Microbial Sulfur Metabolism and Stress Resistance

doi:10.13560/j.cnki.biotech.bull.1985.2023-0616

Abstract

Abstract:

Sulfur metabolism is an important life metabolism in microbes. Sulfur transportation, assimilation, metabolic regulation and biosynthesis of important sulfur-containing compounds by microorganisms not only affect the growth and metabolism of microorganisms, but also influence the stress resistance and robustness of microorganisms in inhibitory environments. Most of current researches are focusing on the microbial sulfate assimilatory reduction process and H₂S production with few studies on microbial sulfur metabolism and stress resistance. This review summarized sulfate transport, assimilatory reduction pathway, and regulatory networks in the process of sulfur metabolism. Combined with the oxidative stress responses of microorganisms under different stress conditions, the review discussed mechanism by which sulfur-containing compounds such as hydrogen sulfide, glutathione and cysteine improve the stress resistance of microorganisms. The revelation of molecular mechanism between sulfur metabolism and microbial stress resistance will not only help understand microbial sulfur metabolism further, but also provide candidate molecular targets for the design and construction of efficient and robust industrial strains.

Key words: sulfur metabolism, oxidative stress responses, stress resistance, sulfate assimilation, H₂S

YAN Xiong-ying, WANG Zhen, WANG Xia, YANG Shi-hui. Microbial Sulfur Metabolism and Stress Resistance[J]. Biotechnology Bulletin, 2023, 39(11): 150-167.

Figures/Tables 10

References 109

[1]	Sano C. History of glutamate production[J]. Am J Clin Nutr, 2009, 90(3): 728S-732S. doi: 10.3945/ajcn.2009.27462F URL
[2]	Otero JM, Nielsen J. Industrial systems biology[J]. Biotechnol Bioeng, 2010, 105(3): 439-460. doi: 10.1002/bit.22592 pmid: 19891008
[3]	Atsumi S, Higashide W, Liao JC. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde[J]. Nat Biotechnol, 2009, 27(12): 1177-1180. doi: 10.1038/nbt.1586 pmid: 19915552
[4]	Galanie S, Thodey K, Trenchard IJ, et al. Complete biosynthesis of opioids in yeast[J]. Science, 2015, 349(6252): 1095-1100. doi: 10.1126/science.aac9373 pmid: 26272907
[5]	Yang SH, Franden MA, Wang X, et al. Transcriptomic profiles of Zymomonas mobilis 8b to furfural acute and long-term stress in both glucose and xylose conditions[J]. Front Microbiol, 2020, 11: 13. doi: 10.3389/fmicb.2020.00013 URL
[6]	Motohashi H, Akaike T. Sulfur-utilizing cytoprotection and energy metabolism[J]. Curr Opin Physiol, 2019, 9: 1-8.
[7]	Aguilar-Barajas E, Díaz-Pérez C, Ramírez-Díaz MI, et al. Bacterial transport of sulfate, molybdate, and related oxyanions[J]. Biometals, 2011, 24(4): 687-707. doi: 10.1007/s10534-011-9421-x pmid: 21301930
[8]	Kertesz MA. Bacterial transporters for sulfate and organosulfur compounds[J]. Res Microbiol, 2001, 152(3-4): 279-290. pmid: 11421275
[9]	Mansilla MC, de Mendoza D. The Bacillus subtilis cysP gene encodes a novel sulphate permease related to the inorganic phosphate transporter(Pit)family[J]. Microbiology, 2000, 146(Pt 4): 815-821. doi: 10.1099/00221287-146-4-815 URL
[10]	Zhang L, Jiang WS, Nan J, et al. The Escherichia coli CysZ is a pH dependent sulfate transporter that can be inhibited by sulfite[J]. Biochim Biophys Acta, 2014, 1838(7): 1809-1816. doi: 10.1016/j.bbamem.2014.03.003 pmid: 24657232
[11]	Rückert C, Koch DJ, Rey DA, et al. Functional genomics and expression analysis of the Corynebacterium glutamicum fpr2-cysIXHDNYZ gene cluster involved in assimilatory sulphate reduction[J]. BMC Genomics, 2005, 6: 121. doi: 10.1186/1471-2164-6-121
[12]	Eichhorn E, van der Ploeg JR, Leisinger T. Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems[J]. J Bacteriol, 2000, 182(10): 2687-2695. doi: 10.1128/JB.182.10.2687-2695.2000 pmid: 10781534
[13]	Thurmond S. Regulation of cysteine biosynthesis in Acinetobacter baylyi ADP1[D]. Georgia: University of Georgia, 2014.
