Sunday, November 24, 2024

Characterization of a widespread sugar phosphate-processing bacterial microcompartment

BiochemistryCharacterization of a widespread sugar phosphate-processing bacterial microcompartment


  • Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F. & Sutter, M. Bacterial microcompartments. Nat. Rev. Microbiol. 16, 277–290 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sutter, M., Melnicki, M. R., Schulz, F., Woyke, T. & Kerfeld, C. A. A catalog of the diversity and ubiquity of bacterial microcompartments. Nat. Commun. 12, 3809 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chowdhury, C., Sinha, S., Chun, S., Yeates, T. O. & Bobik, T. A. Diverse bacterial microcompartment organelles. Microbiol. Mol. Biol. Rev. 78, 438–468 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rae, B. D., Long, B. M., Badger, M. R. & Price, G. D. 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 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jakobson, C. M., Tullman-Ercek, D., Slininger, M. F. & Mangan, N. M. A systems-level model reveals that 1,2-Propanediol utilization microcompartments enhance pathway flux through intermediate sequestration. PLoS Comput. Biol. 13, e1005525 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kerfeld, C. A. et al. Protein structures forming the shell of primitive bacterial organelles. Science 309, 936–938 (2005).

    Article 
    PubMed 

    Google Scholar 

  • Klein, M. G. et al. Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport. J. Mol. Biol. 392, 319–333 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Sutter, M., Greber, B., Aussignargues, C. & Kerfeld, C. A. Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell. Science 356, 1293–1297 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Greber, B. J., Sutter, M. & Kerfeld, C. A. The plasticity of molecular interactions governs bacterial microcompartment shell assembly. Structure 27, 749–763.e4 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tanaka, S. et al. Atomic-level models of the bacterial carboxysome shell. Science 319, 1083–1086 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Cannon, G. C. & Shively, J. M. Characterization of a homogenous preparation of carboxysomes from Thiobacillus neapolitanus. Arch. Microbiol. 134, 52–59 (1983).

    Article 

    Google Scholar 

  • Shively, J. M., Ball, F., Brown, D. H. & Saunders, R. E. Functional organelles in prokaryotes: polyhedral inclusions (Carboxysomes) of Thiobacillus neapolitanus. Science 182, 584–586 (1973).

    Article 
    PubMed 

    Google Scholar 

  • Jorda, J., Lopez, D., Wheatley, N. M. & Yeates, T. O. Using comparative genomics to uncover new kinds of protein‐based metabolic organelles in bacteria. Protein Sci. 22, 179–195 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Axen, S. D., Erbilgin, O. & Kerfeld, C. A. A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Comput. Biol. 10, e1003898 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kerfeld, C. A. & Erbilgin, O. Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol. 23, 22–34 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Erbilgin, O., Sutter, M. & Kerfeld, C. A. The structural basis of coenzyme a recycling in a bacterial organelle. PLoS Biol. 14, e1002399 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Penrod, J. T. & Roth, J. R. Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J. Bacteriol. 188, 2865–2874 (2006).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Havemann, G. D., Sampson, E. M. & Bobik, T. A. PduA is a shell protein of polyhedral organelles involved in coenzyme B12 -dependent degradation of 1,2-propanediol in Salmonella enterica Serovar Typhimurium LT2. J. Bacteriol. 184, 1253–1261 (2002).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rondon, M. R., Horswill, A. R. & Escalante-Semerena, J. C. 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 (1995).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sampson, E. M. & Bobik, T. A. Microcompartments for B 12 -dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J. Bacteriol. 190, 2966–2971 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fan, C. et al. Short N-terminal sequences package proteins into bacterial microcompartments. Proc. Natl. Acad. Sci. USA 107, 7509–7514 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fan, C. & Bobik, T. A. The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. J. Bacteriol. 193, 5623–5628 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kinney, J. N., Salmeen, A., Cai, F. & Kerfeld, C. A. Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J. Biol. Chem. 287, 17729–17736 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Aussignargues, C., Paasch, B. C., Gonzalez-Esquer, R., Erbilgin, O. & Kerfeld, C. A. Bacterial microcompartment assembly: the key role of encapsulation peptides. Commun. Integr. Biol. 8, e1039755 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Liu, Y. et al. PduL is an evolutionarily distinct phosphotransacylase involved in B12 -dependent 1,2-propanediol degradation by Salmonella enterica Serovar Typhimurium LT2. J. Bacteriol. 189, 1589–1596 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Gu, S., Bradley-Clarke, J., Rose, R.-S., Warren, M. J. & Pickersgill, R. W. Enzyme-cargo encapsulation peptides bind between tessellating tiles of the bacterial microcompartment shell. J. Biol. Chem. 300, 107357 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sutter, M. & Kerfeld, C. A. BMC Caller: a webtool to identify and analyze bacterial microcompartment types in sequence data. Biol. Direct 17, 9 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen, I.-M. A. et al. The IMG/M data management and analysis system v.7: content updates and new features. Nucleic Acids Res. 51, D723–D732 (2023).

