摘要
硫化氢(H_2S)是继一氧化氮(NO)和一氧化碳(CO)后发现的第3种气态信号分子,但其细菌生理学研究才刚刚起步。本文根据作者对奥内达希瓦氏菌的研究,结合新近文献,就细菌的H_2S产生机理及其生理功能作了较为全面的阐述。细菌的H_2S产生途径主要有2条,一是通过降解半胱氨酸产生,二是通过厌氧呼吸产生。产生的H_2S除可为互生性微生物提供能源、供氢体和无机矿质营养外,还具有抑制竞争性微生物的生长,有效占领生态位的作用。H_2S在氧化应答中也起着重要的作用,一方面可抑制过氧化氢酶活性,增加过氧化氢对细菌的杀灭效果;另一方面可作为信号分子激活细菌的氧化应答,诱导拮抗系统的表达,保护细胞免受氧化损伤。这两种看似"矛盾"的作用与H_2S的处理时间有关:短时间处理以抑制为主,而延长处理时间则以保护为主。细菌H_2S产生机理及生理功能的阐明可为硫元素生物地球化学循环规律的揭示和感染性病原细菌的控制提供有益的参考。
H2S is the third gaseous signaling molecule next to nitric oxide and carbon monoxide,but studies on its physiological functions in bacteria are just emerging.In this paper,we review recent findings regarding endogenous production and physiological functions of H_2S in facultative anaerobic bacteria,partly based on our own research on Shewanella oneidensis.There are two principal H_2S producing pathways in S.oneidensis: one is through cysteine degradation,and the other is via inorganic sulfur respiration.Endogenous H_2S could either benefit mutual growing bacteria by supplying energy and inorganic,or inhibit competing bacteria.Our review attaches particular importance to the role of H_2S in bacterial oxidative stress response.On one hand,H_2S is able to directly inhibit heme-containing catalase,enhancing killing by H_2O_2.On the other hand,H_2S could activate oxidative response as a signaling molecule,leading to cell protection from the oxidative stress due to elevated expression of H_2O_2 scavenging and repairing systems.Intriguingly,the dominance of either role is determined by H_2S-treating time,that is,inhibition is the immediate response whereas activation of oxidative stress response needs extended treatment.The elucidation of endogenous production and its physiological function of H_2S in facultative anaerobic bacteria would improve understanding of biogeochemical sulfur recycling,and facilitate control of infectious bacterial pathogens.
引文
[1]Chen S,Wang LR,Deng ZX.Twenty years hunting for sulfur in DNA.Protein&Cell,2010,1(1):14–21.
[2]Anbar AD,Knoll AH.Proterozoic ocean chemistry and evolution:a bioinorganic bridge?Science,2002,297(5584):1137–1142.
[3]Wang R.Physiological implications of hydrogen sulfide:a whiff exploration that blossomed.Physiological Reviews,2012,92(2):791–896.
[4]Ono K,Akaike T,Sawa T,Kumagai Y,Wink DA,Tantillo DJ,Hobbs AJ,Nagy P,Xian M,Lin J,Fukuto JM.Redox chemistry and chemical biology of H2S,hydropersulfides,and derived species:implications of their possible biological activity and utility.Free Radical Biology and Medicine,2014,77:82–94.
[5]Luhachack L,Nudler E.Bacterial gasotransmitters:an innate defense against antibiotics.Current Opinion in Microbiology,2014,21:13–17.
[6]Shatalin K,Shatalina E,Mironov A,Nudler E.H2S:a universal defense against antibiotics in bacteria.Science,2011,334(6058):986–990.
[7]Bradley AS,Leavitt WD,Johnston DT.Revisiting the dissimilatory sulfate reduction pathway.Geobiology,2011,9(5):446–457.
[8]Fredrickson JK,Romine MF,Beliaev AS,Auchtung JM,Driscoll ME,Gardner TS,Nealson KH,Osterman AL,Pinchuk G,Reed JL,Rodionov DA,Rodrigues JLM,Saffarini DA,Serres MH,Spormann AM,Zhulin IB,Tiedje JM.Towards environmental systems biology of Shewanella.Nature Reviews Microbiology,2008,6(8):592–603.
[9]Fu HH,Yuan J,Gao HC.Microbial oxidative stress response:novel insights from environmental facultative anaerobic bacteria.Archives of Biochemistry and Biophysics,2015,584:28–35.
[10]Fu HH,Jin M,Wan F,Gao HC.Shewanella oneidensis cytochrome c maturation component Ccm I is essential for heme attachment at the non-canonical motif of nitrite reductase Nrf A.Molecular Microbiology,2015,95(3):410–425.
[11]Gao T,Shi MM,Ju LL,Gao HC.Investigation into Flh FG reveals distinct features of Flh F in regulating flagellum polarity in Shewanella oneidensis.Molecular Microbiology,2015,98(3):571–585.
[12]Shi MM,Gao T,Ju LL,Yao YL,Gao HC.Effects of Flr BC on flagellar biosynthesis of Shewanella oneidensis.Molecular Microbiology,2014,93(6):1269–1283.
[13]Myers CR,Nealson KH.Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor.Science,1988,240(4857):1319–1321.
[14]Shirodkar S,Reed S,Romine M,Saffarini D.The octahaem Sir A catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1.Environmental Microbiology,2011,13(1):108–115.
[15]Wu G,Li N,Mao Y,Zhou G,Gao H.Endogenous generation of hydrogen sulfide and its regulation in Shewanella oneidensis.Frontiers in Microbiology,2015,6:374.
