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Abstract

Subcellular compartmentalization is a defining feature of all cells. In prokaryotes, compartmentalization is generally achieved via protein-based strategies. The two main classes of microbial protein compartments are bacterial microcompartments and encapsulin nanocompartments. Encapsulins self-assemble into proteinaceous shells with diameters between 24 and 42 nm and are defined by the viral HK97-fold of their shell protein. Encapsulins have the ability to encapsulate dedicated cargo proteins, including ferritin-like proteins, peroxidases, and desulfurases. Encapsulation is mediated by targeting sequences present in all cargo proteins. Encapsulins are found in many bacterial and archaeal phyla and have been suggested to play roles in iron storage, stress resistance, sulfur metabolism, and natural product biosynthesis. Phylogenetic analyses indicate that they share a common ancestor with viral capsid proteins. Many pathogens encode encapsulins, and recent evidence suggests that they may contribute toward pathogenicity. The existing information on encapsulin structure, biochemistry, biological function, and biomedical relevance is reviewed here.

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2022-06-21
2024-12-07
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Literature Cited

  1. 1.
    Cornejo E, Abreu N, Komeili A. 2014. Compartmentalization and organelle formation in bacteria. Curr. Opin. Cell Biol. 26:132–38
    [Google Scholar]
  2. 2.
    Diekmann Y, Pereira-Leal JB. 2013. Evolution of intracellular compartmentalization. Biochem. J. 449:319–31
    [Google Scholar]
  3. 3.
    Kerfeld CA, Heinhorst S, Cannon GC. 2010. Bacterial microcompartments. Annu. Rev. Microbiol. 64:391–408
    [Google Scholar]
  4. 4.
    Melnicki MR, Sutter M, Kerfeld CA. 2021. Evolutionary relationships among shell proteins of carboxysomes and metabolosomes. Curr. Opin. Microbiol. 63:1–9
    [Google Scholar]
  5. 5.
    Ochoa JM, Yeates TO. 2021. Recent structural insights into bacterial microcompartment shells. Curr. Opin. Microbiol. 62:51–60
    [Google Scholar]
  6. 6.
    Turmo A, Gonzalez-Esquer CR, Kerfeld CA. 2017. Carboxysomes: metabolic modules for CO2 fixation. FEMS Microbiol. Lett. 364:fnx176
    [Google Scholar]
  7. 7.
    Liu LN. 2021. Advances in the bacterial organelles for CO2 fixation. Trends Microbiol. In press. https://doi.org/10.1016/j.tim.2021.10.004
    [Crossref] [Google Scholar]
  8. 8.
    Bobik TA, Lehman BP, Yeates TO. 2015. Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways. Mol. Microbiol. 98:193–207
    [Google Scholar]
  9. 9.
    Ferlez B, Sutter M, Kerfeld CA 2019. Glycyl radical enzyme-associated microcompartments: redox-replete bacterial organelles. mBio 10:e02327
    [Google Scholar]
  10. 10.
    Prentice MB. 2021. Bacterial microcompartments and their role in pathogenicity. Curr. Opin. Microbiol. 63:19–28
    [Google Scholar]
  11. 11.
    Sutter M, Boehringer D, Gutmann S, Gunther S, Prangishvili D et al. 2008. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat. Struct. Mol. Biol. 15:939–47
    [Google Scholar]
  12. 12.
    Nichols RJ, Cassidy-Amstutz C, Chaijarasphong T, Savage DF. 2017. Encapsulins: molecular biology of the shell. Crit. Rev. Biochem. Mol. Biol. 52:583–94
    [Google Scholar]
  13. 13.
    Greening C, Lithgow T. 2020. Formation and function of bacterial organelles. Nat. Rev. Microbiol. 18:677–89
    [Google Scholar]
  14. 14.
    Jones JA, Giessen TW. 2021. Advances in encapsulin nanocompartment biology and engineering. Biotechnol. Bioeng. 118:491–505
    [Google Scholar]
  15. 15.
    Cassidy-Amstutz C, Oltrogge L, Going CC, Lee A, Teng P et al. 2016. Identification of a minimal peptide tag for in vivo and in vitro loading of encapsulin. Biochemistry 55:3461–68
    [Google Scholar]
  16. 16.
    Altenburg WJ, Rollins N, Silver PA, Giessen TW. 2021. Exploring targeting peptide-shell interactions in encapsulin nanocompartments. Sci. Rep. 11:4951
    [Google Scholar]
  17. 17.
    Nichols RJ, LaFrance B, Phillips NR, Radford DR, Oltrogge LM et al. 2021. Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism. eLife 10:e59288
    [Google Scholar]
  18. 18.
    Andreas MP, Giessen TW. 2021. Large-scale computational discovery and analysis of virus-derived microbial nanocompartments. Nat. Commun. 12:4748
    [Google Scholar]
  19. 19.
