细菌胞际电子转移及其生态生理学意义研究进展
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摘要
胞际电子转移是指细胞内电子以间接或直接的方式传递到细胞外,最终到达细胞周围电子受体的过程.胞际电子转移普遍存在于自然界,尤其存在于电子受体相对匮乏的环境中.胞际电子转移可分为间接和直接胞际电子转移.间接胞际电子转移(胞际基质转移)是主要借助氢、甲酸以及其他代谢产物的电子传递;而直接胞际电子转移则由胞内电子转移偶联胞外电子传递实现.胞际电子转移促进了细胞的基质代谢活性,拓展了细胞的作用空间,具有重要的生理意义.胞际电子转移产生了电流,实现了菌间能源共享,驱动了胞外物质(如重金属、腐殖质)转化,具体重大的生态意义.本文总结相关文献,对细菌胞际电子转移的过程、特点、机理及其生态生理学意义作了系统的分析和探讨.
Intercellular electron transfer( IET) refers to the process within which electrons being indirectly or directly transferred to the exterior of cells and eventually delivered to the electron acceptors around cells. IET widely exists in nature,especially when electron acceptor are deficient.IET can be divided into two categories: indirect IET and direct IET. Indirect IET( intercellular substrate transfer) always occurs with electron transfer of hydrogen,formate,and other metabolites.Direct intracellular electron transfer is achieved by the coupling of intracellular and extracellular electron transfer. IET boosts the activity of cellular substrate metabolism and expands the acting space of cells. Moreover,IET generates electric current which provides driving-power for energy sharing between bacteria and transformation of extracellular material( such as heavy metals and humus). There is no doubt that IET has physiological and ecological significance. This review summarized recent advances,making a systematic analysis of the process,characteristics,mechanism and eco-physiological significance of IET.
Intercellular electron transfer( IET) refers to the process within which electrons being indirectly or directly transferred to the exterior of cells and eventually delivered to the electron acceptors around cells. IET widely exists in nature,especially when electron acceptor are deficient.IET can be divided into two categories: indirect IET and direct IET. Indirect IET( intercellular substrate transfer) always occurs with electron transfer of hydrogen,formate,and other metabolites.Direct intracellular electron transfer is achieved by the coupling of intracellular and extracellular electron transfer. IET boosts the activity of cellular substrate metabolism and expands the acting space of cells. Moreover,IET generates electric current which provides driving-power for energy sharing between bacteria and transformation of extracellular material( such as heavy metals and humus). There is no doubt that IET has physiological and ecological significance. This review summarized recent advances,making a systematic analysis of the process,characteristics,mechanism and eco-physiological significance of IET.
引文
[1] Ma C(马晨),Zhou S-G(周顺桂),Zhuang L(庄莉),et al. Research progress of microbial extracellular respiratory electron transport mechanism. Acta Ecologica Sinica(生态学报),2011,31(7):2008-2018(in Chinese)
[2] Tang Z-R(唐朱睿),Huang C-H(黄彩红),Gao R-T(高如泰),et al. Review on extracellular respiratory bacteria and its spplication in migration and transformation of pollutants. Journal of Agricultural Resources and Environment(农业资源与环境学报),2017,34(4):299-308(in Chinese)
[3] Zhao X-Y(赵昕宇),He X-S(何小松),Tan W-B(檀文炳),et al. Intracellular electron transfer mechanism of typical extracellular respiratory bacteria. Acta Ecologica Sinica(生态学报),2017,37(8):2540-2550(in Chinese)
[4] Madigan MT,Martinko JM,Stahl DA,et al. Brock Biology of Microorganisms.13thEd. San Francisco,CA,USA:Benjamin Cummings,2010
