硫对酵母生物富铬过程中铬胁迫的缓解作用

doi:10.3864/j.issn.0578-1752.2019.06.011

摘要/Abstract

摘要：

【目的】探讨酿酒酵母YSI-3.7在富集Cr（Ⅲ）形成葡萄糖耐量因子（GTF）过程中自身抗氧化机制以及硫在该过程中发挥的作用,以期揭示硫对降低铬胁迫,进而提高生物富铬的作用机理。【方法】以高产GTF酿酒酵母YSI-3.7为目的菌株,通过设置不同浓度的Cr（Ⅲ）、硫组合进行生物富铬,测定不同条件下YSI-3.7菌株的生物富铬量以及相应氧化应激指标（如丙二醛(MDA)、超氧化物歧化酶（SOD）、过氧化氢酶（CAT）等）的变化,分析硫对酵母菌体在Cr（Ⅲ）胁迫下的改善作用。【结果】低浓度Cr（Ⅲ）（200 μg?mL ^-1）会刺激酵母YSI-3.7生长,使其生物量增加;而高浓度Cr（Ⅲ）（>500 μg·mL ^-1）对酵母生长有抑制作用。Cr（Ⅲ）浓度为500 μg?mL ^-1时,酵母中有机铬含量为（725.55±55.08）μg?g ^-1 DCW,总铬含量达（1 255.53±43.75）μg?g ^-1 DCW;Cr（Ⅲ）浓度为800 μg?mL ^-1时,有机铬为（536.25±36.89）μg?g ^-1 DCW,其中,总铬含量达（1 812.22±38.24）μg?g ^-1 DCW。随Cr（Ⅲ）浓度的增加（0—800 μg?mL ^-1）,菌体中MDA含量从11.83 nmol?mL ^-1升高到18.04 nmol?mL ^-1。SOD和CAT活力随Cr（Ⅲ）浓度升高而降低。在较低Cr（Ⅲ）浓度（≤500 μg?mL ^-1）下,谷胱甘肽（GSH）、总巯基、总抗氧化能力（T-AOC）含量均升高,但在高浓度Cr（Ⅲ）（800 μg?mL ^-1）下会降低。1 mmol?L ^-1 Na₂SO₃可以缓解Cr（Ⅲ）的胁迫作用,此时,酵母中蛋白质含量上升,MDA含量降低12.83%,CAT活力基本无影响,SOD活力提高4.41%,GSH、T-AOC、GSH-Px含量分别增加28.83%、14.29%和18.80%。【结论】酵母富铬过程中,Cr（Ⅲ）胁迫作用可造成酵母膜脂过氧化程度加重。在较低铬浓度时（≤500 μg?mL ^-1）,酵母可以通过自身抗氧化酶系统缓解该胁迫作用,其中发挥重要作用的是谷胱甘肽及其相关酶。高浓度Cr（Ⅲ）（800 μg?mL ^-1）下,膜脂过氧化程度进一步加重,酵母自身抗氧化能力不足以抵御Cr（Ⅲ）胁迫。硫（1 mmol?L ^-1 Na₂SO₃）可以通过提高酵母中SOD活力、GSH、T-AOC、GSH-Px含量,减轻Cr（Ⅲ）造成的膜脂过氧化程度,提高酵母自身抗氧化能力,进而提高酵母生物富铬效率。

关键词: 三价铬, 硫, 酿酒酵母, 葡萄糖耐量因子, 氧化应激

Abstract:

