The Biochemistry and Structural Biology of Plant Cell Wall Deconstruction

Gilbert, Harry J.

doi:10.1104/pp.110.156646

Cited by 283 publications

(211 citation statements)

References 118 publications

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“…Does it feature genes devoted to the utilization of plant biomass? The enzymology of plant polysaccharide decomposition has been very thoroughly studied (Gilbert, 2010). So, what is necessary is to scan the Geobacillus dispensable genomes for genes encoding known enzymes for hydrolysis, uptake, and utilization of these polysaccharides and their components.…”

Section: Lessons From Genomesmentioning

confidence: 99%

The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?

2014

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The genus Geobacillus comprises endospore-forming obligate thermophiles. These bacteria have been isolated from cool soils and even cold ocean sediments in anomalously high numbers, given that the ambient temperatures are significantly below their minimum requirement for growth. Geobacilli are active in environments such as hot plant composts, however, and examination of their genome sequences reveals that they are endowed with a battery of sensors, transporters and enzymes dedicated to hydrolysing plant polysaccharides. Although they appear to be relatively minor members of the plant biomass-degrading microbial community, Geobacillus bacteria have achieved a significant population with a worldwide distribution, probably in large part due to adaptive features of their spores. First, their morphology and resistance properties enable them to be mobilized in the atmosphere and transported long distances. Second, their longevity, which in theory may be extreme, enables them to lie quiescent but viable for long periods of time, accumulating gradually over time to achieve surprisingly high population densities. Introduction: an environmental enigmaGeobacillus bacteria are rod-shaped, aerobic or facultatively anaerobic, endospore-forming microbes. Depending on the strain, the temperature range for growth can extend as low as 35 u C or as high as 80 u C. But for most isolates, temperatures between about 45 and 70 u C are required (Nazina et al., 2001). These characteristics make Geobacillus bacteria (geobacilli) attractive to the biotechnology industry as sources of thermostable enzymes (de Champdoré et al., 2007; Karagüler et al., 2007), as platforms for biofuel production (Cripps et al., 2009;Taylor et al., 2009) and as potential components of bioremediation strategies (Markossian et al., 2000;Obojska et al., 2002;Perfumo et al., 2007). Obligate thermophiles, however, face a significant challenge outside the lab: they must survive on a planet with an average annual land surface temperature that has only ranged between 7 and 10 uC over the past three centuries (Rohde et al., 2013). It would be logical to assume, then, that Geobacillus would only be found in substantial numbers in the warmest regions of the planet, such as equatorial deserts or naturally occurring geothermal and hydrothermal hotspots. The truth, however, is rather more complicated.As Fig. 1 illustrates, people have been able to detect Geobacillus nearly everywhere they have thought to look. (This figure is based on a survey of 146 mostly recent references describing the isolation of Geobacillus in natural or human-made environments; for full details, see Table S1, available in Microbiology Online.) One can see at a glance that these bacteria have been isolated from sources on all seven continents as well as the Pacific Ocean and the Mediterranean Sea. What may not be obvious from a twodimensional map is that there has been much diversity in the third dimension as well. Geobacillus has been isolated from the Bolivian Andes at an altitude of 3653 m (Ma...

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Section: Lessons From Genomesmentioning

confidence: 99%

The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?

2014

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“…C ellulose is the most abundant natural product in the biosphere 1 , with plant cell walls representing the most important source, where it serves as a structural component 2 . During plant growth, the cell wall needs to be remodelled involving controlled degradation of cellulose by cellulolytic enzymes 2 .…”

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“…During plant growth, the cell wall needs to be remodelled involving controlled degradation of cellulose by cellulolytic enzymes 2 . Many other organisms, preferring a heterotrophic lifestyle, also express cellulases.…”

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Cellulose degradation and assimilation by the unicellular phototrophic eukaryote Chlamydomonas reinhardtii

et al. 2012

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“…Thus, the side chains in xylan must be removed by arabinofuranosidases, esterases, and glucuronidases before the xylan backbone can be hydrolyzed by endo-acting xylanases (see ref. 2 …”

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confidence: 99%

“…The plant cell wall contains a large number of chemically complex polysaccharides (1), exemplified by xylans, which are polymers of β-1,4-xylopyranose (Xylp) residues that are extensively decorated with O2-and/or O3-linked arabinofuranose (Araf), O2-linked uronic acids and acetyl groups at either O2 or O3. In common with many polysaccharides in the plant cell wall, the decorations of the main chain of xylans hinder the access of enzymes to the backbone structures of this polymer (2). Thus, the side chains in xylan must be removed by arabinofuranosidases, esterases, and glucuronidases before the xylan backbone can be hydrolyzed by endo-acting xylanases (see ref.…”

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confidence: 99%

Introducing endo-xylanase activity into an exo-acting arabinofuranosidase that targets side chains

McKee

Peña

Rogowski

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The degradation of the plant cell wall by glycoside hydrolases is central to environmentally sustainable industries. The major polysaccharides of the plant cell wall are cellulose and xylan, a highly decorated β-1,4-xylopyranose polymer. Glycoside hydrolases displaying multiple catalytic functions may simplify the enzymes required to degrade plant cell walls, increasing the industrial potential of these composite structures. Here we test the hypothesis that glycoside hydrolase family 43 (GH43) provides a suitable scaffold for introducing additional catalytic functions into enzymes that target complex structures in the plant cell wall. We report the crystal structure of Humicola insolens AXHd3 (HiAXHd3), a GH43 arabinofuranosidase that hydrolyses O3-linked arabinose of doubly substituted xylans, a feature of the polysaccharide that is recalcitrant to degradation. HiAXHd3 displays an N-terminal five-bladed β-propeller domain and a C-terminal β-sandwich domain. The interface between the domains comprises a xylan binding cleft that houses the active site pocket. Substrate specificity is conferred by a shallow arabinose binding pocket adjacent to the deep active site pocket, and through the orientation of the xylan backbone. Modification of the rim of the active site introduces endo-xylanase activity, whereas the resultant enzyme variant, Y166A, retains arabinofuranosidase activity. These data show that the active site of HiAXHd3 is tuned to hydrolyse arabinofuranosyl or xylosyl linkages, and it is the topology of the distal regions of the substrate binding surface that confers specificity. This report demonstrates that GH43 provides a platform for generating bespoke multifunctional enzymes that target industrially significant complex substrates, exemplified by the plant cell wall. biofuels | biotechnology | protein engineering | structural biology

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The Biochemistry and Structural Biology of Plant Cell Wall Deconstruction

Cited by 283 publications

References 118 publications

The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?

The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?

Cellulose degradation and assimilation by the unicellular phototrophic eukaryote Chlamydomonas reinhardtii

Introducing endo-xylanase activity into an exo-acting arabinofuranosidase that targets side chains

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