[5] Bryant MPEA,Wolin MJ,Wolfe RS. Methanobacillus omelianskii,a symbiotic association of two species of bacteria. Archives of Microbiology,1967,59:20-21
[6] Wallrabenstein C,Hauschild E,Schink B,et al. Syntrophobacter pfennigii sp. nov.,new syntrophically propionate-oxidizing anaerobe growing in pure culture with propionate and sulfate. Archives of Microbiology, 1993,164:346-352
[7] Boone DR,Bryant MP. Propionate-degrading bacterium,Syntrophobacter wolinii sp. nov. gen. nov.,from methanogeni ecosystems. Applied and Environmental Microbiology,1980,40:626-632
[8] Wolin MJ,Miller TL. Interspecies hydrogen transfer:15years later. ASM News,1982,48:561-565
[9] Hungate RE. Hydrogen as an intermediate in the rumen fermentation. Archiv Für Mikrobiologie,1967,59:158-164
[10] Thiele JH,Chartrain M,Zeikus JG. Control of interspecies electron flow during anaerobic digestion:Role of floc formation in syntrophic methanogenesis. Applied and Environmental Microbiology,1988,54:10-19
[11] Dong X,Stams AJ. Evidence for H2and formate formation during syntrophic butyrate andpropionate degradation. Anaerobe,1995,1:35-39
[12] Dong X-Z(东秀珠).The role of formateand molecular hydrogen in the degradation of propionic acid and butyric acid. Journal of Microbiology(微生物学通报),1997,24(1):51-56(in Chinese)
[13] Stams AJM,Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews Microbiology,2009,7:568-577
[14] Friedrich M,Schink B. Hydrogen formation from glycolate driven by reversed electron transport in membrane vesicles of a syntrophic glycolate-oxidizing bacterium.European Journal of Biochemistry,1993,217:233-240
[15] Paulsen J,Kr9ger A,Thauer RK. ATP-driven succinate oxidation in the catabolism of Desulfuromonas acetoxidans. Archives of Microbiology,1986,144:78-83
[16] Stams AJ,Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews Microbiology,2009,7:568-577
[17] Schink B, Thauer RK. Granular Anaerobic Sludge,Microbiology and Technology. Proceedings of the GASMAT Workshop. Lunteren,the Netherlands 1988:5-7
[18] Stams AJ,Van Dijk JB,Dijkema C,et al. Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Applied and Environmental Microbiology,1993,59:1114-1119
[19] Ren N-Q(任南琪),Xu L-Y(许丽英),Zhang Y(张颖),et al. Dependence on iron and hydrogen producing pathway for novel strain Ethanoligenens sp. B49. Acta Scientiae Circumstantiae(环境科学学报),2006,26(10):1643-1650(in Chinese)
[20] Marcus RA,Sutin N. Electron transfers in chemistry and biology. BBA Reviews on Bioenergetics, 1985, 811:265-322
[21] Cordes M,Giese B. Electron transfer in peptides and proteins. Chemical Society Reviews,2009,38:892-901
[22] Warren JJ,Ener ME,Jr Vlcˇek A, et al. Electron hopping through proteins. Coordination Chemistry Reviews,2012,256:2478-2487
[23] Bssler H,K9hler A. Charge transport in organic semiconductors. Topics in Current Chemistry,2012,312:1-66
[24] Breuer M,Rosso KM,Blumberger J,et al. Multi-haem cytochromes in Shewanella oneidensis MR-1:Structures,functions and opportunities. Journal of the Royal Society Interface,2015,12:20141117
[25] Pirbadian S,Elnaggar MY. Multistep hopping and extracellular charge transfer in microbial redox chains. Physical Chemistry Chemical Physics,2012,14:13802-13808
[26] Malvankar NS,Vargas M,Nevin KP,et al. Tunable metallic-like conductivity in microbial nanowire networks. Nature Nanotechnology,2011,6:573-579
