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Cellular and Molecular Life Sciences

, Volume 73, Issue 14, pp 2809–2819 | Cite as

Starch-degrading polysaccharide monooxygenases

  • Van V. Vu
  • Michael A. MarlettaEmail author
Multi-author review

Abstract

Polysaccharide degradation by hydrolytic enzymes glycoside hydrolases (GHs) is well known. More recently, polysaccharide monooxygenases (PMOs, also known as lytic PMOs or LPMOs) were found to oxidatively degrade various polysaccharides via a copper-dependent hydroxylation. PMOs were previously thought to be either GHs or carbohydrate binding modules (CBMs), and have been re-classified in carbohydrate active enzymes (CAZY) database as auxiliary activity (AA) families. These enzymes include cellulose-active fungal PMOs (AA9, formerly GH61), chitin- and cellulose-active bacterial PMOs (AA10, formerly CBM33), and chitin-active fungal PMOs (AA11). These PMOs significantly boost the activity of GHs under industrially relevant conditions, and thus have great potential in the biomass-based biofuel industry. PMOs that act on starch are the latest PMOs discovered (AA13), which has expanded our perspectives in PMOs studies and starch degradation. Starch-active PMOs have many common structural features and biochemical properties of the PMO superfamily, yet differ from other PMO families in several important aspects. These differences likely correlate, at least in part, to the differences in primary and higher order structures of starch and cellulose, and chitin. In this review we will discuss the discovery, structural features, biochemical and biophysical properties, and possible biological functions of starch-active PMOs, as well as their potential application in the biofuel, food, and other starch-based industries. Important questions regarding various aspects of starch-active PMOs and possible economical driving force for their future studies will also be highlighted.

Keywords

Starch degradation Biofuels Polysaccharide monooxygenases Copper enzymes Auxiliary activity family 13 Plant pathogens 

Abbreviations

AA

Auxiliary activity

CDH

Cellobiose dehydrogenase

GH

Glycoside hydrolase

CBM

Carbohydrate binding modules

LPMOs

Lytic polysaccharide monooxygenases

PMOs

Polysaccharide monooxygenases

XAS

X-ray absorption spectroscopy

XRD

X-ray diffraction

Notes

Acknowledgments

Financial support to M.A.M from the Energy Bioscience Institute (UC Berkeley) and the NSF (CHE 1411538) is gratefully acknowledged. V.V.V was supported by a grant from Nguyen Tat Thanh University, Ho Chi Minh, Vietnam. We thank Dr. John Hangasky for his advice and editorial help.

