The secretome of Agaricus bisporus: Temporal dynamics of plant polysaccharides and lignin degradation

Katharina Duran; Joris Magnin; Antoine H P America; Mao Peng; Roelant Hilgers; Ronald P de Vries; Johan J P Baars; Willem J H van Berkel; Thomas W Kuyper; Mirjam A Kabel

doi:10.1016/j.isci.2023.107087

The secretome of Agaricus bisporus: Temporal dynamics of plant polysaccharides and lignin degradation

Katharina Duran
, Joris Magnin
, Antoine H P America
, Mao Peng
, Roelant Hilgers
, Ronald P de Vries
, Johan J P Baars
, Willem J H van Berkel
, Thomas W Kuyper
, Mirjam A Kabel^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Despite substantial lignocellulose conversion during mycelial growth, previous transcriptome and proteome studies have not yet revealed how secretomes from the edible mushroom Agaricus bisporus develop and whether they modify lignin models in vitro. To clarify these aspects, A. bisporus secretomes collected throughout a 15-day industrial substrate production and from axenic lab-cultures were subjected to proteomics, and tested on polysaccharides and lignin models. Secretomes (day 6-15) comprised A. bisporus endo-acting and substituent-removing glycoside hydrolases, whereas β-xylosidase and glucosidase activities gradually decreased. Laccases appeared from day 6 onwards. From day 10 onwards, many oxidoreductases were found, with numerous multicopper oxidases (MCO), aryl alcohol oxidases (AAO), glyoxal oxidases (GLOX), a manganese peroxidase (MnP), and unspecific peroxygenases (UPO). Secretomes modified dimeric lignin models, thereby catalyzing syringylglycerol-β-guaiacyl ether (SBG) cleavage, guaiacylglycerol-β-guaiacyl ether (GBG) polymerization, and non-phenolic veratrylglycerol-β-guaiacyl ether (VBG) oxidation. We explored A. bisporus secretomes and insights obtained can help to better understand biomass valorization.

Original language	English
Article number	107087
Pages (from-to)	1-22
Number of pages	22
Journal	iScience
Volume	26
Issue number	7
DOIs	https://doi.org/10.1016/j.isci.2023.107087
Publication status	Published - 21 Jul 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s)

Funding

We thank Arend van Peer for kindly providing A. bisporus strain A15. This research received funding from The Netherlands Organisation for Scientific Research (NWO) by an NWO Graduate School Green Top Sector grant ( GSGT.GSGT. 2018.0 18 ), which is conducted in collaboration with CNC Grondstoffen and IsoLife. We thank Arend van Peer for kindly providing A. bisporus strain A15. This research received funding from The Netherlands Organisation for Scientific Research (NWO) by an NWO Graduate School Green Top Sector grant (GSGT.GSGT. 2018.0 18), which is conducted in collaboration with CNC Grondstoffen and IsoLife. Investigation, K.D. and J.M.; Data curation, K.D. A.H.P.A. and M.P.; Formal analysis, K.D. M.A.K. W.J.H.vB. and A.H.P.A.; Methodology, K.D. R.P.dV. T.W.K, J.J.P.B. and M.A.K.; Software, K.D. Validation, R.H. Visualization, K.D.; Supervision, M.A.K. T.W.K, and W.J.H.vB.; Writing – original draft, K.D. and M.A.K.; Writing - review and editing, M.A.K. T.W.K. R.P.dV. R.H. W.J.H.vB.: Conceptualization, K.D. T.W.K. J.J.P.B. and M.A.K. The authors declare no competing interests.

Funders	Funder number
Arend van Peer
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	2018.0 18

Keywords

Biomass
Biotechnology
Microbiology

Access to Document

10.1016/j.isci.2023.107087Licence: CC BY

PIIS2589004223011641Final published version, 4.06 MBLicence: CC BY

Cite this

@article{576da1d22eac4fdd918883e6358102b9,

title = "The secretome of Agaricus bisporus: Temporal dynamics of plant polysaccharides and lignin degradation",

abstract = "Despite substantial lignocellulose conversion during mycelial growth, previous transcriptome and proteome studies have not yet revealed how secretomes from the edible mushroom Agaricus bisporus develop and whether they modify lignin models in vitro. To clarify these aspects, A. bisporus secretomes collected throughout a 15-day industrial substrate production and from axenic lab-cultures were subjected to proteomics, and tested on polysaccharides and lignin models. Secretomes (day 6-15) comprised A. bisporus endo-acting and substituent-removing glycoside hydrolases, whereas β-xylosidase and glucosidase activities gradually decreased. Laccases appeared from day 6 onwards. From day 10 onwards, many oxidoreductases were found, with numerous multicopper oxidases (MCO), aryl alcohol oxidases (AAO), glyoxal oxidases (GLOX), a manganese peroxidase (MnP), and unspecific peroxygenases (UPO). Secretomes modified dimeric lignin models, thereby catalyzing syringylglycerol-β-guaiacyl ether (SBG) cleavage, guaiacylglycerol-β-guaiacyl ether (GBG) polymerization, and non-phenolic veratrylglycerol-β-guaiacyl ether (VBG) oxidation. We explored A. bisporus secretomes and insights obtained can help to better understand biomass valorization.",

