Metabolomics analysis of salt tolerance of Zygosaccharomyces rouxii and guided exogenous fatty acid addition for improved salt tolerance.
Zygosaccharomyces rouxii
cell morphology
fatty acids
intracellular metabolites
salt tolerance
Journal
Journal of the science of food and agriculture
ISSN: 1097-0010
Titre abrégé: J Sci Food Agric
Pays: England
ID NLM: 0376334
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
revised:
09
03
2022
received:
26
07
2021
accepted:
04
05
2022
pubmed:
6
5
2022
medline:
5
10
2022
entrez:
5
5
2022
Statut:
ppublish
Résumé
Zygosaccharomyces rouxii plays an irreplaceable role in the manufacture of traditional fermented foods, which are produced in a high-salt environment. However, there is little research on strategies for improving salt tolerance of Z. rouxii. In this study, metabolomics was used to reveal the changes in intracellular metabolites under salt stress, and the results show that most of the carbohydrate contents decreased, the contents of xanthohumol and glycerol increased (fold change 4.07 and 5.35, respectively), while the contents of galactinol, xylitol and d-threitol decreased (fold change -9.43, -5.83 and -3.59, respectively). In addition, the content of four amino acids and six organic acids decreased, while that of the ten nucleotides increased. Notably, except for stearic acid (C18:0), all fatty acid contents increased. Guided by the metabolomics results, the effect of addition of seven exogenous fatty acids (C12:0, C14:0, C16:0, C18:0, C16:1, C18:1, and C18:2) on the salt tolerance of Z. rouxii was analyzed, and the results suggested that four exogenous fatty acids (C12:0, C16:0, C16:1, and C18:1) can increase the biomass yield and maximum growth rate. Physiological analyses demonstrated that exogenous fatty acids could regulate the distribution of fatty acids in the cell membrane, increase the degree of unsaturation, improve membrane fluidity, and maintain cell integrity, morphology and surface roughness. These results are applicable to revealing the metabolic mechanisms of Z. rouxii under salt stress and screening potential protective agents to improve stress resistance by adding exogenous fatty acids. © 2022 Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
Zygosaccharomyces rouxii plays an irreplaceable role in the manufacture of traditional fermented foods, which are produced in a high-salt environment. However, there is little research on strategies for improving salt tolerance of Z. rouxii.
RESULTS
RESULTS
In this study, metabolomics was used to reveal the changes in intracellular metabolites under salt stress, and the results show that most of the carbohydrate contents decreased, the contents of xanthohumol and glycerol increased (fold change 4.07 and 5.35, respectively), while the contents of galactinol, xylitol and d-threitol decreased (fold change -9.43, -5.83 and -3.59, respectively). In addition, the content of four amino acids and six organic acids decreased, while that of the ten nucleotides increased. Notably, except for stearic acid (C18:0), all fatty acid contents increased. Guided by the metabolomics results, the effect of addition of seven exogenous fatty acids (C12:0, C14:0, C16:0, C18:0, C16:1, C18:1, and C18:2) on the salt tolerance of Z. rouxii was analyzed, and the results suggested that four exogenous fatty acids (C12:0, C16:0, C16:1, and C18:1) can increase the biomass yield and maximum growth rate. Physiological analyses demonstrated that exogenous fatty acids could regulate the distribution of fatty acids in the cell membrane, increase the degree of unsaturation, improve membrane fluidity, and maintain cell integrity, morphology and surface roughness.
CONCLUSION
CONCLUSIONS
These results are applicable to revealing the metabolic mechanisms of Z. rouxii under salt stress and screening potential protective agents to improve stress resistance by adding exogenous fatty acids. © 2022 Society of Chemical Industry.
Substances chimiques
Amino Acids
0
Fatty Acids
0
Nucleotides
0
Stearic Acids
0
Glycerol
PDC6A3C0OX
Xylitol
VCQ006KQ1E
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6263-6272Informations de copyright
© 2022 Society of Chemical Industry.