[14]	Kawano Y, Suzuki K, Ohtsu I. Current understanding of sulfur assimilation metabolism to biosynthesize L-cysteine and recent progress of its fermentative overproduction in microorganisms[J]. Appl Microbiol Biotechnol, 2018, 102(19): 8203-8211. doi: 10.1007/s00253-018-9246-4 pmid: 30046857
[15]	Nakatani T, Ohtsu I, Nonaka G, et al. Enhancement of thioredoxin/glutaredoxin-mediated L-cysteine synthesis from S-sulfocysteine increases L-cysteine production in Escherichia coli[J]. Microb Cell Fact, 2012, 11: 62. doi: 10.1186/1475-2859-11-62 pmid: 22607201
[16]	Funahashi E, Saiki K, Honda K, et al. Finding of thiosulfate pathway for synthesis of organic sulfur compounds in Saccharomyces cerevisiae and improvement of ethanol production[J]. J Biosci Bioeng, 2015, 120(6): 666-669. doi: 10.1016/j.jbiosc.2015.04.011 pmid: 26188417
[17]	Kredich NM. The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli[J]. Mol Microbiol, 1992, 6(19): 2747-2753. pmid: 1435253
[18]	Guédon E, Martin-Verstraete I. Cysteine metabolism and its regulation in bacteria[M]//Wendisch VF, Ed. Amino Acid Biosynthesis - Pathways, Regulation and Metabolic Engineering. Berlin, Heidelberg: Springer Berlin Heidelberg, 2006: 195-218.
[19]	van der Ploeg JR, Eichhorn E, Leisinger T. Sulfonate-sulfur metabolism and its regulation in Escherichia coli[J]. Arch Microbiol, 2001, 176(1-2): 1-8. pmid: 11479697
[20]	Guillouard I, Auger S, Hullo MF, et al. Identification of Bacillus subtilis CysL, a regulator of the cysJI operon, which encodes sulfite reductase[J]. J Bacteriol, 2002, 184(17): 4681-4689. doi: 10.1128/JB.184.17.4681-4689.2002 pmid: 12169591
[21]	Sperandio B, Polard P, Ehrlich DS, et al. Sulfur amino acid metabolism and its control in Lactococcus lactis IL1403[J]. J Bacteriol, 2005, 187(11): 3762-3778. pmid: 15901700
[22]	Rey DA, Pühler A, Kalinowski J. The putative transcriptional repressor McbR, member of the TetR-family, is involved in the regulation of the metabolic network directing the synthesis of sulfur containing amino acids in Corynebacterium glutamicum[J]. J Biotechnol, 2003, 103(1): 51-65. doi: 10.1016/S0168-1656(03)00073-7 URL
[23]	Deparis Q, Claes A, Foulquié-Moreno MR, et al. Engineering tolerance to industrially relevant stress factors in yeast cell factories[J]. FEMS Yeast Res, 2017, 17(4): fox036.
[24]	Beales N. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review[J]. Compr Rev Food Sci Food Saf, 2004, 3(1): 1-20. doi: 10.1111/crfs.2004.3.issue-1 URL
[25]	许可, 王靖楠, 李春. 智能抗逆微生物细胞工厂与绿色生物制造[J]. 合成生物学, 2020, 1(4): 427-439. doi: 10.12211/2096-8280.2020-045
	Xu K, Wang JN, Li C. Intelligent microbial cell factory with tolerance for green biological manufacturing[J]. Synth Biol J, 2020, 1(4): 427-439.
[26]	Xu K, Yu LP, Bai WX, et al. Construction of thermo-tolerant yeast based on an artificial protein quality control system(APQC)to improve the production of bio-ethanol[J]. Chem Eng Sci, 2018, 177: 410-416. doi: 10.1016/j.ces.2017.12.009 URL
[27]	Cunha JT, Soares PO, Baptista SL, et al. Engineered Saccharomyces cerevisiae for lignocellulosic valorization: a review and perspectives on bioethanol production[J]. Bioengineered, 2020, 11(1): 883-903. doi: 10.1080/21655979.2020.1801178 URL
[28]	Caspeta L, Nielsen J. Thermotolerant yeast strains adapted by laboratory evolution show trade-off at ancestral temperatures and preadaptation to other stresses[J]. mBio, 2015, 6(4): e00431.