References

  1. 1.
    Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, Eijsink VG (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222. doi: 10.1126/science.1192231 CrossRefPubMedGoogle Scholar
  2. 2.
    Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49:3305–3316. doi: 10.1021/bi100009p CrossRefPubMedGoogle Scholar
  3. 3.
    Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JC, Johansen KS, Krogh KB, Jørgensen CI, Tovborg M, Anthonsen A, Tryfona T, Walter CP, Dupree P, Xu F, Davies GJ, Walton PH (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA 108:15079–15084. doi: 10.1073/pnas.1105776108 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Phillips CM, Beeson WT, Cate JHD, Marletta MA (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6:1399–1406. doi: 10.1021/cb200351y CrossRefPubMedGoogle Scholar
  5. 5.
    Beeson WT, Phillips CM, Cate JHD, Marletta MA (2012) Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc 134:890–892. doi: 10.1021/ja210657t CrossRefPubMedGoogle Scholar
  6. 6.
    Horn S, Vaaje-Kolstad G, Westereng B, Eijsink VGH (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45–56CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Dimarogona M, Topakas E, Christakopoulos P (2013) Recalcitrant polysaccharide degradation by novel oxidative biocatalysts. Appl Microbiol Biotechnol 97:8455–8465CrossRefPubMedGoogle Scholar
  8. 8.
    Hemsworth GR, Davies GJ, Walton PH (2013) Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr Opin Chem Biol 23:660–668Google Scholar
  9. 9.
    Hemsworth GR, Henrissat B, Davies GJ, Walton PH (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol 10:122–126CrossRefPubMedGoogle Scholar
  10. 10.
    Vu VV, Beeson WT, Span EA, Farquhar ER, Marletta MA (2014) A family of starch-active polysaccharide monooxygenases. Proc Natl Acad Sci USA 111:13822–13827. doi: 10.1073/pnas.1408090111 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Lo Leggio L, Simmons TJ, Poulsen JC, Frandsen KE, Hemsworth GR, Stringer MA, von Freiesleben P, Tovborg M, Johansen KS, De Maria L, Harris PV, Soong CL, Dupree P, Tryfona T, Lenfant N, Henrissat B, Davies GJ, Walton PH (2015) Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat Commun 6:5961. doi: 10.1038/ncomms6961 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Beeson WT, Vu VV, Span EA, Phillips CM, Marletta MA (2015) Cellulose degradation by polysaccharide monooxygenases. Annu Rev Biochem 84:923–946. doi: 10.1146/annurev-biochem-060614-034439 CrossRefPubMedGoogle Scholar
  13. 13.
    Hemsworth GR, Johnston EM, Davies GJ, Walton PH (2015) Lytic polysaccharide monooxygenases in biomass conversion. Trends Biotechnol 33:747–761. doi: 10.1016/j.tibtech.2015.09.006 CrossRefPubMedGoogle Scholar
  14. 14.
    Aachmann FL, Vaaje-Kolstad G, Forsberg Z, Røhr Å, Eijsink VHG, Sørlie M (2015) Lytic polysaccharide monooxygenase. Encyclopedia of Inorganic and Bioinorganic Chemistry. Wiley, New YorkGoogle Scholar
  15. 15.
    Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41. doi: 10.1186/1754-6834-6-41 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Vu VV, Beeson WT, Phillips CM, Cate JH, Marletta MA (2014) Determinants of regioselective hydroxylation in the fungal polysaccharide monooxygenases. J Am Chem Soc 136:562–565. doi: 10.1021/ja409384b CrossRefPubMedGoogle Scholar
  17. 17.
    Westereng B, Cannella D, Wittrup Agger J, Jørgensen H, Larsen Andersen M, Eijsink VG, Felby C (2015) Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Sci Rep 5:18561. doi: 10.1038/srep18561 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Zamocky M, Ludwig R, Peterbauer C, Hallberg BM, Divne C, Nicholls P, Halltrich D (2006) Cellobiose dehydrogenase—a flavocytochrome from wood-degrading, phytopathogenic and saprotropic fungi. Curr Protein Pep Sci 7:255–280. doi: 10.2174/138920306777452367 CrossRefGoogle Scholar
  19. 19.
    Forsberg Z, Mackenzie AK, Sørlie M, Røhr ÅK, Helland R, Arvai AS, Vaaje-Kolstad G, Eijsink VG (2014) Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci USA 111:8446–8451. doi: 10.1073/pnas.1402771111 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kim S, Ståhlberg J, Sandgren M, Paton RS, Beckham GT (2014) Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism. Proc Natl Acad Sci USA 111:149–154. doi: 10.1073/pnas.1316609111 CrossRefPubMedGoogle Scholar
  21. 21.
