CoChat
Sign Up
Cited by 45Bacterial Genetics and BiotechnologyMicrobial Metabolic Engineering and BioproductionMicrobial metabolism and enzyme function

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Biogenesis of a bacterial metabolosome for propanediol utilization

Open access
Yang, Mengru, Wenner, Nicolas, Dykes, Gregory F., Li, Yan, Zhu, Xiaojun, Sun, Yaqi, Huang, Fang, Hinton, Jay C. D., Liu, Lu-Ning·2022·Nature Communications
DOI 10.1038/s41467-022-30608-wPMC PMC9132943

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Bacterial metabolosomes are a family of protein organelles in bacteria. Elucidating how thousands of proteins self-assemble to form functional metabolosomes is essential for understanding their significance in cellular metabolism and pathogenesis. Here we investigate the de novo biogenesis of propanediol-utilization (Pdu) metabolosomes and characterize the roles of the key constituents in generation and intracellular positioning of functional metabolosomes. Our results demonstrate that the Pdu metabolosome undertakes both “Shell first” and “Cargo first” assembly pathways, unlike the β-carboxysome structural analog which only involves the “Cargo first” strategy. Shell and cargo assemblies occur independently at the cell poles. The internal cargo core is formed through the ordered assembly of multiple enzyme complexes, and exhibits liquid-like properties within the metabolosome architecture. Our findings provide mechanistic insight into the molecular principles driving bacterial metabolosome assembly and expand our understanding of liquid-like organelle biogenesis.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-022-30608-w

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 118

  1. Chen, A. H. & Silver, P. A. Designing biological compartmentalization. Trends Cell Biol. 22, 662–670 (2012). · DOI
  2. Yeates, T. O., Jorda, J. & Bobik, T. A. The shells of BMC-type microcompartment organelles in bacteria. J. Mol. Microbiol. Biotechnol. 23, 290–299 (2013).
  3. Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F. & Sutter, M. Bacterial microcompartments. Nat. Rev. Microbiol. 16, 277–290 (2018). · DOI
  4. Liu, L. N., Yang, M., Sun, Y. & Yang, J. Protein stoichiometry, structural plasticity and regulation of bacterial microcompartments. Curr. Opin. Microbiol. 63, 133–141 (2021). · DOI
  5. Kerfeld, C. A. et al. Protein structures forming the shell of primitive bacterial organelles. Science 309, 936–938 (2005). · DOI
  6. Chowdhury, C. et al. Selective molecular transport through the protein shell of a bacterial microcompartment organelle. Proc. Natl Acad. Sci. USA 112, 2990–2995 (2015). · DOI
  7. Crowley, C. S., Sawaya, M. R., Bobik, T. A. & Yeates, T. O. Structure of the PduU shell protein from the Pdu microcompartment of Salmonella. Structure 16, 1324–1332 (2008). · DOI
  8. Faulkner, M. et al. Molecular simulations unravel the molecular principles that mediate selective permeability of carboxysome shell protein. Sci. Rep. 10, 17501 (2020). · DOI
  9. 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). · DOI
  10. Chowdhury, C., Sinha, S., Chun, S., Yeates, T. O. & Bobik, T. A. Diverse bacterial microcompartment organelles. Microbiol. Mol. Biol. Rev. 78, 438–468 (2014). · DOI
  11. Hennacy, J. H. & Jonikas, M. C. Prospects for engineering biophysical CO2 concentrating mechanisms into land plants to enhance yields. Annu. Rev. Plant Biol. 71, 461–485 (2020). · DOI
  12. Rae, B. D. et al. Progress and challenges of engineering a biophysical CO2-concentrating mechanism into higher plants. J. Exp. Bot. 68, 3717–3737 (2017). · DOI
  13. Liu, L. N. Advances in the bacterial organelles for CO2 fixation. Trends Microbiol. 30, 567–580 (2022). · DOI
  14. Sun, Y. et al. Decoding the absolute stoichiometric composition and structural plasticity of α-carboxysomes. mBio. 13, e0362921 (2022). · DOI
  15. Taylor, S. J. & Winter, S. E. Salmonella finds a way: metabolic versatility of Salmonella enterica serovar Typhimurium in diverse host environments. PLoS Pathog. 16, e1008540 (2020). · DOI
  16. Bobik, T. A., Havemann, G. D., Busch, R. J., Williams, D. S. & Aldrich, H. C. The propanediol utilization (pdu) operon of Salmonella enterica serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B12-dependent 1, 2-propanediol degradation. J. Bacteriol. 181, 5967–5975 (1999). · DOI
  17. 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). · DOI
  18. Lee, M. J., Palmer, D. J. & Warren, M. J. Biotechnological advances in bacterial microcompartment technology. Trends Biotechnol. 37, 325–336 (2019). · DOI
  19. Liu, L. N. Bacterial metabolosomes: new insights into their structure and bioengineering. Microb. Biotechnol. 14, 88–93 (2021). · DOI
  20. Faber, F. et al. Respiration of microbiota-derived 1,2-propanediol drives Salmonella expansion during colitis. PLoS Pathog. 13, e1006129 (2017). · DOI
  21. Price-Carter, M., Tingey, J., Bobik, T. A. & Roth, J. R. The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar Typhimurium on ethanolamine or 1, 2-propanediol. J. Bacteriol. 183, 2463–2475 (2001). · DOI
  22. Jeter, R. M. Cobalamin-dependent 1, 2-propanediol utilization by Salmonella typhimurium. Microbiology 136, 887–896 (1990).