【Objective】The objective of this study was to investigate the antioxidative mechanism and role of sulphur during chromium (Ⅲ) enrichment by Saccharomyces cerevisiae. The mechanisms of alleviation chromium (Ⅲ) toxicity against yeast by sulphur were revealed. 【Method】Saccharomyces cerevisiae YSI-3.7 was used in this study. Various incubation conditions were investigated, such as various concentrations Cr(Ⅲ) and sulfate. And the corresponding biomass, total chromium content, organic chromium content and oxidative stress markers (including malondialdehyde (MDA), superoxide dismutase (SOD), catalase (CAT) and so on), were measured and analyzed. 【Result】 Low Cr(Ⅲ) concentration (0-200 μg?mL ^-1) could stimulate the growth of yeast, while high Cr(Ⅲ) concentration (>500 μg?mL ^-1) inhibited its growth. After Saccharomyces cerevisiae YSI-3.7 was incubated with 500 μg?mL ^-1 Cr(Ⅲ) for 44 h, the content of organic Cr in yeast was found to be 725.55±55.08 μg?g ^-1 DCW and that of total Cr was 1255.53±43.75 μg?g ^-1 DCW. After Saccharomyces cerevisiae YSI-3.7 was incubated with 800 μg?mL ^-1 Cr(Ⅲ) for 44 h, the content of organic Cr in yeast was found to be 536.25±36.89 μg?g ^-1 DCW and that of total Cr was 1812.22±38.24 μg?g ^-1 DCW. The content of MDA increased (from 11.83 nmol?mL ^-1 to 18.04 nmol?mL ^-1) with the increasement of Cr(Ⅲ) concentration (0-800 μg?mL ^-1), while the activity of SOD and CAT decreased. The content of GSH, total sulfhydryl and T-AOC increased at lower Cr(Ⅲ) concentration (≤500 μg?mL ^-1), and decreased at the high concentration (800 μg?mL ^-1). The supplementation of 1 mmol?L ^-1 Na₂SO₃during incubation could alleviate the stress of Cr(Ⅲ) against yeast. The protein content increased and MDA content decreased (12.83%) with the addition of 1 mmol?L ^-1 Na₂SO₃ during incubation. The activity of CAT was almost unaffected. The activity of SOD was increased to 4.41%. GSH, T-AOC and GSH-Px content increased to 28.83%, 14.29% and 18.80%, respectively. 【Conclusion】During the Cr(Ⅲ) bio-enrichment process by yeast, Cr(Ⅲ) stress could aggravate the lipid peroxidation of cell membrane. At low Cr(Ⅲ) concentration(0-500 μg?mL ^-1), yeast could protect itself from this stress by its own antioxidant enzymes, among which glutathione and its related enzymes played an important role. At high concentration of Cr(Ⅲ) (800 μg?mL ^-1) , the degree of membrane lipid peroxidation was aggravated and the yeast’s own antioxidant capacity was not enough to protect itself from Cr(Ⅲ) stress. Supplementation of S (1 mmol?L ^-1 Na₂SO₃) could mitigate membrane lipid peroxidation caused by Cr(Ⅲ)by improving SOD activity, GSH, T-AOC and GSH-Px content in yeast, improving the antioxidant capacity of yeast itself and Cr(Ⅲ) bio-enrichment by yeast.

Key words: Cr(Ⅲ);, S, Saccharomyces cerevisiae, GTF, oxidative stress

李函彤,甲承立,张书文,芦晶,逄晓阳,刘鹭,吕加平. 硫对酵母生物富铬过程中铬胁迫的缓解作用[J]. 中国农业科学, 2019, 52(6): 1078-1089.

LI HanTong,JIA ChengLi,ZHANG ShuWen,LU Jing,PANG XiaoYang,LIU Lu,LÜ JiaPing. Chromium (III) Stress Alleviation by Sulfur Compounds During Chromium Bio-enrichment by Saccharomyces cerevisiae[J]. Scientia Agricultura Sinica, 2019, 52(6): 1078-1089.