[29]	Tian XJ, Yu QQ, Shao LL, et al. Comparative transcriptomic study of Escherichia coli O157: H7 in response to ohmic heating and conventional heating[J]. Food Res Int, 2021, 140: 109989. doi: 10.1016/j.foodres.2020.109989 URL
[30]	Zhou LZ, Ma Y, Wang KH, et al. Omics-guided bacterial engineering of Escherichia coli ER2566 for recombinant protein expression[J]. Appl Microbiol Biotechnol, 2023, 107(2-3): 853-865. doi: 10.1007/s00253-022-12339-6
[31]	Samappito J, Yamada M, Klanrit P, et al. Characterization of a thermo-adapted strain of Zymomonas mobilis for ethanol production at high temperature[J]. 3 Biotech, 2018, 8(11): 474. doi: 10.1007/s13205-018-1493-7 pmid: 30456008
[32]	Lu Z, Sethu R, Imlay JA. Endogenous superoxide is a key effector of the oxygen sensitivity of a model obligate anaerobe[J]. Proc Natl Acad Sci USA, 2018, 115(14): E3266-E3275.
[33]	Sund CJ, Rocha ER, Tzianabos AO, et al. The Bacteroides fragilis transcriptome response to oxygen and H₂O₂: the role of OxyR and its effect on survival and virulence[J]. Mol Microbiol, 2008, 67(1): 129-142. doi: 10.1111/mmi.2008.67.issue-1 URL
[34]	Betteken MI, Rocha ER, Smith CJ. Dps and DpsL mediate survival in vitro and in vivo during the prolonged oxidative stress response in Bacteroides fragilis[J]. J Bacteriol, 2015, 197(20): 3329-3338. doi: 10.1128/JB.00342-15 pmid: 26260459
[35]	Lauret R, Morel-Deville F, Berthier F, et al. Carbohydrate utilization in Lactobacillus sake[J]. Appl Environ Microbiol, 1996, 62(6): 1922-1927. doi: 10.1128/aem.62.6.1922-1927.1996 URL
[36]	Veiga-da-Cunha M, Santos H, Van Schaftingen E. Pathway and regulation of erythritol formation in Leuconostoc oenos[J]. J Bacteriol, 1993, 175(13): 3941-3948. pmid: 8391532
[37]	Yang SH, Fei Q, Zhang YP, et al. Zymomonas mobilis as a model system for production of biofuels and biochemicals[J]. Microb Biotechnol, 2016, 9(6): 699-717. doi: 10.1111/mbt2.2016.9.issue-6 URL
[38]	LaCroix RA, Sandberg TE, O'Brien EJ, et al. Use of adaptive laboratory evolution to discover key mutations enabling rapid growth of Escherichia coli K-12 MG1655 on glucose minimal medium[J]. Appl Environ Microbiol, 2015, 81(1): 17-30. doi: 10.1128/AEM.02246-14 URL
[39]	González-Ramos D, Gorter de Vries AR, Grijseels SS, et al. A new laboratory evolution approach to select for constitutive acetic acid tolerance in Saccharomyces cerevisiae and identification of causal mutations[J]. Biotechnol Biofuels, 2016, 9: 173. doi: 10.1186/s13068-016-0583-1 pmid: 27525042
[40]	Xu N, Lv HF, Wei L, et al. Impaired oxidative stress and sulfur assimilation contribute to acid tolerance of Corynebacterium glutamicum[J]. Appl Microbiol Biotechnol, 2019, 103(4): 1877-1891. doi: 10.1007/s00253-018-09585-y
[41]	Yang Q, Yang YF, Tang Y, et al. Development and characterization of acidic-pH-tolerant mutants of Zymomonas mobilis through adaptation and next-generation sequencing-based genome resequencing and RNA-Seq[J]. Biotechnol Biofuels, 2020, 13: 144. doi: 10.1186/s13068-020-01781-1
[42]	Zaldivar J, Martinez A, Ingram LO. Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli[J]. Biotechnol Bioeng, 1999, 65(1): 24-33. doi: 10.1002/(sici)1097-0290(19991005)65:1<24::aid-bit4>3.0.co;2-2 pmid: 10440668
[43]	Hadi SM, Shahabuddin, Rehman A. Specificity of the interaction of furfural with DNA[J]. Mutat Res, 1989, 225(3): 101-106.