[16]Zhou GQ,Yin JH,Chen HJ,Hua YJ,Sun LL,Gao HC.Combined effect of loss of the caa3 oxidase and Crp regulation drives Shewanella to thrive in redox-stratified environments.The ISME Journal,2013,7(9):1752–1763.
[17]You CH,Okano H,Hui S,Zhang ZG,Kim MS,Gunderson CW,Wang YP,Lenz P,Yan DL,Hwa T.Coordination of bacterial proteome with metabolism by cyclic AMP signalling.Nature,2013,500(7462):301–306.
[18]Gao HC,Wang XH,Yang ZK,Palzkill T,Zhou JZ.Probing regulon of Arc A in Shewanella oneidensis MR-1 by integrated genomic analyses.BMC Genomics,2008,9:42.
[19]Wan F,Mao YT,Dong YY,Ju LL,Wu GF,Gao HC.Impaired cell envelope resulting from arc A mutation largely accounts for enhanced sensitivity to hydrogen peroxide in Shewanella oneidensis.Scientific Reports,2015,5:10228.
[20]Madigan MT,Martinko JM,Bender KS,Buckley DH,Stahl DA,Brock T.Brock Biology of Microorganisms(14th ed.).Tokyo:Pearson,2015.
[21]Pietri R,Lewis A,León RG,Casabona G,Kiger L,Yeh SR,Fernandez-Alberti S,Marden MC,Cadilla CL,López-Garriga J.Factors controlling the reactivity of hydrogen sulfide with hemeproteins.Biochemistry,2009,48(22):4881–4894.
[22]Enning D,Garrelfs J.Corrosion of iron by sulfate-reducing bacteria:new views of an old problem.Applied and Environmental Microbiology,2014,80(4):1226–1236.
[23]Lohmayer R,Kappler A,L?sekann-Behrens T,Planer-Friedrich B.Sulfur species as redox partners and electron shuttles for ferrihydrite reduction by Sulfurospirillum deleyianum.Applied and Environmental Microbiology,2014,80(10):3141–3149.
[24]Flynn TM,O'Loughlin EJ,Mishra B,Di Christina TJ,Kemner KM.Sulfur-mediated electron shuttling during bacterial iron reduction.Science,2014,344(6187):1039–1042.
[25]Mirzoyan N,Schreier HJ.Effect of sulfide on growth of marine bacteria.Archives of Microbiology,2014,196(4):279–287.
[26]Nagy P.Kinetics and mechanisms of thiol-disulfide exchange covering direct substitution and thiol oxidation-mediated pathways.Antioxidants&Redox Signaling,2013,18(13):1623–1641.
[27]Francoleon NE,Carrington SJ,Fukuto JM.The reaction of H2S with oxidized thiols:generation of persulfides and implications to H2S biology.Archives of Biochemistry and Biophysics,2011,516(2):146–153.
[28]Nicoletti FP,Comandini A,Bonamore A,Boechi L,Boubeta FM,Feis A,Smulevich G,Boffi A.Sulfide binding properties of truncated hemoglobins.Biochemistry,2010,49(10):2269–2278.
[29]Ríos-González BB,Román-Morales EM,Pietri R,López-Garriga J.Hydrogen sulfide activation in hemeproteins:the sulfheme scenario.Journal of Inorganic Biochemistry,2014,133:78–86.
[30]Hoffman M,Rajapakse A,Shen XL,Gates KS.Generation of DNA-damaging reactive oxygen species via the autoxidation of hydrogen sulfide under physiologically relevant conditions:chemistry relevant to both the genotoxic and cell signaling properties of H2S.Chemical Research in Toxicology,2012,25(8):1609–1615.
[31]Wu GF,Wan F,Fu HH,Li N,Gao HC.A matter of timing:contrasting effects of hydrogen sulfide on oxidative stress response in Shewanella oneidensis.Journal of Bacteriology,2015,197(22):3563–3572.
[32]Fu LH,Hu KD,Hu LY,Li YH,Hu LB,Yan H,Liu YS,Zhang H.An antifungal role of hydrogen sulfide on the postharvest pathogens Aspergillus niger and Penicillium italicum.PLo S One,2014,9(8):e104206.
[33]Huang JH.Impact of microorganisms on arsenic biogeochemistry:a review.Water,Air,&Soil Pollution,2014,225:1848.
[34]Lindsay MBJ,Moncur MC,Bain JG,Jambor JL,Ptacek CJ,Blowes DW.Geochemical and mineralogical aspects of sulfide mine tailings.Applied Geochemistry,2015,57:157–177.
[35]Newman DK,Beveridge TJ,Morel F.Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum.Applied and Environmental Microbiology,1997,63(5):2022–2028.
[36]Fendorf S,Michael HA,van Geen A.Spatial and temporal variations of groundwater arsenic in South and Southeast Asia.Science,2010,328(5982):1123–1127.
[37]Burton ED,Johnston SG,Planer-Friedrich B.Coupling of arsenic mobility to sulfur transformations during microbial sulfate reduction in the presence and absence of humic acid.Chemical Geology,2013,343:12–24.
[38]Caro AA,Thompson S,Tackett J.Increased oxidative stress and cytotoxicity by hydrogen sulfide in Hep G2 cells overexpressing cytochrome P450 2E1.Cell Biology and Toxicology,2011,27(6):439–453.
[39]Kabil O,Motl N,Banerjee R.H2S and its role in redox signaling.Biochimica et Biophysica Acta,2014,1844(8):1355–1366.