    Article 
    PubMed 

    Google Scholar 

  • Nielsen, K. M., Johnsen, P. J., Bensasson, D. & Daffonchio, D. Release and persistence of extracellular DNA in the environment. Environ. Biosaf. Res. 6, 37–53 (2007).

    Article 

    Google Scholar 

  • Levy-Booth, D. J. et al. Cycling of extracellular DNA in the soil environment. Soil Biol. Biochem. 39, 2977–2991 (2007).

    Article 

    Google Scholar 

  • Lomax, M. S. & Greenberg, G. R. Characteristics of the deo operon: role in thymine utilization and sensitivity to deoxyribonucleosides. J. Bacteriol. 96, 501–514 (1968).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jørgensen, P., Collins, J. & Valentin-Hansen, P. On the structure of the deo operon of Escherichia coli. Mol. Gen. Genet. 155, 93–102 (1977).

    Article 
    PubMed 

    Google Scholar 

  • Melnicki, M. R., Sutter, M. & Kerfeld, C. A. Evolutionary relationships among shell proteins of carboxysomes and metabolosomes. Curr. Opin. Microbiol. 63, 1–9 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sutter, M. et al. Electrochemical cofactor recycling of bacterial microcompartments. Proc. Natl. Acad. Sci. USA https://doi.org/10.1073/pnas.2414220121 (2024).

  • Fillenberg, S. B., Grau, F. C., Seidel, G. & Muller, Y. A. Structural insight into operator dre-sites recognition and effector binding in the GntR/HutC transcription regulator NagR. Nucleic Acids Res. 43, 1283–1296 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Matilla, M. A., Velando, F., Martín-Mora, D., Monteagudo-Cascales, E. & Krell, T. A catalogue of signal molecules that interact with sensor kinases, chemoreceptors and transcriptional regulators. FEMS Microbiol. Rev. 46, fuab043 (2022).

    Article 
    PubMed 

    Google Scholar 

  • Heine, A., Luz, J. G., Wong, C.-H. & Wilson, I. A. Analysis of the class I aldolase binding site architecture based on the crystal structure of 2-deoxyribose-5-phosphate aldolase at 0.99 Å resolution. J. Mol. Biol. 343, 1019–1034 (2004).

    Article 
    PubMed 

    Google Scholar 

  • Zhang, R.-G. et al. The 2.2Å resolution structure of RpiB/AlsB from Escherichia coli illustrates a new approach to the ribose-5-phosphate isomerase reaction. J. Mol. Biol. 332, 1083–1094 (2003).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Valentin‐Hansen, P., Boëtius, F., Hammer‐Jespersen, K. & Svendsen, I. The primary structure of Escherichia coli K12 2‐deoxyribose 5‐phosphate aldolase: nucleotide sequence of the deoC gene and the amino acid sequence of the enzyme. Eur. J. Biochem. 125, 561–566 (1982).

    Article 
    PubMed 

    Google Scholar 

  • Sarkar, D. et al. Atomic view of photosynthetic metabolite permeability pathways and confinement in synthetic carboxysome shells. Proc. Natl. Acad. Sci. USA 121, e2402277121 (2024).

