Regulation of carbon metabolic fluxes to enhance lipid and succinate production in oleaginous fungus Mortierella alpina.


Journal

World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472

Informations de publication

Date de publication:
12 Aug 2024
Historique:
received: 14 01 2024
accepted: 14 07 2024
medline: 12 8 2024
pubmed: 12 8 2024
entrez: 11 8 2024
Statut: epublish

Résumé

Mortierella alpina is popular for lipid production, but the low carbon conversion rate and lipid yield are major obstacles for its economic performance. Here, external addition of organic acids involved in tricarboxylic acid cycle was used to tune carbon flux and improve lipid production. Citrate was determined to be the best organic acid that can be used for enhancing lipid production. By the addition of citrate, the lipid titer and content were approximately 1.24 and 1.34 times higher, respectively. Meanwhile, citrate supplement also promoted the accumulation of succinate, an important value-added platform chemical. Owing to the improved lipid and succinate production through adding citrate, the carbon conversion rate of M. alpina reached up to 52.17%, much higher than that of the control group (14.11%). The addition of citrate could redistribute carbon flux by regulating the expression level of genes related to tricarboxylic acid cycle metabolism. More carbon fluxes flow to lipid and succinate synthesis, which greatly improved the carbon conversion efficiency of M. alpina. This study provides an effective and straightforward strategy with potential economic benefits to improve carbon conversion efficiency in M. alpina.

Identifiants

pubmed: 39128979
doi: 10.1007/s11274-024-04082-z
pii: 10.1007/s11274-024-04082-z
doi:

Substances chimiques

Succinic Acid AB6MNQ6J6L
Carbon 7440-44-0
Citric Acid 2968PHW8QP
Lipids 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

298

Subventions

Organisme : The Start-up Funding of Central South University
ID : Grant No. 202045023
Organisme : The Natural Science Foundation of Hunan Province
ID : Grant No. 2021JJ30803

