Title: Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta

Abstract

The fungi that cause brown rot of wood are essential contributors to biomass recycling in forest ecosystems. Their highly efficient cellulolytic systems, which may have practical applications, apparently depend on a combination of two mechanisms: nonselective oxidation of the lignocellulose by reactive oxygen species (ROS) coupled with hydrolysis of the polysaccharide components by a limited set of glycoside hydrolases (GHs). Since the production of strongly oxidizing ROS appears incompatible with the operation of GHs, it has been proposed that the fungi regulate ROS production by maintaining concentration gradients of the chelated metal ions they use to generate extracellular oxidants. However, calculations have indicated that this protective mechanism is physically infeasible. We examined a different hypothesis, that expression of ROS and GH components is temporally staggered by brown rot fungi in wood. We sectioned thin wafers of spruce and aspen that had been colonized directionally by Postia placenta and measured expression of relevant genes and some of the encoded enzymes, thus using the spatial distribution of fungal hyphae to resolve a fine-scale temporal sequence. Hierarchical clustering of gene expression for eight oxidoreductases thought to have a role in ROS production and of eight GHs revealed a zone of oxidoreductase upregulation atmore » the hyphal front that persisted about 48 h before upregulation of the GHs. Additional evidence for differential expression was provided by localization of endoglucanase, xylanase, mannanase, and laccase activities in the colonized wood. Our results support a two-step mechanism for brown rot, in which substrate oxidation precedes enzymatic hydrolysis.« less

Authors:

Zhang, Jiwei; Presley, Gerald N.; Hammel, Kenneth E. ;

• Search DOE PAGES for author "Hammel, Kenneth E."
• Search DOE PAGES for ORCID "0000-0002-2935-5847"

Ryu, Jae-San; Menke, Jon R.; Figueroa, Melania; Hu, Dehong ;

• Search DOE PAGES for author "Hu, Dehong"
• Search DOE PAGES for ORCID "0000-0002-3974-2963"

Orr, Galya; Schilling, Jonathan S.

Publication Date:

Mon Sep 12 00:00:00 EDT 2016

Research Org.:

Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Org.:

USDOE

OSTI Identifier:

1324321

Alternate Identifier(s):

OSTI ID: 1340881

Report Number(s):

PNNL-SA-114266
Journal ID: ISSN 0027-8424

Grant/Contract Number:  

Early Career Grant SC0004012; BER SC0012742; User Facility grant #48607 at PNNL; AC05-76RL01830

Resource Type:

Published Article

Journal Name:

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

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 113 Journal Issue: 39; Journal ID: ISSN 0027-8424

Publisher:

National Academy of Sciences, Washington, DC (United States)

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Gene; wood decay; brown rot fungus; Postia placenta; biomass; Environmental Molecular Sciences Laboratory; biodegradation; bioconversion; decomposition; lignocellulose; cellulase