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 -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 upregulated during growth on cellulose medium were putative iron reductases, quinone reductase, and structurally divergent oxidases potentially involved in extracellular generation of Fe(II) and H2O2. These observations are consistent with a biodegradative role for Fenton chemistry in which Fe(II) and H2O2 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.cellulose ͉ fenton ͉ lignin ͉ cellulase ͉ brown-rot
Efficient lignin depolymerization is unique to the wood decay basidiomycetes, collectively referred to as white rot fungi.
Phanerochaete chrysosporium
simultaneously degrades lignin and cellulose, whereas the closely related species,
Ceriporiopsis subvermispora,
also depolymerizes lignin but may do so with relatively little cellulose degradation. To investigate the basis for selective ligninolysis, we conducted comparative genome analysis of
C. subvermispora
and
P. chrysosporium
. Genes encoding manganese peroxidase numbered 13 and five in
C. subvermispora
and
P. chrysosporium
, respectively. In addition, the
C. subvermispora
genome contains at least seven genes predicted to encode laccases, whereas the
P. chrysosporium
genome contains none. We also observed expansion of the number of
C. subvermispora
desaturase-encoding genes putatively involved in lipid metabolism. Microarray-based transcriptome analysis showed substantial up-regulation of several desaturase and MnP genes in wood-containing medium. MS identified MnP proteins in
C. subvermispora
culture filtrates, but none in
P. chrysosporium
cultures. These results support the importance of MnP and a lignin degradation mechanism whereby cleavage of the dominant nonphenolic structures is mediated by lipid peroxidation products. Two
C. subvermispora
genes were predicted to encode peroxidases structurally similar to
P. chrysosporium
lignin peroxidase and, following heterologous expression in
Escherichia coli
, the enzymes were shown to oxidize high redox potential substrates, but not Mn
2+
. Apart from oxidative lignin degradation, we also examined cellulolytic and hemicellulolytic systems in both fungi. In summary, the
C. subvermispora
genetic inventory and expression patterns exhibit increased oxidoreductase potential and diminished cellulolytic capability relative to
P. chrysosporium
.
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