    Demchuk AM, Patel TR. 2020. The biomedical and bioengineering potential of protein nanocompartments. Biotechnol. Adv. 41:107547
    [Google Scholar]
  20. 20.
    Gabashvili AN, Chmelyuk NS, Efremova MV, Malinovskaya JA, Semkina AS, Abakumov MA. 2020. Encapsulins—bacterial protein nanocompartments: structure, properties, and application. Biomolecules 10:966
    [Google Scholar]
  21. 21.
    Giessen TW. 2016. Encapsulins: microbial nanocompartments with applications in biomedicine, nanobiotechnology and materials science. Curr. Opin. Chem. Biol. 34:1–10
    [Google Scholar]
  22. 22.
    Giessen TW, Silver PA. 2017. Engineering carbon fixation with artificial protein organelles. Curr. Opin. Biotechnol. 46:42–50
    [Google Scholar]
  23. 23.
    Giessen TW, Silver PA. 2017. Widespread distribution of encapsulin nanocompartments reveals functional diversity. Nat. Microbiol. 2:17029
    [Google Scholar]
  24. 24.
    Valdés-Stauber N, Scherer S. 1994. Isolation and characterization of Linocin M18, a bacteriocin produced by Brevibacterium linens. Appl. Environ. Microbiol. 60:3809–14
    [Google Scholar]
  25. 25.
    Rosenkrands I, Rasmussen PB, Carnio M, Jacobsen S, Theisen M, Andersen P. 1998. Identification and characterization of a 29-kilodalton protein from Mycobacterium tuberculosis culture filtrate recognized by mouse memory effector cells. Infect. Immun. 66:2728–35
    [Google Scholar]
  26. 26.
    Hicks PM, Chang LS, Kelly RM. 2001. Homomultimeric protease and putative bacteriocin homolog from Thermotoga maritima. Methods Enzymol. 330:455–60
    [Google Scholar]
  27. 27.
    Hicks PM, Rinker KD, Baker JR, Kelly RM. 1998. Homomultimeric protease in the hyperthermophilic bacterium Thermotoga maritima has structural and amino acid sequence homology to bacteriocins in mesophilic bacteria. FEBS Lett. 440:393–98
    [Google Scholar]
  28. 28.
    Anast JM, Schmitz-Esser S. 2020. The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes. PLOS ONE 15:e0233945
    [Google Scholar]
  29. 29.
    Oliveira MM, Ramos ETA, Drechsel MM, Vidal MS, Schwab S, Baldani JI. 2018. Gluconacin from Gluconacetobacterdiazotrophicus PAL5 is an active bacteriocin against phytopathogenic and beneficial sugarcane bacteria. J. Appl. Microbiol. 125:1812–26
    [Google Scholar]
  30. 30.
    Ward DE, Shockley KR, Chang LS, Levy RD, Michel JK et al. 2002. Proteolysis in hyperthermophilic microorganisms. Archaea 1:63–74
    [Google Scholar]
  31. 31.
    Olano C, Garcia I, González A, Rodriguez M, Rozas D et al. 2014. Activation and identification of five clusters for secondary metabolites in Streptomyces albus J1074. Microb. Biotechnol. 7:242–56
    [Google Scholar]
  32. 32.
    Teran LC, Distefano M, Bellich B, Petrosino S, Bertoncin P et al. 2020. Proteomic studies of the biofilm matrix including outer membrane vesicles of Burkholderia multivorans C1576, a strain of clinical importance for cystic fibrosis. Microorganisms 8:1826
    [Google Scholar]
  33. 33.
    Li X, He Y, Zhang L, Xu Z, Ben H et al. 2019. Discovery of potential pathways for biological conversion of poplar wood into lipids by co-fermentation of Rhodococci strains. Biotechnol. Biofuels 12:60
    [Google Scholar]
  34. 34.
    Loncar N, Rozeboom HJ, Franken LE, Stuart MCA, Fraaije MW. 2020. Structure of a robust bacterial protein cage and its application as a versatile biocatalytic platform through enzyme encapsulation. Biochem. Biophys. Res. Commun. 529:548–53
    [Google Scholar]
  35. 35.
    Tamura A, Fukutani Y, Takami T, Fujii M, Nakaguchi Y et al. 2015. Packaging guest proteins into the encapsulin nanocompartment from Rhodococcus erythropolis N771. Biotechnol. Bioeng. 112:13–20
    [Google Scholar]
  36. 36.
    Giessen TW, Orlando BJ, Verdegaal AA, Chambers MG, Gardener J et al. 2019. Large protein organelles form a new iron sequestration system with high storage capacity. eLife 8:e46070
    [Google Scholar]
  37. 37.
    Winter N, Triccas JA, Rivoire B, Pessolani MC, Eiglmeier K et al. 1995. Characterization of the gene encoding the immunodominant 35 kDa protein of Mycobacterium leprae. Mol. Microbiol. 16:865–76
    [Google Scholar]
  38. 38.