[27] Pirbadian S,Barchinger SE,Leung KM,et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proceedings of the National Academy of Sciences of the United States of America,2014,111:12883-12888
[28] El-Naggar MY,Wanger G,Leung KM,et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proceedings of the National Academy of Sciences of the United States of America,2010,107:18127-18131
[29] Bouhenni RA,Vora GJ,Biffinger JC,et al. The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanalysis, 2010,22:856-864
[30] Polizzi NF,Skourtis SS,Beratan DN. Physical constraints on charge transport through bacterial nanowires.Faraday Discussions,2012,155:43-62
[31] Ma J-L(马金莲),Ma C(马晨),Tang J(汤佳),et al. Electron shuttle-mediated extracellular electron transfer of microorganisms:Mechanism and application. Chemical Progress(化学进展),2015,27(12):1833-1840(in Chinese)
[32] Kappler A,Wuestner ML,Ruecker A,et al. Biochar as an electron shuttle between bacteria and Fe(III)minerals. Environmental Science and Technology Letters,2016,1:339-344
[33] Paquete CM,Fonseca BM,Cruz DR,et al. Exploring the molecular mechanisms of electron shuttling across the microbe/metal space. Frontiers in Microbiology,2014,5:1-12
[34] Liu F,Rotaru A,Shrestha PM,et al. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environmental Microbiology,2015,17:648-655
[35] Liu F,Rotaru AE,Shrestha PM,et al. Promoting direct interspecies electron transfer with activated carbon.Energy and Environmental Science,2012,5:8982-8989
[36] Kato S,Hashimoto K,Watanabe K. Methanogenesis facilitated by electric syntrophy via(semi)conductive iron-oxide minerals. Environmental Microbiology,2012,14:1646-1654
[37] Ren G-P(任桂平),Sun M-Y(孙曼仪),Lu A-H(鲁安怀),et al. The mechanism of the microbial extracellular electron transfer promoted by natural hematite inredsoil. Bulletin of Mineralogy,Petrology and Geochemistry(矿物岩石地球化学通报),2017,36(1):92-97(in Chinese)
[38] Xu DK,Gu TY. Carbon source starvation triggered more aggressive corrosion against carbon steel by the Desulfovibrio vulgaris biofilm. International Biodeterioration&Biodegradation,2014,91:74-81
[39] Chen YJ,Tang Q,Senko JM,et al. Long-term survival of Desulfovibrio vulgaris on carbon steel and associated pitting corrosion. Corrosion Science,2015,90:89-100
[40] Zhu GL,Yang Y,Liu J,et al. Enhanced photocurrent production by the synergy of hematite nanowire-arrayed photoanode and bioengineered Shewanella oneidensis MR-1. Biosensors&Bioelectronics,2017,94:227-234
[41] Lu A-H(鲁安怀),Li Y(李艳),Wang X(王鑫),et al. The utilization of solar energy by non-phototrophic microorganisms through semiconducting minerals. Microbiology China(微生物通报),2013,40(1):190-202(in Chinese)
[42] Lu AH,Li Y,Jin S,et al. Growth of non-phototrophic microorganisms using solar energy through mineralphotocatalysis. Nature Communications,3:768, doi:10.1038/ncomms1768
[43] Lu AH,Li Y,Jin S. Interactions between semiconducting minerals and bacteria under light. Elements, 8:125-130
[44] Zhao Z-Q(赵智强). Establishment and Enhancement of Direct Interspecies Electron Transfer between Syntrophic Microorganisms during Anaerobic Methanogenesis.PHD Thesis. Dalian:Dalian University of Technology,2017(in Chinese)
[45] Nakamura R,Kai F,Okamoto A,et al. Self-constructed electrically conductive bacterial networks. Angewandte Chemie,2009,48:508-511
[46] Li DB,Cheng YY,Li LL,et al. Light-driven microbial dissimilatory electron transfer to hematite. Physical Chemistry Chemical Physics,2014,16:23003-23011
