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Characterization of a cellulosome dockerin domain from the anaerobic fungus Piromyces equi.

Raghothama S, Eberhardt RY, Simpson P, Wigelsworth D, White P, Hazlewood GP, Nagy T, Gilbert HJ, Williamson MP
Nat Struct Biol 8 775-8 (2001)
Cited: 28 times
EuropePMC logo PMID: 11524680

Abstract

The recycling of photosynthetically fixed carbon in plant cell walls is a key microbial process. In anaerobes, the degradation is carried out by a high molecular weight multifunctional complex termed the cellulosome. This consists of a number of independent enzyme components, each of which contains a conserved dockerin domain, which functions to bind the enzyme to a cohesin domain within the protein scaffoldin protein. Here we describe the first three-dimensional structure of a fungal dockerin, the N-terminal dockerin of Cel45A from the anaerobic fungus Piromyces equi. The structure contains a novel fold of 42 residues. The ligand binding site consists of residues Trp 35, Tyr 8 and Asp 23, which are conserved in all fungal dockerins. The binding site is on the opposite side of the N- and C-termini of the molecule, implying that tandem dockerin domains, seen in the majority of anaerobic fungal plant cell wall degrading enzymes, could present multiple simultaneous binding sites and, therefore, permit tailoring of binding to catalytic demands.

Articles - 1e8p mentioned but not cited (1)

  1. Search for allosteric disulfide bonds in NMR structures. Schmidt B, Hogg PJ. BMC Struct. Biol. 7 49 (2007)


Reviews citing this publication (6)

  1. Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Fontes CM, Gilbert HJ. Annu. Rev. Biochem. 79 655-681 (2010)
  2. Noncellulosomal cohesin- and dockerin-like modules in the three domains of life. Peer A, Smith SP, Bayer EA, Lamed R, Borovok I. FEMS Microbiol. Lett. 291 1-16 (2009)
  3. Anaerobic gut fungi: Advances in isolation, culture, and cellulolytic enzyme discovery for biofuel production. Haitjema CH, Solomon KV, Henske JK, Theodorou MK, O'Malley MA. Biotechnol. Bioeng. 111 1471-1482 (2014)
  4. Driving biomass breakdown through engineered cellulosomes. Gilmore SP, Henske JK, O'Malley MA. Bioengineered 6 204-208 (2015)
  5. Fungal protein production: design and production of chimeric proteins. Punt PJ, Levasseur A, Visser H, Wery J, Record E. Annu. Rev. Microbiol. 65 57-69 (2011)
  6. Cellulosomes: Highly Efficient Cellulolytic Complexes. Alves VD, Fontes CMGA, Bule P. Subcell Biochem 96 323-354 (2021)

Articles citing this publication (21)