    Kwak J, McCue LA, Trczianka K, Kendrick KE. 2001. Identification and characterization of a developmentally regulated protein, EshA, required for sporogenic hyphal branches in Streptomyces griseus. J. Bacteriol. 183:3004–15
    [Google Scholar]
  39. 39.
    Saito N, Matsubara K, Watanabe M, Kato F, Ochi K. 2003. Genetic and biochemical characterization of EshA, a protein that forms large multimers and affects developmental processes in Streptomyces griseus. J. Biol. Chem. 278:5902–11
    [Google Scholar]
  40. 40.
    Salerno P, Persson J, Bucca G, Laing E, Ausmees N et al. 2013. Identification of new developmentally regulated genes involved in Streptomyces coelicolor sporulation. BMC Microbiol. 13:281
    [Google Scholar]
  41. 41.
    Saito N, Xu J, Hosaka T, Okamoto S, Aoki H et al. 2006. EshA accentuates ppGpp accumulation and is conditionally required for antibiotic production in Streptomyces coelicolor A3(2). J. Bacteriol. 188:4952–61
    [Google Scholar]
  42. 42.
    Kawamoto S, Watanabe M, Saito N, Hesketh A, Vachalova K et al. 2001. Molecular and functional analyses of the gene (eshA) encoding the 52-kilodalton protein of Streptomyces coelicolor A3(2) required for antibiotic production. J. Bacteriol. 183:6009–16
    [Google Scholar]
  43. 43.
    Yin P, Li Y-Y, Zhou J, Wang Y-H, Zhang S-L et al. 2013. Direct proteomic mapping of Streptomyces avermitilis wild and industrial strain and insights into avermectin production. J. Proteom. 79:1–12
    [Google Scholar]
  44. 44.
    Kuhl M, Gläser L, Rebets Y, Rückert C, Sarkar N et al. 2020. Microparticles globally reprogram Streptomyces albus toward accelerated morphogenesis, streamlined carbon core metabolism, and enhanced production of the antituberculosis polyketide pamamycin. Biotechnol. Bioeng. 117:3858–75
    [Google Scholar]
  45. 45.
    Nichols RJ, LaFrance B, Phillips NR, Oltrogge LM, Valentin-Alvarado LE et al. 2021. Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism. eLife 10:e59288
    [Google Scholar]
  46. 46.
    Ward AC, Allenby NE. 2018. Genome mining for the search and discovery of bioactive compounds: the Streptomyces paradigm. FEMS Microbiol. Lett. 365:fny240
    [Google Scholar]
  47. 47.
    Bader CD, Panter F, Müller R. 2020. In depth natural product discovery—Myxobacterial strains that provided multiple secondary metabolites. Biotechnol. Adv. 39:107480
    [Google Scholar]
  48. 48.
    Suhanovsky MM, Teschke CM. 2015. Nature's favorite building block: deciphering folding and capsid assembly of proteins with the HK97-fold. Virology 479–480:487–97
    [Google Scholar]
  49. 49.
    Duda RL, Teschke CM. 2019. The amazing HK97 fold: versatile results of modest differences. Curr. Opin. Virol. 36:9–16
    [Google Scholar]
  50. 50.
    Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V et al. 2006. Pfam: clans, web tools and services. Nucleic Acids. Res. 34:D247–51
    [Google Scholar]
  51. 51.
    Soding J. 2005. Protein homology detection by HMM–HMM comparison. Bioinformatics 21:951–60
    [Google Scholar]
  52. 52.
    Boto L. 2010. Horizontal gene transfer in evolution: facts and challenges. Proc. Biol. Sci. 277:819–27
    [Google Scholar]
  53. 53.
    Kanhere A, Vingron M. 2009. Horizontal Gene Transfers in prokaryotes show differential preferences for metabolic and translational genes. BMC Evol. Biol. 9:9
    [Google Scholar]
  54. 54.
    Krupovic M, Koonin EV. 2017. Multiple origins of viral capsid proteins from cellular ancestors. PNAS 114:E2401–10
    [Google Scholar]
  55. 55.
    Helgstrand C, Wikoff WR, Duda RL, Hendrix RW, Johnson JE, Liljas L. 2003. The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 Å resolution. J. Mol. Biol. 334:885–99
    [Google Scholar]
  56. 56.
    Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE. 2000. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129–33
    [Google Scholar]
  57. 57.
    Baker ML, Jiang W, Rixon FJ, Chiu W. 2005. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79:14967–70
    [Google Scholar]
  58. 58.
    Caston JR. 2021. Cryo-EM structure of a thermophilic encapsulin offers clues to its functions. IUCrJ 8:333–34
    [Google Scholar]
  59. 59.
    Wiryaman T, Toor N. 2021. Cryo-EM structure of a thermostable bacterial nanocompartment. IUCrJ 8:342–50
    [Google Scholar]
  60. 60.