[47] Belchik SM,Kennedy DW,Dohnalkova AC,et al.Extracellular reduction of hexavalent chromium by cytochromes MtrC and Omc A of Shewanella oneidensis MR-1. Applied and Environmental Microbiology,2011,77:4035-4041
[48] Mehta T,Coppi MV,Childers SE,et al. Outer membrane c-type cytochromes required for Fe(III)and Mn(IV)oxide reduction in Geobacter sulfurreducens.Applied and Environmental Microbiology, 2005, 71:8634-8641
[49] Cologgi DL,Lampa-Pastirk S,Speers A M,et al.Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proceedings of the National Academy of Sciences of the United States of America,2011,108:15248-15252
[50] Tang Z-R(唐朱睿),Huang C-H(黄彩红),Gao R-T(高如泰),et al. Review on extracellular respiratory bacteria and its application in migration and transformation of pollutants. Journal of Agricultural Resources and Environment(农业资源与环境学报),2017,34(4):299-308(in Chinese)
[51] Yu YY,Guo CX,Yong YC,et al. Nitrogen doped carbon nanoparticles enhanced extracellular electron transfer for high-performance microbial fuel cells anode.Chemosphere,2015,140:26-33
[52] Jiang X,Hu J,Lieber AM,et al. Nanoparticle facilitated extracellular electron transfer in microbial fuel cells.Nano Letters,2014,14:6737-6742
[53] Wu C-Y(武春媛),Li F-B(李芳柏),Zhou S-G(周顺桂). Humus respiration and its ecological significance. Acta Ecologica Sinica(生态学报),2009,29(3):1535-1542(in Chinese)
[2] Tang Z-R(唐朱睿),Huang C-H(黄彩红),Gao R-T(高如泰),et al. Review on extracellular respiratory bacteria and its spplication in migration and transformation of pollutants. Journal of Agricultural Resources and Environment(农业资源与环境学报),2017,34(4):299-308(in Chinese)
[3] Zhao X-Y(赵昕宇),He X-S(何小松),Tan W-B(檀文炳),et al. Intracellular electron transfer mechanism of typical extracellular respiratory bacteria. Acta Ecologica Sinica(生态学报),2017,37(8):2540-2550(in Chinese)
[4] Madigan MT,Martinko JM,Stahl DA,et al. Brock Biology of Microorganisms.13thEd. San Francisco,CA,USA:Benjamin Cummings,2010
[5] Bryant MPEA,Wolin MJ,Wolfe RS. Methanobacillus omelianskii,a symbiotic association of two species of bacteria. Archives of Microbiology,1967,59:20-21
[6] Wallrabenstein C,Hauschild E,Schink B,et al. Syntrophobacter pfennigii sp. nov.,new syntrophically propionate-oxidizing anaerobe growing in pure culture with propionate and sulfate. Archives of Microbiology, 1993,164:346-352
[7] Boone DR,Bryant MP. Propionate-degrading bacterium,Syntrophobacter wolinii sp. nov. gen. nov.,from methanogeni ecosystems. Applied and Environmental Microbiology,1980,40:626-632
[8] Wolin MJ,Miller TL. Interspecies hydrogen transfer:15years later. ASM News,1982,48:561-565
[9] Hungate RE. Hydrogen as an intermediate in the rumen fermentation. Archiv Für Mikrobiologie,1967,59:158-164
[10] Thiele JH,Chartrain M,Zeikus JG. Control of interspecies electron flow during anaerobic digestion:Role of floc formation in syntrophic methanogenesis. Applied and Environmental Microbiology,1988,54:10-19
[11] Dong X,Stams AJ. Evidence for H2and formate formation during syntrophic butyrate andpropionate degradation. Anaerobe,1995,1:35-39
[12] Dong X-Z(东秀珠).The role of formateand molecular hydrogen in the degradation of propionic acid and butyric acid. Journal of Microbiology(微生物学通报),1997,24(1):51-56(in Chinese)
[13] Stams AJM,Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews Microbiology,2009,7:568-577
