Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces

The Lipomyces clade contains oleaginous yeast species with advantageous metabolic features for biochemical and biofuel production. Limited knowledge about the metabolic networks of the species and limited tools for genetic engineering have led to a relatively small amount of research on the microbes...

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Main Authors: Jeffrey J. Czajka, Yichao Han, Joonhoon Kim, Stephen J. Mondo, Beth A. Hofstad, AnaLaura Robles, Sajeet Haridas, Robert Riley, Kurt LaButti, Jasmyn Pangilinan, William Andreopoulos, Anna Lipzen, Juying Yan, Mei Wang, Vivian Ng, Igor V. Grigoriev, Joseph W. Spatafora, Jon K. Magnuson, Scott E. Baker, Kyle R. Pomraning
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fbioe.2024.1356551/full
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author Jeffrey J. Czajka
Jeffrey J. Czajka
Yichao Han
Yichao Han
Joonhoon Kim
Joonhoon Kim
Joonhoon Kim
Stephen J. Mondo
Stephen J. Mondo
Stephen J. Mondo
Beth A. Hofstad
Beth A. Hofstad
AnaLaura Robles
AnaLaura Robles
Sajeet Haridas
Robert Riley
Kurt LaButti
Jasmyn Pangilinan
William Andreopoulos
Anna Lipzen
Juying Yan
Mei Wang
Vivian Ng
Igor V. Grigoriev
Igor V. Grigoriev
Joseph W. Spatafora
Jon K. Magnuson
Jon K. Magnuson
Jon K. Magnuson
Scott E. Baker
Scott E. Baker
Scott E. Baker
Kyle R. Pomraning
Kyle R. Pomraning
author_facet Jeffrey J. Czajka
Jeffrey J. Czajka
Yichao Han
Yichao Han
Joonhoon Kim
Joonhoon Kim
Joonhoon Kim
Stephen J. Mondo
Stephen J. Mondo
Stephen J. Mondo
Beth A. Hofstad
Beth A. Hofstad
AnaLaura Robles
AnaLaura Robles
Sajeet Haridas
Robert Riley
Kurt LaButti
Jasmyn Pangilinan
William Andreopoulos
Anna Lipzen
Juying Yan
Mei Wang
Vivian Ng
Igor V. Grigoriev
Igor V. Grigoriev
Joseph W. Spatafora
Jon K. Magnuson
Jon K. Magnuson
Jon K. Magnuson
Scott E. Baker
Scott E. Baker
Scott E. Baker
Kyle R. Pomraning
Kyle R. Pomraning
author_sort Jeffrey J. Czajka
collection DOAJ
description The Lipomyces clade contains oleaginous yeast species with advantageous metabolic features for biochemical and biofuel production. Limited knowledge about the metabolic networks of the species and limited tools for genetic engineering have led to a relatively small amount of research on the microbes. Here, a genome-scale metabolic model (GSM) of Lipomyces starkeyi NRRL Y-11557 was built using orthologous protein mappings to model yeast species. Phenotypic growth assays were used to validate the GSM (66% accuracy) and indicated that NRRL Y-11557 utilized diverse carbohydrates but had more limited catabolism of organic acids. The final GSM contained 2,193 reactions, 1,909 metabolites, and 996 genes and was thus named iLst996. The model contained 96 of the annotated carbohydrate-active enzymes. iLst996 predicted a flux distribution in line with oleaginous yeast measurements and was utilized to predict theoretical lipid yields. Twenty-five other yeasts in the Lipomyces clade were then genome sequenced and annotated. Sixteen of the Lipomyces species had orthologs for more than 97% of the iLst996 genes, demonstrating the usefulness of iLst996 as a broad GSM for Lipomyces metabolism. Pathways that diverged from iLst996 mainly revolved around alternate carbon metabolism, with ortholog groups excluding NRRL Y-11557 annotated to be involved in transport, glycerolipid, and starch metabolism, among others. Overall, this study provides a useful modeling tool and data for analyzing and understanding Lipomyces species metabolism and will assist further engineering efforts in Lipomyces.