Références
Yoshikawa S, Kurihara H, Kawai Y, Yamazaki K, Tanaka A, Nishikiori T et al., Effect of halotolerant starter microorganisms on chemical characteristics of fermented chum salmon (Oncorhynchus keta) sauce. J Agric Food Chem 58:6410-6417 (2010). https://doi.org/10.1021/jf904548u.
Li C, Jiang W, Ma N, Zhu Y, Dong X, Wang D et al., Bioaccumulation of cadmium by growing Zygosaccharomyces rouxii and Saccharomyces cerevisiae. Bioresour Technol 155:116-121 (2014). https://doi.org/10.1016/j.biortech.2013.12.098.
Qi W, Hou LH, Guo HL, Wang CL, Fan ZC, Liu JF et al., Effect of salt-tolerant yeast of Candida versatilis and Zygosaccharomyces rouxii on the production of biogenic amines during soy sauce fermentation. J Sci Food Agric 94:1537-1542 (2014). https://doi.org/10.1002/jsfa.6454.
Devanthi PVP, Linforth R, Kadri HE and Gkatzionis K, Water-in-oil-in-water double emulsion for the delivery of starter cultures in reduced-salt moromi fermentation of soy sauce. Food Chem 257:243-251 (2018). https://doi.org/10.1016/j.foodchem.2018.03.022.
Wei Q, Wang H, Chen Z, Lv Z, Xie Y and Lu F, Profiling of dynamic changes in the microbial community during the soy sauce fermentation process. Appl Microbiol Biotechnol 97:9111-9119 (2013). https://doi.org/10.1007/s00253-013-5146-9.
Wang D, Hao Z, Zhao J, Jin Y, Huang J, Zhou R et al., Comparative physiological and transcriptomic analyses reveal salt tolerance mechanisms of Zygosaccharomyces rouxii. Process Biochem 82:59-67 (2019). https://doi.org/10.1016/j.procbio.2019.04.009.
Wang D, Zhang M, Huang J, Zhou R, Jin Y and Wu C, Zygosaccharomyces rouxii combats salt stress by maintaining cell membrane structure and functionality. J Microbiol Biotechnol 30:62-70 (2020). https://doi.org/10.4014/jmb.1904.04006.
Dakal TC, Solieri L and Giudici P, Adaptive response and tolerance to sugar and salt stress in the food yeast Zygosaccharomyces rouxii. Int J Food Microbiol 185:140-157 (2014). https://doi.org/10.1016/j.ijfoodmicro.2014.05.015.
Ohta E, Nakayama Y, Mukai Y, Bamba T and Fukusaki E, Metabolomic approach for improving ethanol stress tolerance in Saccharomyces cerevisiae. J Biosci Bioeng 121:399-405 (2016). https://doi.org/10.1016/j.jbiosc.2015.08.006.
Hasunuma T, Sanda T, Yamada R, Yoshimura K, Ishii J and Kondo A, Metabolic pathway engineering based on metabolomics confers acetic and formic acid tolerance to a recombinant xylose-fermenting strain of Saccharomyces cerevisiae. Microb Cell Fact 10:2 (2011). https://doi.org/10.1186/1475-2859-10-2.
Park MK, Seo JA and Kim YS, Comparative study on metabolic changes of aspergillus oryzae isolated from fermented foods according to culture conditions. Int J Food Microbiol 307:108270 (2019). https://doi.org/10.1016/j.ijfoodmicro.2019.108270.
He G, Wu C, Huang J and Zhou R, Effect of exogenous proline on metabolic response of Tetragenococcus halophilus under salt stress. J Microbiol Biotechnol 27:1681-1691 (2017). https://doi.org/10.4014/jmb.1702.02060.
Qi Y, Liu H, Chen X and Liu L, Engineering microbial membranes to increase stress tolerance of industrial strains. Metab Eng 53:24-34 (2019). https://doi.org/10.1016/j.ymben.2018.12.010.
Wu C, Zhang J, Wang M, Du G and Chen J, Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39:1031-1039 (2012). https://doi.org/10.1007/s10295-012-1104-2.