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参考文献 57

[1]	徐晨晨 . 微量元素铬对营养代谢调控的研究进展. 家禽科学, 2012(1):12-15. doi: 10.3969/j.issn.1673-1085.2012.01.003
	XU C C . Research progress on the regulation of nutrient metabolism by trace element chromium.Poultry Science, 2012(1):12-15. (in Chinese) doi: 10.3969/j.issn.1673-1085.2012.01.003
[2]	YEH G Y, EISENBERG D M, KAPTCHUK T J, PHILLIPS R.S. Systematic review of herbs and dietary supplements for glycemic control in diabetes. Diabetes Care, 2003,26(4):1277-1294. doi: 10.2337/diacare.26.4.1277 pmid: 12663610
[3]	HATFIELD M J, GILLESPIE S, CHEN Y, LI Z, CASSADY C J, VINCENT J B . Low-molecular-weight chromium-binding substance from chicken liver and American alligator liver. Comparative Biochemistry & Physiology, Part B, Biochemistry & Molecular Biology 2006, 144(4):423-431. doi: 10.1016/j.cbpb.2006.04.012 pmid: 16815060
[4]	CHEN Y, WATSON H M, GAO J, SINHA S H, CASSADY C J, VINCENT J.B. Characterization of the organic component of low-molecular-weight chromium-binding substance and its binding of chromium. Journal of Nutrition, 2011,141(7):1225-1232. doi: 10.3945/jn.111.139147 pmid: 21593351
[5]	BERNER T O, MURPHY M M, SLESINSKI R . Determining the safety of chromium tripicolinate for addition to foods as a nutrient supplement. Food & Chemical Toxicology, 2004,42(6):1029. doi: 10.1016/j.fct.2004.02.015 pmid: 15110112
[6]	MOLIN M, RENAULT J P, LAGNIEL G, PIN S, TOLEDANO M, LABARRE J . Ionizing radiation induces a Yap1-dependent peroxide stress response in yeast. Free Radical Biology & Medicine, 2007,43:136-144. doi: 10.1016/j.freeradbiomed.2007.04.007 pmid: 17561102
[7]	LI H, GUO A, WANG H . Mechanisms of oxidative browning of wine. Food Chemistry, 2008,108(1):1-13. doi: 10.1016/j.foodchem.2007.10.065
[8]	FERREIRA J, DU TOIT M , DU TOIT W J . The effects of copper and high sugar concentrations on growth, fermentation efficiency and volatile acidity production of different commercial wine yeast strains. Australian Journal of Grape & Wine Research, 2006,12(1):50-56. doi: 10.1111/j.1755-0238.2006.tb00043.x
[9]	廖芸, 曾英杰, 许笑男, 钟秋平, 赵久香 . 铜离子对荔枝酒降酸酵母发酵性能及醋酸代谢的影响. 食品科技, 2014(10):43-47.
	LIAO Y, ZENG Y J, XU X N, ZHONG Q P, ZHAO J X . Effect of copper ion on the fermentation performance and acetic acid metabolism of lychee wine yeast.Food Science and Technology, 2014(10):43-47. (in Chinese)
[10]	PANDA S K . Impact of copper on reactive oxygen species, lipid peroxidation and antioxidants in Lemna minor. Biologia Plantarum, 2008,52(3):561-564. doi: 10.1007/s10535-008-0111-7
[11]	GAETKE L M, CHOW C K . Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology, 2003,189(1/2):147. doi: 10.1016/S0300-483X(03)00159-8 pmid: 12821289
[12]	LIN C C, KAO C H . Effect of NaCl stress on H₂O₂ metabolism in rice leaves. Plant Growth Regulation, 2000,30(2):151-155. doi: 10.1023/A:1006345126589
[13]	BRENNAN R J , SCHIESTL R H . Cadmium is an inducer of oxidative stress in yeast. Mutation Research, 1996, 356(2): 171-178. doi: 10.1016/0027-5107(96)00051-6 pmid: 8841482
[14]	MENEZES R A, AMARAL C, BATISTA-NASCIMMENTO L, SANTOS C, RODRIGUES-POUSADA C . Contribution of Yap1 towards Saccharomyces cerevisiae adaptation to arsenic-mediated oxidative stress. Biochemical Journal, 2008,414(2):301-311.
[15]	BEYERSMANN D, HARTWIG A . Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Archives of Toxicology, 2008,82(8):493-512. doi: 10.1007/s00204-008-0313-y
[16]	HARRIS G K, SHI X L . Signaling by carcinogenic metals and metal-induced reactive oxygen species. Mutation Research, 2003, 533(1):183-200.
[17]	BEYERSMANN D, HARTWIG A . Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Archives of Toxicology, 2008,82(8):493-512. doi: 10.1007/s00204-008-0313-y
[18]	刘鹭, 吕加平, 高艳红 . 空间搭载高产葡萄糖耐量因子(GTF)酵母的选育. 微生物学通报, 2009,36(2):223-230.
	LIU L, LÜ J P, GAO Y H . Breeding of high yield glucose tolerance factor (GTF) yeast in space. Microbiology, 2009,36(2):223-230. (in Chinese)
[19]	ALEXANDER J, AASETH J . Uptake of chromate in human red-blood-cells and isolated rat-liver cells - the role of the anion carrier. Analyst, 1995,120(3):931-933. doi: 10.1039/AN9952000931 pmid: 7741257
[20]	SUMMERS A O . Damage control: Regulating defenses against toxic metals and metalloids. Current Opinion Microbiology, 2009,12(2):138. doi: 10.1016/j.mib.2009.02.003 pmid: 19282236
[21]	SALNIKOW K, ZHIKOVICH A . Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic and chromium. Chemical Research Toxicology, 2008,21(1):28-24. doi: 10.1021/tx700198a pmid: 17970581