    LaFrance B, Cassidy-Amstutz C, Nichols RJ, Oltrogge L, Nogales E, Savage DF. 2021. The encapsulin from Thermatoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein. bioRxiv 441214. https://doi.org/10.1101/2021.04.26.441214
    [Crossref]
  61. 61.
    Ross J, McIver Z, Lambert T, Piergentili C, Gallagher KJ et al. 2021. Pore dynamics and asymmetric cargo loading in an encapsulin nanocompartment. bioRxiv 439977. https://doi.org/10.1101/2021.04.15.439977
    [Crossref]
  62. 62.
    Clancy Kelley L-L, Dillard BD, Tempel W, Chen L, Shaw N et al. 2007. Structure of the hypothetical protein PF0899 from Pyrococcus furiosus at 1.85 Å resolution. Acta Crystallogr. F 63:549–52
    [Google Scholar]
  63. 63.
    Tang Y, Mu A, Zhang Y, Zhou S, Wang W et al. 2021. Cryo-EM structure of Mycobacterium smegmatis DyP-loaded encapsulin. PNAS 118:e2025658118
    [Google Scholar]
  64. 64.
    Andrews SC. 2010. The Ferritin-like superfamily: evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim. Biophys. Acta Gen. Subj. 1800:691–705
    [Google Scholar]
  65. 65.
    McHugh CA, Fontana J, Nemecek D, Cheng N, Aksyuk AA et al. 2014. A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. EMBO J. 33:1896–911
    [Google Scholar]
  66. 66.
    He D, Piergentili C, Ross J, Tarrant E, Tuck LR et al. 2019. Conservation of the structural and functional architecture of encapsulated ferritins in bacteria and archaea. Biochem. J. 476:975–89
    [Google Scholar]
  67. 67.
    He D, Hughes S, Vanden-Hehir S, Georgiev A, Altenbach K et al. 2016. Structural characterization of encapsulated ferritin provides insight into iron storage in bacterial nanocompartments. eLife 5:e18972
    [Google Scholar]
  68. 68.
    Akita F, Chong KT, Tanaka H, Yamashita E, Miyazaki N et al. 2007. The crystal structure of a virus-like particle from the hyperthermophilic archaeon Pyrococcus furiosus provides insight into the evolution of viruses. J. Mol. Biol. 368:1469–83
    [Google Scholar]
  69. 69.
    Heinemann J, Maaty WS, Gauss GH, Akkaladevi N, Brumfield SK et al. 2011. Fossil record of an archaeal HK97-like provirus. Virology 417:362–68
    [Google Scholar]
  70. 70.
    Yao H, Wang Y, Lovell S, Kumar R, Ruvinsky AM et al. 2012. The structure of the BfrB–Bfd complex reveals protein–protein interactions enabling iron release from bacterioferritin. J. Am. Chem. Soc. 134:13470–81
    [Google Scholar]
  71. 71.
    Arosio P, Elia L, Poli M. 2017. Ferritin, cellular iron storage and regulation. IUBMB Life 69:414–22
    [Google Scholar]
  72. 72.
    Pysz MA, Conners SB, Montero CI, Shockley KR, Johnson MR et al. 2004. Transcriptional analysis of biofilm formation processes in the anaerobic, hyperthermophilic bacterium Thermotoga maritima. Appl. Environ. Microbiol. 70:6098–112
    [Google Scholar]
  73. 73.
    Ikeyama N, Murakami T, Toyoda A, Mori H, Iino T et al. 2020. Microbial interaction between the succinate-utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron. MicrobiologyOpen 9:e1111
    [Google Scholar]
  74. 74.
    Zeng X, Zhang X, Shao Z. 2020. Metabolic adaptation to sulfur of hyperthermophilic Palaeococcus pacificus DY20341T from deep-sea hydrothermal sediments. Int. J. Mol. Sci. 21:368
    [Google Scholar]
  75. 75.
    Kim D, Choi J, Lee S, Hyun H, Lee K, Cho K. 2019. Mutants defective in the production of encapsulin show a tan-phase-locked phenotype in Myxococcus xanthus. J. Microbiol. 57:795–802
    [Google Scholar]
  76. 76.
    Okamoto Y, Onoda A, Sugimoto H, Takano Y, Hirota S et al. 2014. H2O2-dependent substrate oxidation by an engineered diiron site in a bacterial hemerythrin. Chem. Commun. 50:3421–23
    [Google Scholar]
  77. 77.
    Alvarez-Carreno C, Alva V, Becerra A, Lazcano A 2018. Structure, function and evolution of the hemerythrin-like domain superfamily. Protein Sci. 27:848–60
    [Google Scholar]
  78. 78.
    Rivera M. 2017. Bacterioferritin: structure, dynamics, and protein–protein interactions at play in iron storage and mobilization. Acc. Chem. Res. 50:331–40
    [Google Scholar]
  79. 79.
