Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>

ABSTRACT Biorefining of renewable feedstocks is one of the most promising routes to replace fossil-based products. Since many common fermentation hosts, such as Saccharomyces cerevisiae, are naturally unable to convert many component plant cell wall polysaccharides, the identification of organisms w...

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Autores principales:	Ryan J. Protzko, Christina A. Hach, Samuel T. Coradetti, Magdalena A. Hackhofer, Sonja Magosch, Nils Thieme, Gina M. Geiselman, Adam P. Arkin, Jeffrey M. Skerker, John E. Dueber, J. Philipp Benz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Rhodosporidium toruloides aerobic catabolism carbon metabolism galacturonic acid yeasts Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0782c0bc15c5451dab0198f2593c74c0
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spelling	oai:doaj.org-article:0782c0bc15c5451dab0198f2593c74c02021-12-02T19:47:38ZGenomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>10.1128/mSystems.00389-192379-5077https://doaj.org/article/0782c0bc15c5451dab0198f2593c74c02019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00389-19https://doaj.org/toc/2379-5077ABSTRACT Biorefining of renewable feedstocks is one of the most promising routes to replace fossil-based products. Since many common fermentation hosts, such as Saccharomyces cerevisiae, are naturally unable to convert many component plant cell wall polysaccharides, the identification of organisms with broad catabolism capabilities represents an opportunity to expand the range of substrates used in fermentation biorefinery approaches. The red basidiomycete yeast Rhodosporidium toruloides is a promising and robust host for lipid- and terpene-derived chemicals. Previous studies demonstrated assimilation of a range of substrates, from C5/C6 sugars to aromatic molecules similar to lignin monomers. In the current study, we analyzed the potential of R. toruloides to assimilate d-galacturonic acid, a major sugar in many pectin-rich agricultural waste streams, including sugar beet pulp and citrus peels. d-Galacturonic acid is not a preferred substrate for many fungi, but its metabolism was found to be on par with those of d-glucose and d-xylose in R. toruloides. A genomewide analysis by combined transcriptome sequencing (RNA-seq) and RB-TDNA-seq revealed those genes with high relevance for fitness on d-galacturonic acid. While R. toruloides was found to utilize the nonphosphorylative catabolic pathway known from ascomycetes, the maximal velocities of several enzymes exceeded those previously reported. In addition, an efficient downstream glycerol catabolism and a novel transcription factor were found to be important for d-galacturonic acid utilization. These results set the basis for use of R. toruloides as a potential host for pectin-rich waste conversions and demonstrate its suitability as a model for metabolic studies with basidiomycetes. IMPORTANCE The switch from the traditional fossil-based industry to a green and sustainable bioeconomy demands the complete utilization of renewable feedstocks. Many currently used bioconversion hosts are unable to utilize major components of plant biomass, warranting the identification of microorganisms with broader catabolic capacity and characterization of their unique biochemical pathways. d-Galacturonic acid is a plant component of bioconversion interest and is the major backbone sugar of pectin, a plant cell wall polysaccharide abundant in soft and young plant tissues. The red basidiomycete and oleaginous yeast Rhodosporidium toruloides has been previously shown to utilize a range of sugars and aromatic molecules. Using state-of-the-art functional genomic methods and physiological and biochemical assays, we elucidated the molecular basis underlying the efficient metabolism of d-galacturonic acid. This study identified an efficient pathway for uronic acid conversion to guide future engineering efforts and represents the first detailed metabolic analysis of pectin metabolism in a basidiomycete fungus.Ryan J. ProtzkoChristina A. HachSamuel T. CoradettiMagdalena A. HackhoferSonja MagoschNils ThiemeGina M. GeiselmanAdam P. ArkinJeffrey M. SkerkerJohn E. DueberJ. Philipp BenzAmerican Society for MicrobiologyarticleRhodosporidium toruloidesaerobic catabolismcarbon metabolismgalacturonic acidyeastsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Rhodosporidium toruloides aerobic catabolism carbon metabolism galacturonic acid yeasts Microbiology QR1-502