[22]	PEREIRA Y, LAGNIEL G, GODAT E, BAUDOUIN-CORNU P, JUNOT C, LABARRE J . Chromate causes sulfur starvation in yeast. Toxicological Sciences, 2008,106(2):400-412. doi: 10.1002/app.12197 pmid: 18794233
[23]	冯建永, 庞民好, 张金林, 刘颖超 . 复杂盐碱对黄顶菊种子萌发和幼苗生长的影响及机理初探. 草业学报, 2010,19(5):77-86. doi: 10.11686/cyxb20100512
	FENG J Y, PANG M H, ZHANG J L, LIU Y C . Study on complex effects on saline flaveriabidentis seed germination and seedling growth and its mechanism. Acta prataculturae sinica, 2010,19(5):77-86. (in Chinese) doi: 10.11686/cyxb20100512
[24]	高春生, 王春秀, 张书松 . 水体铜对黄河鲤肝胰脏抗氧化酶活性和总抗氧化能力的影响. 农业环境科学学报, 2008,27(3):1157-1162. doi: 10.3321/j.issn:1672-2043.2008.03.055
	GAO C S, WANG C X, ZHANG S S . Effect of water copper on antioxidant enzyme activity and total antioxidant capacity of hepatopancreas in the Yellow River carp. Journal of Agricultural Environmental Science, 2008,27(3):1157-1162. (in Chinese) doi: 10.3321/j.issn:1672-2043.2008.03.055
[25]	GADJEV I, STONE J M, GECHEV T S . Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. International Review of Cell & Molecular Biology, 2008,270:87-144. doi: 10.1016/S1937-6448(08)01403-2 pmid: 19081535
[26]	TIWARI K, DWIVEDI K, SINGH S . Chromium (VI) induced phytotoxicity and oxidative stress in pea ( Pisum sativum L.): Biochemical changes and translocation of essential nutrients. Journal of Environmental Biology, 2009,30(3):389. pmid: 20120464
[27]	PEREIRA M D, HERDERIRO R S, FERNANDES P N , ELEUTHERIO E C A, PANEK A D . Targets of oxidative stress in yeast sod mutants. Biochinica et Biophysica Acta, 2003,1620(1-3):245-251. doi: 10.1016/S0304-4165(03)00003-5 pmid: 12595095
[28]	APEL K, HIRTIRT H . Reactive oxygen species: Metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology, 2004,55:373-399. doi: 10.1146/annurev.arplant.55.031903.141701
[29]	MITTLER R, VANDERAUWERA S, GOLLERY M, BREUSEGEM F V . Reactive oxygen gene network of plants. Trends in Plant Science, 2004,9(10):490-498. doi: 10.1016/j.tplants.2004.08.009 pmid: 15465684
[30]	KEUNEN E, REMANS T, BOHLER S, VANGRONSVELD J, CUYPERS A . Metal-induced oxidative stress and plant mitochondria. International Journal of Molecular Sciences, 2011,12(10):6894-6918. doi: 10.3390/ijms12106894 pmid: 3211017
[31]	MANGABEIRA P A, FERREIRA A S , DE ALMEIDA A A F, FERNANDES V F, LUCENA E, SOUZA V L, DOS SANTOS JÚNIOR A J, OLIVEIRA A H, GRENIER-LOUSTALOT M F, BARBIER F, SILVA D C . Compartmentalization and ultrastructural alterations induced by chromium in aquatic macrophytes. Biometals, 2011,24(6):1017-1026. doi: 10.1007/s10534-011-9459-9 pmid: 21562773
[32]	DAUD M K, MEI L, VARIATH M T, ALI S, LI C, RAFIQ M T, ZHU S J . Chromium (VI) uptake and tolerance potential in cotton cultivars: Effect on their root physiology, ultramorphology, and oxidative metabolism. Biomed Research International, 2014,2014(2):975946. doi: 10.1155/2014/975946 pmid: 4053220
[33]	赵风斌, 王丽卿, 季高华, 李为星 . 盐胁迫对3种沉水植物生物学指标及叶片中丙二醛含量的影响. 环境污染与防治, 2012,34(10):40-44. doi: 10.3969/j.issn.1001-3865.2012.10.009
	ZHAO F B, WANG L Q, JI G H, LI W X . Effects of salt stress on the biological indexes of 3 submerged plants and the content of malondialdehyde in leaves. Environmental Pollution and Prevention, 2012,34(10):40-44. (in Chinese) doi: 10.3969/j.issn.1001-3865.2012.10.009
[34]	孟衡玲, 张薇, 卢丙越, 何芳芳, 鲁海菊 . 金银花幼苗对盐胁迫的生理响应. 江苏农业科学, 2015,43(4):247-249. doi: 10.15889/j.issn.1002-1302.2015.04.090
	MENG H L, ZHANG W, LU B Y, HE F F, LU H J . Physiological response of Lonicera japonica seedlings to salt stress. Jiangsu Agricultural Sciences, 2015,43(4):247-249. (in Chinese) doi: 10.15889/j.issn.1002-1302.2015.04.090
[35]	吴灵琼, 成水平, 杨立华, 吴振斌 . Cd ²⁺和Cu ²⁺对美人蕉的氧化胁迫及抗性机理研究 . 农业环境科学学报, 2007,26(4):1365-1369. doi: 10.3321/j.issn:1672-2043.2007.04.033
	WU L Q, CHENG S P, YANG L H, WU Z B . Effects of Cd ²⁺ and Cu ²⁺ on oxidative stress and resistance mechanism of Canna indica. Journal of Agricultural Environmental Science, 2007,26(4):1365-1369. (in Chinese) doi: 10.3321/j.issn:1672-2043.2007.04.033
[36]	SHAH K, KUMAR R G, VERMA S, DUBEY R S . Effects of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Science, 2001,161(6):1135-1144. doi: 10.1016/S0168-9452(01)00517-9
[37]	杜君, 李海兰, 李慧, 战吉宬, 黄卫东 . 铜对葡萄酒酿酒酵母的氧化胁迫机制. 中国农业科学, 2011,44(2):369-378. doi: 10.3864/j.issn.0578-1752.2011.02.017
