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Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion.

ABSTRACT: Brown-rot fungi such as Postia placenta are common inhabitants of forest ecosystems and are also largely responsible for the destructive decay of wooden structures. Rapid depolymerization of cellulose is a distinguishing feature of brown-rot, but the biochemical mechanisms and underlying genetics are poorly understood. Systematic examination of the P. placenta genome, transcriptome, and secretome revealed unique extracellular enzyme systems, including an unusual repertoire of extracellular glycoside hydrolases. Genes encoding exocellobiohydrolases and cellulose-binding domains, typical of cellulolytic microbes, are absent in this efficient cellulose-degrading fungus. When P. placenta was grown in medium containing cellulose as sole carbon source, transcripts corresponding to many hemicellulases and to a single putative beta-1-4 endoglucanase were expressed at high levels relative to glucose-grown cultures. These transcript profiles were confirmed by direct identification of peptides by liquid chromatography-tandem mass spectrometry (LC-MS/MS). Also up-regulated during growth on cellulose medium were putative iron reductases, quinone reductase, and structurally divergent oxidases potentially involved in extracellular generation of Fe(II) and H(2)O(2). These observations are consistent with a biodegradative role for Fenton chemistry in which Fe(II) and H(2)O(2) react to form hydroxyl radicals, highly reactive oxidants capable of depolymerizing cellulose. The P. placenta genome resources provide unparalleled opportunities for investigating such unusual mechanisms of cellulose conversion. More broadly, the genome offers insight into the diversification of lignocellulose degrading mechanisms in fungi. Comparisons with the closely related white-rot fungus Phanerochaete chrysosporium support an evolutionary shift from white-rot to brown-rot during which the capacity for efficient depolymerization of lignin was lost.

SUBMITTER: Martinez D

PROVIDER: S-EPMC2644145 | biostudies-literature | 2009 Feb

REPOSITORIES: biostudies-literature

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Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion.

Martinez Diego D Challacombe Jean J Morgenstern Ingo I Hibbett David D Schmoll Monika M Kubicek Christian P CP Ferreira Patricia P Ruiz-Duenas Francisco J FJ Martinez Angel T AT Kersten Phil P Hammel Kenneth E KE Vanden Wymelenberg Amber A Gaskell Jill J Lindquist Erika E Sabat Grzegorz G Bondurant Sandra Splinter SS Larrondo Luis F LF Canessa Paulo P Vicuna Rafael R Yadav Jagjit J Doddapaneni Harshavardhan H Subramanian Venkataramanan V Pisabarro Antonio G AG Lavín José L JL Oguiza José A JA Master Emma E Henrissat Bernard B Coutinho Pedro M PM Harris Paul P Magnuson Jon Karl JK Baker Scott E SE Bruno Kenneth K Kenealy William W Hoegger Patrik J PJ Kües Ursula U Ramaiya Preethi P Lucas Susan S Salamov Asaf A Shapiro Harris H Tu Hank H Chee Christine L CL Misra Monica M Xie Gary G Teter Sarah S Yaver Debbie D James Tim T Mokrejs Martin M Pospisek Martin M Grigoriev Igor V IV Brettin Thomas T Rokhsar Dan D Berka Randy R Cullen Dan D

Proceedings of the National Academy of Sciences of the United States of America 20090204 6

Brown-rot fungi such as Postia placenta are common inhabitants of forest ecosystems and are also largely responsible for the destructive decay of wooden structures. Rapid depolymerization of cellulose is a distinguishing feature of brown-rot, but the biochemical mechanisms and underlying genetics are poorly understood. Systematic examination of the P. placenta genome, transcriptome, and secretome revealed unique extracellular enzyme systems, including an unusual repertoire of extracellular glyco ...[more]

PMID: 19193860

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Project description:UnlabelledIdentification of the specific genes and enzymes involved in the fungal degradation of lignocellulosic biomass derived from feedstocks with various compositions is essential to the development of improved bioenergy processes. In order to elucidate the effect of substrate composition on gene expression in wood-rotting fungi, we employed microarrays based on the annotated genomes of the brown- and white-rot fungi, Rhodonia placenta (formerly Postia placenta) and Phanerochaete chrysosporium, respectively. We monitored the expression of genes involved in the enzymatic deconstruction of the cell walls of three 4-year-old Populus trichocarpa (poplar) trees of genotypes with distinct cell wall chemistries, selected from a population of several hundred trees grown in a common garden. The woody substrates were incubated with wood decay fungi for 10, 20, and 30 days. An analysis of transcript abundance in all pairwise comparisons highlighted 64 and 84 differentially expressed genes (>2-fold, P < 0.05) in P. chrysosporium and P. placenta, respectively. Cross-fungal comparisons also revealed an array of highly differentially expressed genes (>4-fold, P < 0.01) across different substrates and time points. These results clearly demonstrate that gene expression profiles of P. chrysosporium and P. placenta are influenced by wood substrate composition and the duration of incubation. Many of the significantly expressed genes encode "proteins of unknown function," and determining their role in lignocellulose degradation presents opportunities and challenges for future research.ImportanceThis study describes the variation in expression patterns of two wood-degrading fungi (brown- and white-rot fungi) during colonization and incubation on three different naturally occurring poplar substrates of differing chemical compositions, over time. The results clearly show that the two fungi respond differentially to their substrates and that several known and, more interestingly, currently unknown genes are highly misregulated in response to various substrate compositions. These findings highlight the need to characterize several unknown proteins for catalytic function but also as potential candidate proteins to improve the efficiency of enzymatic cocktails to degrade lignocellulosic substrates in industrial applications, such as in a biochemically based bioenergy platform.

Project description:Wood-degrading brown rot fungi are essential recyclers of plant biomass in forest ecosystems. Their efficient cellulolytic systems, which have potential biotechnological applications, apparently depend on a combination of two mechanisms: lignocellulose oxidation by reactive oxygen species (ROS) and polysaccharide hydrolysis by a limited set of glycoside hydrolases (GHs). Given that ROS are strongly oxidizing and non-selective, these two steps are likely segregated. A common hypothesis has been that brown rot fungi use a concentration gradient of chelated metal ions to confine ROS generation inside wood cell walls before enzymes can infiltrate. We examined an alternative: that lignocellulose-oxidation (LOX) components involved in ROS production are differentially expressed by brown rot fungi ahead of GH components. We used spatial mapping to resolve a temporal sequence in Postia placenta, sectioning thin wood wafers colonized directionally. Among sections, we measured gene expression by whole transcriptome sequencing (RNAseq) and assayed relevant enzyme activities. We found a marked pattern of LOX upregulation in a narrow (5-mm; 48-hr) zone at the hyphal front, which included many genes likely involved in ROS generation. Upregulation of GH5 endoglucanases and many other GHs clearly occurred later, behind the hyphal front, with notable exceptions of two likely expansins and a GH28 pectinase. Our results support a staggered mechanism for brown rot that is controlled by differential expression rather than microenvironmental gradients. This mechanism likely results in an oxidative pretreatment of lignocellulose, possibly facilitated by expansin- and pectinase-assisted cell wall swelling, before cellulases and hemicellulases are deployed for polysaccharide depolymerization. We sequenced mRNA from 9 Postia placenta samples taken from 3 wood sections of wafer design, with 3 bioreplicates for each wood section, to compare the gene expression during brown rot processes. Three wood sections of the wafer are representing early to late decay stages.

Dataset Information

Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion.

Publications

Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion.

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