Navarro-Tapia E, Querol A and Pérez-Torrado R, Membrane fluidification by ethanol stress activates unfolded protein response in yeasts. J Microbial Biotechnol 11:465-475 (2018). https://doi.org/10.1111/1751-7915.13032.
Zhu G, Yin N, Luo Q, Liu J and Wu J, Enhancement of sphingolipid synthesisimproves osmotic tolerance of Saccharomyces cerevisiae. Appl Environ Microbiol 86:e02911-e02919 (2020). https://doi.org/10.1128/AEM.02911-19.
Yin N, Zhu G, Luo Q, Liu J, Chen X and Liu L, Engineering of membrane phospholipid component enhances salt stress tolerance in Saccharomyces cerevisiae. Biotechnol Bioeng 117:710-720 (2020). https://doi.org/10.1002/bit.27244.
Lennen RM, Kruziki MA, Kumar K, Zinkel RA and Pfleger BF, Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Appl Environ Microbiol 77:8114-8128 (2011). https://doi.org/10.1128/AEM.05421-11.
Besada-Lombana PB, Fernandez-Moya R, Fenster J and Silva NAD, Engineering Saccharomyces cerevisiae fatty acid composition for increased tolerance to octanoic acid. Biotechnol Bioeng 114:1531-1538 (2017). https://doi.org/10.1002/bit.26288.
Wang D, Zhang M, Huang J, Zhou R, Jin Y, Zhao D et al., Heat preadaptation improved the ability of Zygosaccharomyces rouxii to salt stress: a combined physiological and transcriptomic analysis. Appl Microbiol Biotechnol 105:259-270 (2021). https://doi.org/10.1007/s00253-020-11005-z.
Wu C, Zhang J, Chen W, Wang M, Du G and Chen J, A combined physiological and proteomic approach to reveal lactic-acid-induced alterations in Lactobacillus casei Zhang and its mutant with enhanced lactic acid tolerance. Appl Microbiol Biotechnol 93:707-722 (2012). https://doi.org/10.1007/s00253-011-3757-6.
Zheng J, Liang R, Zhang L, Wu C, Zhou R and Liao X, Characterization of microbial communities in strong aromatic liquor fermentation pit muds of different ages assessed by combined DGGE and PLFA analyses. Food Res Int 54:660-666 (2013). https://doi.org/10.1016/j.foodres.2013.07.058.
Liao ZG, Tang T, Guan XJ, Dong W, Zhang J, Zhao GW et al., Improvement of transmembrane transport mechanism study of imperatorin on P-glycoprotein-mediated drug transport. Molecules 21:e1606 (2016). https://doi.org/10.3390/molecules21121606.
Ansari S, Gupta P, Mahanty SK and Prasad R, The uptake of amino acids by erg mutants of Candida albicans. Med Mycol 31:377-386 (1993). https://doi.org/10.1080/02681219380000481.
Yin Y, Shen M, Tan Z, Yu S, Liu J and Jiang G, Particle coating-dependent interaction of molecular weight fractionated natural organic matter: impacts on the aggregation of silver nanoparticles. Environ Sci Technol 49:6581-6589 (2015). https://doi.org/10.1021/es5061287.
Wu Y, Ding W, Jia L and He Q, The rheological properties of tara gum (Caesalpinia spinosa). Food Chem 168:366-371 (2015). https://doi.org/10.1016/j.foodchem.2014.07.083.
Peng Z, Vogel RF, Ehrmann MA, Waldhuber A and Xiong T, Phosphotransferase systems in Enterococcus faecalis OG1RF enhance the anti-stress capacity in vitro and in vivo. Res Microbiol 168:558-566 (2017). https://doi.org/10.1016/j.resmic.2017.03.003.
Buechel ER and Pinkett HW, Transcription factors and ABC transporters: from pleiotropic drug resistance to cellular signaling in yeast. FEBS Lett 594:3943-3964 (2020). https://doi.org/10.1002/1873-3468.13964.
Wen J, Deng X, Li Z, Dudley EG, Anantheswaran RC, Knabel SJ et al., Transcriptomic response of listeria monocytogenes during the transition to the long-term-survival phase. Appl Environ Microbiol 77:5966-5572 (2011). https://doi.org/10.1128/AEM.00596-11.