	DU J, LI H L, LI H, ZHAN J C, HUANG W D . Oxidative stress of wine yeasts under copper exposure. Scientia Agricultura Sinica, 2011,44(2):369-378. (in Chinese) doi: 10.3864/j.issn.0578-1752.2011.02.017
[38]	DEVI S R, YAMMAOTO Y, MASTUMOTO H . An intracellular mechanism of aluminum tolerance associaced antioxidant status in cultured tobacco cells. Journal of Inorganic Biochemistry, 2003,97(1):59-68. doi: 10.1016/S0162-0134(03)00182-X pmid: 14507461
[39]	金承涛 . Al ³⁺、高温对酿酒酵母的胁迫作用及其耐性机制的研究 [D]. 杭州: 浙江大学, 2005.
	JIN C T . The effect of Al ³⁺, high temperature stress on Saccharomyces cerevisiae and its tolerance mechanism research [D]. Hangzhou: Zhejiang University, 2005.
[40]	LI J S, JIA H L, WANG J, CAO Q H, WEN Z C . Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na +/H + antiporter system in the hydrogen peroxide-dependent manner in saltstress Arabidopsis thaliana root. Protoplasma, 2014,251(4):899-912. doi: 10.1007/s00709-013-0592-x pmid: 24318675
[41]	CHRISTOU A, MANGANARIS G A, PAPADOPOULOS I, FOTOPOULOS V . Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiole defence pathways. Journal of Experimental Botany, 2013,64:1953-1966. doi: 10.1093/jxb/ert055 pmid: 3638822
[42]	SHI H T, YE T T, CHAN Z L . Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass. Plant Physiology & Biochemistry, 2013,71(2):226-234. doi: 10.1016/j.plaphy.2013.07.021 pmid: 23974354
[43]	安志装, 王校常, 严蔚东, 施卫明, 曹志洪 . 植物螯合肽及其在重金属胁迫下的适应机制. 植物生理学报, 2001,37(5):463-467. doi: 10.1088/0256-307X/18/11/313
	AN Z Z, WANG X C, YAN W D, SHI W M, CAO Z H . Phytochelatins and its adaptive mechanism under heavy metal stress. Plant Physiology Communications, 2001,37(5):463-467. (in Chinese) doi: 10.1088/0256-307X/18/11/313
[44]	李文学, 陈同斌 . 超富集植物吸收富集重金属的生理和分子生物学机制. 应用生态学报, 2003,14(4):627-631.
	LI W X, CHEN T B . Physiobgical and molecular biological mechanisms of heavy metal absorption and accumulation in hyperaccumulators. Chinese Journal of Applied Ecology, 2003,14(4):627-631. (in Chinese)
[45]	郞飞波, 张国平 . 植物螯合肽及其在重金属耐性中的作用. 应用生态学报, 2003,14(4):632-636.
	LANG F B, ZHANG G P . Phytochelatin and its function in heavy metal tolerance of higher plants. Chinese Journal of Applied Ecology, 2003,14(4):632-636. (in Chinese).
[46]	王宁 . 重金属胁迫与生物样品中巯基化合物的应答作用[D]. 延吉: 延边大学, 2014.
	WANG N . Heavy metal stress and the response of sulfhydryl compounds in biological samples [D]. Yanji: Yanbian University , 2014. (in Chinese)
[47]	COLEMAN J, BLAKE-KALFF M, DAVIES E . Detoxification of xenobiotics by plants: Chemical modification and vacuolar compartmentation. Trends in Plant Science, 1997,2(4):144-151. doi: 10.1016/S1360-1385(97)01019-4
[48]	FREEMAN J L, PERSANS M W , NIEMAN K . Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyper accumulators. Plant Cell, 2004,16(8):2176-2191. doi: 10.1105/tpc.104.023036 pmid: 15269333
[49]	COBBETT C, GOLDSBROUGH P . Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology, 2002,53(1):159. doi: 10.1146/annurev.arplant.53.100301.135154
[50]	NOCTOR G, GOMEZ L, VANACKER H, FOYER C H . Interaction between biosynthesis, compartmentation and tansport in the control of gluthione homeostasis and signaling. Journal of Experimental Botany, 2002,53(372):1283-1304. doi: 10.1093/jexbot/53.372.1283 pmid: 11997376
[51]	SUGIYAMA K, IZAWA S, INOUE Y . The Yap 1p- dependent induction of glutathione synthesis in heat shock response of Saccharomyces cerevisiae. Journal of Biological Chemistry, 2000,275(20):15535-15540.
[52]	IZAWA S, INOUE Y, KIMURA A . Oxidative stress response in yeast: Effect of glutathione on adaptatin to hydrogen peroxide stress in Saccharomyces cerevisiae. FEBS Letters, 1995,368(1):73-76. doi: 10.1016/0014-5793(95)00603-7 pmid: 7615092
[53]	WESTWATER J, MCLAREN N F, DORMER U H, JAMIESON D J . The adaptive response of Saccharomyces cerevisiae to mercury exposure. Yeast, 2002,19(3):233-239.
[54]	SHANMUGANATHANA, AVERY SV, WILLETTS S A . Copper- induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Letters, 2004,556(1-3):253-259.
[55]	SUGIYAMA K, KAWANRA A, IZAWA S, INOUE Y . Role of glutathione in heat-shock-induced cell death of Saccharomyces cerevisiae. Biochemical Journal, 2000,352(1):71-78.
[56]	TONGUL B, KAVAKCIOGLU B, TARHAN L . Chloramine T induced oxidative stress and the response of antioxidant system inPhanerochaete chrysosporium. Folia Microbiologica, 2017(1-2):1-9.
[57]	MUKAI K, MORINCOTO H, OKAUCHI Y, NAGAOKA S . Kinetic study of reactions between tocopheroxyl radicals and fatty acids. Lipids, 1993,28(8):753-756. doi: 10.1007/BF02535999

