How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation

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The recent years have witnessed considerable developments in the interpretation of the three-dimensional structures of plant polysaccharide-degrading enzymes in the context of their functional specificity. A plethora of new structures of catalytic, carbohydrate-binding and protein-scaffolding modules involved in (hemi)cellulose catabolism has emerged in harness with sophisticated biochemical analysis. Despite significant advances, a full understanding of the intricacies of substrate recognition and catalysis by these diverse and specialised enzymes remains an important goal, especially if the application potential of these biocatalysts is to be fully realised.

Introduction

A significant amount of attention [1•, 2, 3, 4, 5] is presently focussed on the quest to replace petroleum with plant biomass for chemical and fuel production, widely referred to as the ‘bio-refinery’ concept [6]. Where biomass saccharification followed by microbial fermentation is concerned, polysaccharide-degrading enzymes are of key importance [2]. In this context, the industrial application of enzymes in starch degradation is a mature and fundamentally well-understood technology [7]. Recent attention on the application of enzymes in lignocellulose degradation has almost exclusively centred on improving the efficiency and lowering the production costs of multi-component cellulase mixtures composed of exo-β(1  4)-glucanases and endo-β(1  4)-glucanases (see [8, 9••, 10] for recent comprehensive reviews). This focus has been motivated by the fact that dilute acid treatment at high temperature, one of the most common pre-treatment steps, hydrolyses nearly all of the hemicellulosic and pectic polysaccharides, exposing the recalcitrant para-crystalline cellulose to enzyme attack [9••]. However, dilute acid hydrolysis of hemicellulose produces relatively low yields of the component monosaccharides and slow reaction kinetics, which limit process economics [9••]. Potential applications of other polysaccharide hydrolases to aid in the extraction or hydrolysis of specific non-cellulosic polysaccharides have been largely unexplored. However, these enzymes and their appended non-catalytic carbohydrate-binding modules (CBMs) are likely to become increasingly important in the near future for both the analysis [11••, 12] and breakdown of selected and engineered plants for biofuel production [9••]. Thus, this review will focus on recent advances regarding the structure and function of proteins involved in the degradation of some key hemicelluloses from dicotolydenous and woody plants, namely the xyloglucans (XGs), galactoglucomannans (GGMs) and glucuronoarabinoxylans (GAXs). New developments in the characterisation and application of CBMs and cellulosomes will also be discussed.

Section snippets

Bacteria and fungi: masters of lignocellulose saccharification

Structurally complex and biologically recalcitrant, the plant cell wall and its metabolism are currently poorly understood. In particular, the nanoscale organisation of the component polymers  polysaccharides, polypeptides and polyphenolics  is essentially unknown [13]. Microbes interact with plant cell walls in many contexts, for example, as pathogens, symbionts or saprotrophs, and as a consequence have evolved numerous catalytic strategies to attack wall components, the majority of which are

Enzyme modularity and substrate targeting: CBMs and cellulosomes

Enzyme secretion by plant cell wall degrading micro-organisms can be divided along two lines. The majority secrete mixtures of individual enzymes into their surroundings, many of which possess a multi-modular structure composed of a catalytic module linked to one or more CBMs [15, 18•, 19]. The latter function to improve enzyme efficacy by targeting the catalytic module to surfaces of insoluble substrates [19] and possibly through substrate disruption [20••]. An alternative approach for

Hemicellulose degradation: a diversity of linkages and a multitude of enzymes

Pectins notwithstanding [14, 22], the hemicellulosic polysaccharides present an amazing array of sugars connected by bonds of diverse stereochemistry and regiochemistry. Although many of the CAZyme mechanisms are well established, the past two years have witnessed an impressive amount of effort in the structural analysis of polysaccharidases to elucidate the molecular basis of substrate recognition leading to catalysis. The following sections provide a brief tour of recent advances in the

Future prospects

It is widely established that enzyme access is the major limitation preventing efficient saccharification of the plant cell wall. Indeed, the access problem is the primary reason why the economic viability of lignocellulose-derived biofuels is limited by the cost of enzymes deployed in the process. There is thus an urgent need to discover new, efficient enzymes that display novel activities against the complex matrix polysaccharides for the further refinement of non-chemical methods for plant

References and recommended reading

Papers of particular interest, published within the annual period of the review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Protein representations were created using PyMOL v0.99rc6 (http://pymol.sourceforge.net/). HS thanks the Swedish Research Council (VR), the Swedish Agency for Innovation Systems (VINNOVA) for financial support. HB and HJG acknowledge funding from Formas and the Forestry Commission, respectively, under the WoodWisdom-Net framework. HB is a fellow (Rådsforskare) and grantee of the Swedish Research Council.

References (85)

  • K. Yaoi et al.

    The structural basis for the exo-mode of action in GH74 oligoxyloglucan reducing end-specific cellobiohydrolase

    J Mol Biol

    (2007)
  • Y. Kitago et al.

