微生物VBNC状态形成及复苏机制
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摘要
99%以上的微生物因处于活的但非可培养(viable but non-culturable,VBNC)状态而无法分离培养。复苏促进因子(resuscitation-promoting factors,Rpfs)是培养获取VBNC菌的最重要突破。结合课题组近十余年从环境功能视角利用Rpf复苏培养VBNC菌的研究,本文在阐述微生物VBNC状态的形成及复苏进展的基础上,从VBNC菌形成及复苏过程出发,探究"探索因子"与群体感应的内在关系。并总结了课题组利用Rpf所复苏培养的具有潜在环境功能的VBNC菌种。本论文将为揭示微生物VBNC状态的形成及复苏机制提供新的思路,并为认识和重新评价Rpf法复苏培养VBNC菌在污染环境微生物修复中的作用提供理论依据。
It is estimated that the majority(>99%) of microorganisms resist cultivation because they are in a viable but non-culturable(VBNC) state. Resuscitation-promoting factors(Rpfs) are one of the most important breakthroughs in the cultivation of VBNC bacteria. In the past decade, our group focused on resuscitation of VBNC bacteria by Rpf for exploring their potential environmental functions. Incorporated our previous studies in this mini-reiew, we provided the overview of formation and resuscitation of VBNC bacteria, and explored the relationship between"scout cells" and quorum-sensing based on the process of formation and reversion of VBNC cells. Moreover, we also summarized the VBNC bacteria possessed potential enivronmental functions which were previously isolated from various environments with Rpf addition. This review provides not only a new insight into revealing the the mechanisms of formation and resuscitation of VBNC bacteria, but also a theoretical basis for understanding and re-evaluating the role of Rpf method in the application for environmental bioremediation.
It is estimated that the majority(>99%) of microorganisms resist cultivation because they are in a viable but non-culturable(VBNC) state. Resuscitation-promoting factors(Rpfs) are one of the most important breakthroughs in the cultivation of VBNC bacteria. In the past decade, our group focused on resuscitation of VBNC bacteria by Rpf for exploring their potential environmental functions. Incorporated our previous studies in this mini-reiew, we provided the overview of formation and resuscitation of VBNC bacteria, and explored the relationship between"scout cells" and quorum-sensing based on the process of formation and reversion of VBNC cells. Moreover, we also summarized the VBNC bacteria possessed potential enivronmental functions which were previously isolated from various environments with Rpf addition. This review provides not only a new insight into revealing the the mechanisms of formation and resuscitation of VBNC bacteria, but also a theoretical basis for understanding and re-evaluating the role of Rpf method in the application for environmental bioremediation.
引文
[1]Pinto D,Santos MA,Chambel L.Thirty years of viable but nonculturable state research:Unsolved molecular mechanisms.Critical Reviews in Microbiology,2015,41(1):61–76.
[2]Epstein SS.Microbial awakenings.Nature,2009,457(7233):1083.
[3]Galloway WRJD,Hodgkinson JT,Bowden SD,Welch M,Spring DR.Quorum sensing in Gram-negative bacteria:small-molecule modulation of AHL and AI-2 quorum sensing pathways.Chemical Reviews,2011,111(1):28–67.
[4]Su XM,Liu YD,Hashmi MZ,Hu JX,Ding LX,Wu M,Shen CF.Rhodococcus biphenylivorans sp.nov.,a polychlorinated biphenyl-degrading bacterium.Antonie Van Leeuwenhoek,2015,107(1):55–63.
[5]Yu XY,Zhang L,Ren B,Yang N,Liu M,Liu XT,Zhang LX,Ding LX.Arthrobacter liuii sp.nov.,resuscitated from Xinjiang desert soil.International Journal of Systematic and Evolutionary Microbiology,2015,65(3):896–901.
[6]Su XM,Sun FQ,Wang YL,Hashmi MZ,Guo L,Ding LX,Shen CF.Identification,characterization and molecular analysis of the viable but nonculturable Rhodococcus biphenylivorans.Scientific Reports,2015,5:18590.
[7]Epstein SS.The phenomenon of microbial uncultivability.Current Opinion in Microbiology,2013,16(5):636–642.
[8]Winterberg H.Zur Methodik der Bakterienz?hlung.Zeitschrift für Hygiene und Infektionskrankheiten,1898,29(1):75–93.
[9]Amann J.Die direkte Z?hlung der Wasserbakterien mittels des Ultramikroskops.Centralbl Bakteriol,1911,29:381–384.