    Kim SJ, Shoda M. 1999. Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes. Appl. Environ. Microbiol. 65:1029–35
    [Google Scholar]
  80. 80.
    Ahmad M, Roberts JN, Hardiman EM, Singh R, Eltis LD, Bugg TD. 2011. Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase. Biochemistry 50:5096–107
    [Google Scholar]
  81. 81.
    Rahmanpour R, Bugg TD. 2013. Assembly in vitro of Rhodococcus jostii RHA1 encapsulin and peroxidase DypB to form a nanocompartment. FEBS J. 280:2097–104
    [Google Scholar]
  82. 82.
    Putri RM, Allende-Ballestero C, Luque D, Klem R, Rousou KA et al. 2017. Structural characterization of native and modified encapsulins as nanoplatforms for in vitro catalysis and cellular uptake. ACS Nano 11:12796–804
    [Google Scholar]
  83. 83.
    Lien KA, Dinshaw K, Nichols RJ, Cassidy-Amstutz C, Knight M et al. 2020. A nanocompartment system contributes to defense against oxidative stress in Mycobacterium tuberculosis. eLife 10:e74358
    [Google Scholar]
  84. 84.
    Tracey JC, Coronado M, Giessen TW, Lau MCY, Silver PA, Ward BB. 2019. The discovery of twenty-eight new encapsulin sequences, including three in anammox bacteria. Sci. Rep. 9:20122
    [Google Scholar]
  85. 85.
    Cipollone R, Ascenzi P, Visca P. 2007. Common themes and variations in the rhodanese superfamily. IUBMB Life 59:51–59
    [Google Scholar]
  86. 86.
    Black KA, Dos Santos PC 2015. Shared-intermediates in the biosynthesis of thio-cofactors: mechanism and functions of cysteine desulfurases and sulfur acceptors. Biochim. Biophys. Acta Mol. Cell. Res. 1853:1470–80
    [Google Scholar]
  87. 87.
    Gorges J, Panter F, Kjaerulff L, Hoffmann T, Kazmaier U, Muller R. 2018. Structure, total synthesis, and biosynthesis of chloromyxamides: myxobacterial tetrapeptides featuring an uncommon 6-chloromethyl-5-methoxypipecolic acid building block. Angew. Chem. Int. Ed 57:14270–75
    [Google Scholar]
  88. 88.
    Kavanagh KL, Jornvall H, Persson B, Oppermann U. 2008. The SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell. Mol. Life Sci. 65:3895–906
    [Google Scholar]
  89. 89.
    Ouchi T, Tomita T, Horie A, Yoshida A, Takahashi K et al. 2013. Lysine and arginine biosyntheses mediated by a common carrier protein in Sulfolobus. Nat. Chem. Biol. 9:277–83
    [Google Scholar]
  90. 90.
    Kerfeld CA, Aussignargues C, Zarzycki J, Cai F, Sutter M. 2018. Bacterial microcompartments. Nat. Rev. Microbiol. 16:277–90
    [Google Scholar]
  91. 91.
    Chandrayan SK, McTernan PM, Hopkins RC, Sun J, Jenney FE Jr., Adams MW. 2012. Engineering hyperthermophilic archaeon Pyrococcus furiosus to overproduce its cytoplasmic [NiFe]-hydrogenase. J. Biol. Chem. 287:3257–64
    [Google Scholar]
  92. 92.
    Menon AL, Poole FL II, Cvetkovic A, Trauger SA, Kalisiak E et al. 2009. Novel multiprotein complexes identified in the hyperthermophilic archaeon Pyrococcus furiosus by non-denaturing fractionation of the native proteome. Mol. Cell. Proteom. 8:735–51
    [Google Scholar]
  93. 93.
    Ash PA, Kendall-Price SET, Vincent KA 2019. Unifying activity, structure, and spectroscopy of [NiFe] hydrogenases: combining techniques to clarify mechanistic understanding. Acc. Chem. Res. 52:3120–31
    [Google Scholar]
  94. 94.
    Chou C-J, Shockley KR, Conners SB, Lewis DL, Comfort DA et al. 2007. Impact of substrate glycoside linkage and elemental sulfur on bioenergetics of and hydrogen production by the hyperthermophilic archaeon Pyrococcus furiosus. Appl. Environ. Microbiol. 73:6842–53
    [Google Scholar]
  95. 95.
    Fiala G, Stetter KO. 1986. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch. Microbiol. 145:56–61
    [Google Scholar]
  96. 96.
    Silva PJ, van den Ban EC, Wassink H, Haaker H, de Castro B et al. 2000. Enzymes of hydrogen metabolism in Pyrococcus furiosus. Eur. J. Biochem. 267:6541–51
    [Google Scholar]
  97. 97.
    Mongkolsuk S, Praituan W, Loprasert S, Fuangthong M, Chamnongpol S. 1998. Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J. Bacteriol. 180:2636–43
    [Google Scholar]
  98. 98.
