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Metabolomic Analysis of Response to Nitrogen-Limiting Conditions in Yarrowia Spp

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Metabolomic Analysis of Response to Nitrogen-Limiting Conditions in Yarrowia Spp H OH metabolites OH Article Metabolomic Analysis of Response to Nitrogen-Limiting Conditions in Yarrowia spp. Sivamoke Dissook, Sastia Prama Putri * and Eiichiro Fukusaki Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan; [email protected] (S.D.); [email protected] (E.F.) * Correspondence: [email protected]; Tel.: +81-6-6879-7416 Abstract: Yarrowia is a yeast genus that has been used as a model oleaginous taxon for a wide array of studies. However, information regarding metabolite changes within Yarrowia spp. under different environmental conditions is still limited. Among various factors affecting Yarrowia metabolism, nitrogen-limiting conditions have a profound effect on the metabolic state of yeast. In this study, a time-course LC-MS/MS-based metabolome analysis of Y. lipolytica was performed to determine the optimal cultivation time and carbon-to-nitrogen ratio for studying the effects of nitrogen-limiting conditions on Yarrowia; we found that cultivation time of 36 h and carbon-to-nitrogen ratio of 4:1 and 5:0 was suitable for studying the effects of nitrogen-limiting conditions on Yarrowia and these conditions were applied to six strains of Yarrowia. These six strains of Yarrowia showed similar responses to nitrogen-limiting conditions; however, each strain had a unique metabolomic profile. Purine and pyrimidine metabolism were the most highly affected biological pathways in nitrogen- limiting conditions, indicating that these conditions affect energy availability within cells. This stress leads to a shift in cells to the utilization of a less ATP-dependent biological pathway. This information will be beneficial for the development of Yarrowia strains for further scientific and industrial applications. Keywords: Yarrowia; LC-MS/MS; metabolome Citation: Dissook, S.; Putri, S.P.; Fukusaki, E. Metabolomic Analysis of Response to Nitrogen-Limiting 1. Introduction Conditions in Yarrowia spp. Yarrowia is a fungal genus in the family Dipodascaceae. This genus was initially Metabolites 2021, 11, 16. https://doi. considered monotypic, containing only Yarrowia lipolytica, which has been used as a model org/10.3390/metabo11010016 oleaginous organism for a wide range of studies, including studies of lipid accumulation and degradation, peroxisome biogenesis, dimorphism, and protein secretion pathways [1]. Received: 10 November 2020 Wild-type Y. lipolytica can utilize glucose, fructose, glycerol, and hydrophobic substrates as Accepted: 24 December 2020 carbon sources [2,3]. Owing to this property, the yeast species has potential applications in Published: 29 December 2020 industrial microbiology, particularly for the biosynthesis of lipids [4]. Based on molecular phylogenetics studies, the genus now includes several additional species [5–7]. Publisher’s Note: MDPI stays neu- Altering the carbon-to-nitrogen (C:N) ratio in the culture medium could drastically tral with regard to jurisdictional claims in published maps and institutional change the metabolomic profile in yeasts, and the precise effects may vary among different affiliations. strains [8–11]. Substantial work over the past few years has focused on characterizing and engineering oleaginous yeast [12]. Nonetheless, the metabolic response of Yarrowia spp., especially the recently added species, under nitrogen-limiting conditions is not well char- acterized. The nitrogen-limiting condition is a metabolic condition. Therefore, a complete Copyright: © 2020 by the authors. Li- understanding of its effects cannot be achieved without studying intracellular metabo- censee MDPI, Basel, Switzerland. This lites [13]. article is an open access article distributed In this study we conducted the time-course sampling of one Y. lipolytica strain to probe under the terms and conditions of the the suitable time points for multiple strains study. Since the variable changes in this study Creative Commons Attribution (CC BY) highly affect the growth of Y. lipolytica, it might not be suitable to choose the sampling license (https://creativecommons.org/ point based on the growth phase alone. Therefore, we considered the metabolome profile licenses/by/4.0/). Metabolites 2021, 11, 16. https://doi.org/10.3390/metabo11010016 https://www.mdpi.com/journal/metabolites Metabolites 2021, 11, x FOR PEER REVIEW 2 of 15 study highly affect the growth of Y. lipolytica, it might not be suitable to choose the sam- Metabolites 2021, 11, 16 pling point based on the growth phase alone. Therefore, we considered the metabolome2 of 14 profile to help understand the dynamic of metabolic changes occuring during the cultiva- tion with several different C:N ratios and determined the crucial sampling time point and C:Nto help ratio understand for multiple the strains dynamic study. of We metabolic further studied changes the occuring metabolic during responses the cultivation of several withYarrowia several strains different to nitrogen