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spelling doaj.art-e4235ff99f1948b58b602ca0631e234b2024-04-04T05:07:44ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852024-04-011210.3389/fbioe.2024.13565511356551Genome-scale model development and genomic sequencing of the oleaginous clade LipomycesJeffrey J. Czajka0Jeffrey J. Czajka1Yichao Han2Yichao Han3Joonhoon Kim4Joonhoon Kim5Joonhoon Kim6Stephen J. Mondo7Stephen J. Mondo8Stephen J. Mondo9Beth A. Hofstad10Beth A. Hofstad11AnaLaura Robles12AnaLaura Robles13Sajeet Haridas14Robert Riley15Kurt LaButti16Jasmyn Pangilinan17William Andreopoulos18Anna Lipzen19Juying Yan20Mei Wang21Vivian Ng22Igor V. Grigoriev23Igor V. Grigoriev24Joseph W. Spatafora25Jon K. Magnuson26Jon K. Magnuson27Jon K. Magnuson28Scott E. Baker29Scott E. Baker30Scott E. Baker31Kyle R. Pomraning32Kyle R. Pomraning33Energy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesUS Department of Energy Joint BioEnergy Institute, Emeryville, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesDepartment of Agricultural Biology, Colorado State University, Fort Collins, CO, United StatesEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesDepartment of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesUS Department of Energy Joint BioEnergy Institute, Emeryville, CA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesUS Department of Energy Joint BioEnergy Institute, Emeryville, CA, United StatesEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesEnergy and Environment Directorate, Pacific Northwest National Laboratory, Richland, WA, United StatesUS Department of Energy Agile BioFoundry, Emeryville, CA, United StatesThe Lipomyces clade contains oleaginous yeast species with advantageous metabolic features for biochemical and biofuel production. Limited knowledge about the metabolic networks of the species and limited tools for genetic engineering have led to a relatively small amount of research on the microbes. Here, a genome-scale metabolic model (GSM) of Lipomyces starkeyi NRRL Y-11557 was built using orthologous protein mappings to model yeast species. Phenotypic growth assays were used to validate the GSM (66% accuracy) and indicated that NRRL Y-11557 utilized diverse carbohydrates but had more limited catabolism of organic acids. The final GSM contained 2,193 reactions, 1,909 metabolites, and 996 genes and was thus named iLst996. The model contained 96 of the annotated carbohydrate-active enzymes. iLst996 predicted a flux distribution in line with oleaginous yeast measurements and was utilized to predict theoretical lipid yields. Twenty-five other yeasts in the Lipomyces clade were then genome sequenced and annotated. Sixteen of the Lipomyces species had orthologs for more than 97% of the iLst996 genes, demonstrating the usefulness of iLst996 as a broad GSM for Lipomyces metabolism. Pathways that diverged from iLst996 mainly revolved around alternate carbon metabolism, with ortholog groups excluding NRRL Y-11557 annotated to be involved in transport, glycerolipid, and starch metabolism, among others. Overall, this study provides a useful modeling tool and data for analyzing and understanding Lipomyces species metabolism and will assist further engineering efforts in Lipomyces.https://www.frontiersin.org/articles/10.3389/fbioe.2024.1356551/fulloleaginous yeastsgenome-scale metabolic modelflux balance analysisLipomycesgenome sequencing
spellingShingle Jeffrey J. Czajka
Jeffrey J. Czajka
Yichao Han
Yichao Han
Joonhoon Kim
Joonhoon Kim
Joonhoon Kim
Stephen J. Mondo
Stephen J. Mondo
Stephen J. Mondo
Beth A. Hofstad
Beth A. Hofstad
AnaLaura Robles
AnaLaura Robles
Sajeet Haridas
Robert Riley
Kurt LaButti
Jasmyn Pangilinan
William Andreopoulos
Anna Lipzen
Juying Yan
Mei Wang
Vivian Ng
Igor V. Grigoriev
Igor V. Grigoriev
Joseph W. Spatafora
Jon K. Magnuson
Jon K. Magnuson
Jon K. Magnuson
Scott E. Baker
Scott E. Baker
Scott E. Baker
Kyle R. Pomraning
Kyle R. Pomraning
Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
Frontiers in Bioengineering and Biotechnology
oleaginous yeasts
genome-scale metabolic model
flux balance analysis
Lipomyces
genome sequencing
title Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
title_full Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
title_fullStr Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
title_full_unstemmed Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
title_short Genome-scale model development and genomic sequencing of the oleaginous clade Lipomyces
title_sort genome scale model development and genomic sequencing of the oleaginous clade lipomyces
topic oleaginous yeasts
genome-scale metabolic model
flux balance analysis
Lipomyces
genome sequencing
url https://www.frontiersin.org/articles/10.3389/fbioe.2024.1356551/full
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