The Wrappers of the 1,2-Propanediol Utilization Bacterial Microcompartments

  • Naimat K. Bari
  • Gaurav Kumar
  • Sharmistha SinhaEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1112)


The propanediol utilization bacterial microcompartments are specialized protein-based organelles in Salmonella that facilitate the catabolism of 1,2-propanediol when available as the sole carbon source. This smart prokaryotic cell organelle compartmentalizes essential enzymes and substrates in a volume of a few attoliters compared to the femtoliter volume of a bacterial cell thereby enhancing the enzyme kinetics and properly orchestrating the downstream pathways. A shell or coat, which is composed of a few thousand protein subunits, wraps a chain of consecutively acting enzymes and serves as ducts for the diffusion of substrates, cofactors, and products into and out of the core of the microcompartment. In this article we bring together the properties of the wrappers of the propanediol utilization bacterial microcompartments to update our understanding on the mechanism of the formation of these unique wraps, their assembly, and interaction with the encapsulated enzymes.


Bacterial microcompartments BMC domain fold Shell proteins Propanediol utilization 


  1. Aussignargues C, Paasch BC, Gonzalez-Esquer R, Erbilgin O, Kerfeld CA (2015) Bacterial microcompartment assembly: the key role of encapsulation peptides. Commun Integr Biol 8:e1039755CrossRefGoogle Scholar
  2. Axen SD, Erbilgin O, Kerfeld CA (2014) A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Comput Biol 10:e1003898CrossRefGoogle Scholar
  3. Badía J, Ros J, Aguilar J (1985) Fermentation mechanism of fucose and rhamnose in Salmonella typhimurium and Klebsiella pneumoniae. J Bacteriol 161:435–437PubMedPubMedCentralGoogle Scholar
  4. Baldoma L, Aguilar J (1988) Metabolism of L-fucose and L-rhamnose in Escherichia coli: aerobic-anaerobic regulation of L-lactaldehyde dissimilation. J Bacteriol 170:416–421CrossRefGoogle Scholar
  5. Beeby M, Bobik TA, Yeates TO (2009) Exploiting genomic patterns to discover new supramolecular protein assemblies. Protein Sci 18:69–79. CrossRefPubMedGoogle Scholar
  6. Bobik TA (2006) Polyhedral organelles compartmenting bacterial metabolic processes. Appl Microbiol Biotechnol 70:517–525. CrossRefPubMedGoogle Scholar
  7. Cai F, Menon BB, Cannon GC, Curry KJ, Shively JM, Heinhorst S (2009) The pentameric vertex proteins are necessary for the icosahedral carboxysome shell to function as a CO2 leakage barrier. PLoS One 4:e7521CrossRefGoogle Scholar
  8. Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM (2001) Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 67:5351–5361CrossRefGoogle Scholar
  9. Chen P, Andersson DI, Roth JR (1994) The control region of the pdu/cob regulon in Salmonella typhimurium. J Bacteriol 176:5474–5482CrossRefGoogle Scholar
  10. Chen AH, Robinson-Mosher A, Savage DF, Silver PA, Polka JK (2013) The bacterial carbon-fixing organelle is formed by shell envelopment of preassembled cargo. PLoS One 8:e76127CrossRefGoogle Scholar
  11. Cheng S, Liu Y, Crowley CS, Yeates TO, Bobik TA (2008) Bacterial microcompartments: their properties and paradoxes. BioEssays 30:1084–1095CrossRefGoogle Scholar
  12. Cheng S, Sinha S, Fan C, Liu Y, Bobik TA (2011) Genetic analysis of the protein shell of the microcompartments involved in coenzyme B12-dependent 1,2-propanediol degradation by Salmonella. J Bacteriol 193:1385–1392CrossRefGoogle Scholar
  13. Chowdhury C, Sinha S, Chun S, Yeates TO, Bobik TA (2014) Diverse bacterial microcompartment organelles. Microbiol Mol Biol Rev 78:438–468CrossRefGoogle Scholar
  14. Chowdhury C, Chun S, Pang A, Sawaya MR, Sinha S, Yeates TO, Bobik TA (2015) Selective molecular transport through the protein shell of a bacterial microcompartment organelle. Proc Natl Acad Sci U S A 112:2990–2995. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chowdhury C, Chun S, Sawaya MR, Yeates TO, Bobik TA (2016) The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene. Mol Microbiol 101:770–783. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Crowley CS, Sawaya MR, Bobik TA, Yeates TO (2008) Structure of the PduU shell protein from the Pdu microcompartment of Salmonella. Structure 16:1324–1332CrossRefGoogle Scholar
