Origin of fungal biomass degrading enzymes: Evolution, diversity and function of enzymes of early lineage fungi

Lene Lange, Bo Pilgaard, Florian-Alexander Herbst, Peter Kamp Busk, Frank Gleason, Anders Gorm Pedersen

Publikation: Bidrag til tidsskriftReviewForskningpeer review

Resumé

The aim of this study was to elucidate the evolution of enzyme secretome of early lineage fungi to contribute to resolving the basal part of Fungal Kingdom and pave the way for industrial evaluation of their unique enzymes. By combining results of advanced sequence analysis with secretome mass spectrometry and phylogenetic trees, we provide evidence for that plant cell wall degrading enzymes of higher fungi share a common ancestor with enzymes from aerobic ancient fungi. Sequence analysis (HotPep, confirmed by dbCAN-HMM models) enabled prediction of enzyme function directly from sequence. For the first time, oxidative enzymes are described here in early lineage fungi (Chytridiomycota & Cryptomycota), which supports the conceptually new understanding that fungal LPMOs were also present in the early evolution of the Fungal Kingdom. Phylogenetic analysis of fungal AA9 proteins suggests an LPMO-common-ancestor with Ascomycetes and Basidiomycetes and describes a new clade of AA9s. We identified two very strong biomass degraders, Rhizophlyctis rosea (soil-inhabiting) and Neocallimastix californiae (rumen), with a rich spectrum of cellulolytic, xylanolytic and pectinolytic enzymes, characteristically including several different enzymes with the same function. Their secretome composition suggests horizontal gene transfer was involved in transition to terrestrial and rumen habitats. Methods developed for recombinant production and protein characterization of enzymes from zoosporic fungi pave the way for biotechnological exploitation of unique enzymes from early lineage fungi with potential to contribute to improved biomass conversion. The phyla of ancient fungi through evolution have developed to be very different and together they constitute a rich enzyme discovery pool.
OriginalsprogEngelsk
TidsskriftFungal Biology Reviews
Vol/bind33
Udgave nummer1
Sider (fra-til)82-97
Antal sider16
ISSN1749-4613
DOI
StatusUdgivet - jan. 2019

Citer dette

Lange, Lene ; Pilgaard, Bo ; Herbst, Florian-Alexander ; Busk, Peter Kamp ; Gleason, Frank ; Pedersen, Anders Gorm. / Origin of fungal biomass degrading enzymes : Evolution, diversity and function of enzymes of early lineage fungi. I: Fungal Biology Reviews. 2019 ; Bind 33, Nr. 1. s. 82-97.
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Origin of fungal biomass degrading enzymes : Evolution, diversity and function of enzymes of early lineage fungi. / Lange, Lene; Pilgaard, Bo; Herbst, Florian-Alexander; Busk, Peter Kamp; Gleason, Frank; Pedersen, Anders Gorm.

I: Fungal Biology Reviews, Bind 33, Nr. 1, 01.2019, s. 82-97.

Publikation: Bidrag til tidsskriftReviewForskningpeer review

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T1 - Origin of fungal biomass degrading enzymes

T2 - Evolution, diversity and function of enzymes of early lineage fungi

AU - Lange, Lene

AU - Pilgaard, Bo

AU - Herbst, Florian-Alexander

AU - Busk, Peter Kamp

AU - Gleason, Frank

AU - Pedersen, Anders Gorm

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AB - The aim of this study was to elucidate the evolution of enzyme secretome of early lineage fungi to contribute to resolving the basal part of Fungal Kingdom and pave the way for industrial evaluation of their unique enzymes. By combining results of advanced sequence analysis with secretome mass spectrometry and phylogenetic trees, we provide evidence for that plant cell wall degrading enzymes of higher fungi share a common ancestor with enzymes from aerobic ancient fungi. Sequence analysis (HotPep, confirmed by dbCAN-HMM models) enabled prediction of enzyme function directly from sequence. For the first time, oxidative enzymes are described here in early lineage fungi (Chytridiomycota & Cryptomycota), which supports the conceptually new understanding that fungal LPMOs were also present in the early evolution of the Fungal Kingdom. Phylogenetic analysis of fungal AA9 proteins suggests an LPMO-common-ancestor with Ascomycetes and Basidiomycetes and describes a new clade of AA9s. We identified two very strong biomass degraders, Rhizophlyctis rosea (soil-inhabiting) and Neocallimastix californiae (rumen), with a rich spectrum of cellulolytic, xylanolytic and pectinolytic enzymes, characteristically including several different enzymes with the same function. Their secretome composition suggests horizontal gene transfer was involved in transition to terrestrial and rumen habitats. Methods developed for recombinant production and protein characterization of enzymes from zoosporic fungi pave the way for biotechnological exploitation of unique enzymes from early lineage fungi with potential to contribute to improved biomass conversion. The phyla of ancient fungi through evolution have developed to be very different and together they constitute a rich enzyme discovery pool.

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