  23. Cheng, S., Liu, Y., Crowley, C. S., Yeates, T. O. & Bobik, T. A. Bacterial microcompartments: their properties and paradoxes. Bioessays 30, 1084–1095 (2008). · DOI
  24. Yang, M. et al. Decoding the stoichiometric composition and organisation of bacterial metabolosomes. Nat. Commun. 11, 1–11 (2020). · DOI · Paper page
  25. Stewart, K. L., Stewart, A. M. & Bobik, T. A. Prokaryotic organelles: bacterial microcompartments in E. coli and Salmonella. EcoSal Plus https://doi.org/10.1128/ecosalplus.ESP-0025-2019 (2020). · DOI
  26. Sutter, M. et al. Visualization of bacterial microcompartment facet assembly using high-speed atomic force microscopy. Nano Lett. 16, 1590–1595 (2016). · DOI
  27. Cheng, S., Sinha, S., Fan, C., Liu, Y. & Bobik, T. A. 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 (2011). · DOI · Paper page
  28. Sinha, S., Cheng, S., Fan, C. & Bobik, T. A. The PduM protein is a structural component of the microcompartments involved in coenzyme B12-dependent 1, 2-propanediol degradation by Salmonella enterica. J. Bacteriol. 194, 1912–1918 (2012). · DOI
  29. Havemann, G. D. & Bobik, T. A. 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 (2003). · DOI
  30. Wheatley, N. M., Gidaniyan, S. D., Liu, Y., Cascio, D. & Yeates, T. O. Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins. Protein Sci. 22, 660–665 (2013). · DOI
  31. Kennedy, N. W., Ikonomova, S. P., Slininger Lee, M., Raeder, H. W. & Tullman-Ercek, D. Self-assembling shell proteins PduA and PduJ have essential and redundant roles in bacterial microcompartment assembly. J. Mol. Biol. 433, 166721 (2021). · DOI
  32. 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). · DOI
  33. Leal, N. A., Havemann, G. D. & Bobik, T. A. PduP is a coenzyme-a-acylating propionaldehyde dehydrogenase associated with the polyhedral bodies involved in B12-dependent 1, 2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Arch. Microbiol 180, 353–361 (2003). · DOI
  34. Cheng, S., Fan, C., Sinha, S. & Bobik, T. A. The PduQ enzyme is an alcohol dehydrogenase used to recycle NAD+ internally within the Pdu microcompartment of Salmonella enterica. PLoS ONE 7, e47144 (2012). · DOI
  35. Palacios, S., Starai, V. J. & Escalante-Semerena, J. C. Propionyl coenzyme A is a common intermediate in the 1, 2-propanediol and propionate catabolic pathways needed for expression of the prpBCDE operon during growth of Salmonella enterica on 1, 2-propanediol. J. Bacteriol. 185, 2802–2810 (2003). · DOI
  36. Sampson, E. M., Johnson, C. L. & Bobik, T. A. Biochemical evidence that the pduS gene encodes a bifunctional cobalamin reductase. Microbiology 151, 1169–1177 (2005). · DOI
  37. Maurice, M. S. et al. Structural characterization of the active site of the PduO-type ATP: Co (I) rrinoid adenosyltransferase from Lactobacillus reuteri. J. Biol. Chem. 282, 2596–2605 (2007). · DOI
  38. Fan, C. & Bobik, T. A. The PduX enzyme of Salmonella enterica is an L-threonine kinase used for coenzyme B12 synthesis. J. Biol. Chem. 283, 11322–11329 (2008). · DOI
  39. Parsons, J. B. et al. Synthesis of empty bacterial microcompartments, directed organelle protein incorporation, and evidence of filament-associated organelle movement. Mol. Cell 38, 305–315 (2010). · DOI
  40. Fan, C. et al. Short N-terminal sequences package proteins into bacterial microcompartments. Proc. Natl Acad. Sci. USA 107, 7509–7514 (2010). · DOI
  41. 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). · DOI
  42. Liu, Y., Jorda, J., Yeates, T. O. & Bobik, T. A. The PduL phosphotransacylase is used to recycle coenzyme A within the Pdu microcompartment. J. Bacteriol. 197, 2392–2399 (2015). · DOI
  43. Lehman, B. P., Chowdhury, C. & Bobik, T. A. The N terminus of the PduB protein binds the protein shell of the Pdu microcompartment to its enzymatic core. J. Bacteriol. 199, e00785–00716 (2017). · DOI
  44. 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). · DOI
  45. Huang, F. et al. Rubisco accumulation factor 1 (Raf1) plays essential roles in mediating Rubisco assembly and carboxysome biogenesis. Proc. Natl Acad. Sci. USA 117, 17418–17428 (2020). · DOI