[44]	Khan QA, Hadi SM. Effect of furfural on plasmid DNA[J]. Biochem Mol Biol Int, 1993, 29(6): 1153-1160. pmid: 8330021
[45]	闻远, 夏娟, 戚良华, 等. 抗氧化基因过表达提高运动发酵单胞菌糠醛耐受性[J]. 生物技术通报, 2019, 35(8): 85-94. doi: 10.13560/j.cnki.biotech.bull.1985.2019-0040
	Wen Y, Xia J, Qi LH, et al. Enhanced furfural tolerance in Zymomonas mobilis by the overexpression of antioxidant genes[J]. Biotechnol Bull, 2019, 35(8): 85-94.
[46]	Jiang T, Li CY, Teng YX, et al. Recent advances in improving metabolic robustness of microbial cell factories[J]. Curr Opin Biotechnol, 2020, 66: 69-77. doi: 10.1016/j.copbio.2020.06.006 URL
[47]	常瀚文, 郑鑫铃, 骆健美, 等. 抗逆元件及其在高效微生物细胞工厂构建中的应用进展[J]. 生物技术通报, 2020, 36(6): 13-34. doi: 10.13560/j.cnki.biotech.bull.1985.2020-0259
	Chang HW, Zheng XL, Luo JM, et al. Tolerance elements and their application progress on the construction of highly-efficient microbial cell factory[J]. Biotechnol Bull, 2020, 36(6): 13-34.
[48]	Yan XY, Wang X, Yang YF, et al. Cysteine supplementation enhanced inhibitor tolerance of Zymomonas mobilis for economic lignocellulosic bioethanol production[J]. Bioresour Technol, 2022, 349: 126878. doi: 10.1016/j.biortech.2022.126878 URL
[49]	Geng BN, Liu SY, Chen YH, et al. A plasmid-free Zymomonas mobilis mutant strain reducing reactive oxygen species for efficient bioethanol production using industrial effluent of xylose mother liquor[J]. Front Bioeng Biotechnol, 2022, 10: 1110513. doi: 10.3389/fbioe.2022.1110513 URL
[50]	Nieves IU, Geddes CC, Miller EN, et al. Effect of reduced sulfur compounds on the fermentation of phosphoric acid pretreated sugarcane bagasse by ethanologenic Escherichia coli[J]. Bioresour Technol, 2011, 102(8): 5145-5152. doi: 10.1016/j.biortech.2011.02.008 URL
[51]	Moraitis C, Curran BPG. Reactive oxygen species may influence the heat shock response and stress tolerance in the yeast Saccharomyces cerevisiae[J]. Yeast, 2004, 21(4): 313-323. doi: 10.1002/yea.v21:4 URL
[52]	Li RX, Shen W, Yang YF, et al. Investigation of the impact of a broad range of temperatures on the physiological and transcriptional profiles of Zymomonas mobilis ZM4 for high-temperature-tolerant recombinant strain development[J]. Biotechnol Biofuels, 2021, 14(1): 146. doi: 10.1186/s13068-021-02000-1
[53]	Zhang CC, Gui Y, Chen X, et al. Transcriptional homogenization of Lactobacillus rhamnosus hsryfm 1301 under heat stress and oxidative stress[J]. Appl Microbiol Biotechnol, 2020, 104(6): 2611-2621. doi: 10.1007/s00253-020-10407-3
[54]	Dijkstra AR, Alkema W, Starrenburg MJC, et al. Fermentation-induced variation in heat and oxidative stress phenotypes of Lactococcus lactis MG1363 reveals transcriptome signatures for robustness[J]. Microb Cell Fact, 2014, 13: 148. doi: 10.1186/s12934-014-0148-6 URL
[55]	Liu YP, Tang HZ, Lin ZL, et al. Mechanisms of acid tolerance in bacteria and prospects in biotechnology and bioremediation[J]. Biotechnol Adv, 2015, 33(7): 1484-1492. doi: 10.1016/j.biotechadv.2015.06.001 pmid: 26057689