spellingShingle	Rhodosporidium toruloides aerobic catabolism carbon metabolism galacturonic acid yeasts Microbiology QR1-502 Ryan J. Protzko Christina A. Hach Samuel T. Coradetti Magdalena A. Hackhofer Sonja Magosch Nils Thieme Gina M. Geiselman Adam P. Arkin Jeffrey M. Skerker John E. Dueber J. Philipp Benz Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
description	ABSTRACT Biorefining of renewable feedstocks is one of the most promising routes to replace fossil-based products. Since many common fermentation hosts, such as Saccharomyces cerevisiae, are naturally unable to convert many component plant cell wall polysaccharides, the identification of organisms with broad catabolism capabilities represents an opportunity to expand the range of substrates used in fermentation biorefinery approaches. The red basidiomycete yeast Rhodosporidium toruloides is a promising and robust host for lipid- and terpene-derived chemicals. Previous studies demonstrated assimilation of a range of substrates, from C5/C6 sugars to aromatic molecules similar to lignin monomers. In the current study, we analyzed the potential of R. toruloides to assimilate d-galacturonic acid, a major sugar in many pectin-rich agricultural waste streams, including sugar beet pulp and citrus peels. d-Galacturonic acid is not a preferred substrate for many fungi, but its metabolism was found to be on par with those of d-glucose and d-xylose in R. toruloides. A genomewide analysis by combined transcriptome sequencing (RNA-seq) and RB-TDNA-seq revealed those genes with high relevance for fitness on d-galacturonic acid. While R. toruloides was found to utilize the nonphosphorylative catabolic pathway known from ascomycetes, the maximal velocities of several enzymes exceeded those previously reported. In addition, an efficient downstream glycerol catabolism and a novel transcription factor were found to be important for d-galacturonic acid utilization. These results set the basis for use of R. toruloides as a potential host for pectin-rich waste conversions and demonstrate its suitability as a model for metabolic studies with basidiomycetes. IMPORTANCE The switch from the traditional fossil-based industry to a green and sustainable bioeconomy demands the complete utilization of renewable feedstocks. Many currently used bioconversion hosts are unable to utilize major components of plant biomass, warranting the identification of microorganisms with broader catabolic capacity and characterization of their unique biochemical pathways. d-Galacturonic acid is a plant component of bioconversion interest and is the major backbone sugar of pectin, a plant cell wall polysaccharide abundant in soft and young plant tissues. The red basidiomycete and oleaginous yeast Rhodosporidium toruloides has been previously shown to utilize a range of sugars and aromatic molecules. Using state-of-the-art functional genomic methods and physiological and biochemical assays, we elucidated the molecular basis underlying the efficient metabolism of d-galacturonic acid. This study identified an efficient pathway for uronic acid conversion to guide future engineering efforts and represents the first detailed metabolic analysis of pectin metabolism in a basidiomycete fungus.
format	article
author	Ryan J. Protzko Christina A. Hach Samuel T. Coradetti Magdalena A. Hackhofer Sonja Magosch Nils Thieme Gina M. Geiselman Adam P. Arkin Jeffrey M. Skerker John E. Dueber J. Philipp Benz
author_facet	Ryan J. Protzko Christina A. Hach Samuel T. Coradetti Magdalena A. Hackhofer Sonja Magosch Nils Thieme Gina M. Geiselman Adam P. Arkin Jeffrey M. Skerker John E. Dueber J. Philipp Benz
author_sort	Ryan J. Protzko
title	Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
title_short	Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
title_full	Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
title_fullStr	Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
title_full_unstemmed	Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>
title_sort	genomewide and enzymatic analysis reveals efficient <sc>d</sc>-galacturonic acid metabolism in the basidiomycete yeast <named-content content-type="genus-species">rhodosporidium toruloides</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0782c0bc15c5451dab0198f2593c74c0
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Genomewide and Enzymatic Analysis Reveals Efficient <sc>d</sc>-Galacturonic Acid Metabolism in the Basidiomycete Yeast <named-content content-type="genus-species">Rhodosporidium toruloides</named-content>

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