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Title: Multi-Omics Driven Metabolic Network Reconstruction and Analysis of Lignocellulosic Carbon Utilization in Rhodosporidium toruloides

Abstract

An oleaginous yeast Rhodosporidium toruloides is a promising host for converting lignocellulosic biomass to bioproducts and biofuels. In this work, we performed multi-omics analysis of lignocellulosic carbon utilization in R. toruloides and reconstructed the genome-scale metabolic network of R. toruloides. High-quality metabolic network models for model organisms and orthologous protein mapping were used to build a draft metabolic network reconstruction. The reconstruction was manually curated to build a metabolic model using functional annotation and multi-omics data including transcriptomics, proteomics, metabolomics, and RB-TDNA sequencing. The multi-omics data and metabolic model were used to investigate R. toruloides metabolism including lipid accumulation and lignocellulosic carbon utilization. The developed metabolic model was validated against high-throughput growth phenotyping and gene fitness data, and further refined to resolve the inconsistencies between prediction and data. We believe that this is the most complete and accurate metabolic network model available for R. toruloides to date.

Authors:
 [1];  [2];  [3];  [3];  [4];  [3];  [3];  [5];  [3];  [1];  [6];  [7];  [8];  [1]
+ Show Author Affiliations
  1. USDOE Agile BioFoundry, Emeryville, CA (United States); USDOE Joint BioEnergy Institute, Emeryville, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. USDOE Agile BioFoundry, Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  3. USDOE Agile BioFoundry, Emeryville, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  4. USDOE Joint BioEnergy Institute, Emeryville, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  6. USDOE Agile BioFoundry, Emeryville, CA (United States); USDOE Joint BioEnergy Institute, Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of California, Berkeley, CA (United States)
  8. USDOE Agile BioFoundry, Emeryville, CA (United States); USDOE Joint BioEnergy Institute, Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1798736
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2296-4185
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; Rhodosporidium toruloides; multi-omics; metabolic networks; genome-scale models; lignocellulosic biomass

Citation Formats

Kim, Joonhoon, Coradetti, Samuel T., Kim, Young-Mo, Gao, Yuqian, Yaegashi, Junko, Zucker, Jeremy D., Munoz, Nathalie, Zink, Erika M., Burnum-Johnson, Kristin E., Baker, Scott E., Simmons, Blake A., Skerker, Jeffrey M., Gladden, John M., and Magnuson, Jon K. Multi-Omics Driven Metabolic Network Reconstruction and Analysis of Lignocellulosic Carbon Utilization in Rhodosporidium toruloides. United States: N. p., 2021. Web. doi:10.3389/fbioe.2020.612832.
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Kim, Joonhoon, Coradetti, Samuel T., Kim, Young-Mo, Gao, Yuqian, Yaegashi, Junko, Zucker, Jeremy D., Munoz, Nathalie, Zink, Erika M., Burnum-Johnson, Kristin E., Baker, Scott E., Simmons, Blake A., Skerker, Jeffrey M., Gladden, John M., & Magnuson, Jon K. Multi-Omics Driven Metabolic Network Reconstruction and Analysis of Lignocellulosic Carbon Utilization in Rhodosporidium toruloides. United States. https://doi.org/10.3389/fbioe.2020.612832
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Kim, Joonhoon, Coradetti, Samuel T., Kim, Young-Mo, Gao, Yuqian, Yaegashi, Junko, Zucker, Jeremy D., Munoz, Nathalie, Zink, Erika M., Burnum-Johnson, Kristin E., Baker, Scott E., Simmons, Blake A., Skerker, Jeffrey M., Gladden, John M., and Magnuson, Jon K. Fri . "Multi-Omics Driven Metabolic Network Reconstruction and Analysis of Lignocellulosic Carbon Utilization in Rhodosporidium toruloides". United States. https://doi.org/10.3389/fbioe.2020.612832. https://www.osti.gov/servlets/purl/1798736.
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@article{osti_1798736,
title = {Multi-Omics Driven Metabolic Network Reconstruction and Analysis of Lignocellulosic Carbon Utilization in Rhodosporidium toruloides},
author = {Kim, Joonhoon and Coradetti, Samuel T. and Kim, Young-Mo and Gao, Yuqian and Yaegashi, Junko and Zucker, Jeremy D. and Munoz, Nathalie and Zink, Erika M. and Burnum-Johnson, Kristin E. and Baker, Scott E. and Simmons, Blake A. and Skerker, Jeffrey M. and Gladden, John M. and Magnuson, Jon K.},
abstractNote = {An oleaginous yeast Rhodosporidium toruloides is a promising host for converting lignocellulosic biomass to bioproducts and biofuels. In this work, we performed multi-omics analysis of lignocellulosic carbon utilization in R. toruloides and reconstructed the genome-scale metabolic network of R. toruloides. High-quality metabolic network models for model organisms and orthologous protein mapping were used to build a draft metabolic network reconstruction. The reconstruction was manually curated to build a metabolic model using functional annotation and multi-omics data including transcriptomics, proteomics, metabolomics, and RB-TDNA sequencing. The multi-omics data and metabolic model were used to investigate R. toruloides metabolism including lipid accumulation and lignocellulosic carbon utilization. The developed metabolic model was validated against high-throughput growth phenotyping and gene fitness data, and further refined to resolve the inconsistencies between prediction and data. We believe that this is the most complete and accurate metabolic network model available for R. toruloides to date.},
doi = {10.3389/fbioe.2020.612832},
journal = {Frontiers in Bioengineering and Biotechnology},
number = ,
volume = 8,
place = {United States},
year = {Fri Jan 08 00:00:00 EST 2021},
month = {Fri Jan 08 00:00:00 EST 2021}
}
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https://doi.org/10.3389/fbioe.2020.612832
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Works referenced in this record:

Metabolic network analysis and experimental study of lipid production in Rhodosporidium toruloides grown on single and mixed substrates
journal, March 2015

  • Bommareddy, Rajesh Reddy; Sabra, Wael; Maheshwari, Garima
  • Microbial Cell Factories, Vol. 14, Issue 1
  • DOI: 10.1186/s12934-015-0217-5

LIQUID: an-open source software for identifying lipids in LC-MS/MS-based lipidomics data
journal, January 2017

BOFdat: Generating biomass objective functions for genome-scale metabolic models from experimental data
journal, April 2019

  • Lachance, Jean-Christophe; Lloyd, Colton J.; Monk, Jonathan M.
  • PLOS Computational Biology, Vol. 15, Issue 4
  • DOI: 10.1371/journal.pcbi.1006971

FIMO: scanning for occurrences of a given motif
journal, February 2011

ATP citrate lyase mediated cytosolic acetyl-CoA biosynthesis increases mevalonate production in Saccharomyces cerevisiae
journal, March 2016

BiGG Models: A platform for integrating, standardizing and sharing genome-scale models
journal, October 2015

  • King, Zachary A.; Lu, Justin; Dräger, Andreas
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1049

Connecting extracellular metabolomic measurements to intracellular flux states in yeast
journal, January 2009

  • Mo, Monica L.; Palsson, Bernhard Ø; Herrgård, Markus J.
  • BMC Systems Biology, Vol. 3, Issue 1
  • DOI: 10.1186/1752-0509-3-37

C/N ratio and carbon source-dependent lipid production profiling in Rhodotorula toruloides
journal, January 2020

  • Lopes, Helberth Júnnior Santos; Bonturi, Nemailla; Kerkhoven, Eduard Johannes
  • Applied Microbiology and Biotechnology, Vol. 104, Issue 6
  • DOI: 10.1007/s00253-020-10386-5

DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008

RNA interference in the oleaginous yeast Rhodosporidium toruloides
journal, April 2019

  • Liu, Xiangjian; Zhang, Yue; Liu, Hongdi
  • FEMS Yeast Research, Vol. 19, Issue 3
  • DOI: 10.1093/femsyr/foz031

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
journal, November 2018

C-4 sterol demethylation enzymes distinguish bacterial and eukaryotic sterol synthesis
journal, May 2018

  • Lee, Alysha K.; Banta, Amy B.; Wei, Jeremy H.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 23
  • DOI: 10.1073/pnas.1802930115

Lipid production in batch and fed-batch cultures of Rhodosporidium toruloidesfrom 5 and 6 carbon carbohydrates
journal, May 2012

  • Wiebe, Marilyn G.; Koivuranta, Kari; Penttilä, Merja
  • BMC Biotechnology, Vol. 12, Issue 1
  • DOI: 10.1186/1472-6750-12-26

Phylogenomics of Sterol Synthesis: Insights into the Origin, Evolution, and Diversity of a Key Eukaryotic Feature
journal, January 2009

  • Desmond, Elie; Gribaldo, Simonetta
  • Genome Biology and Evolution, Vol. 1
  • DOI: 10.1093/gbe/evp036

The PRIDE database and related tools and resources in 2019: improving support for quantification data
journal, November 2018

  • Perez-Riverol, Yasset; Csordas, Attila; Bai, Jingwen
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1106

Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
journal, February 2019

Metabolomic Profiling of Rhodosporidium toruloides Grown on Glycerol for Carotenoid Production during Different Growth Phases
journal, October 2014

  • Lee, Jaslyn Jie Lin; Chen, Liwei; Shi, Jiahua
  • Journal of Agricultural and Food Chemistry, Vol. 62, Issue 41
  • DOI: 10.1021/jf502987q

Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms
journal, April 2015

Functional genomics of lipid metabolism in the oleaginous yeast Rhodosporidium toruloides
journal, March 2018

  • Coradetti, Samuel T.; Pinel, Dominic; Geiselman, Gina M.
  • eLife, Vol. 7
  • DOI: 10.7554/eLife.32110

Identification of a 3β-Hydroxysteroid Dehydrogenase/ 3-Ketosteroid Reductase Involved in α-Tomatine Biosynthesis in Tomato
journal, March 2019

  • Lee, Hyoung Jae; Nakayasu, Masaru; Akiyama, Ryota
  • Plant and Cell Physiology, Vol. 60, Issue 6
  • DOI: 10.1093/pcp/pcz049

MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
journal, May 2016

Reconstruction of genome-scale metabolic model of Yarrowia lipolytica and its application in overproduction of triacylglycerol
journal, December 2017

Metabolic network reconstruction of Chlamydomonas offers insight into light‐driven algal metabolism
journal, January 2011

  • Chang, Roger L.; Ghamsari, Lila; Manichaikul, Ani
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.52

Global reconstruction of the human metabolic network based on genomic and bibliomic data
journal, January 2007

  • Duarte, N. C.; Becker, S. A.; Jamshidi, N.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
  • DOI: 10.1073/pnas.0610772104

MEMOTE for standardized genome-scale metabolic model testing
journal, March 2020

  • Lieven, Christian; Beber, Moritz E.; Olivier, Brett G.
  • Nature Biotechnology, Vol. 38, Issue 3
  • DOI: 10.1038/s41587-020-0446-y

MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data
journal, July 2010

  • Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro
  • BMC Bioinformatics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2105-11-395

The Engineering Potential of Rhodosporidium toruloides as a Workhorse for Biotechnological Applications
journal, March 2018

Xylose Metabolism and the Effect of Oxidative Stress on Lipid and Carotenoid Production in Rhodotorula toruloides: Insights for Future Biorefinery
journal, August 2020

  • Pinheiro, Marina Julio; Bonturi, Nemailla; Belouah, Isma
  • Frontiers in Bioengineering and Biotechnology, Vol. 8
  • DOI: 10.3389/fbioe.2020.01008

Genome‐scale model of Rhodotorula toruloides metabolism
journal, September 2019

  • Tiukova, Ievgeniia A.; Prigent, Sylvain; Nielsen, Jens
  • Biotechnology and Bioengineering, Vol. 116, Issue 12
  • DOI: 10.1002/bit.27162

WoLF PSORT: protein localization predictor
journal, May 2007

  • Horton, P.; Park, K. -J.; Obayashi, T.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm259

Production of d-arabitol from d-xylose by the oleaginous yeast Rhodosporidium toruloides IFO0880
journal, November 2017

  • Jagtap, Sujit Sadashiv; Rao, Christopher V.
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 1
  • DOI: 10.1007/s00253-017-8581-1

Proteome analysis of xylose metabolism in Rhodotorula toruloides during lipid production
journal, June 2019

  • Tiukova, Ievgeniia A.; Brandenburg, Jule; Blomqvist, Johanna
  • Biotechnology for Biofuels, Vol. 12, Issue 1
  • DOI: 10.1186/s13068-019-1478-8

Characterization and remediation of sample index swaps by non-redundant dual indexing on massively parallel sequencing platforms
journal, May 2018

OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003

Multiplexed CRISPR-Cas9-Based Genome Editing of Rhodosporidium toruloides
journal, March 2019

MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features
journal, June 2008

A comprehensive genome-scale model for Rhodosporidium toruloides IFO0880 accounting for functional genomics and phenotypic data
journal, December 2019

  • Dinh, Hoang V.; Suthers, Patrick F.; Chan, Siu Hung Joshua
  • Metabolic Engineering Communications, Vol. 9
  • DOI: 10.1016/j.mec.2019.e00101

COBRApy: COnstraints-Based Reconstruction and Analysis for Python
journal, January 2013

  • Ebrahim, Ali; Lerman, Joshua A.; Palsson, Bernhard O.
  • BMC Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1752-0509-7-74

Glucose-mediated regulation of glycerol uptake in Rhodosporidium toruloides : Insights through transcriptomic analysis on dual substrate fermentation
journal, June 2016

  • Bommareddy, Rajesh Reddy; Sabra, Wael; Zeng, An-Ping
  • Engineering in Life Sciences, Vol. 17, Issue 3
  • DOI: 10.1002/elsc.201600010

Rhodosporidium toruloides: a new platform organism for conversion of lignocellulose into terpene biofuels and bioproducts
journal, October 2017

Catabolism of coniferyl aldehyde, ferulic acid and p-coumaric acid by Saccharomyces cerevisiae yields less toxic products
journal, September 2015