keywords = "Biomass, Biotechnology, Microbiology",

author = "Katharina Duran and Joris Magnin and America, \{Antoine H P\} and Mao Peng and Roelant Hilgers and \{de Vries\}, \{Ronald P\} and Baars, \{Johan J P\} and \{van Berkel\}, \{Willem J H\} and Kuyper, \{Thomas W\} and Kabel, \{Mirjam A\}",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = jul,

day = "21",

doi = "10.1016/j.isci.2023.107087",

language = "English",

volume = "26",

pages = "1--22",

journal = "iScience",

issn = "2589-0042",

publisher = "Elsevier Inc.",

number = "7",

}

TY - JOUR

T1 - The secretome of Agaricus bisporus

T2 - Temporal dynamics of plant polysaccharides and lignin degradation

AU - Duran, Katharina

AU - Magnin, Joris

AU - America, Antoine H P

AU - Peng, Mao

AU - Hilgers, Roelant

AU - de Vries, Ronald P

AU - Baars, Johan J P

AU - van Berkel, Willem J H

AU - Kuyper, Thomas W

AU - Kabel, Mirjam A

PY - 2023/7/21

Y1 - 2023/7/21

N2 - Despite substantial lignocellulose conversion during mycelial growth, previous transcriptome and proteome studies have not yet revealed how secretomes from the edible mushroom Agaricus bisporus develop and whether they modify lignin models in vitro. To clarify these aspects, A. bisporus secretomes collected throughout a 15-day industrial substrate production and from axenic lab-cultures were subjected to proteomics, and tested on polysaccharides and lignin models. Secretomes (day 6-15) comprised A. bisporus endo-acting and substituent-removing glycoside hydrolases, whereas β-xylosidase and glucosidase activities gradually decreased. Laccases appeared from day 6 onwards. From day 10 onwards, many oxidoreductases were found, with numerous multicopper oxidases (MCO), aryl alcohol oxidases (AAO), glyoxal oxidases (GLOX), a manganese peroxidase (MnP), and unspecific peroxygenases (UPO). Secretomes modified dimeric lignin models, thereby catalyzing syringylglycerol-β-guaiacyl ether (SBG) cleavage, guaiacylglycerol-β-guaiacyl ether (GBG) polymerization, and non-phenolic veratrylglycerol-β-guaiacyl ether (VBG) oxidation. We explored A. bisporus secretomes and insights obtained can help to better understand biomass valorization.

AB - Despite substantial lignocellulose conversion during mycelial growth, previous transcriptome and proteome studies have not yet revealed how secretomes from the edible mushroom Agaricus bisporus develop and whether they modify lignin models in vitro. To clarify these aspects, A. bisporus secretomes collected throughout a 15-day industrial substrate production and from axenic lab-cultures were subjected to proteomics, and tested on polysaccharides and lignin models. Secretomes (day 6-15) comprised A. bisporus endo-acting and substituent-removing glycoside hydrolases, whereas β-xylosidase and glucosidase activities gradually decreased. Laccases appeared from day 6 onwards. From day 10 onwards, many oxidoreductases were found, with numerous multicopper oxidases (MCO), aryl alcohol oxidases (AAO), glyoxal oxidases (GLOX), a manganese peroxidase (MnP), and unspecific peroxygenases (UPO). Secretomes modified dimeric lignin models, thereby catalyzing syringylglycerol-β-guaiacyl ether (SBG) cleavage, guaiacylglycerol-β-guaiacyl ether (GBG) polymerization, and non-phenolic veratrylglycerol-β-guaiacyl ether (VBG) oxidation. We explored A. bisporus secretomes and insights obtained can help to better understand biomass valorization.

KW - Biomass

KW - Biotechnology

KW - Microbiology

UR - https://www.scopus.com/pages/publications/85163157509

U2 - 10.1016/j.isci.2023.107087

DO - 10.1016/j.isci.2023.107087

M3 - Article

C2 - 37426348

SN - 2589-0042

VL - 26

SP - 1

EP - 22

JO - iScience

JF - iScience

IS - 7

M1 - 107087

ER -

The secretome of Agaricus bisporus: Temporal dynamics of plant polysaccharides and lignin degradation

Abstract

Bibliographical note

Funding

Keywords

Access to Document

Other files and links

Fingerprint

Cite this