	Cr（Ⅲ） (μg?mL^-1)
	0	200	500	800
生物量 Biomass (g/100 mL)	1.40±0.07	1.06±0.01	0.97±0.05	0.45±0.02
有机铬 Organic chromium (μg·g^-1DCW)	0	224.74±6.41	725.55±55.08	536.25±36.89
总铬 Total chromium (μg·g^-1DCW)	0	409.04±12.65	1255.53±43.75	1812.22±38.24
有机铬/总铬 Organic/total chromium (%)	0	54.94±1.90	57.79±2.45	29.59±2.48

检测指标 Index	Cr（Ⅲ）浓度 Cr（Ⅲ） concentration (μg?mL^-1)
检测指标 Index	0	200	500	800
丙二醛 MDA (nmol?mL^-1)	11.83±0.38	15.54±0.41	16.91±0.33	18.04±0.44
超氧化物岐化酶 SOD (U?mg^-1prot)	8.61±0.19	8.28±0.11	7.93±0.07	7.35±0.21
过氧化氢酶 CAT (U?mg^-1prot)	9.09±0.28	7.83±0.14	4.72±0.09	3.64±0.03
还原型谷胱甘肽 GSH (μmol?g^-1 prot)	31.42±1.54	40.22±1.38	48.52±2.01	43.84±1.94
氧化型谷胱甘肽 GSSG (μmol?g^-1 prot)	7.86±0.21	9.56±0.32	12.38±0.52	15.46±0.61
谷胱甘肽氧化酶 GSH-Px (U?g^-1 prot)	1044.51±10.22	1274.32±5.89	763.01±3.21	534.68±6.76
总巯基 -SH (μg?g^-1 prot)	38.51±1.14	53.44±2.71	59.05±2.98	35.74±1.97
总抗氧化能力 T-AOC (U?g^-1 prot)	0.8±0.21	0.85±0.19	1.61±0.32	0.35±0.01