    Alegria TG, Meireles DA, Cussiol JR, Hugo M, Trujillo M et al. 2017. Ohr plays a central role in bacterial responses against fatty acid hydroperoxides and peroxynitrite. PNAS 114:E132–41
    [Google Scholar]
  99. 99.
    Seidler NW. 2013. Basic biology of GAPDH. Adv. Exp. Med. Biol. 985:1–36
    [Google Scholar]
  100. 100.
    Seidler NW. 2013. GAPDH and intermediary metabolism. Adv. Exp. Med. Biol. 985:37–59
    [Google Scholar]
  101. 101.
    Barber RD, Harmer DW, Coleman RA, Clark BJ. 2005. GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol. Genom. 21:389–95
    [Google Scholar]
  102. 102.
    Brasen C, Esser D, Rauch B, Siebers B. 2014. Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol. Mol. Biol. Rev. 78:89–175
    [Google Scholar]
  103. 103.
    Siebers B, Schonheit P. 2005. Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr. Opin. Microbiol. 8:695–705
    [Google Scholar]
  104. 104.
    Charron C, Talfournier F, Isupov MN, Branlant G, Littlechild JA et al. 1999. Crystallization and preliminary X-ray diffraction studies of d-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic archaeon Methanothermus fervidus. Acta. Crystallogr. D 55:1353–55
    [Google Scholar]
  105. 105.
    van der Oost J, Schut G, Kengen SW, Hagen WR, Thomm M, de Vos WM. 1998. The ferredoxin-dependent conversion of glyceraldehyde-3-phosphate in the hyperthermophilic archaeon Pyrococcus furiosus represents a novel site of glycolytic regulation. J. Biol. Chem. 273:28149–54
    [Google Scholar]
  106. 106.
    Brunner NA, Brinkmann H, Siebers B, Hensel R. 1998. NAD+-dependent glyceraldehyde-3-phosphate dehydrogenase from Thermoproteus tenax. The first identified archaeal member of the aldehyde dehydrogenase superfamily is a glycolytic enzyme with unusual regulatory properties. J. Biol. Chem. 273:6149–56
    [Google Scholar]
  107. 107.
    Zwickl P, Fabry S, Bogedain C, Haas A, Hensel R. 1990. Glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic archaebacterium Pyrococcus woesei: characterization of the enzyme, cloning and sequencing of the gene, and expression in Escherichia coli. J. Bacteriol. 172:4329–38
    [Google Scholar]
  108. 108.
    Schut GJ, Brehm SD, Datta S, Adams MW. 2003. Whole-genome DNA microarray analysis of a hyperthermophile and an archaeon: Pyrococcus furiosus grown on carbohydrates or peptides. J. Bacteriol. 185:3935–47
    [Google Scholar]
  109. 109.
    Sakuraba H, Yoneda K, Yoshihara K, Satoh K, Kawakami R et al. 2007. Sequential aldol condensation catalyzed by hyperthermophilic 2-deoxy-d-ribose-5-phosphate aldolase. Appl. Environ. Microbiol. 73:7427–34
    [Google Scholar]
  110. 110.
    Sakuraba H, Tsuge H, Shimoya I, Kawakami R, Goda S et al. 2003. The first crystal structure of archaeal aldolase. Unique tetrameric structure of 2-deoxy-d-ribose-5-phosphate aldolase from the hyperthermophilic archaea Aeropyrum pernix. J. Biol. Chem. 278:10799–806
    [Google Scholar]
  111. 111.
    Rashid N, Imanaka H, Fukui T, Atomi H, Imanaka T. 2004. Presence of a novel phosphopentomutase and a 2-deoxyribose 5-phosphate aldolase reveals a metabolic link between pentoses and central carbon metabolism in the hyperthermophilic archaeon Thermococcus kodakaraensis. J. Bacteriol. 186:4185–91
    [Google Scholar]
  112. 112.
    Lomax MS, Greenberg GR. 1968. Characteristics of the deo operon: role in thymine utilization and sensitivity to deoxyribonucleosides. J. Bacteriol. 96:501–14
    [Google Scholar]
  113. 113.
    Jia B, Liu J, Van Duyet L, Sun Y, Xuan YH, Cheong G-W. 2015. Proteome profiling of heat, oxidative, and salt stress responses in Thermococcus kodakarensis KOD1. Front. Microbiol. 6:605
    [Google Scholar]
  114. 114.
    Orita I, Sato T, Yurimoto H, Kato N, Atomi H et al. 2006. The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon Thermococcus kodakaraensis. J. Bacteriol. 188:4698–704
    [Google Scholar]
  115. 115.
    Salleron L, Magistrelli G, Mary C, Fischer N, Bairoch A, Lane L. 2014. DERA is the human deoxyribose phosphate aldolase and is involved in stress response. Biochim. Biophys. Acta Mol. Cell. Res. 1843:2913–25
    [Google Scholar]
  116. 116.