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Baldeweg F, Warncke P, Fischer D, Gressler M (2019) Fungal biosurfactants from mortierella alpina. Org Lett 21:1444–1448
doi: 10.1021/acs.orglett.9b00193 pubmed: 30789272
Chang L, Tang X, Lu H, Zhang H, Chen YQ, Chen H, Chen W (2019) Role of adenosine monophosphate deaminase during fatty acid accumulation in oleaginous fungus mortierella alpina. J Agric Food Chem 67:9551–9559
doi: 10.1021/acs.jafc.9b03603 pubmed: 31379157
Chang L, Lu H, Chen H, Tang X, Zhao J, Zhang H, Chen YQ, Chen W (2022) Lipid metabolism research in oleaginous fungus mortierella alpina: current progress and future prospects. Biotechnol Adv 54:107794
doi: 10.1016/j.biotechadv.2021.107794 pubmed: 34245810
Chang L, Chen H, Yang B, Chen H, Chen W (2023) Redistributing carbon flux by impairing saccharide synthesis to enhance lipid yield in oleaginous fungus mortierella alpina. ACS Synth Biol 12:1750–1760
doi: 10.1021/acssynbio.3c00046 pubmed: 37166287
de Oliveira PZ, de Souza Vandenberghe LP, Rodrigues C, de Melo Pereira GV, Soccol CR (2022) Exploring cocoa pod husks as a potential substrate for citric acid production by solid-state fermentation using aspergillus Niger mutant strain. Process Biochem 113:107–112
doi: 10.1016/j.procbio.2021.12.020
Eroshin V, Satroutdinov A, Dedyukhina E, Chistyakova T (2000) Arachidonic acid production by mortierella alpina with growth-coupled lipid synthesis. Process Biochem 35:1171–1175
doi: 10.1016/S0032-9592(00)00151-5
Feng Y, Zhang X, Yang H, Feng X, Chen M (2024) Study on the regulation of mortierella alpina morphology and high yield of arachidonic acid by metal ions. Systems Microbiology and Biomanufacturing
Gao B, Gan M, Sun C, Chen H, Liu X, Liu Q, Wang Y, Cheng H, Zhou H, Chen Z (2023) Bioleaching of ion-adsorption rare earth ores by biogenic lixiviants derived from agriculture waste via a cell-free cascade enzymatic process. Hydrometallurgy 202:106189
doi: 10.1016/j.hydromet.2023.106189
Ji X-J, Ren L-J, Nie Z-K, Huang H, Ouyang P-K (2014a) Fungal arachidonic acid-rich oil: research, development and industrialization. Crit Rev Biotechnol 34:197–214
doi: 10.3109/07388551.2013.778229 pubmed: 23631634
Ji X-J, Zhang A-H, Nie Z-K, Wu W-J, Ren L-J, Huang H (2014b) Efficient arachidonic acid-rich oil production by mortierella alpina through a repeated fed-batch fermentation strategy. Bioresour Technol 170:356–360
doi: 10.1016/j.biortech.2014.07.098 pubmed: 25151081
Kikukawa H, Sakuradani E, Ando A, Shimizu S, Ogawa J (2018) Arachidonic acid production by the oleaginous fungus mortierella alpina 1s-4: a review. J Adv Res 11:15–22
doi: 10.1016/j.jare.2018.02.003 pubmed: 30034872 pmcid: 6052653
Koh H-J, Lee S-M, Son B-G, Lee S-H, Ryoo ZY, Chang K-T, Park J-W, Park D-C, Song BJ, Veech RL (2004) Cytosolic nadp+-dependent isocitrate dehydrogenase plays a key role in lipid metabolism. J Biol Chem 279:39968–39974
doi: 10.1074/jbc.M402260200 pubmed: 15254034
Li X, Lin Y, Chang M, Jin Q, Wang X (2015a) Efficient production of arachidonic acid by mortierella alpina through integrating fed-batch culture with a two-stage Ph control strategy. Bioresour Technol 181:275–282
doi: 10.1016/j.biortech.2015.01.009 pubmed: 25661306
Li X, Liu R, Li J, Chang M, Liu Y, Jin Q, Wang X (2015b) Enhanced arachidonic acid production from mortierella alpina combining atmospheric and room temperature plasma (artp) and diethyl sulfate treatments. Bioresour Technol 177:134–140
doi: 10.1016/j.biortech.2014.11.051 pubmed: 25484124
Ling X-p, Zeng S-y, Chen C-x, Liu X-t, Lu Y-h (2016) Enhanced arachidonic acid production using a bioreactor culture of mortierella alpina with a combined organic nitrogen source. Bioresour Bioprocess 3:1–6
doi: 10.1186/s40643-016-0121-9
Ling F, Tang X, Zhang H, Chen YQ, Zhao J, Chen H, Chen W (2021) Role of the mitochondrial citrate-oxoglutarate carrier in lipid accumulation in the oleaginous fungus mortierella alpina. Biotechnol Lett 43:1455–1466
doi: 10.1007/s10529-021-03133-x pubmed: 33907945
Liu X, Zhao G, Sun S, Fan C, Feng X, Xiong P (2022) Biosynthetic pathway and metabolic engineering of succinic acid. Front Bioeng Biotech 10:843887
doi: 10.3389/fbioe.2022.843887
Lu F, Wang Z, Zhao W, Chu J, Zhuang Y (2016) A simple novel approach for real-time monitoring of sodium gluconate production by on-line physiological parameters in batch fermentation by aspergillus Niger. Bioresour Technol 202:133–141
doi: 10.1016/j.biortech.2015.11.077 pubmed: 26706727
Lu H, Chen H, Tang X, Yang Q, Zhang H, Chen YQ, Chen W (2019) Evaluation of metabolome sample preparation and extraction methodologies for oleaginous filamentous fungi mortierella alpina. Metabolomics 15:1–10
doi: 10.1007/s11306-019-1506-5
Lu H, Chen H, Tang X, Yang Q, Zhang H, Chen YQ, Chen W (2020) Time-resolved multi-omics analysis reveals the role of nutrient stress-induced resource reallocation for tag accumulation in oleaginous fungus mortierella alpina. Biotechnol Biofuels 13:1–17
doi: 10.1186/s13068-020-01757-1
Lu J, Li J, Gao H, Zhou D, Xu H, Cong Y, Zhang W, Xin F, Jiang M (2021) Recent progress on bio-succinic acid production from lignocellulosic biomass. World J Microb Biot 37:1–8
doi: 10.1007/s11274-020-02979-z
Nghiem NP, Kleff S, Schwegmann S (2017) Succinic acid: technology development and commercialization. Fermentation 3:26
doi: 10.3390/fermentation3020026
