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Title: Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi

Abstract

ABSTRACT Brown rot fungi are wood-degrading fungi that employ both oxidative and hydrolytic mechanisms to degrade wood. Hydroxyl radicals that facilitate the oxidative component are powerful nonselective oxidants and are incompatible with hydrolytic enzymes unless they are spatially segregated in wood. Differential gene expression has been implicated in the segregation of these reactions inPostia placenta, but it is unclear if this two-step mechanism varies in other brown rot fungi with different traits and life history strategies that occupy different niches in nature. We employed proteomics to analyze a progression of wood decay on thin wafers, using brown rot fungi with significant taxonomic and niche distances:Serpula lacrymans(Boletales; “dry rot” lumber decay) andGloeophyllum trabeum(order Gloeophyllales; slash, downed wood). Both fungi produced greater oxidoreductase diversity upon wood colonization and greater glycoside hydrolase activity later, consistent with a two-step mechanism. The two fungi invested very differently, however, in terms of growth (infrastructure) versus protein secretion (resource capture), with the ergosterol/extracted protein ratio being 7-fold higher withS. lacrymansthan withG. trabeum. In line with the native substrate associations of these fungi, hemicellulase-specific activities were dominated by mannanase inS. lacrymansand by xylanase inG. trabeum. Consistent with previous observations,S. lacrymansdid not produce glycoside hydrolase 6 (GH6) cellobiohydrolases (CBHs)more » in this study, despite taxonomically belonging to the order Boletales, which is distinguished among brown rot fungi by having CBH genes. This work suggests that distantly related brown rot fungi employ staggered mechanisms to degrade wood, but the underlying strategies vary among taxa. IMPORTANCEWood-degrading fungi are important in forest nutrient cycling and offer promise in biotechnological applications. Brown rot fungi are unique among these fungi in that they use a nonenzymatic oxidative pretreatment before enzymatic carbohydrate hydrolysis, enabling selective removal of carbohydrates from lignin. This capacity has independently evolved multiple times, but it is unclear if different mechanisms underpin similar outcomes. Here, we grew fungi directionally on wood wafers and we found similar two-step mechanisms in taxonomically divergent brown rot fungi. The results, however, revealed strikingly different growth strategies, withS. lacrymansinvesting more in biomass production than secretion of proteins andG. trabeumshowing the opposite pattern, with a high diversity of uncharacterized proteins. The “simplified”S. lacrymanssecretomic system could help narrow gene targets central to oxidative brown rot pretreatments, and a comparison of its distinctions withG. trabeumand other brown rot fungi (e.g.,Postia placenta) might offer similar traction in noncatabolic genes.« less

Authors:
; ;
Publication Date:
Research Org.:
Univ. of Minnesota, Minneapolis, MN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1536859
DOE Contract Number:  
SC0004012; SC0012742
Resource Type:
Journal Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 83; Journal Issue: 7; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
Biotechnology & Applied Microbiology; Microbiology

Citation Formats

Presley, Gerald N., Schilling, Jonathan S., and Löffler, Frank E. Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi. United States: N. p., 2017. Web. doi:10.1128/aem.02987-16.
Presley, Gerald N., Schilling, Jonathan S., & Löffler, Frank E. Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi. United States. doi:10.1128/aem.02987-16.
Presley, Gerald N., Schilling, Jonathan S., and Löffler, Frank E. Fri . "Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi". United States. doi:10.1128/aem.02987-16.
@article{osti_1536859,
title = {Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi},
author = {Presley, Gerald N. and Schilling, Jonathan S. and Löffler, Frank E.},
abstractNote = {ABSTRACT Brown rot fungi are wood-degrading fungi that employ both oxidative and hydrolytic mechanisms to degrade wood. Hydroxyl radicals that facilitate the oxidative component are powerful nonselective oxidants and are incompatible with hydrolytic enzymes unless they are spatially segregated in wood. Differential gene expression has been implicated in the segregation of these reactions inPostia placenta, but it is unclear if this two-step mechanism varies in other brown rot fungi with different traits and life history strategies that occupy different niches in nature. We employed proteomics to analyze a progression of wood decay on thin wafers, using brown rot fungi with significant taxonomic and niche distances:Serpula lacrymans(Boletales; “dry rot” lumber decay) andGloeophyllum trabeum(order Gloeophyllales; slash, downed wood). Both fungi produced greater oxidoreductase diversity upon wood colonization and greater glycoside hydrolase activity later, consistent with a two-step mechanism. The two fungi invested very differently, however, in terms of growth (infrastructure) versus protein secretion (resource capture), with the ergosterol/extracted protein ratio being 7-fold higher withS. lacrymansthan withG. trabeum. In line with the native substrate associations of these fungi, hemicellulase-specific activities were dominated by mannanase inS. lacrymansand by xylanase inG. trabeum. Consistent with previous observations,S. lacrymansdid not produce glycoside hydrolase 6 (GH6) cellobiohydrolases (CBHs) in this study, despite taxonomically belonging to the order Boletales, which is distinguished among brown rot fungi by having CBH genes. This work suggests that distantly related brown rot fungi employ staggered mechanisms to degrade wood, but the underlying strategies vary among taxa. IMPORTANCEWood-degrading fungi are important in forest nutrient cycling and offer promise in biotechnological applications. Brown rot fungi are unique among these fungi in that they use a nonenzymatic oxidative pretreatment before enzymatic carbohydrate hydrolysis, enabling selective removal of carbohydrates from lignin. This capacity has independently evolved multiple times, but it is unclear if different mechanisms underpin similar outcomes. Here, we grew fungi directionally on wood wafers and we found similar two-step mechanisms in taxonomically divergent brown rot fungi. The results, however, revealed strikingly different growth strategies, withS. lacrymansinvesting more in biomass production than secretion of proteins andG. trabeumshowing the opposite pattern, with a high diversity of uncharacterized proteins. The “simplified”S. lacrymanssecretomic system could help narrow gene targets central to oxidative brown rot pretreatments, and a comparison of its distinctions withG. trabeumand other brown rot fungi (e.g.,Postia placenta) might offer similar traction in noncatabolic genes.},
doi = {10.1128/aem.02987-16},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 7,
volume = 83,
place = {United States},
year = {2017},
month = {1}
}