Abstract
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.
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References
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:e1039755
Axen SD, Erbilgin O, Kerfeld CA (2014) A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Comput Biol 10:e1003898
BadÃa J, Ros J, Aguilar J (1985) Fermentation mechanism of fucose and rhamnose in Salmonella typhimurium and Klebsiella pneumoniae. J Bacteriol 161:435–437
Baldoma L, Aguilar J (1988) Metabolism of L-fucose and L-rhamnose in Escherichia coli: aerobic-anaerobic regulation of L-lactaldehyde dissimilation. J Bacteriol 170:416–421
Beeby M, Bobik TA, Yeates TO (2009) Exploiting genomic patterns to discover new supramolecular protein assemblies. Protein Sci 18:69–79. https://doi.org/10.1002/pro.1
Bobik TA (2006) Polyhedral organelles compartmenting bacterial metabolic processes. Appl Microbiol Biotechnol 70:517–525. https://doi.org/10.1007/s00253-005-0295-0
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:e7521
Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM (2001) Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 67:5351–5361
Chen P, Andersson DI, Roth JR (1994) The control region of the pdu/cob regulon in Salmonella typhimurium. J Bacteriol 176:5474–5482
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:e76127
Cheng S, Liu Y, Crowley CS, Yeates TO, Bobik TA (2008) Bacterial microcompartments: their properties and paradoxes. BioEssays 30:1084–1095
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 193:1385–1392
Chowdhury C, Sinha S, Chun S, Yeates TO, Bobik TA (2014) Diverse bacterial microcompartment organelles. Microbiol Mol Biol Rev 78:438–468
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. https://doi.org/10.1111/mmi.13423
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. https://doi.org/10.1128/jb.00785-16
Crowley CS, Sawaya MR, Bobik TA, Yeates TO (2008) Structure of the PduU shell protein from the Pdu microcompartment of Salmonella. Structure 16:1324–1332
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 285:37838–37846
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. https://doi.org/10.1074/jbc.M709285200
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 193:5623–5628
Fan C et al (2010) Short N-terminal sequences package proteins into bacterial microcompartments. Proc Natl Acad Sci 107:7509–7514
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 109:14995–15000
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. https://doi.org/10.4172/2329-9002.1000118
Faulkner M et al (2017) Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale 9:10662–10673. https://doi.org/10.1039/c7nr02524f
Drews G, Niklowitz W (1956) Beiträge zur Cytologie der Blaualgen. II. Zentroplasma und granulare Einschlüsse von Phormidium uncinatum. Arch Mikrobiol 24(2):147–162
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 185:5086–5095
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 184:1253–1261
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. https://doi.org/10.1002/pro.2196
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:e1004067
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. https://doi.org/10.1126/science.1113397
Kerfeld CA, Heinhorst S, Cannon GC (2010) Annu Rev Microbiol 64:391–408. https://doi.org/10.1146/annurev.micro.112408.134211
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. https://doi.org/10.1016/j.jmb.2009.03.056
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–e00716
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 67:91–96
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. https://doi.org/10.1107/s0907444912039315
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. https://doi.org/10.1074/jbc.M114.569285
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. https://doi.org/10.1021/acs.jpcb.7b07232
Penrod JT, Roth JR (2006) Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J Bacteriol 188:2865–2874. https://doi.org/10.1128/JB.188.8.2865-2874.2006
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 91:505–513
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. https://doi.org/10.1093/jxb/erm112
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 77:357–379
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 177:7119–7124
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 106:8883–8887
Shively JM, Ball F, Brown DH, Saunders RE (1973a) Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182:584–586
Shively JM, Ball FL, Kline BW (1973b) Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neapolitanus. J Bacteriol 116:1405–1411
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 194:1912–1918
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 426:2328–2345
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. https://doi.org/10.1126/science.aan3289
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 192:6056–6063
Tanaka S, Sawaya MR, Phillips M, Yeates TO (2009) Insights from multiple structures of the shell proteins from the beta-carboxysome. Protein Sci 18:108–120
Tanaka S, Sawaya MR, Yeates TO (2010) Structure and mechanisms of a protein-based organelle in. E coli Sci 327:81–84. https://doi.org/10.1126/science.1179513
Thiennimitr P et al (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108:17480–17485
Wheatley NM, Gidaniyan SD, Liu Y, Cascio D, Yeates TO (2013) Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins. Protein Sci 22:660–665
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 2:58–60
Winter SE et al (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–429
Yeates TO, Thompson MC, Bobik TA (2011) The protein shells of bacterial microcompartment organelles. Curr Opin Struct Biol 21:223–231. https://doi.org/10.1016/j.sbi.2011.01.006
Yeates TO, Jorda J, Bobik TA (2013) The shells of BMC-type microcompartment organelles in bacteria. J Mol Microbiol Biotechnol 23:290–299. https://doi.org/10.1159/000351347
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Bari, N.K., Kumar, G., Sinha, S. (2018). The Wrappers of the 1,2-Propanediol Utilization Bacterial Microcompartments. In: Chattopadhyay, K., Basu, S. (eds) Biochemical and Biophysical Roles of Cell Surface Molecules. Advances in Experimental Medicine and Biology, vol 1112. Springer, Singapore. https://doi.org/10.1007/978-981-13-3065-0_23
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