[56]	Kanjee U, Houry WA. Mechanisms of acid resistance in Escherichia coli[J]. Annu Rev Microbiol, 2013, 67: 65-81. doi: 10.1146/micro.2013.67.issue-1 URL
[57]	Krulwich TA, Sachs G, Padan E. Molecular aspects of bacterial pH sensing and homeostasis[J]. Nat Rev Microbiol, 2011, 9(5): 330-343. doi: 10.1038/nrmicro2549 pmid: 21464825
[58]	Papadimitriou K, Alegría Á, Bron PA, et al. Stress physiology of lactic acid bacteria[J]. Microbiol Mol Biol Rev, 2016, 80(3): 837-890. doi: 10.1128/MMBR.00076-15 URL
[59]	Follmann M, Ochrombel I, Krämer R, et al. Functional genomics of pH homeostasis in Corynebacterium glutamicum revealed novel links between pH response, oxidative stress, iron homeostasis and methionine synthesis[J]. BMC Genomics, 2009, 10: 621. doi: 10.1186/1471-2164-10-621 pmid: 20025733
[60]	Miller EN, Jarboe LR, Turner PC, et al. Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180[J]. Appl Environ Microbiol, 2009, 75(19): 6132-6141. doi: 10.1128/AEM.01187-09 URL
[61]	Kanna MC, Matsumura Y. Effect of low-concentration furfural on sulfur amino acid biosynthesis in Saccharomyces cerevisiae[J]. J Jpn Petrol Inst, 2015, 58(3): 165-168. doi: 10.1627/jpi.58.165 URL
[62]	Kim D, Hahn JS. Roles of the Yap1 transcription factor and antioxidants in Saccharomyces cerevisiae's tolerance to furfural and 5-hydroxymethylfurfural, which function as thiol-reactive electrophiles generating oxidative stress[J]. Appl Environ Microbiol, 2013, 79(16): 5069-5077. doi: 10.1128/AEM.00643-13 URL
[63]	Liu ZL, Ma MG. Pathway-based signature transcriptional profiles as tolerance phenotypes for the adapted industrial yeast Saccharomyces cerevisiae resistant to furfural and HMF[J]. Appl Microbiol Biotechnol, 2020, 104(8): 3473-3492. doi: 10.1007/s00253-020-10434-0
[64]	Liu ZL, Slininger PJ, Gorsich SW. Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains[J]. Appl Biochem Biotechnol, 2005, 121-124: 451-460.
[65]	Yang YF, Hu MM, Tang Y, et al. Progress and perspective on lignocellulosic hydrolysate inhibitor tolerance improvement in Zymomonas mobilis[J]. Bioresour Bioprocess, 2018, 5(1): 6. doi: 10.1186/s40643-018-0193-9
[66]	He MX, Wu B, Shui ZX, et al. Transcriptome profiling of Zymomonas mobilis under furfural stress[J]. Appl Microbiol Biotechnol, 2012, 95(1): 189-199. doi: 10.1007/s00253-012-4155-4 URL
[67]	Yi X, Gu HQ, Gao QQ, et al. Transcriptome analysis of Zymomonas mobilis ZM4 reveals mechanisms of tolerance and detoxification of phenolic aldehyde inhibitors from lignocellulose pretreatment[J]. Biotechnol Biofuels, 2015, 8: 153. doi: 10.1186/s13068-015-0333-9 URL
[68]	Tan T, Liu C, Liu L, et al. Hydrogen sulfide formation as well as ethanol production in different media by cysND- and/or cysIJ-inactivated mutant strains of Zymomonas mobilis ZM4[J]. Bioprocess Biosyst Eng, 2013, 36(10): 1363-1373. doi: 10.1007/s00449-012-0839-5 URL