  1. The genome of the anaerobic fungus Orpinomyces sp. strain C1A reveals the unique evolutionary history of a remarkable plant biomass degrader. Youssef NH, Couger MB, Struchtemeyer CG, Liggenstoffer AS, Prade RA, Najar FZ, Atiyeh HK, Wilkins MR, Elshahed MS. Appl. Environ. Microbiol. 79 4620-4634 (2013)
  2. Phylogenetic diversity and community structure of anaerobic gut fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores. Liggenstoffer AS, Youssef NH, Couger MB, Elshahed MS. ISME J 4 1225-1235 (2010)
  3. Unconventional mode of attachment of the Ruminococcus flavefaciens cellulosome to the cell surface. Rincon MT, Cepeljnik T, Martin JC, Lamed R, Barak Y, Bayer EA, Flint HJ. J. Bacteriol. 187 7569-7578 (2005)
  4. Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Solomon KV, Haitjema CH, Henske JK, Gilmore SP, Borges-Rivera D, Lipzen A, Brewer HM, Purvine SO, Wright AT, Theodorou MK, Grigoriev IV, Regev A, Thompson DA, O'Malley MA. Science 351 1192-1195 (2016)
  5. Structural classification of small, disulfide-rich protein domains. Cheek S, Krishna SS, Grishin NV. J. Mol. Biol. 359 215-237 (2006)
  6. Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in the cow rumen. Dai X, Tian Y, Li J, Luo Y, Liu D, Zheng H, Wang J, Dong Z, Hu S, Huang L. Appl. Environ. Microbiol. 81 1375-1386 (2015)
  7. Incorporation of fungal cellulases in bacterial minicellulosomes yields viable, synergistically acting cellulolytic complexes. Mingardon F, Chanal A, López-Contreras AM, Dray C, Bayer EA, Fierobe HP. Appl. Environ. Microbiol. 73 3822-3832 (2007)
  8. beta-Glucosidase in cellulosome of the anaerobic fungus Piromyces sp. strain E2 is a family 3 glycoside hydrolase. Steenbakkers PJ, Harhangi HR, Bosscher MW, van der Hooft MM, Keltjens JT, van der Drift C, Vogels GD, op den Camp HJ. Biochem. J. 370 963-970 (2003)
  9. Characterization of a double dockerin from the cellulosome of the anaerobic fungus Piromyces equi. Nagy T, Tunnicliffe RB, Higgins LD, Walters C, Gilbert HJ, Williamson MP. J. Mol. Biol. 373 612-622 (2007)
  10. Transcriptomic analysis of lignocellulosic biomass degradation by the anaerobic fungal isolate Orpinomyces sp. strain C1A. Couger MB, Youssef NH, Struchtemeyer CG, Liggenstoffer AS, Elshahed MS. Biotechnol Biofuels 8 208 (2015)
  11. A parts list for fungal cellulosomes revealed by comparative genomics. Haitjema CH, Gilmore SP, Henske JK, Solomon KV, de Groot R, Kuo A, Mondo SJ, Salamov AA, LaButti K, Zhao Z, Chiniquy J, Barry K, Brewer HM, Purvine SO, Wright AT, Hainaut M, Boxma B, van Alen T, Hackstein JHP, Henrissat B, Baker SE, Grigoriev IV, O'Malley MA. Nat Microbiol 2 17087 (2017)
  12. An intron-containing glycoside hydrolase family 9 cellulase gene encodes the dominant 90 kDa component of the cellulosome of the anaerobic fungus Piromyces sp. strain E2. Steenbakkers PJ, Ubhayasekera W, Goossen HJ, van Lierop EM, van der Drift C, Vogels GD, Mowbray SL, Op den Camp HJ. Biochem. J. 365 193-204 (2002)
  13. Application of microbial genes to recalcitrant biomass utilization and environmental conservation. Ohmiya K, Sakka K, Kimura T, Morimoto K. J. Biosci. Bioeng. 95 549-561 (2003)
  14. A serpin in the cellulosome of the anaerobic fungus Piromyces sp. strain E2. Steenbakkers PJ, Irving JA, Harhangi HR, Swinkels WJ, Akhmanova A, Dijkerman R, Jetten MS, van der Drift C, Whisstock JC, Op den Camp HJ. Mycol. Res. 112 999-1006 (2008)
  15. Designing chimeric enzymes inspired by fungal cellulosomes. Gilmore SP, Lillington SP, Haitjema CH, de Groot R, O'Malley MA. Synth Syst Biotechnol 5 23-32 (2020)
  16. Designing novel cellulase systems through agent-based modeling and global sensitivity analysis. Apte AA, Senger RS, Fong SS. Bioengineered 5 243-253 (2014)
  17. Cellulosome Localization Patterns Vary across Life Stages of Anaerobic Fungi. Lillington SP, Chrisler W, Haitjema CH, Gilmore SP, Smallwood CR, Shutthanandan V, Evans JE, O'Malley MA. mBio 12 e0083221 (2021)
  18. Combinatorial assembly and optimisation of designer cellulosomes: a galactomannan case study. Vanderstraeten J, da Fonseca MJM, De Groote P, Grimon D, Gerstmans H, Kahn A, Moraïs S, Bayer EA, Briers Y. Biotechnol Biofuels Bioprod 15 60 (2022)
  19. Enhanced features of Dictyoglomus turgidum Cellulase A engineered with carbohydrate binding module 11 from Clostridium thermocellum. Cattaneo C, Cesaro P, Spertino S, Icardi S, Cavaletto M. Sci Rep 8 4402 (2018)
  20. Structure and enzymatic characterization of CelD endoglucanase from the anaerobic fungus Piromyces finnis. Dementiev A, Lillington SP, Jin S, Kim Y, Jedrzejczak R, Michalska K, Joachimiak A, O'Malley MA. Appl Microbiol Biotechnol 107 5999-6011 (2023)
  21. Two-site recognition of Staphylococcus aureus peptidoglycan by lysostaphin SH3b. Gonzalez-Delgado LS, Walters-Morgan H, Salamaga B, Robertson AJ, Hounslow AM, Jagielska E, Sabała I, Williamson MP, Lovering AL, Mesnage S. Nat. Chem. Biol. 16 24-30 (2020)


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