C:N ratios-limiting and conditions determined, including the crucial one samplinglaboratory time strain point, Y. lipo- and lyticaC:N ratio PO1d for [14] multiple, three strainsformer study. Candida We lipolytica further studiedspecies thefrom metabolic different responses study groups of several (cur- Yarrowiarently identifiedstrains to as nitrogen-limiting Yarrowia spp.), C conditions,. lipolytica JCM including 2304 one[15], laboratory C. lipolytica strain, JCM Y.21924 lipolytica [16], andPO1d C. [lipolytica14], three JCM former 8061Candida, and two lipolytica recentlyspecies identified from species, different Y. studydeformans groups JCM (currently 1694 [17] andidentified Y. keelungensis as Yarrowia JCMspp.), 14894C. [1 lipolytica8]. This informationJCM 2304 [will15], beC. beneficial lipolytica JCM for the 21924 development [16], and C.and lipolytica manipulationJCM 8061, of Yarrowia and two sp recentlyp. for fu identifiedture applications. species, Y. deformans JCM 1694 [17] and Y. keelungensis JCM 14894 [18]. This information will be beneficial for the development and 2.manipulation Results and of DiscussionYarrowia spp. for future applications. 2.1. Growth of Y. Lipolytica under Different Carbon-to-Nitrogen Ratios 2. Results and Discussion To determine the crucial sampling time point and C:N ratio for analyses of the effect 2.1. Growth of Y. Lipolytica under Different Carbon-to-Nitrogen Ratios of nitrogen-limiting conditions, time course sampling under various C:N compositions was Toperformed determine using the crucialY. lipolytica sampling PO1d. time The point extracellular and C:N ratio glucose for analyses concentrations of the effect and growthof nitrogen-limiting of Y. lipolytica conditions, cultivated time with course different sampling C:N underratios variousare shown C:N in compositions Figure 1. There was performedwere three usingdifferentY. lipolytica stable physiologicalPO1d. The extracellular states: (1) C glucosearbon-restri concentrationscted conditions and growth (0:5), (2) of Y.intermediate lipolytica cultivated C:N ratios with (4;1, different 2:2, and C:N1:4), ratiosand (3) are nitrogen shown- inrestricted Figure1 .condition There weres (5:0) three; all statisticaldifferent stable test results physiological can be found states: in (1)Table Carbon-restricted S1. Under carbon conditions-restricted (0:5), conditions, (2) intermediate growth increasedC:N ratios steadily (4;1, 2:2, from and 0 1:4), h to and 12 h (3), remained nitrogen-restricted constant for conditions 24 h, and cells (5:0); reached all statistical the high- test results can be found in Table S1. Under carbon-restricted conditions, growth increased est OD600 at 36 h. For intermediate C:N ratios, growth increased rapidly from 0 h to 12 h, steadily from 0 h to 12 h, remained constant for 24 h, and cells reached the highest OD600 slowed from 12 h to 24 h, and the highest OD600 was reached at 36 h. Under nitrogen- at 36 h. For intermediate C:N ratios, growth increased rapidly from 0 h to 12 h, slowed restricted conditions, growth increased slowly from 0 h to 24 h and increased steadily from 12 h to 24 h, and the highest OD600 was reached at 36 h. Under nitrogen-restricted from 24 h until cells reached the highest OD600 at 36 h. In this study, all OD600 values de- conditions, growth increased slowly from 0 h to 24 h and increased steadily from 24 h creased after 36 h of cultivation. In both carbon- and nitrogen-restricted conditions, the until cells reached the highest OD at 36 h. In this study, all OD values decreased growth profiles suggested that cells600 took approximately 24 h to adjust600 to the new condi- after 36 h of cultivation. In both carbon- and nitrogen-restricted conditions, the growth tion before entering the exponential growth phase. For intermediate C:N ratios, especially profiles suggested that cells took approximately 24 h to adjust to the new condition before 4:1 and 2:2, three phases of cell growth were observed, 0–12 h, 12–24 h, and 24–36 h. These entering the exponential growth phase. For intermediate C:N ratios, especially 4:1 and data suggest that the conditions changed during cultivation, and cells had to adapt for 2:2, three phases of cell growth were observed, 0–12 h, 12–24 h, and 24–36 h. These data increasedsuggest that growth. the conditions Interestingly, changed this during phenomen cultivation,on was andnot observed cells had tofor adapt a C:N for ratio increased of 1:4. Thgrowth.ese results Interestingly, show that this Y. lipolytica phenomenon is very was sensitive not observed to changes for ain C:N the ratioC:N ratio. of 1:4. Surpris- These ingly,results Y. show lipolytica that growthY. lipolytica did notis very depend sensitive on glucose to changes availability in the, as C:N evidenced ratio. Surprisingly, by the con- Y.tinued lipolytica growthgrowth in glucose did not-depleted depend onconditions glucose availability,(C:N 0:5 and as 1:4 evidenced at 24 h, 2:2 by at the 36 continued h). Yeast ingrowth the C:N in glucose-depleted5:0 condition could conditions not utilize (C:N glucose 0:5 and effectively 1:4 at 24 h,, even 2:2 atwith 36 h).
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