[14] Friedrich M,Schink B. Hydrogen formation from glycolate driven by reversed electron transport in membrane vesicles of a syntrophic glycolate-oxidizing bacterium.European Journal of Biochemistry,1993,217:233-240
[15] Paulsen J,Kr9ger A,Thauer RK. ATP-driven succinate oxidation in the catabolism of Desulfuromonas acetoxidans. Archives of Microbiology,1986,144:78-83
[16] Stams AJ,Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews Microbiology,2009,7:568-577
[17] Schink B, Thauer RK. Granular Anaerobic Sludge,Microbiology and Technology. Proceedings of the GASMAT Workshop. Lunteren,the Netherlands 1988:5-7
[18] Stams AJ,Van Dijk JB,Dijkema C,et al. Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Applied and Environmental Microbiology,1993,59:1114-1119
[19] Ren N-Q(任南琪),Xu L-Y(许丽英),Zhang Y(张颖),et al. Dependence on iron and hydrogen producing pathway for novel strain Ethanoligenens sp. B49. Acta Scientiae Circumstantiae(环境科学学报),2006,26(10):1643-1650(in Chinese)
[20] Marcus RA,Sutin N. Electron transfers in chemistry and biology. BBA Reviews on Bioenergetics, 1985, 811:265-322
[21] Cordes M,Giese B. Electron transfer in peptides and proteins. Chemical Society Reviews,2009,38:892-901
[22] Warren JJ,Ener ME,Jr Vlcˇek A, et al. Electron hopping through proteins. Coordination Chemistry Reviews,2012,256:2478-2487
[23] Bssler H,K9hler A. Charge transport in organic semiconductors. Topics in Current Chemistry,2012,312:1-66
[24] Breuer M,Rosso KM,Blumberger J,et al. Multi-haem cytochromes in Shewanella oneidensis MR-1:Structures,functions and opportunities. Journal of the Royal Society Interface,2015,12:20141117
[25] Pirbadian S,Elnaggar MY. Multistep hopping and extracellular charge transfer in microbial redox chains. Physical Chemistry Chemical Physics,2012,14:13802-13808
[26] Malvankar NS,Vargas M,Nevin KP,et al. Tunable metallic-like conductivity in microbial nanowire networks. Nature Nanotechnology,2011,6:573-579
[27] Pirbadian S,Barchinger SE,Leung KM,et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proceedings of the National Academy of Sciences of the United States of America,2014,111:12883-12888
[28] El-Naggar MY,Wanger G,Leung KM,et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proceedings of the National Academy of Sciences of the United States of America,2010,107:18127-18131
[29] Bouhenni RA,Vora GJ,Biffinger JC,et al. The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanalysis, 2010,22:856-864
[30] Polizzi NF,Skourtis SS,Beratan DN. Physical constraints on charge transport through bacterial nanowires.Faraday Discussions,2012,155:43-62
[31] Ma J-L(马金莲),Ma C(马晨),Tang J(汤佳),et al. Electron shuttle-mediated extracellular electron transfer of microorganisms:Mechanism and application. Chemical Progress(化学进展),2015,27(12):1833-1840(in Chinese)
[32] Kappler A,Wuestner ML,Ruecker A,et al. Biochar as an electron shuttle between bacteria and Fe(III)minerals. Environmental Science and Technology Letters,2016,1:339-344
[33] Paquete CM,Fonseca BM,Cruz DR,et al. Exploring the molecular mechanisms of electron shuttling across the microbe/metal space. Frontiers in Microbiology,2014,5:1-12
[34] Liu F,Rotaru A,Shrestha PM,et al. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environmental Microbiology,2015,17:648-655
[35] Liu F,Rotaru AE,Shrestha PM,et al. Promoting direct interspecies electron transfer with activated carbon.Energy and Environmental Science,2012,5:8982-8989
