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Title: Genomewide and Enzymatic Analysis Reveals Efficient D-Galacturonic Acid Metabolism in the Basidiomycete Yeast Rhodosporidium toruloides

Journal Article · · mSystems
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [2];  [2]; ORCiD logo [2];  [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [2];  [5]
  1. Univ. of California, Berkeley, CA (United States); Energy Biosciences Inst., Berkeley, CA (United States)
  2. Technische Univ. München, Freising (Germany)
  3. Energy Biosciences Inst., Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Energy Biosciences Inst., Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  5. Univ. of Queensland, Brisbane, QLD (Australia)

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. 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.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; 1330914; OO1605; OO6J01
OSTI ID:
1591856
Journal Information:
mSystems, Vol. 4, Issue 6; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 17 works
Citation information provided by
Web of Science

References (59)

l-galactonate dehydratase is part of the fungal path for d-galacturonic acid catabolism journal August 2006
Cellodextrin Transport in Yeast for Improved Biofuel Production journal September 2010
Metabolic network analysis and experimental study of lipid production in Rhodosporidium toruloides grown on single and mixed substrates journal March 2015
Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species journal May 2014
Identification and characterization of Sulfolobus solfataricusD-gluconate dehydratase: a key enzyme in the non-phosphorylated Entner–Doudoroff pathway journal March 2005
A comparative systems analysis of polysaccharide-elicited responses in Neurospora crassa reveals carbon source-specific cellular adaptations : Fungal polysaccharide-specific responses revealed journal December 2013
Sulfur Amino Acids Regulate Translational Capacity and Metabolic Homeostasis through Modulation of tRNA Thiolation journal July 2013
d-Galacturonic acid catabolism in microorganisms and its biotechnological relevance journal January 2009
RNA interference in the oleaginous yeast Rhodosporidium toruloides journal April 2019
Biological control of postharvest green mold decay of oranges by Rhodotorula glutinis journal October 2004
Lipid production in batch and fed-batch cultures of Rhodosporidium toruloidesfrom 5 and 6 carbon carbohydrates journal May 2012
Gal83 mediates the interaction of the Snf1 kinase complex with the transcription activator Sip4 journal December 1999
Effects of cultivation techniques and media on yields and morphology of the basidiomycete Armillaria mellea journal August 1987
tRNA thiolation links translation to stress responses in Saccharomyces cerevisiae journal January 2015
Functional genomics of lipid metabolism in the oleaginous yeast Rhodosporidium toruloides journal March 2018
Transcriptional activators Cat8 and Sip4 discriminate between sequence variants of the carbon source-responsive promoter element in the yeast Saccharomyces cerevisiae journal March 2004
Identification and characterization of a galacturonic acid transporter from Neurospora crassa and its application for Saccharomyces cerevisiae fermentation processes journal January 2014
Glycerol metabolism and transport in yeast and fungi: established knowledge and ambiguities: Glycerol catabolism in yeast journal January 2017
Pectin-rich biomass as feedstock for fuel ethanol production journal June 2012
Carotenoids production by the yeast Rhodotorula mucilaginosa: Use of agricultural wastes as a carbon source journal September 2005
The Engineering Potential of Rhodosporidium toruloides as a Workhorse for Biotechnological Applications journal March 2018
The Transporter Classification Database: recent advances journal January 2009
An extremely thermostable aldolase from Sulfolobus solfataricus with specificity for non-phosphorylated substrates journal October 1999
An NADP+-dependent glycerol dehydrogenase in Aspergillus nidulans is inducible by D-galacturonate journal October 1992
The importance of the glycerol 3-phosphate shuttle during aerobic growth ofSaccharomyces cerevisiae journal March 1998
The transcriptional activator GaaR of Aspergillus niger is required for release and utilization of d- galacturonic acid from pectin journal May 2016
Multiplexed CRISPR-Cas9-Based Genome Editing of Rhodosporidium toruloides journal March 2019
An extremely thermostable aldolase from Sulfolobus solfataricus with specificity for non-phosphorylated substrates journal November 1999
Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status journal October 2006
Identification in the Mold Hypocrea jecorina of the First Fungal d -Galacturonic Acid Reductase journal August 2005
Glycerol catabolism in Aspergillus nidulans journal March 1991
Enzymes for the NADPH-dependent reduction of dihydroxyacetone and D-glyceraldehyde and L-glyceraldehyde in the mould Hypocrea jecorina journal September 2006
Rhodosporidium toruloides: a new platform organism for conversion of lignocellulose into terpene biofuels and bioproducts journal October 2017
The Transporter Classification Database (TCDB): recent advances journal November 2015
The Pfam protein families database: towards a more sustainable future journal December 2015
De Novo Assembly and Genome Analyses of the Marine-Derived Scopulariopsis brevicaulis Strain LF580 Unravels Life-Style Traits and Anticancerous Scopularide Biosynthetic Gene Cluster journal October 2015
Analysis Tool Web Services from the EMBL-EBI journal May 2013
The Transporter Classification Database journal November 2013
Yeast interactions and wine flavour journal September 2003
Engineering Saccharomyces cerevisiae for co-utilization of d-galacturonic acid and d-glucose from citrus peel waste journal November 2018
Evolving Views of Pectin Biosynthesis journal April 2013
Bioaerosol in Composting Facilities: Occupational Health Risk Assessment journal September 2009
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
The Missing Link in the Fungal D-Galacturonate Pathway: IDENTIFICATION OF THE L-THREO-3-DEOXY-HEXULOSONATE ALDOLASE journal July 2007
Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown journal August 2016
The EMBL-EBI bioinformatics web and programmatic tools framework journal April 2015
TCDB: the Transporter Classification Database for membrane transport protein analyses and information journal January 2006
A novel Zn 2 Cys 6 transcription factor BcGaaR regulates D-galacturonic acid utilization in B otrytis cinerea : BcGaaR regulates GalA utilization in journal January 2016
An evolutionary conserved d-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation journal November 2008
Galacturonic Acid Inhibits the Growth of Saccharomyces cerevisiae on Galactose, Xylose, and Arabinose journal May 2012
A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides journal January 2012
Monoterpene production by the carotenogenic yeast Rhodosporidium toruloides journal March 2019
Pectin structure and biosynthesis journal June 2008
The sole introduction of two single-point mutations establishes glycerol utilization in Saccharomyces cerevisiae CEN.PK derivatives journal January 2017
Apple Pomace: A Versatile Substrate for Biotechnological Applications journal January 2008
Bioaerosols from composting facilities—a review journal April 2014
Some Pink Yeasts Associated with Softening of Olives journal November 1969
Metabolic network analysis and experimental study of lipid production in Rhodosporidium toruloides grown on single and mixed substrates text January 2015
Bioaerosol in Composting Facilities : Occupational Health Risk Assessment journal January 2008