    Crystal structure of Cel44A, a glycoside hydrolase family 44 endoglucanase from Clostridium thermocellum

    J Biol Chem

    (2007)
  • M. Hrmova et al.

    A barley xyloglucan xyloglucosyl transferase covalently links xyloglucan, cellulosic substrates, and (1,3;1,4)-beta-d-glucans

    J Biol Chem

    (2007)
  • T. Ishimizu et al.

    A novel alpha-1,2-l-fucosidase acting on xyloglucan oligosaccharides is associated with endo-beta-mannosidase

    J Biochem (Tokyo)

    (2007)
  • A.L. Lovering et al.

    Mechanistic and structural analysis of a family 31 alpha-glycosidase and its glycosyl-enzyme intermediate

    J Biol Chem

    (2005)
  • M. Nagae et al.

    Structural basis of the catalytic reaction mechanism of novel 1,2-alpha-l-fucosidase from Bifidobacterium bifidum

    J Biol Chem

    (2007)
  • Y.H.P. Zhang et al.

    Fractionating recalcitrant lignocellulose at modest reaction conditions

    Biotechnol Bioeng

    (2007)
  • J. Lundqvist et al.

    Characterization of galactoglucomannan extracted from spruce (Picea abies) by heat-fractionation at different conditions

    Carbohydr Polym

    (2003)
  • K. Le Nours et al.

    The structure and characterization of a modular endo-beta-1,4-mannanase from Cellulomonas fimi

    Biochemistry

    (2005)
  • V.M. Ducros et al.

    Substrate distortion by a beta-mannanase: snapshots of the Michaelis and covalent-intermediate complexes suggest a B(2,5) conformation for the transition state

    Angew Chem Int Ed Engl

    (2002)
  • Anderson L, Hägglund P, Stoll D, Lo Leggio L, Drakenberg T, Stålbrand H: Kinetics and stereochemistry of the...
  • R. Schröder et al.

    LeMAN4 endo-beta-mannanase from ripe tomato fruit can act as a mannan transglycosylase or hydrolase

    Planta

    (2006)
  • K.M. Cho et al.

    A cel44C-man26A gene of endophytic Paenibacillus polymyxa GS01 has multi-glycosyl hydrolases in two catalytic domains

    Appl Microbiol Biotechnol

    (2006)
  • D.A. Comfort et al.

    Biochemical analysis of Thermotoga maritima GH36 alpha-galactosidase (TmGalA) confirms the mechanistic commonality of clan GH-D glycoside hydrolases

    Biochemistry

    (2007)
  • M.D. Joshi et al.

    Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase

    Biochemistry

    (2001)
  • L.A. van den Broek et al.

    Cloning and characterization of arabinoxylan arabinofuranohydrolase-D3 (AXHd3) from Bifidobacterium adolescentis DSM20083

    Appl Microbiol Biotechnol

    (2005)
  • L.E. Kellett et al.

    Xylanase B and an arabinofuranosidase from Pseudomonas fluorescens subsp. cellulosa contain identical cellulose-binding domains and are encoded by adjacent genes

    Biochem J

    (1990)
  • J.K. Bourne

    Biofuels: boon or boondoggle?

    Natl Geogr

    (2007)
  • C. Schubert

    Can biofuels finally take center stage?

    Nat Biotechnol

    (2006)
  • Anonymous

    Bioenergy centers receive $375 million

    Chem Eng News

    (2007)
  • European Commission

    Energy Research in the 7th Framework Programme

    (2007)
  • E. Kintisch

    Energy research  BP bets big on UC Berkeley for novel biofuels center

    Science

    (2007)
  • A.J. Ragauskas et al.

    The path forward for biofuels and biomaterials

    Science

    (2006)
  • M. van der Maarel et al.

    Properties and applications of starch-converting enzymes of the alpha-amylase family

    J Biotechnol

    (2002)
  • Y.H.P. Zhang et al.

    Outlook for cellulase improvement: screening and selection strategies

    Biotechnol Adv

    (2006)
  • S. Bauer et al.

    Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls

    Proc Natl Acad Sci U S A

    (2006)
  • L. McCartney et al.

    Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers

    Anal Biochem

    (2004)
  • S.Y. Ding et al.

    Versatile derivatives of carbohydrate-binding modules for imaging of complex carbohydrates approaching the molecular level of resolution

    Biotechniques

    (2006)
  • N. Carpita et al.

    The cell wall

  • J. Geisler-Lee et al.

    Poplar carbohydrate-active enzymes. Gene identification and expression analyses

    Plant Physiol

    (2006)
  • G.J. Davies et al.

    Recent structural insights into the expanding world of carbohydrate-active enzymes

    Curr Opin Struct Biol

    (2005)
  • H. Hashimoto

    Recent structural studies of carbohydrate-binding modules

    Cell Mol Life Sci

    (2006)
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