含硫化合物 S compound	浓度 Concentration (mmol?L^-1)	生物量 Biomass (g/100 mL)	有机铬 Organic chromium (μg·g^-1·DCW)	总铬 Total chromium (μg·g^-1·DCW)	有机铬率 Percentage of organic chromium (%)
0	对照组 Control	1.002±0.1	755.63±4.23	1431.93±10.12	52.77±1.24
Na₂SO₃	0.5	0.92±0.07	1198.16±9.43	1578.21±11.27	75.92±3.75
	1	0.85±0.08	1607.02±6.78	1876.32±9.43	85.65±2.36
	5	0.60±0.04	2052.43±10.58	2755.04±11.38	74.50±3.57
	10	0.49±0.03	609.58±4.98	1746.95±8.79	34.84±1.98
	15	0.32±0.02	477.39±2.75	740.18±8.02	64.50±1.63
Na₂S	0.5	1.005±0.25	895.98±5.72	1601.45±5.98	55.95±1.48
	1	1.08±0.07	1261.16±6.27	1868.74±9.98	67.75±2.32
	5	0.781±0.03	691.63±3.61	2302.31±11.54	30.04±1.03
	10	0.69±0.08	613.83±2.88	3516.62±21.32	17.46±0.98
	15	0.15±0.04	318.70±1.02	3834.02±20.98	8.31±0.45
（NH₄）₂SO₃	0.5	0.996±0.05	721.01±2.79	2101.45±14.32	34.31±1.74
	1	0.942±0.04	861.12±5.97	2868.14±16.45	30.02±1.05
	5	0.276±0.02	542.19±4.34	3000.21±18.91	18.07±1.13
	10	0.121±0.02	301.21±2.83	1812.62±13.69	16.62±0.45
	15	0.085±0.01	100.32±1.56	1367.02±9.13	7.33±0.41