  • Adeboye, Peter Temitope; Bettiga, Maurizio; Aldaeus, Fredrik
  • Microbial Cell Factories, Vol. 14, Issue 1
  • DOI: 10.1186/s12934-015-0338-x

Transcriptional Activity and Protein Levels of Horizontally Acquired Genes in Yeast Reveal Hallmarks of Adaptation to Fermentative Environments
journal, April 2020

  • Devia, Joaquín; Bastías, Camila; Kessi-Pérez, Eduardo I.
  • Frontiers in Genetics, Vol. 11
  • DOI: 10.3389/fgene.2020.00293

A genome‐scale metabolic reconstruction for Escherichia coli K‐12 MG1655 that accounts for 1260 ORFs and thermodynamic information
journal, January 2007

  • Feist, Adam M.; Henry, Christopher S.; Reed, Jennifer L.
  • Molecular Systems Biology, Vol. 3, Issue 1
  • DOI: 10.1038/msb4100155

Promiscuity and diversity in 3-ketosteroid reductases
journal, July 2015

  • Penning, Trevor M.; Chen, Mo; Jin, Yi
  • The Journal of Steroid Biochemistry and Molecular Biology, Vol. 151
  • DOI: 10.1016/j.jsbmb.2014.12.003

A toolset of constitutive promoters for metabolic engineering of Rhodosporidium toruloides
journal, June 2019

  • Nora, Luísa Czamanski; Wehrs, Maren; Kim, Joonhoon
  • Microbial Cell Factories, Vol. 18, Issue 1
  • DOI: 10.1186/s12934-019-1167-0

Engineering Rhodosporidium toruloides for increased lipid production : Engineering
journal, November 2015

  • Zhang, Shuyan; Skerker, Jeffrey M.; Rutter, Charles D.
  • Biotechnology and Bioengineering, Vol. 113, Issue 5
  • DOI: 10.1002/bit.25864

Escher: A Web Application for Building, Sharing, and Embedding Data-Rich Visualizations of Biological Pathways
journal, August 2015

The ortholog conjecture revisited: the value of orthologs and paralogs in function prediction
journal, July 2020

Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage
journal, April 2018

  • Gonçalves, Carla; Wisecaver, Jennifer H.; Kominek, Jacek
  • eLife, Vol. 7
  • DOI: 10.7554/eLife.33034

Coenzyme q System in the Classification of the Yeast Genera Rhodotorula and Cryptococcus, and the Yeast-Like Genera Sporobolomyces and Rhodosporidium
journal, January 1973

  • Yamada, Yuzo; KondÔ, Keiji
  • The Journal of General and Applied Microbiology, Vol. 19, Issue 1
  • DOI: 10.2323/jgam.19.59

Eukaryotic Acquisition of a Bacterial Operon
journal, March 2019

A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory
journal, January 2008

  • Nogales, Juan; Palsson, Bernhard Ø; Thiele, Ines
  • BMC Systems Biology, Vol. 2, Issue 1
  • DOI: 10.1186/1752-0509-2-79

A detailed genome-wide reconstruction of mouse metabolism based on human Recon 1
journal, January 2010

  • Sigurdsson, Martin I.; Jamshidi, Neema; Steingrimsson, Eirikur
  • BMC Systems Biology, Vol. 4, Issue 1
  • DOI: 10.1186/1752-0509-4-140

Fast and efficient genetic transformation of oleaginous yeast Rhodosporidium toruloides by using electroporation
journal, March 2017

iML1515, a knowledgebase that computes Escherichia coli traits
journal, October 2017

  • Monk, Jonathan M.; Lloyd, Colton J.; Brunk, Elizabeth
  • Nature Biotechnology, Vol. 35, Issue 10
  • DOI: 10.1038/nbt.3956

A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides
journal, January 2012

  • Zhu, Zhiwei; Zhang, Sufang; Liu, Hongwei
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms2112

Monoterpene production by the carotenogenic yeast Rhodosporidium toruloides
journal, March 2019

MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009

  • Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
  • Analytical Chemistry, Vol. 81, Issue 9
  • DOI: 10.1021/ac802689c

MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

  • Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1183

Enzyme-fusion strategies for redirecting and improving carotenoid synthesis in S. cerevisiae
journal, June 2019

  • Rabeharindranto, Hery; Castaño-Cerezo, Sara; Lautier, Thomas
  • Metabolic Engineering Communications, Vol. 8
  • DOI: 10.1016/j.mec.2019.e00086

Homologous gene targeting of a carotenoids biosynthetic gene in Rhodosporidium toruloides by Agrobacterium-mediated transformation
journal, March 2017

MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014

  • Kim, Sangtae; Pevzner, Pavel A.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6277

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014

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