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Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate

BACKGROUND: Efficient and economically viable production of biofuels from lignocellulosic biomass is dependent on mechanical and chemical pretreatment and enzymatic hydrolysis of plant material. These processing steps yield simple sugars as well as plant-derived and process-added organic acids, suga...

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Autores principales: Pomraning, Kyle R., Collett, James R., Kim, Joonhoon, Panisko, Ellen A., Culley, David E., Dai, Ziyu, Deng, Shuang, Hofstad, Beth A., Butcher, Mark G., Magnuson, Jon K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593508/
https://www.ncbi.nlm.nih.gov/pubmed/31289462
http://dx.doi.org/10.1186/s13068-019-1510-z
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author Pomraning, Kyle R.
Collett, James R.
Kim, Joonhoon
Panisko, Ellen A.
Culley, David E.
Dai, Ziyu
Deng, Shuang
Hofstad, Beth A.
Butcher, Mark G.
Magnuson, Jon K.
author_facet Pomraning, Kyle R.
Collett, James R.
Kim, Joonhoon
Panisko, Ellen A.
Culley, David E.
Dai, Ziyu
Deng, Shuang
Hofstad, Beth A.
Butcher, Mark G.
Magnuson, Jon K.
author_sort Pomraning, Kyle R.
collection PubMed
description BACKGROUND: Efficient and economically viable production of biofuels from lignocellulosic biomass is dependent on mechanical and chemical pretreatment and enzymatic hydrolysis of plant material. These processing steps yield simple sugars as well as plant-derived and process-added organic acids, sugar-derived dehydration products, aldehydes, phenolics and other compounds that inhibit the growth of many microorganisms. Lipomyces starkeyi is an oleaginous yeast capable of robust growth on a variety of sugars and lipid accumulation on pretreated lignocellulosic substrates making it attractive as an industrial producer of biofuels. Here, we examined gene expression during batch growth and lipid accumulation in a 20-L bioreactor with either a blend of pure glucose and xylose or pretreated corn stover (PCS) that had been enzymatically hydrolyzed as the carbon sources. RESULTS: We monitored sugar and ammonium utilization as well as biomass accumulation and found that growth of L. starkeyi is inhibited with PCS hydrolysate as the carbon source. Both acetic acid and furfural are present at concentrations toxic to L. starkeyi in PCS hydrolysate. We quantified gene expression at seven time-points for each carbon source during batch growth and found that gene expression is similar at physiologically equivalent points. Analysis of promoter regions revealed that gene expression during the transition to lipid accumulation is regulated by carbon and nitrogen catabolite repression, regardless of carbon source and is associated with decreased expression of the translation machinery and suppression of the cell cycle. We identified 73 differentially expressed genes during growth phase in the bioreactor that may be involved in detoxification of corn stover hydrolysate. CONCLUSIONS: Growth of L. starkeyi is inhibited by compounds present in PCS hydrolysate. Here, we monitored key metabolites to establish physiologically equivalent comparisons during a batch bioreactor run comparing PCS hydrolysate and purified sugars. L. starkeyi’s response to PCS hydrolysate is primarily at the beginning of the run during growth phase when inhibitory compounds are presumably at their highest concentration and inducing the general detoxification response by L. starkeyi. Differentially expressed genes identified herein during growth phase will aid in the improvement of industrial strains capable of robust growth on substrates containing various growth inhibitory compounds. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-019-1510-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-65935082019-07-09 Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate Pomraning, Kyle R. Collett, James R. Kim, Joonhoon Panisko, Ellen A. Culley, David E. Dai, Ziyu Deng, Shuang Hofstad, Beth A. Butcher, Mark G. Magnuson, Jon K. Biotechnol Biofuels Research BACKGROUND: Efficient and economically viable production of biofuels from lignocellulosic biomass is dependent on mechanical and chemical pretreatment and enzymatic hydrolysis of plant material. These processing steps yield simple sugars as well as plant-derived and process-added organic acids, sugar-derived dehydration products, aldehydes, phenolics and other compounds that inhibit the growth of many microorganisms. Lipomyces starkeyi is an oleaginous yeast capable of robust growth on a variety of sugars and lipid accumulation on pretreated lignocellulosic substrates making it attractive as an industrial producer of biofuels. Here, we examined gene expression during batch growth and lipid accumulation in a 20-L bioreactor with either a blend of pure glucose and xylose or pretreated corn stover (PCS) that had been enzymatically hydrolyzed as the carbon sources. RESULTS: We monitored sugar and ammonium utilization as well as biomass accumulation and found that growth of L. starkeyi is inhibited with PCS hydrolysate as the carbon source. Both acetic acid and furfural are present at concentrations toxic to L. starkeyi in PCS hydrolysate. We quantified gene expression at seven time-points for each carbon source during batch growth and found that gene expression is similar at physiologically equivalent points. Analysis of promoter regions revealed that gene expression during the transition to lipid accumulation is regulated by carbon and nitrogen catabolite repression, regardless of carbon source and is associated with decreased expression of the translation machinery and suppression of the cell cycle. We identified 73 differentially expressed genes during growth phase in the bioreactor that may be involved in detoxification of corn stover hydrolysate. CONCLUSIONS: Growth of L. starkeyi is inhibited by compounds present in PCS hydrolysate. Here, we monitored key metabolites to establish physiologically equivalent comparisons during a batch bioreactor run comparing PCS hydrolysate and purified sugars. L. starkeyi’s response to PCS hydrolysate is primarily at the beginning of the run during growth phase when inhibitory compounds are presumably at their highest concentration and inducing the general detoxification response by L. starkeyi. Differentially expressed genes identified herein during growth phase will aid in the improvement of industrial strains capable of robust growth on substrates containing various growth inhibitory compounds. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-019-1510-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-26 /pmc/articles/PMC6593508/ /pubmed/31289462 http://dx.doi.org/10.1186/s13068-019-1510-z Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Pomraning, Kyle R.
Collett, James R.
Kim, Joonhoon
Panisko, Ellen A.
Culley, David E.
Dai, Ziyu
Deng, Shuang
Hofstad, Beth A.
Butcher, Mark G.
Magnuson, Jon K.
Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title_full Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title_fullStr Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title_full_unstemmed Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title_short Transcriptomic analysis of the oleaginous yeast Lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
title_sort transcriptomic analysis of the oleaginous yeast lipomyces starkeyi during lipid accumulation on enzymatically treated corn stover hydrolysate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593508/
https://www.ncbi.nlm.nih.gov/pubmed/31289462
http://dx.doi.org/10.1186/s13068-019-1510-z
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