[69]	Hu DS, Wang ZQ, He MX, et al. Functional gene identification and corresponding tolerant mechanism of high furfural-tolerant Zymomonas mobilis strain F211[J]. Front Microbiol, 2021, 12: 736583. doi: 10.3389/fmicb.2021.736583 URL
[70]	Tang Y, Wang Y, Yang Q, et al. Molecular mechanism of enhanced ethanol tolerance associated with hfq overexpression in Zymomonas mobilis[J]. Front Bioeng Biotechnol, 2022, 10: 1098021. doi: 10.3389/fbioe.2022.1098021 URL
[71]	Li J, Shi S, Tu MB, et al. Detoxification of organosolv-pretreated pine prehydrolysates with anion resin and cysteine for butanol fermentation[J]. Appl Biochem Biotechnol, 2018, 186(3): 662-680. doi: 10.1007/s12010-018-2769-4 pmid: 29717408
[72]	Roe AJ, O'Byrne C, McLaggan D, et al. Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity[J]. Microbiology, 2002, 148(Pt 7): 2215-2222. doi: 10.1099/00221287-148-7-2215 URL
[73]	Shatalin K, Shatalina E, Mironov A, et al. H₂S: a universal defense against antibiotics in bacteria[J]. Science, 2011, 334(6058): 986-990. doi: 10.1126/science.1209855 pmid: 22096201
[74]	Shatalin K, Nuthanakanti A, Kaushik A, et al. Inhibitors of bacterial H₂S biogenesis targeting antibiotic resistance and tolerance[J]. Science, 2021, 372(6547): 1169-1175. doi: 10.1126/science.abd8377 URL
[75]	Ma Y, Yang XM, Wang HO, et al. CBS-derived H₂S facilitates host colonization of Vibrio cholerae by promoting the iron-dependent catalase activity of KatB[J]. PLoS Pathog, 2021, 17(7): e1009763. doi: 10.1371/journal.ppat.1009763 URL
[76]	Wei MY, Liu JY, Li H, et al. Proteomic analysis reveals the protective role of exogenous hydrogen sulfide against salt stress in rice seedlings[J]. Nitric Oxide, 2021, 111-112: 14-30.
[77]	Liu YB, Long MX, Yin YJ, et al. Physiological roles of mycothiol in detoxification and tolerance to multiple poisonous chemicals in Corynebacterium glutamicum[J]. Arch Microbiol, 2013, 195(6): 419-429. doi: 10.1007/s00203-013-0889-3 URL
[78]	Han K, Hong J, Lim HC. Relieving effects of glycine and methionine from acetic acid inhibition in Escherichia coli fermentation[J]. Biotechnol Bioeng, 1993, 41(3): 316-324. pmid: 18609555
[79]	Aroca A, Benito JM, Gotor C, et al. Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis[J]. J Exp Bot, 2017, 68(17): 4915-4927. doi: 10.1093/jxb/erx294 URL
[80]	Lin YL, Shi JY, Feng W, et al. Periplasmic biomineralization for semi-artificial photosynthesis[J]. Sci Adv, 2023, 9(29): eadg5858. doi: 10.1126/sciadv.adg5858 URL
[81]	Mironov A, Seregina T, Nagornykh M, et al. Mechanism of H₂S-mediated protection against oxidative stress in Escherichia coli[J]. Proc Natl Acad Sci USA, 2017, 114(23): 6022-6027. doi: 10.1073/pnas.1703576114 URL
[82]	Xiao AY, Maynard MR, Piett CG, et al. Sodium sulfide selectively induces oxidative stress, DNA damage, and mitochondrial dysfunction and radiosensitizes glioblastoma(GBM)cells[J]. Redox Biol, 2019, 26: 101220. doi: 10.1016/j.redox.2019.101220 URL