  17. Crowley CS, Cascio D, Sawaya MR, Kopstein JS, Bobik TA, Yeates TO (2010) Structural insight into the mechanisms of transport across the Salmonella enterica Pdu microcompartment shell. J Biol Chem 285:37838–37846CrossRefGoogle Scholar
  18. Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC (2008) CO2 fixation kinetics of Halothiobacillus neapolitanus mutant carboxysomes lacking carbonic anhydrase suggest the shell acts as a diffusional barrier for CO2. J Biol Chem 283:10377–10384. CrossRefPubMedGoogle Scholar
  19. Fan C, Bobik TA (2011) The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. J Bacteriol 193:5623–5628CrossRefGoogle Scholar
  20. Fan C et al (2010) Short N-terminal sequences package proteins into bacterial microcompartments. Proc Natl Acad Sci 107:7509–7514CrossRefGoogle Scholar
  21. Fan C, Cheng S, Sinha S, Bobik TA (2012) Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments. Proc Natl Acad Sci 109:14995–15000CrossRefGoogle Scholar
  22. Farah Abdul-Rahman EP, Jeffrey LB (2013) The distribution of polyhedral bacterial microcompartments suggests frequent horizontal transfer and operon reassembly. J Phylogenet Evol Biol 1:1–7. CrossRefGoogle Scholar
  23. Faulkner M et al (2017) Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale 9:10662–10673. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Drews G, Niklowitz W (1956) Beiträge zur Cytologie der Blaualgen. II. Zentroplasma und granulare Einschlüsse von Phormidium uncinatum. Arch Mikrobiol 24(2):147–162CrossRefGoogle Scholar
  25. Havemann GD, Bobik TA (2003) Protein content of polyhedral organelles involved in coenzyme B12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar typhimurium LT2. J Bacteriol 185:5086–5095CrossRefGoogle Scholar
  26. Havemann GD, Sampson EM, Bobik TA (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. J Bacteriol 184:1253–1261CrossRefGoogle Scholar
  27. Jorda J, Lopez D, Wheatley NM, Yeates TO (2013) Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria. Protein Sci 22:179–195. CrossRefPubMedGoogle Scholar
  28. Jorda J, Liu Y, Bobik TA, Yeates TO (2015) Exploring bacterial organelle interactomes: a model of the protein-protein interaction network in the Pdu microcompartment. PLoS Comput Biol 11:e1004067CrossRefGoogle Scholar
  29. Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO (2005) Protein structures forming the shell of primitive bacterial organelles. Science 309:936–938. CrossRefPubMedGoogle Scholar
  30. Kerfeld CA, Heinhorst S, Cannon GC (2010) Annu Rev Microbiol 64:391–408. CrossRefPubMedGoogle Scholar
  31. Klein MG et al (2009) Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport. J Mol Biol 392:319–333. CrossRefPubMedGoogle Scholar
  32. Lehman BP, Chowdhury C, Bobik TA (2017) The N terminus of the PduB protein binds the protein shell of the Pdu microcompartment to its enzymatic core. J Bacteriol 199:e00785–e00716CrossRefGoogle Scholar
  33. Pang A, Warren MJ, Pickersgill RW (2011) Structure of PduT, a trimeric bacterial microcompartment protein with a 4Fe–4S cluster-binding site. Acta Crystallogr D Biol Crystallogr 67:91–96CrossRefGoogle Scholar
  34. Pang A, Liang M, Prentice MB, Pickersgill RW (2012) Substrate channels revealed in the trimeric lactobacillus reuteri bacterial microcompartment shell protein PduB. Acta Crystallogr D Biol Crystallogr 68:1642–1652. CrossRefPubMedGoogle Scholar