  46. Huang, F. et al. Roles of RbcX in carboxysome biosynthesis in the cyanobacterium Synechococcus elongatus PCC7942. Plant Physiol. 179, 184–194 (2019). · DOI
  47. Wang, H. et al. Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature 566, 131–135 (2019). · DOI
  48. Chen, A. H., Robinson-Mosher, A., Savage, D. F., Silver, P. A. & Polka, J. K. The bacterial carbon-fixing organelle is formed by shell envelopment of preassembled cargo. PLoS ONE 8, e76127 (2013). · DOI
  49. Sun, Y., Wollman, A. J. M., Huang, F., Leake, M. C. & Liu, L. N. Single-organelle quantification reveals the stoichiometric and structural variability of carboxysomes dependent on the environment. Plant Cell 31, 1648–1664 (2019). · DOI
  50. Menon, B. B., Dou, Z., Heinhorst, S., Shively, J. M. & Cannon, G. C. Halothiobacillus neapolitanus carboxysomes sequester heterologous and chimeric RubisCO species. PLoS ONE 3, e3570 (2008). · DOI
  51. Iancu, C. V. et al. Organization, structure, and assembly of α-carboxysomes determined by electron cryotomography of intact cells. J. Mol. Biol. 396, 105–117 (2010). · DOI
  52. Dai, W. et al. Visualizing individual RuBisCO and its assembly into carboxysomes in marine cyanobacteria by cryo-electron tomography. J. Mol. Biol. 430, 4156–4167 (2018). · DOI
  53. Li, T. et al. Reprogramming bacterial protein organelles as a nanoreactor for hydrogen production. Nat. Commun. 11, 5448 (2020). · DOI
  54. Ailion, M., Bobik, T. A. & Roth, J. R. Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium. J. Bacteriol. 175, 7200–7208 (1993). · DOI
  55. Chen, P., Ailion, M., Bobik, T., Stormo, G. & Roth, J. Five promoters integrate control of the cob/pdu regulon in Salmonella typhimurium. J. Bacteriol. 177, 5401–5410 (1995). · DOI
  56. Guzman, L.-M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121–4130 (1995). · DOI
  57. Lee, N., Francklyn, C. & Hamilton, E. P. Arabinose-induced binding of AraC protein to araI2 activates the araBAD operon promoter. Proc. Natl Acad. Sci. USA 84, 8814–8818 (1987). · DOI
  58. Kim, E. Y., Jakobson, C. M. & Tullman-Ercek, D. Engineering transcriptional regulation to control Pdu microcompartment formation. PLoS ONE 9, e113814 (2014). · DOI
  59. Meisner, J. & Goldberg, J. B. The Escherichia coli rhaSR-PrhaBAD inducible promoter system allows tightly controlled gene expression over a wide range in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 82, 6715–6727 (2016). · DOI
  60. Sutter, M., Wilson, S. C., Deutsch, S. & Kerfeld, C. A. Two new high-resolution crystal structures of carboxysome pentamer proteins reveal high structural conservation of CcmL orthologs among distantly related cyanobacterial species. Photosynth. Res. 118, 9–16 (2013). · DOI
  61. 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). · DOI
  62. 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). · DOI
  63. Erbilgin, O., Sutter, M. & Kerfeld, C. A. The structural basis of coenzyme A recycling in a bacterial organelle. PLoS Biol. 14, e1002399 (2016). · DOI
  64. Parsons, J. B. et al. Characterisation of PduS, the pdu metabolosome corrin reductase, and evidence of substructural organisation within the bacterial microcompartment. PLoS ONE 5, e14009 (2010). · DOI
  65. Colgan, A. M. et al. The impact of 18 ancestral and horizontally-acquired regulatory proteins upon the transcriptome and sRNA landscape of Salmonella enterica serovar Typhimurium. PLoS Genet. 12, e1006258 (2016). · DOI
  66. Mullineaux, C. W. & Sarcina, M. Probing the dynamics of photosynthetic membranes with fluorescence recovery after photobleaching. Trends Plant Sci. 7, 237–240 (2002). · DOI
  67. Oltrogge, L. M. et al. Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation. Nat. Struct. Mol. Biol. 27, 281–287 (2020). · DOI
  68. Connolly, J. P. R. et al. Host-associated niche metabolism controls enteric infection through fine-tuning the regulation of type 3 secretion. Nat. Commun. 9, 4187 (2018). · DOI
