J. M., C. E. Bradburne, H. C. Aldrich, T. A. Bobik, J. L. Mehiman, S. Jin, and S. H. Baker. 1998. Sequence homologs of the carboxysomal polypeptide CsoS1 of the thiobacilli are present in cyanobacteria and enteric bacteria that form carboxysomes-polyhedral bodies. Can. J. Bot.76:906-916. / Can. J. Bot. (1998)
  34. Shively, J. M., and R. S. English. 1991. The carboxysome, a prokaryotic organelle: a mini-review. Can. J. Bot.69:957-962. (10.1139/b91-123) / Can. J. Bot. (1991)
  35. Shively, J. M., G. van Keulen, and W. G. Meijer. 1998. Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu. Rev. Microbiol.52:191-230. (10.1146/annurev.micro.52.1.191) / Annu. Rev. Microbiol. (1998)
  36. 10.1128/jb.177.5.1357-1366.1995
  37. 10.1128/jb.139.1.39-47.1979
  38. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem.218:97-106. (10.1016/S0021-9258(18)65874-0) / J. Biol. Chem. (1956)
  39. Wu Tian, F., D. Liu Yong, and R. Song Li. 2000. Selection and ultrastructural observation of a high-CO2-requiring mutant of cyanobacterium Synechococcus sp. PCC7942. Acta Bot. Sin.42:116-121. / Synechococcus sp. PCC7942. Acta Bot. Sin. (2000)
Dates
Type When
Created 16 years, 4 months ago (April 23, 2009, 2:32 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 2:08 p.m.)
Indexed 3 months, 2 weeks ago (May 16, 2025, 3:48 a.m.)
Issued 23 years, 6 months ago (March 1, 2002)
Published 23 years, 6 months ago (March 1, 2002)
Published Print 23 years, 6 months ago (March 1, 2002)
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@article{Havemann_2002, title={PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B 12 -Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2}, volume={184}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.184.5.1253-1261.2002}, DOI={10.1128/jb.184.5.1253-1261.2002}, number={5}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Havemann, Gregory D. and Sampson, Edith M. and Bobik, Thomas A.}, year={2002}, month=mar, pages={1253–1261} }