  35. Pang A, Frank S, Brown I, Warren MJ, Pickersgill RW (2014) Structural insights into higher order assembly and function of the bacterial microcompartment protein PduA. J Biol Chem 289:22377–22384. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Park J, Chun S, Bobik TA, Houk KN, Yeates TO (2017) Molecular dynamics simulations of selective metabolite transport across the propanediol bacterial microcompartment shell. J Phys Chem B 121:8149–8154. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Penrod JT, Roth JR (2006) Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J Bacteriol 188:2865–2874. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Price GD, Badger MR (1989) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO(2)-requiring phenotype : evidence for a central role for Carboxysomes in the CO(2) concentrating mechanism. Plant Physiol 91:505–513CrossRefGoogle Scholar
  39. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461. CrossRefPubMedGoogle Scholar
  40. Rae BD, Long BM, Badger MR, Price GD (2013) Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77:357–379CrossRefGoogle Scholar
  41. Rondon MR, Horswill AR, Escalante-Semerena JC (1995) DNA polymerase I function is required for the utilization of ethanolamine, 1,2-propanediol, and propionate by Salmonella typhimurium LT2. J Bacteriol 177:7119–7124CrossRefGoogle Scholar
  42. Sagermann M, Ohtaki A, Nikolakakis K (2009) Crystal structure of the EutL shell protein of the ethanolamine ammonia lyase microcompartment. Proc Natl Acad Sci U S A 106:8883–8887CrossRefGoogle Scholar
  43. Shively JM, Ball F, Brown DH, Saunders RE (1973a) Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182:584–586CrossRefGoogle Scholar
  44. Shively JM, Ball FL, Kline BW (1973b) Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neapolitanus. J Bacteriol 116:1405–1411PubMedPubMedCentralGoogle Scholar
  45. Sinha S, Cheng S, Fan C, Bobik TA (2012) The PduM protein is a structural component of the microcompartments involved in coenzyme B(12)-dependent 1,2-propanediol degradation by Salmonella enterica. J Bacteriol 194:1912–1918CrossRefGoogle Scholar
  46. Sinha S, Cheng S, Sung YW, McNamara DE, Sawaya MR, Yeates TO, Bobik TA (2014) Alanine scanning mutagenesis identifies an asparagine–arginine–lysine triad essential to assembly of the shell of the Pdu microcompartment. J Mol Biol 426:2328–2345CrossRefGoogle Scholar
  47. Sutter M, Greber B, Aussignargues C, Kerfeld CA (2017) Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell. Science 356:1293–1297. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Takenoya M, Nikolakakis K, Sagermann M (2010) Crystallographic insights into the pore structures and mechanisms of the EutL and EutM shell proteins of the ethanolamine-utilizing microcompartment of Escherichia coli. J Bacteriol 192:6056–6063CrossRefGoogle Scholar
  49. Tanaka S, Sawaya MR, Phillips M, Yeates TO (2009) Insights from multiple structures of the shell proteins from the beta-carboxysome. Protein Sci 18:108–120PubMedGoogle Scholar
  50. Tanaka S, Sawaya MR, Yeates TO (2010) Structure and mechanisms of a protein-based organelle in. E coli Sci 327:81–84. CrossRefGoogle Scholar
  51. Thiennimitr P et al (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108:17480–17485CrossRefGoogle Scholar
  52. Wheatley NM, Gidaniyan SD, Liu Y, Cascio D, Yeates TO (2013) Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins. Protein Sci 22:660–665CrossRefGoogle Scholar
  53. Winter SE, Baumler AJ (2011) A breathtaking feat: to compete with the gut microbiota, Salmonella drives its host to provide a respiratory electron acceptor. Gut Microbes 2:58–60CrossRefGoogle Scholar
  54. Winter SE et al (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–429CrossRefGoogle Scholar
  55. Yeates TO, Thompson MC, Bobik TA (2011) The protein shells of bacterial microcompartment organelles. Curr Opin Struct Biol 21:223–231. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yeates TO, Jorda J, Bobik TA (2013) The shells of BMC-type microcompartment organelles in bacteria. J Mol Microbiol Biotechnol 23:290–299. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Naimat K. Bari
    • 1
  • Gaurav Kumar
    • 1
  • Sharmistha Sinha
    • 1
    Email author
  1. 1.Institute of Nano Science and TechnologyMohaliIndia

Personalised recommendations