    Wu M, Beckham GT, Larsson AM, Ishida T, Kim S, Payne CM, Himmel ME, Crowley MF, Horn SJ, Westereng B, Igarashi K, Samejima M, Ståhlberg J, Eijsink VG, Sandgren M (2013) Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the basidiomycota fungus Phanerochaete chrysosporium. J Biol Chem 288:12828–12839. doi: 10.1074/jbc.M113.459396 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Whittaker JW (2003) Free radical catalysis by galactose oxidase. Chem Rev 103:2347–2364. doi: 10.1021/cr020425z CrossRefPubMedGoogle Scholar
  23. 23.
    Glass NL, Schmoll M, Cate JHD, Coradetti S (2013) Plant cell wall deconstruction by Ascomycete fungi. Annu Rev Microbiol 67:477–498. doi: 10.1146/annurev-micro-092611-150044 CrossRefPubMedGoogle Scholar
  24. 24.
    Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JH, Glass NL (2009) Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci USA 106:22157–22162. doi: 10.1073/pnas.0906810106 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Bennati-Granier C, Garajova S, Champion C, Grisel S, Haon M, Zhou S, Fanuel M, Ropartz D, Rogniaux H, Gimbert I, Record E, Berrin JG (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8:90CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Isaksen T, Westereng B, Aachmann FL, Agger JW, Kracher D, Kittl R, Ludwig R, Haltrich D, Eijsink VG, Horn SJ (2013) A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem 289:2632–2642. doi: 10.1074/jbc.M113.530196 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Agger JW, Isaksen T, Várnai A, Vidal-Melgosa S, Willats WG, Ludwig R, Horn SJ, Eijsink VG, Westereng B (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci USA 111:6287–6292. doi: 10.1073/pnas.1323629111 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Borisova AS, Isaksen T, Dimarogona M, Kognole AA, Mathiesen G, Várnai A, Røhr ÅK, Payne CM, Sørlie M, Sandgren M, Eijsink VG (2015) Structural and functional characterization of a lytic polysaccharide monooxygenase with broad substrate specificity. J Biol Chem 290:22955–22969. doi: 10.1074/jbc.M115.660183 CrossRefPubMedGoogle Scholar
  29. 29.
    Frommhagen M, Sforza S, Westphal AH, Visser J, Hinz SW, Koetsier MJ, van Berkel WJ, Gruppen H, Kabel MA (2015) Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels 8:101. doi: 10.1186/s13068-015-0284-1 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pérez S, Bertoft E (2010) The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch/Stärke 62:389–420. doi: 10.1002/star.201000013 CrossRefGoogle Scholar
  31. 31.
    Ubbink J, Burbidge A, Mezzenga R (2008) Food structure and functionality: a soft matter perspective. Soft Matter 4:1569–1581. doi: 10.1039/B802183J CrossRefGoogle Scholar
  32. 32.
    Harris P, Wogulis M (2010) Polypeptides having amylolytic enhancing activity and polynucleotides encoding same. Patent No: WO/2010/059413 (2010)Google Scholar
  33. 33.
    Ishikawa K, Nakatani H, Katsuya Y, Fukusawa C (2007) Kinetic and structural analysis of enzyme sliding on a substrate: multiple attack in β-amylase. Biochemistry 46:792–798. doi: 10.1021/bi061605w CrossRefPubMedGoogle Scholar
  34. 34.
    Tessema M, Csöregi E, Ruzgas T, Kenausis G, Solomon T, Gorton L (1997) Oligosaccharide dehydrogenase-modified graphite electrodes for the amperometric determination of sugars in a flow injection system. Anal Chem 69:4039–4044CrossRefPubMedGoogle Scholar
  35. 35.
    Kobayashi Y, Horikoshi K (1980) Purification and properties of NAD+-dependent maltose dehydrogenase produced by alkalophilic Corynebacterium sp. No. 93-1. Biochim Biophys Acta 614:256–265CrossRefPubMedGoogle Scholar
  36. 36.
    Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. doi: 10.1111/j.1364-3703.2011.00783.x CrossRefPubMedGoogle Scholar
  37. 37.
    Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ (2012) Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8:e1002514. doi: 10.1371/journal.ppat.1002514 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Marin-Navarro J, Polaina J (2011) Glucoamylases: structural and biotechnological aspects. Appl Microbiol Biotechnol 89:1267–1273CrossRefPubMedGoogle Scholar
  39. 39.
    Berry CS (1986) Resistant starch: formation and measurement of starch that survives exhaustive digestion with amylolytic enzymes during the determination of dietary fibre. J Cereal Sci 4:301–314. doi: 10.1016/S0733-5210(86)80034-0 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.NTT Hi-Tech Institute (NHTI)Nguyen Tat Thanh UniversityHo Chi Minh CityVietnam
  2. 2.Department of Chemistry and Department of Molecular & Cell BiologyUniversity of California, BerkeleyBerkeleyUSA

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