Pinu FR, Villas-Boas SG and Martin D, Pre-fermentative supplementation of fatty acids alters the metabolic activity of wine yeasts. Food Res Int 121:835-844 (2019). https://doi.org/10.1016/j.foodres.2019.01.005.
He G, Wu C, Huang J and Zhou R, Metabolic response of Tetragenococcus halophilus under salt stress. Biotechnol Bioprocess Eng 22:366-375 (2017). https://doi.org/10.1007/s12257-017-0015-5.
Parsons JB, Frank MW, Subramanian C, Saenkham P and Rock CO, Metabolic basis for the differential susceptibility of gram-positive pathogens to fatty acid synthesis inhibitors. Proc Natl Acad Sci USA 108:15378-15383 (2011). https://doi.org/10.1073/pnas.1109208108.
Khoomrung S, Laoteng K, Jitsue S and Cheevadhanarak S, Significance of fatty acid supplementation on profiles of cell growth, fatty acid, and gene expression of three desaturases in Mucor rouxii. Appl Microbiol Biotechnol 80:499-506 (2008). https://doi.org/10.1007/s00253-008-1569-0.
Liu H, Dai L, Wang F, Li X, Liu W, Pan B et al., A new understanding: gene expression, cell characteristic and antioxidant enzymes of Zygosaccharomyces rouxii under the D-fructose regulation. Enzyme Microb Technol 132:109409 (2020). https://doi.org/10.1016/j.enzmictec.2019.109409.
Herndon JL, Peters RE, Hofer RN, Simmons TB and Giles DK, Exogenous polyunsaturated fatty acids (PUFAs) promote changes in growth, phospholipid composition, membrane permeability and virulence phenotypes in Escherichia coli. BMC Microbiol 20:305 (2020). https://doi.org/10.1186/s12866-020-01988-0.
Duan LL, Shi Y, Jiang R, Yang Q, Wang YQ, Liu PT et al., Effects of adding unsaturated fatty acids on fatty acid composition of Saccharomyces cerevisiae and major volatile compounds in wine. S Afr J Enol Vitic 36:285-295 (2015). https://doi.org/10.21548/36-2-962.
Jin T, Rover MR, Petersen EM, Chi Z and Jarboe LR, Damage to the microbial cell membrane during pyrolytic sugar utilization and strategies for increasing resistance. J Ind Microbiol Biotechnol 44:1279-1292 (2017). https://doi.org/10.1007/s10295-017-1958-4.
Ballweg S and Ernst R, Control of membrane fluidity: the OLE pathway in focus. Biol Chem 398:215-228 (2017). https://doi.org/10.1515/hsz-2016-0277.
Yang Y, Xia Y, Hu W, Tao L and Ai L, Membrane fluidity of Saccharomyces cerevisiae from Huangjiu (Chinese rice wine) is variably regulated by OLE1 to offset the disruptive effect of ethanol. Appl Environ Microbiol 85:e01620-e01619 (2019). https://doi.org/10.1128/AEM.01620-19.
Yao S, Zhou R, Jin Y, Zhang L, Huang J and Wu C, Co-culture with Tetragenococcus halophilus changed the response of Zygosaccharomyces rouxii to salt stress. Process Biochem 95:279-287 (2020). https://doi.org/10.1016/j.procbio.2020.02.021.
Pandurangan M, Enkhtaivan G, Veerappan M, Mistry B, Patel R, Moon SH et al., Renal-protective and ameliorating impacts of omega-3 fatty acids against aspartame damaged MDCK cells. Biofactors 43:847-857 (2017). https://doi.org/10.1002/biof.1387.
Yao S, Hao L, Zhou R, Jin Y, Huang J and Wu C, Co-culture with Tetragenococcus halophilus improved the ethanol tolerance of Zygosaccharomyces rouxii by maintaining cell surface properties. Food Microbiol 97:103750 (2021). https://doi.org/10.1016/j.fm.2021.103750.