  69. Wade, Y., Daniel, R. A. & Leak, D. J. Heterologous microcompartment assembly in Bacillaceae: establishing the components necessary for scaffold formation. ACS Synth. Biol. 8, 1642–1654 (2019). · DOI
  70. Juodeikis, R. et al. Effect of metabolosome encapsulation peptides on enzyme activity, coaggregation, incorporation, and bacterial microcompartment formation. MicrobiologyOpen 9, e1010 (2020). · DOI
  71. Marsh, J. A. et al. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153, 461–470 (2013). · DOI
  72. Kalnins, G. et al. Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles. Nat. Commun. 11, 388 (2020). · DOI
  73. Uddin, I., Frank, S., Warren, M. J. & Pickersgill, R. W. A generic self-assembly process in microcompartments and synthetic protein nanotubes. Small 14, e1704020 (2018). · DOI
  74. Pang, A., Frank, S., Brown, I., Warren, M. J. & Pickersgill, R. W. Structural insights into higher order assembly and function of the bacterial microcompartment protein PduA. J. Biol. Chem. 289, 22377–22384 (2014). · DOI
  75. Kerfeld, C. A. & Erbilgin, O. Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol. 23, 22–34 (2015). · DOI
  76. Cai, F. et al. Advances in understanding carboxysome assembly in Prochlorococcus and Synechococcus implicate CsoS2 as a critical component. Life 5, 1141–1171 (2015). · DOI
  77. Hill, N. C., Tay, J. W., Altus, S., Bortz, D. M. & Cameron, J. C. Life cycle of a cyanobacterial carboxysome. Sci. Adv. 6, eaba1269 (2020). · DOI
  78. MacCready, J. S., Tran, L., Basalla, J. L., Hakim, P. & Vecchiarelli, A. G. The McdAB system positions α-carboxysomes in proteobacteria. Mol. Microbiol. 16, 277–297 (2021). · DOI
  79. Savage, D. F., Afonso, B., Chen, A. H. & Silver, P. A. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327, 1258–1261 (2010). · DOI · Paper page
  80. Sun, Y. et al. Light modulates the biosynthesis and organization of cyanobacterial carbon fixation machinery through photosynthetic electron flow. Plant Physiol. 171, 530–541 (2016). · DOI
  81. MacCready, J. S. et al. Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria. Elife 7, e39723 (2018). · DOI
  82. MacCready, J. S., Basalla, J. L. & Vecchiarelli, A. G. Origin and evolution of carboxysome positioning systems in cyanobacteria. Mol. Biol. Evol. 37, 1434–1451 (2020). · DOI
  83. Shin, Y. & Brangwynne, C. P. Liquid phase condensation in cell physiology and disease. Science 357, eaaf4382 (2017). · DOI
  84. Greening, C. & Lithgow, T. Formation and function of bacterial organelles. Nat. Rev. Microbiol. 18, 677–689 (2020). · DOI
  85. Alberti, S., Gladfelter, A. & Mittag, T. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176, 419–434 (2019). · DOI · Paper page
  86. Parry, B. R. et al. The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell 156, 183–194 (2014). · DOI · Paper page
  87. Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340 (2012). · DOI
  88. Lee, M. J., Brown, I. R., Juodeikis, R., Frank, S. & Warren, M. J. Employing bacterial microcompartment technology to engineer a shell-free enzyme-aggregate for enhanced 1,2-propanediol production in Escherichia coli. Metab. Eng. 36, 48–56 (2016). · DOI
  89. Jakobson, C. M., Slininger Lee, M. F. & Tullman‐Ercek, D. De novo design of signal sequences to localize cargo to the 1, 2‐propanediol utilization microcompartment. Protein Sci. 26, 1086–1092 (2017). · DOI
  90. Elowitz, M. B., Surette, M. G., Wolf, P.-E., Stock, J. B. & Leibler, S. Protein mobility in the cytoplasm of Escherichia coli. J. Bacteriol. 181, 197–203 (1999). · DOI
  91. Casella, S. et al. Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol. Plant 10, 1434–1448 (2017). · DOI
  92. Kroger, C. et al. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14, 683–695 (2013). · DOI
  93. Freeman Rosenzweig, E. S. et al. The eukaryotic CO2-concentrating organelle is liquid-like and exhibits dynamic reorganization. Cell 171, 148–162 e119 (2017). · DOI
  94. He, S. et al. The structural basis of Rubisco phase separation in the pyrenoid. Nat. Plants 6, 1480–1490 (2020). · DOI