[36] Kato S,Hashimoto K,Watanabe K. Methanogenesis facilitated by electric syntrophy via(semi)conductive iron-oxide minerals. Environmental Microbiology,2012,14:1646-1654
[37] Ren G-P(任桂平),Sun M-Y(孙曼仪),Lu A-H(鲁安怀),et al. The mechanism of the microbial extracellular electron transfer promoted by natural hematite inredsoil. Bulletin of Mineralogy,Petrology and Geochemistry(矿物岩石地球化学通报),2017,36(1):92-97(in Chinese)
[38] Xu DK,Gu TY. Carbon source starvation triggered more aggressive corrosion against carbon steel by the Desulfovibrio vulgaris biofilm. International Biodeterioration&Biodegradation,2014,91:74-81
[39] Chen YJ,Tang Q,Senko JM,et al. Long-term survival of Desulfovibrio vulgaris on carbon steel and associated pitting corrosion. Corrosion Science,2015,90:89-100
[40] Zhu GL,Yang Y,Liu J,et al. Enhanced photocurrent production by the synergy of hematite nanowire-arrayed photoanode and bioengineered Shewanella oneidensis MR-1. Biosensors&Bioelectronics,2017,94:227-234
[41] Lu A-H(鲁安怀),Li Y(李艳),Wang X(王鑫),et al. The utilization of solar energy by non-phototrophic microorganisms through semiconducting minerals. Microbiology China(微生物通报),2013,40(1):190-202(in Chinese)
[42] Lu AH,Li Y,Jin S,et al. Growth of non-phototrophic microorganisms using solar energy through mineralphotocatalysis. Nature Communications,3:768, doi:10.1038/ncomms1768
[43] Lu AH,Li Y,Jin S. Interactions between semiconducting minerals and bacteria under light. Elements, 8:125-130
[44] Zhao Z-Q(赵智强). Establishment and Enhancement of Direct Interspecies Electron Transfer between Syntrophic Microorganisms during Anaerobic Methanogenesis.PHD Thesis. Dalian:Dalian University of Technology,2017(in Chinese)
[45] Nakamura R,Kai F,Okamoto A,et al. Self-constructed electrically conductive bacterial networks. Angewandte Chemie,2009,48:508-511
[46] Li DB,Cheng YY,Li LL,et al. Light-driven microbial dissimilatory electron transfer to hematite. Physical Chemistry Chemical Physics,2014,16:23003-23011
[47] Belchik SM,Kennedy DW,Dohnalkova AC,et al.Extracellular reduction of hexavalent chromium by cytochromes MtrC and Omc A of Shewanella oneidensis MR-1. Applied and Environmental Microbiology,2011,77:4035-4041
[48] Mehta T,Coppi MV,Childers SE,et al. Outer membrane c-type cytochromes required for Fe(III)and Mn(IV)oxide reduction in Geobacter sulfurreducens.Applied and Environmental Microbiology, 2005, 71:8634-8641
[49] Cologgi DL,Lampa-Pastirk S,Speers A M,et al.Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proceedings of the National Academy of Sciences of the United States of America,2011,108:15248-15252
[50] Tang Z-R(唐朱睿),Huang C-H(黄彩红),Gao R-T(高如泰),et al. Review on extracellular respiratory bacteria and its application in migration and transformation of pollutants. Journal of Agricultural Resources and Environment(农业资源与环境学报),2017,34(4):299-308(in Chinese)
[51] Yu YY,Guo CX,Yong YC,et al. Nitrogen doped carbon nanoparticles enhanced extracellular electron transfer for high-performance microbial fuel cells anode.Chemosphere,2015,140:26-33
[52] Jiang X,Hu J,Lieber AM,et al. Nanoparticle facilitated extracellular electron transfer in microbial fuel cells.Nano Letters,2014,14:6737-6742
[53] Wu C-Y(武春媛),Li F-B(李芳柏),Zhou S-G(周顺桂). Humus respiration and its ecological significance. Acta Ecologica Sinica(生态学报),2009,29(3):1535-1542(in Chinese)