    Niforou K, Cheimonidou C, Trougakos IP. 2014. Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol. 2:323–32
    [Google Scholar]
  117. 117.
    Burston SG, Clarke AR. 1995. Molecular chaperones: physical and mechanistic properties. Essays Biochem. 29:125–36
    [Google Scholar]
  118. 118.
    De Oliveira DMP, Forde BM, Kidd TJ, Harris PNA, Schembri MA et al. 2020. Antimicrobial resistance in ESKAPE pathogens. Clin. Microbiol. Rev. 33:00181
    [Google Scholar]
  119. 119.
    Saxena S, Spaink HP, Forn-Cuni G. 2021. Drug resistance in nontuberculous mycobacteria: mechanisms and models. Biology 10:96
    [Google Scholar]
  120. 120.
    Kanabalan RD, Lee LJ, Lee TY, Chong PP, Hassan L et al. 2021. Human tuberculosis and Mycobacterium tuberculosis complex: a review on genetic diversity, pathogenesis and omics approaches in host biomarkers discovery. Microbiol. Res. 246:126674
    [Google Scholar]
  121. 121.
    Weldingh K, Andersen P. 1999. Immunological evaluation of novel Mycobacterium tuberculosis culture filtrate proteins. FEMS Immunol. Med. Microbiol. 23:159–64
    [Google Scholar]
  122. 122.
    Zhang YJ, Reddy MC, Ioerger TR, Rothchild AC, Dartois V et al. 2013. Tryptophan biosynthesis protects mycobacteria from CD4 T-cell-mediated killing. Cell 155:1296–308
    [Google Scholar]
  123. 123.
    Triccas JA, Roche PW, Winter N, Feng CG, Butlin CR, Britton WJ. 1996. A 35-kilodalton protein is a major target of the human immune response to Mycobacterium leprae. Infect. Immun. 64:5171–77
    [Google Scholar]
  124. 124.
    Bo M, Jasemi S, Uras G, Erre GL, Passiu G, Sechi LA 2020. Role of infections in the pathogenesis of rheumatoid arthritis: focus on mycobacteria. Microorganisms 8:1459
    [Google Scholar]
  125. 125.
    Aitken JM, Phan K, Bodman SE, Sharma S, Watt A et al. 2021. A Mycobacterium species for Crohn's disease?. Pathology 53:818–23
    [Google Scholar]
  126. 126.
    Bannantine JP, Huntley JFJ, Miltner E, Stabel JR, Bermudez LE. 2003. The Mycobacterium avium subsp. paratuberculosis 35 kDa protein plays a role in invasion of bovine epithelial cells. Microbiology 149:2061–69
    [Google Scholar]
  127. 127.
    Lee K-I, Whang J, Choi H-G, Son Y-J, Jeon HS et al. 2016. Mycobacterium avium MAV2054 protein induces macrophage apoptosis by targeting mitochondria and reduces intracellular bacterial growth. Sci. Rep. 6:37804
    [Google Scholar]
  128. 128.
    Bannantine JP, Radosevich TJ, Stabel JR, Berger S, Griffin JF, Paustian ML. 2007. Production and characterization of monoclonal antibodies against a major membrane protein of Mycobacterium avium subsp. paratuberculosis. Clin. Vaccine Immunol. 14:312–17
    [Google Scholar]
  129. 129.
    Bannantine JP, Bayles DO, Waters WR, Palmer MV, Stabel JR, Paustian ML. 2008. Early antibody response against Mycobacterium avium subspecies paratuberculosis antigens in subclinical cattle. Proteome Sci. 6:5
    [Google Scholar]
  130. 130.
    Li L, Munir S, Bannantine JP, Sreevatsan S, Kanjilal S, Kapur V. 2007. Rapid expression of Mycobacterium avium subsp. paratuberculosis recombinant proteins for antigen discovery. Clin. Vaccine Immunol. 14:102–5
    [Google Scholar]
  131. 131.
    Shin SJ, Yoo HS, McDonough SP, Chang YF. 2004. Comparative antibody response of five recombinant antigens in related to bacterial shedding levels and development of serological diagnosis based on 35 kDa antigen for Mycobacterium avium subsp. paratuberculosis. J. Vet. Sci. 5:111–17
    [Google Scholar]
  132. 132.
    Tilocca B, Soggiu A, Greco V, Piras C, Arrigoni N et al. 2020. Immunoinformatic-based prediction of candidate epitopes for the diagnosis and control of paratuberculosis (Johne's disease). Pathogens 9:705
    [Google Scholar]
  133. 133.
    Li L, Wagner B, Freer H, Schilling M, Bannantine JP et al. 2017. Early detection of Mycobacterium avium subsp. paratuberculosis infection in cattle with multiplex-bead based immunoassays. PLOS ONE 12:e0189783
    [Google Scholar]
  134. 134.