  95. Ouyang, M. et al. Liquid-liquid phase transition drives intra-chloroplast cargo sorting. Cell 180, 1144–1159 e1120 (2020). · DOI
  96. Mcclelland, M. et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413, 852–856 (2001). · DOI
  97. Zinder, N. D. & Lederberg, J. Genetic exchange in Salmonella. J. Bacteriol. 64, 679–699 (1952). · DOI
  98. Vogel, H. J. & Bonner, D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218, 97 (1956). · DOI
  99. Martínez‐García, E. & de Lorenzo, V. Engineering multiple genomic deletions in Gram-negative bacteria: analysis of the multi‐resistant antibiotic profile of Pseudomonas putida KT2440. Environ. Microbiol. 13, 2702–2716 (2011). · DOI
  100. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640 (2000). · DOI
  101. Koskiniemi, S., Pränting, M., Gullberg, E., Näsvall, J. & Andersson, D. I. Activation of cryptic aminoglycoside resistance in Salmonella enterica. Mol. Microbiol. 80, 1464–1478 (2011). · DOI
  102. Schmieger, H. A method for detection of phage mutants with altered transducing ability. Mol. Gen. Genet. 110, 378–381 (1971). · DOI
  103. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343–345 (2009). · DOI
  104. Corcoran, C. P. et al. reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol. Microbiol. 84, 428–445 (2012). · DOI
  105. Faulkner, M. et al. Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale 9, 10662–10673 (2017). · DOI
  106. Fang, Y. et al. Engineering and modulating functional cyanobacterial CO2-fixing organelles. Front. Plant Sci. 9, 739 (2018). · DOI
  107. Chen, T. et al. Incorporation of functional rubisco activases into engineered carboxysomes to enhance carbon fixation. ACS Synth. Biol. 11, 154–161 (2022). · DOI
  108. Bolte, S. & Cordelières, F. P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213–232 (2006). · DOI
  109. Dunn, K. W., Kamocka, M. M. & McDonald, J. H. A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. Cell Physiol. 300, C723–742 (2011). · DOI
  110. Mullineaux, C. W., Tobin, M. J. & Jones, G. R. Mobility of photosynthetic complexes in thylakoid membranes. Nature 390, 421–424 (1997). · DOI
  111. Kirchhoff, H., Haferkamp, S., Allen, J. F., Epstein, D. B. & Mullineaux, C. W. Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol. 146, 1571–1578 (2008). · DOI
  112. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinforma. 10, 421 (2009). · DOI · Paper page
  113. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014). · DOI
  114. Katoh, K., Misawa, K., Kuma, K. I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002). · DOI · Paper page
  115. 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). · DOI
  116. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490–e9490 (2010). · DOI · Paper page
  117. Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021). · DOI
  118. Pei, J. & Grishin, N. V. AL2CO: calculation of positional conservation in a protein sequence alignment. Bioinformatics 17, 700–712 (2001). · DOI

Metadata

Authors
Yang, M., Wenner, N., Dykes, G. F., Li, Y., Zhu, X., Sun, Y., Huang, F., Hinton, J. C. D., & Liu, L.-N.
Affiliations
University of Liverpool (GB)
Corresponding author
Liu, Lu-Ning
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-05-25
Volume
13
Issue
1
Pages
2920-2920
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-022-30608-w
PMC
PMC9132943
OpenAlex
W4281491296
Cited by
45
References
4
Citations by year
2026: 10 · 2025: 17 · 2024: 10 · 2023: 6 · 2022: 2
FWCI
5.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Wellcome Trust (106914/Z/15/Z)
  • National Natural Science Foundation of China (32070109)
  • Royal Society (URF\R\180030, RGF\EA\181061, RGF\EA\180233)
  • RCUK | Biotechnology and Biological Sciences Research Council (BB/V009729/1, BB/M024202/1, BB/R003890/1)
  • National Key R&D Program of China
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords
enzyme complex assembly
MeSH terms
Bacteria, Bacterial Proteins, Organelles, Propylene Glycol

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review