  • Cai, F. et al. The structure of CcmP, a tandem bacterial microcompartment domain protein from the β-carboxysome, forms a subcompartment within a microcompartment. J. Biol. Chem. 288, 16055–16063 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Larsson, A. M., Hasse, D., Valegård, K. & Andersson, I. Crystal structures of β-carboxysome shell protein CcmP: ligand binding correlates with the closed or open central pore. J. Exp. Bot. 68, 3857–3867 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, R. et al. Structure of Escherichia coli ribose-5-phosphate isomerase. Structure 11, 31–42 (2003).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen, J., Wu, H., Zhang, W. & Mu, W. Ribose-5-phosphate isomerases: characteristics, structural features, and applications. Appl Microbiol. Biotechnol. 104, 6429–6441 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Roos, A. K. et al. Mycobacterium tuberculosis Ribose-5-phosphate Isomerase has a known fold, but a novel active site. J. Mol. Biol. 335, 799–809 (2004).

    Article 
    PubMed 

    Google Scholar 

  • Stern, A. L., Naworyta, A., Cazzulo, J. J. & Mowbray, S. L. Structures of type B ribose 5‐phosphate isomerase from Trypanosoma cruzi shed light on the determinants of sugar specificity in the structural family. FEBS J. 278, 793–808 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Sharkey, T. D. Pentose phosphate pathway reactions in photosynthesizing cells. Cells 10, 1547 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Petit, E. et al. Involvement of a bacterial microcompartment in the metabolism of fucose and rhamnose by Clostridium phytofermentans. PLoS ONE 8, e54337 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zarzycki, J., Erbilgin, O. & Kerfeld, C. A. Bioinformatic characterization of glycyl radical enzyme-associated bacterial microcompartments. Appl. Environ. Microbiol. 81, 8315–8329 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cameron, J. C., Wilson, S. C., Bernstein, S. L. & Kerfeld, C. A. Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155, 1131–1140 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Cot, S. S.-W., So, A. K.-C. & Espie, G. S. A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria. J. Bacteriol. 190, 936–945 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Borden, J. S. & Savage, D. F. New discoveries expand possibilities for carboxysome engineering. Curr. Opin. Microbiol. 61, 58–66 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, T. et al. Reprogramming bacterial protein organelles as a nanoreactor for hydrogen production. Nat. Commun. 11, 5448 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jiang, Q. et al. Synthetic engineering of a new biocatalyst encapsulating [NiFe]-hydrogenases for enhanced hydrogen production. J. Mater. Chem. B 11, 2684–2692 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kirst, H. et al. Toward a glycyl radical enzyme containing synthetic bacterial microcompartment to produce pyruvate from formate and acetate. Proc. Natl. Acad. Sci. USA 119, e2116871119 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lawrence, A. D. et al. Solution structure of a bacterial microcompartment targeting peptide and its application in the construction of an ethanol bioreactor. ACS Synth. Biol. 3, 454–465 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Doron, L., Sutter, M. & Kerfeld, C. A. Characterization of a novel aromatic substrate-processing microcompartment in Actinobacteria. mBio 14, e01216-23 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Raba, D. A. & Kerfeld, C. A. The potential of bacterial microcompartment architectures for phytonanotechnology. Environ. Microbiol. Rep. 14, 700–710 (2022).

    Article 
    PubMed 

    Google Scholar 

  • Dwyer, M. E. et al. Towards chloroplastic nanofactories: formation of proteinaceous scaffolds for metabolic engineering. Plant Biotechnol. J. https://doi.org/10.1111/pbi.14462 (2024).

  • Aussignargues, C. et al. Structure and function of a bacterial microcompartment shell protein engineered to bind a [4Fe-4S] cluster. J. Am. Chem. Soc. 138, 5262–5270 (2016).

  • Hagen, A., Sutter, M., Sloan, N. & Kerfeld, C. A. Programmed loading and rapid purification of engineered bacterial microcompartment shells. Nat. Commun. 9, 2881 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hagen, A. R. et al. In vitro assembly of diverse bacterial microcompartment shell architectures. Nano Lett. 18, 7030–7037 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Plegaria, J. S. & Kerfeld, C. A. Engineering nanoreactors using bacterial microcompartment architectures. Curr. Opin. Biotechnol. 51, 1–7 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Ferlez, B., Sutter, M. & Kerfeld, C. A. A designed bacterial microcompartment shell with tunable composition and precision cargo loading. Metab. Eng. 54, 286–291 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Plegaria, J. S., Yates, M. D., Glaven, S. M. & Kerfeld, C. A. Redox characterization of electrode-immobilized bacterial microcompartment shell proteins engineered to bind metal centers. ACS Appl. Bio Mater. 3, 685–692 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Doron, L. & Kerfeld, C. A. Bacterial microcompartments as a next-generation metabolic engineering tool: utilizing nature’s solution for confining challenging catabolic pathways. Biochem. Soc. Trans. 52, 997–1010 (2024).