    Abdellrazeq GS, Fry LM, Elnaggar MM, Bannantine JP, Schneider DA et al. 2020. Simultaneous cognate epitope recognition by bovine CD4 and CD8 T cells is essential for primary expansion of antigen-specific cytotoxic T-cells following ex vivo stimulation with a candidate Mycobacterium avium subsp. paratuberculosis peptide vaccine. Vaccine 38:2016–25
    [Google Scholar]
  135. 135.
    Franceschi V, Mahmoud AH, Abdellrazeq GS, Tebaldi G, Macchi F et al. 2019. Capacity to elicit cytotoxic CD8 T cell activity against Mycobacterium avium subsp. paratuberculosis is retained in a vaccine candidate 35 kDa peptide modified for expression in mammalian cells. Front. Immunol. 10:2859
    [Google Scholar]
  136. 136.
    Chomkatekaew C, Boonklang P, Sangphukieo A, Chewapreecha C. 2020. An evolutionary arms race between Burkholderia pseudomallei and host immune system: What do we know?. Front. Microbiol. 11:612568
    [Google Scholar]
  137. 137.
    José RJ, Periselneris JN, Brown JS. 2020. Opportunistic bacterial, viral and fungal infections of the lung. Medicine 48:366–72
    [Google Scholar]
  138. 138.
    Bowman JA, Utter GH. 2020. Evolving strategies to manage Clostridium difficile colitis. J. Gastrointest. Surg. 24:484–91
    [Google Scholar]
  139. 139.
    Harvey PC, Watson M, Hulme S, Jones MA, Lovell M et al. 2011. Salmonella enterica serovar typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect. Immun. 79:4105–21
    [Google Scholar]
  140. 140.
    Klumpp J, Fuchs TM. 2007. Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology 153:1207–20
    [Google Scholar]
  141. 141.
    Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V et al. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. PNAS 108:17480–85
    [Google Scholar]
  142. 142.
    Srikumar S, Fuchs TM. 2011. Ethanolamine utilization contributes to proliferation of Salmonella enterica serovar Typhimurium in food and in nematodes. Appl. Environ. Microbiol. 77:281–90
    [Google Scholar]
  143. 143.
    Pitts AC, Tuck LR, Faulds-Pain A, Lewis RJ, Marles-Wright J. 2012. Structural insight into the Clostridium difficile ethanolamine utilisation microcompartment. PLOS ONE 7:e48360
    [Google Scholar]
  144. 144.
    Maadani A, Fox KA, Mylonakis E, Garsin DA. 2007. Enterococcus faecalis mutations affecting virulence in the Caenorhabditis elegans model host. Infect. Immun. 75:2634–37
    [Google Scholar]
  145. 145.
    Ott SL, Wells SJ, Wagner BA. 1999. Herd-level economic losses associated with Johne's disease on US dairy operations. Prev. Vet. Med. 40:179–92
    [Google Scholar]
  146. 146.
    Rasmussen P, Barkema HW, Mason S, Beaulieu E, Hall DC. 2021. Economic losses due to Johne's disease (paratuberculosis) in dairy cattle. J. Dairy Sci. 104:3123–43
    [Google Scholar]
  147. 147.
    Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. 2016. A new view of the tree of life. Nat. Microbiol. 1:16048
    [Google Scholar]
  148. 148.
    Sekiguchi Y, Ohashi A, Parks DH, Yamauchi T, Tyson GW, Hugenholtz P. 2015. First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking. PeerJ. 3:e740
    [Google Scholar]
  149. 149.
    Holm L. 2020. DALI and the persistence of protein shape. Protein Sci. 29:128–40
    [Google Scholar]
  150. 150.
    Contreras H, Joens MS, McMath LM, Le VP, Tullius MV et al. 2014. Characterization of a Mycobacterium tuberculosis nanocompartment and its potential cargo proteins. J. Biol. Chem. 289:18279–89
    [Google Scholar]
  151. 151.
    Snijder J, Kononova O, Barbu IM, Uetrecht C, Rurup WF et al. 2016. Assembly and mechanical properties of the cargo-free and cargo-loaded bacterial nanocompartment encapsulin. Biomacromolecules 17:2522–29
    [Google Scholar]
  152. 152.
    Rurup WF, Cornelissen JJ, Koay MS. 2015. Recombinant expression and purification of “virus-like” bacterial encapsulin protein cages. Methods Mol. Biol. 1252:61–67
    [Google Scholar]
  153. 153.
    Ross J, Lambert T, Piergentili C, He D, Waldron KJ et al. 2020. Mass spectrometry reveals the assembly pathway of encapsulated ferritins and highlights a dynamic ferroxidase interface. Chem. Commun. 56:3417–20
    [Google Scholar]
  154. 154.
    Piergentili C, Ross J, He D, Gallagher KJ, Stanley WA et al. 2020. Dissecting the structural and functional roles of a putative metal entry site in encapsulated ferritins. J. Biol. Chem. 295:15511–26
    [Google Scholar]
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