[83]	Attene-Ramos MS, Wagner ED, Gaskins HR, et al. Hydrogen sulfide induces direct radical-associated DNA damage[J]. Mol Cancer Res, 2007, 5(5): 455-459. pmid: 17475672
[84]	Shackelford R, Ozluk E, Islam MZ, et al. Hydrogen sulfide and DNA repair[J]. Redox Biol, 2021, 38: 101675. doi: 10.1016/j.redox.2020.101675 URL
[85]	Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple[J]. Free Radic Biol Med, 2001, 30(11): 1191-1212. doi: 10.1016/S0891-5849(01)00480-4 URL
[86]	Ask M, Mapelli V, Höck H, et al. Engineering glutathione biosynthesis of Saccharomyces cerevisiae increases robustness to inhibitors in pretreated lignocellulosic materials[J]. Microb Cell Fact, 2013, 12: 87. doi: 10.1186/1475-2859-12-87
[87]	Rahman I, Kode A, Biswas SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method[J]. Nat Protoc, 2006, 1(6): 3159-3165. doi: 10.1038/nprot.2006.378 pmid: 17406579
[88]	Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, et al. Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants[J]. FEMS Microbiol Rev, 2005, 29(4): 653-671. pmid: 16102596
[89]	Dumond H, Danielou N, Pinto M, et al. A large-scale study of Yap1p-dependent genes in normal aerobic and H₂O₂-stress conditions: the role of Yap1p in cell proliferation control in yeast[J]. Mol Microbiol, 2000, 36(4): 830-845. pmid: 10844671
[90]	Jo I, Chung IY, Bae HW, et al. Structural details of the OxyR peroxide-sensing mechanism[J]. Proc Natl Acad Sci USA, 2015, 112(20): 6443-6448. doi: 10.1073/pnas.1424495112 pmid: 25931525
[91]	Herrero E, Ros J, Bellí G, et al. Redox control and oxidative stress in yeast cells[J]. Biochim Biophys Acta, 2008, 1780(11): 1217-1235. doi: 10.1016/j.bbagen.2007.12.004 pmid: 18178164
[92]	Seib KL, Wu HJ, Srikhanta YN, et al. Characterization of the OxyR regulon of Neisseria gonorrhoeae[J]. Mol Microbiol, 2007, 63(1): 54-68. doi: 10.1111/mmi.2007.63.issue-1 URL
[93]	Ohtsu I, Wiriyathanawudhiwong N, Morigasaki S, et al. The L-cysteine/L-cystine shuttle system provides reducing equivalents to the periplasm in Escherichia coli[J]. J Biol Chem, 2010, 285(23): 17479-17487. doi: 10.1074/jbc.M109.081356 pmid: 20351115
[94]	Fujishiro T, Nakamura R, Kunichika K, et al. Structural diversity of cysteine desulfurases involved in iron-sulfur cluster biosynthesis[J]. Biophys Physicobiol, 2022, 19: 1-18. doi: 10.2142/biophysico.bppb-v19.0001 pmid: 35377584
[95]	Braymer JJ, Freibert SA, Rakwalska-Bange M, et al. Mechanistic concepts of iron-sulfur protein biogenesis in biology[J]. Biochim Biophys Acta Mol Cell Res, 2021, 1868(1): 118863. doi: 10.1016/j.bbamcr.2020.118863 URL
[96]	Lill R, Freibert SA. Mechanisms of mitochondrial iron-sulfur protein biogenesis[J]. Annu Rev Biochem, 2020, 89: 471-499. doi: 10.1146/annurev-biochem-013118-111540 pmid: 31935115
[97]	Martien JI, Hebert AS, Stevenson DM, et al. Systems-level analysis of oxygen exposure in Zymomonas mobilis: implications for isoprenoid production[J]. mSystems, 2019, 4(1): e00284-18.