  • Li, T. et al. Nanoengineering carboxysome shells for protein cages with programmable cargo targeting. ACS Nano 18, 7473–7484 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lee, M. J., Palmer, D. J. & Warren, M. J. Biotechnological advances in bacterial microcompartment technology. Trends Biotechnol. 37, 325–336 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Stewart, A. M., Stewart, K. L., Yeates, T. O. & Bobik, T. A. Advances in the world of bacterial microcompartments. Trends Biochem. Sci. 46, 406–416 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Frank, S., Lawrence, A. D., Prentice, M. B. & Warren, M. J. Bacterial microcompartments moving into a synthetic biological world. J. Biotechnol. 163, 273–279 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Young, E. J. et al. Engineering the bacterial microcompartment domain for molecular scaffolding applications. Front. Microbiol. 8, 1441 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Planamente, S. & Frank, S. Bio-engineering of bacterial microcompartments: a mini review. Biochem. Soc. Trans. 47, 765–777 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Prentice, M. B. Bacterial microcompartments and their role in pathogenicity. Curr. Opin. Microbiol. 63, 19–28 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Jakobson, C. M. & Tullman-Ercek, D. Dumpster diving in the gut: bacterial microcompartments as part of a host-associated lifestyle. PLoS Pathog. 12, e1005558 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Haridas, M., Abdelraheem, E. M. M. & Hanefeld, U. 2-Deoxy-d-ribose-5-phosphate aldolase (DERA): applications and modifications. Appl Microbiol. Biotechnol. 102, 9959–9971 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Voutilainen, S. et al. Substrate specificity of 2-deoxy-D-ribose 5-phosphate aldolase (DERA) assessed by different protein engineering and machine learning methods. Appl. Microbiol. Biotechnol. 104, 10515–10529 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Liu, J. & Wong, C.-H. Aldolase-catalyzed asymmetric synthesis of novel pyranose synthons as a new entry to heterocycles and epothilones. Angew. Chem. Int. Ed. 41, 1404–1407 (2002).

    Article 

    Google Scholar 

  • Gijsen, H. J. M. & Wong, C.-H. Unprecedented asymmetric aldol reactions with three aldehyde substrates catalyzed by 2-deoxyribose-5-phosphate aldolase. J. Am. Chem. Soc. 116, 8422–8423 (1994).

    Article 

    Google Scholar 

  • Kim, T. et al. Rational engineering of 2-deoxyribose-5-phosphate aldolases for the biosynthesis of (R)-1,3-butanediol. J. Biol. Chem. 295, 597–609 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Chambre, D. et al. 2-Deoxyribose-5-phosphate aldolase, a remarkably tolerant aldolase towards nucleophile substrates. Chem. Commun. 55, 7498–7501 (2019).

    Article 

    Google Scholar 

  • Sakuraba, H. et al. Sequential aldol condensation catalyzed by hyperthermophilic 2-deoxy- d -ribose-5-phosphate aldolase. Appl. Environ. Microbiol. 73, 7427–7434 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wood, T. Spectrophotometric assay for d-ribose-5-phosphate ketol-isomerase and for d-ribulose-5-phosphate 3-epimerase. Anal. Biochem. 33, 297–306 (1970).

    Article 
    PubMed 

    Google Scholar 

  • Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858 (1996).

    Article 
    PubMed 

    Google Scholar 

  • Perkins, D. N., Pappin, D. J. C., Creasy, D. M. & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551–3567 (1999).

    Article 
    PubMed 

    Google Scholar 

  • Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Crooks, G. E., Hon, G., Chandonia, J.-M. & Brenner, S. E. WebLogo: a sequence logo generator: figure 1. Genome Res. 14, 1188–1190 (2004).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tamura, K., Stecher, G. & Kumar, S. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320–W324 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article 
    PubMed 

    Google Scholar 

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