Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>

ABSTRACT Bacteria of the phylum Bacteroidetes are regarded as highly efficient carbohydrate metabolizers, but most species are limited to (semi)soluble glycans. The soil Bacteroidetes species Cytophaga hutchinsonii and Sporocytophaga myxococcoides have long been known as efficient cellulose metaboli...

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Autores principales:	Marcel Taillefer, Magnus Ø. Arntzen, Bernard Henrissat, Phillip B. Pope, Johan Larsbrink
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	carbohydrate-active enzymes cellulase cellulose proteomics soil microbiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/db1266adf3d543838eda652ef0e912bb
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spelling	oai:doaj.org-article:db1266adf3d543838eda652ef0e912bb2021-12-02T18:15:45ZProteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>10.1128/mSystems.00240-182379-5077https://doaj.org/article/db1266adf3d543838eda652ef0e912bb2018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00240-18https://doaj.org/toc/2379-5077ABSTRACT Bacteria of the phylum Bacteroidetes are regarded as highly efficient carbohydrate metabolizers, but most species are limited to (semi)soluble glycans. The soil Bacteroidetes species Cytophaga hutchinsonii and Sporocytophaga myxococcoides have long been known as efficient cellulose metabolizers, but neither species conforms to known cellulolytic mechanisms. Both species require contact with their substrate but do not encode cellulosomal systems of cell surface-attached enzyme complexes or the polysaccharide utilization loci found in many other Bacteroidetes species. Here, we have fractionated the cellular compartments of each species from cultures growing on crystalline cellulose and pectin, respectively, and analyzed them using label-free quantitative proteomics as well as enzymatic activity assays. The combined results enabled us to highlight enzymes likely to be important for cellulose conversion and to infer their cellular localization. The combined proteomes represent a wide array of putative cellulolytic enzymes and indicate specific and yet highly redundant mechanisms for cellulose degradation. Of the putative endoglucanases, especially enzymes of hitherto-unstudied glycoside hydrolase family, 8 were abundant, indicating an overlooked important role during cellulose metabolism. Furthermore, both species generated a large number of abundant hypothetical proteins during cellulose conversion, providing a treasure trove of targets for future enzymology studies. IMPORTANCE Cellulose is the most abundant renewable polymer on earth, but its recalcitrance limits highly efficient conversion methods for energy-related and material applications. Though microbial cellulose conversion has been studied for decades, recent advances showcased that large knowledge gaps still exist. Bacteria of the phylum Bacteroidetes are regarded as highly efficient carbohydrate metabolizers, but most species are limited to (semi)soluble glycans. A few species, including the soil bacteria C. hutchinsonii and S. myxococcoides, are regarded as cellulose specialists, but their cellulolytic mechanisms are not understood, as they do not conform to the current models for enzymatic cellulose turnover. By unraveling the proteome setups of these two bacteria during growth on both crystalline cellulose and pectin, we have taken a significant step forward in understanding their idiosyncratic mode of cellulose conversion. This report provides a plethora of new enzyme targets for improved biomass conversion.Marcel TailleferMagnus Ø. ArntzenBernard HenrissatPhillip B. PopeJohan LarsbrinkAmerican Society for Microbiologyarticlecarbohydrate-active enzymescellulasecelluloseproteomicssoil microbiologyMicrobiologyQR1-502ENmSystems, Vol 3, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbohydrate-active enzymes cellulase cellulose proteomics soil microbiology Microbiology QR1-502
spellingShingle	carbohydrate-active enzymes cellulase cellulose proteomics soil microbiology Microbiology QR1-502 Marcel Taillefer Magnus Ø. Arntzen Bernard Henrissat Phillip B. Pope Johan Larsbrink Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
description	ABSTRACT Bacteria of the phylum Bacteroidetes are regarded as highly efficient carbohydrate metabolizers, but most species are limited to (semi)soluble glycans. The soil Bacteroidetes species Cytophaga hutchinsonii and Sporocytophaga myxococcoides have long been known as efficient cellulose metabolizers, but neither species conforms to known cellulolytic mechanisms. Both species require contact with their substrate but do not encode cellulosomal systems of cell surface-attached enzyme complexes or the polysaccharide utilization loci found in many other Bacteroidetes species. Here, we have fractionated the cellular compartments of each species from cultures growing on crystalline cellulose and pectin, respectively, and analyzed them using label-free quantitative proteomics as well as enzymatic activity assays. The combined results enabled us to highlight enzymes likely to be important for cellulose conversion and to infer their cellular localization. The combined proteomes represent a wide array of putative cellulolytic enzymes and indicate specific and yet highly redundant mechanisms for cellulose degradation. Of the putative endoglucanases, especially enzymes of hitherto-unstudied glycoside hydrolase family, 8 were abundant, indicating an overlooked important role during cellulose metabolism. Furthermore, both species generated a large number of abundant hypothetical proteins during cellulose conversion, providing a treasure trove of targets for future enzymology studies. IMPORTANCE Cellulose is the most abundant renewable polymer on earth, but its recalcitrance limits highly efficient conversion methods for energy-related and material applications. Though microbial cellulose conversion has been studied for decades, recent advances showcased that large knowledge gaps still exist. Bacteria of the phylum Bacteroidetes are regarded as highly efficient carbohydrate metabolizers, but most species are limited to (semi)soluble glycans. A few species, including the soil bacteria C. hutchinsonii and S. myxococcoides, are regarded as cellulose specialists, but their cellulolytic mechanisms are not understood, as they do not conform to the current models for enzymatic cellulose turnover. By unraveling the proteome setups of these two bacteria during growth on both crystalline cellulose and pectin, we have taken a significant step forward in understanding their idiosyncratic mode of cellulose conversion. This report provides a plethora of new enzyme targets for improved biomass conversion.
format	article
author	Marcel Taillefer Magnus Ø. Arntzen Bernard Henrissat Phillip B. Pope Johan Larsbrink
author_facet	Marcel Taillefer Magnus Ø. Arntzen Bernard Henrissat Phillip B. Pope Johan Larsbrink
author_sort	Marcel Taillefer
title	Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
title_short	Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
title_full	Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
title_fullStr	Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
title_full_unstemmed	Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>
title_sort	proteomic dissection of the cellulolytic machineries used by soil-dwelling <italic toggle="yes">bacteroidetes</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/db1266adf3d543838eda652ef0e912bb
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Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling <italic toggle="yes">Bacteroidetes</italic>

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