[98]	Miao JX, Wang MM, Ma L, et al. Effects of amino acids on the lignocellulose degradation by Aspergillus fumigatus Z5: insights into performance, transcriptional, and proteomic profiles[J]. Biotechnol Biofuels, 2019, 12: 4. doi: 10.1186/s13068-018-1350-2
[99]	Van Laer K, Hamilton CJ, Messens J. Low-molecular-weight thiols in thiol-disulfide exchange[J]. Antioxid Redox Signal, 2013, 18(13): 1642-1653. doi: 10.1089/ars.2012.4964 URL
[100]	Dumitrescu DG, Gordon EM, Kovalyova Y, et al. A microbial transporter of the dietary antioxidant ergothioneine[J]. Cell, 2022, 185(24): 4526-4540.e18. doi: 10.1016/j.cell.2022.10.008 pmid: 36347253
[101]	Sundquist AR, Fahey RC. The function of gamma-glutamylcysteine and bis-gamma-glutamylcystine reductase in Halobacterium halobium[J]. J Biol Chem, 1989, 264(2): 719-725. pmid: 2910862
[102]	Turner E, Hager LJ, Shapiro BM. Ovothiol replaces glutathione peroxidase as a hydrogen peroxide scavenger in sea urchin eggs[J]. Science, 1988, 242(4880): 939-941. pmid: 3187533
[103]	Helmann JD. Bacillithiol, a new player in bacterial redox homeostasis[J]. Antioxid Redox Signal, 2011, 15(1): 123-133. doi: 10.1089/ars.2010.3562 URL
[104]	Newton GL, Buchmeier N, Fahey RC. Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria[J]. Microbiol Mol Biol Rev, 2008, 72(3): 471-494. doi: 10.1128/MMBR.00008-08 URL
[105]	Ling XB, Wei HW, Wang J, et al. Mammalian metallothionein-2A and oxidative stress[J]. Int J Mol Sci, 2016, 17(9): 1483. doi: 10.3390/ijms17091483 URL
[106]	Qin L, Dong SX, Yu J, et al. Stress-driven dynamic regulation of multiple tolerance genes improves robustness and productive capacity of Saccharomyces cerevisiae in industrial lignocellulose fermentation[J]. Metab Eng, 2020, 61: 160-170. doi: 10.1016/j.ymben.2020.06.003 URL
[107]	Foo JL, Jensen HM, Dahl RH, et al. Improving microbial biogasoline production in Escherichia coli using tolerance engineering[J]. mBio, 2014, 5(6): e01932.
[108]	Qiu ZQ, Deng ZJ, Tan HM, et al. Engineering the robustness of Saccharomyces cerevisiae by introducing bifunctional glutathione synthase gene[J]. J Ind Microbiol Biotechnol, 2015, 42(4): 537-542. doi: 10.1007/s10295-014-1573-6 URL
[109]	Thakur M, Anand A. Hydrogen sulfide: an emerging signaling molecule regulating drought stress response in plants[J]. Physiol Plant, 2021, 172(2): 1227-1243. doi: 10.1111/ppl.v172.2 URL

Protein	Function	Gene source	Host	Resistance	Reference
MetC-CysK operon	Cysteine biosynthesis	Lactococcus lactis	Lactococcus lactis	High temperature（temp.）	[54]
GSH1/CYS3/GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Lignocellulose hydrolysates	[86]
SOD1-GSH1-GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Lignocellulose hydrolysates	[106]
YAP1^C620F- CTT1/CTA1 /GSH1/GSH2/GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Furfural	[62]
GCSGS	Glutathione biosynthesis	S. thermophilus	S. cerevisiae	High temp., furfural, HMF, Cd²⁺	[108]
GshA/AspB/MetC	Glutathione and H₂S biosynthesis	Z. mobilis	Z. mobilis	Furfural	[48]
MetR	Methionine biosynthesis regulator	E. coli	E. coli	Isopentenol	[107]
CysCND	Sulfur assimilation	Z. mobilis	Z. mobilis	Furfural, acetate	[5]
McbR	Sulfur assimilation regulator	C. glutamicum	C. glutamicum	Acidic pH	[40]
TauE	Anion permease, Sulfite exporter	Z. mobilis	Z. mobilis	Furfural	[69]

Protein	Function	Gene source	Host	Resistance	Reference
MetC-CysK operon	Cysteine biosynthesis	Lactococcus lactis	Lactococcus lactis	High temperature（temp.）	[54]
GSH1/CYS3/GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Lignocellulose hydrolysates	[86]
SOD1-GSH1-GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Lignocellulose hydrolysates	[106]
YAP1^C620F- CTT1/CTA1 /GSH1/GSH2/GLR1	Glutathione biosynthesis	S. cerevisiae	S. cerevisiae	Furfural	[62]
GCSGS	Glutathione biosynthesis	S. thermophilus	S. cerevisiae	High temp., furfural, HMF, Cd²⁺	[108]
GshA/AspB/MetC	Glutathione and H₂S biosynthesis	Z. mobilis	Z. mobilis	Furfural	[48]
MetR	Methionine biosynthesis regulator	E. coli	E. coli	Isopentenol	[107]
CysCND	Sulfur assimilation	Z. mobilis	Z. mobilis	Furfural, acetate	[5]
McbR	Sulfur assimilation regulator	C. glutamicum	C. glutamicum	Acidic pH	[40]
TauE	Anion permease, Sulfite exporter	Z. mobilis	Z. mobilis	Furfural	[69]