Nisha A, Rastogi NK, Venkateswaran G (2011) Optimization of media components for enhanced arachidonic acid production by mortierella alpina under submerged cultivation. Biotechnol Bioproc E 16:229–237
doi: 10.1007/s12257-010-0294-6
Owen OE, Kalhan SC, Hanson RW (2002) The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem 277:30409–30412
doi: 10.1074/jbc.R200006200 pubmed: 12087111
Rodríguez-Frómeta RA, Gutiérrez A, Torres-Martínez S, Garre V (2013) Malic enzyme activity is not the only bottleneck for lipid accumulation in the oleaginous fungus mucor circinelloides. Appl Biochem Biotech 97:3063–3072
Shanmugam S, Sun C, Zeng X, Wu Y-R (2018) High-efficient production of biobutanol by a novel clostridium sp. strain wst with uncontrolled Ph strategy. Bioresour Technol 256:543–547
doi: 10.1016/j.biortech.2018.02.077 pubmed: 29486913
Sonnabend R, Seiler L, Gressler M (2022) Regulation of the leucine metabolism in mortierella alpina. J Fungi 8:196
doi: 10.3390/jof8020196
Tang X, Chen H, Mei T, Ge C, Gu Z, Zhang H, Chen YQ, Chen W (2018) Characterization of an omega-3 desaturase from phytophthora parasitica and application for eicosapentaenoic acid production in mortierella alpina. Front Microbiol 9:1878
doi: 10.3389/fmicb.2018.01878 pubmed: 30154780 pmcid: 6102326
Uprety BK, Morrison EN, Emery RN, Farrow SC (2022) Customizing lipids from oleaginous microbes: leveraging exogenous and endogenous approaches. Trends Biotechnol 40:482–508
doi: 10.1016/j.tibtech.2021.09.004 pubmed: 34625276
Wang J, Zeng A-p, Yuan W (2022) Succinic acid fermentation from agricultural wastes: the producing microorganisms and their engineering strategies. Curr Opin Environ Sci Health 25:100313
doi: 10.1016/j.coesh.2021.100313
Wu W-J, Zhang A-H, Peng C, Ren L-J, Song P, Yu Y-D, Huang H, Ji X-J (2017) An efficient multi-stage fermentation strategy for the production of microbial oil rich in arachidonic acid in mortierella alpina. Bioresour Bioprocess 4:1–9
doi: 10.1186/s40643-017-0138-8
Xue J, Balamurugan S, Li D-W, Liu Y-H, Zeng H, Wang L, Yang W-D, Liu J-S, Li H-Y (2017) Glucose-6-phosphate dehydrogenase as a target for highly efficient fatty acid biosynthesis in microalgae by enhancing nadph supply. Metab Eng 41:212–221
doi: 10.1016/j.ymben.2017.04.008 pubmed: 28465173
Yang B, Chen H, Stanton C, Ross RP, Zhang H, Chen YQ, Chen W (2015) Review of the roles of conjugated linoleic acid in health and disease. J Funct Foods 15:314–325
doi: 10.1016/j.jff.2015.03.050
Yang B, Chen H, Gao H, Wang J, Stanton C, Ross RP, Zhang H, Chen W (2018) Bifidobacterium breve ccfm683 could ameliorate dss-induced colitis in mice primarily via conjugated linoleic acid production and gut microbiota modulation. J Funct Foods 49:61–72
doi: 10.1016/j.jff.2018.08.014
Yang W, Dong S, Yang J, Mohamed H, Shah AM, Nazir Y, Gao X, Fan H, Song Y (2021) Molecular mechanism of citrate efflux by the mitochondrial citrate transporter ct in filamentous fungus mucor circinelloides wj11. Front Microbiol 12:673881
doi: 10.3389/fmicb.2021.673881 pubmed: 34054781 pmcid: 8160456
Yao L, Shen H, Wang N, Tatlay J, Li L, Tan TW, Lee YK (2017) Elevated acetyl-coa by amino acid recycling fuels microalgal neutral lipid accumulation in exponential growth phase for biofuel production. Plant Biotechnol J 15:497–509
doi: 10.1111/pbi.12648 pubmed: 27734577
Yu L, Qin W, Lan WZ, Zhou P, Zhu M (2003) Improved arachidonic acids production from the fungus mortierella alpina by glutamate supplementation. Bioresour Technol 88:265–268
doi: 10.1016/S0960-8524(02)00312-7 pubmed: 12618051
Zhang H, Cui Q, Song X (2021) Research advances on arachidonic acid production by fermentation and genetic modification of mortierella alpina. World J Microb Biot 37:1–9
doi: 10.1007/s11274-020-02984-2
Zhou P-P, Meng J, Bao J (2017) Fermentative production of high titer citric acid from corn stover feedstock after dry dilute acid pretreatment and biodetoxification. Bioresour Technol 224:563–572
doi: 10.1016/j.biortech.2016.11.046 pubmed: 27913168
Zhu M, Yu L-J, Li W, Zhou P-P, Li C-Y (2006) Optimization of arachidonic acid production by fed-batch culture of mortierella alpina based on dynamic analysis. Enzyme Microb Tech 38:735–740
doi: 10.1016/j.enzmictec.2005.07.025

Auteurs

Chongran Sun (C)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Tao Yang (T)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Shuangfei Zhang (S)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Qikun Wen (Q)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Binyuan Gao (B)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Qianzi Liu (Q)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.

Haina Cheng (H)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.
Key Laboratory of Biometallurgy, Ministry of Education, Changsha, Hunan, China.

Yuguang Wang (Y)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China.
Key Laboratory of Biometallurgy, Ministry of Education, Changsha, Hunan, China.

Zhu Chen (Z)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China. zhuchen@csu.edu.cn.
Key Laboratory of Biometallurgy, Ministry of Education, Changsha, Hunan, China. zhuchen@csu.edu.cn.

Hongbo Zhou (H)

Department of Bioengineering, School of Minerals Processing and Bioengineering, Central South University, 932 South Lushan Road, Changsha, 410083, Hunan, P.R. China. zhouhb@mail.csu.edu.cn.
Key Laboratory of Biometallurgy, Ministry of Education, Changsha, Hunan, China. zhouhb@mail.csu.edu.cn.

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