[10]Staley JT,Konopka A.Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats.Annual Review of Microbiology,1985,39(1):321–346.
[11]Vartoukian SR,Palmer RM,Wade WG.Strategies for culture of‘unculturable’bacteria.FEMS Microbiology Letters,2010,309(1):1–7.
[12]Eichorst SA,Breznak JA,Schmidt TM.Isolation and characterization of soil bacteria that define Terriglobus gen.nov.,in the phylum Acidobacteria.Applied and Environmental Microbiology,2007,73(8):2708–2717.
[13]Miller MB,Bassler BL.Quorum sensing in bacteria.Annual Review in Microbiology,2001,55(1):165–199.
[14]Cano RJ,Borucki MK.Revival and identification of bacterial spores in 25-to 40-million-year-old dominican amber.Science,1995,268(5213):1060–1064.
[15]Colwell RR,Brayton PR,Grimes DJ,Roszak DB,Huq SA,Palmer LM.Viable but non-culturable Vibrio cholerae and related pathogens in the environment:implications for release of genetically engineered microorganisms.Nature Biotechnology,1985,3(9):817–820.
[16]Signoretto C,Burlacchini G,del Mar LleòM,Pruzzo C,Zampini M,Pane L,Franzini G,Canepari P.Adhesion of Enterococcus faecalis in the nonculturable state to plankton is the main mechanism responsible for persistence of this bacterium in both lake and seawater.Applied and Environmental Microbiology,2004,70(11):6892–6896.
[17]Signoretto C,Burlacchini G,Pruzzo C,Canepari P.Persistence of Enterococcus faecalis in aquatic environments via surface interactions with copepods.Applied and Environmental Microbiology,2005,71(5):2756–2761.
[18]Whitesides MD,Oliver JD.Resuscitation of Vibrio vulnificusfrom the viable but nonculturable state.Applied and Environmental Microbiology,1997,63(3):1002–1005.
[19]Du M,Chen JX,Zhang XH,Li AJ,Li Y.Characterization and resuscitation of viable but nonculturable Vibrio alginolyticusVIB283.Archives of Microbiology,2007,188(3):283–288.
[20]Mc Dougald D,Rice SA,Weichart D,Kjelleberg S.Nonculturability:adaptation or debilitation?FEMS Microbiology Ecology,1998,25(1):1–9.
[21]Nystr?m T.Conditional senescence in bacteria:death of the immortals.Molecular Microbiology,2003,48(1):17–23.
[22]Nystr?m T.Not quite dead enough:on bacterial life,culturability,senescence,and death.Archives of Microbiology,2001,176(3):159–164.
[23]Kaprelyants AS,Mukamolova GV,Kell DB.Estimation of dormant Micrococcus luteus cells by penicillin lysis and by resuscitation in cell-free spent culture medium at high dilution.FEMS Microbiology Letters,1994,115(2-3):347–352.
[24]Mukamolova GV,Kaprelyants AS,Kell DB.Secretion of an antibacterial factor during resuscitation of dormant cells in Micrococcus luteus cultures held in an extended stationary phase.Antonie Van Leeuwenhoek,1995,67(3):289–295.
[25]Mukamolova GV,Kaprelyants AS,Young DI,Young M,Kell DB.A bacterial cytokine.Proceedings of the National Academy of Sciences of the United States of America,1998,95(15):8916–8921.
[26]Mukamolova GV,Kormer SS,Kell DB,Kaprelyants AS.Stimulation of the multiplication of Micrococcus luteus by an autocrine growth factor.Archives of Microbiology,1999,172(1):9–14.
[27]Cohen-Gonsaud M,Keep NH,Davies AP,Ward J,Henderson B,Labesse G.Resuscitation-promoting factors possess a lysozyme-like domain.Trends in Biochemical Sciences,2004,29(1):7–10.
[28]Cohen-Gonsaud M,Barthe P,Bagnéris C,Henderson B,Ward J,Roumestand C,Keep NH.The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes.Nature Structural&Molecular Biology,2005,12(3):270–273.
[29]Mukamolova GV,Murzin AG,Salina EG,Demina GR,Kell DB,Kaprelyants AS,Young M.Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation.Molecular Microbiology,2006,59(1):84–98.
[30]Nikitushkin VD,Demina GR,Shleeva MO,Guryanova SV,Ruggiero A,Berisio R,Kaprelyants AS.A product of Rpf B and Rip A joint enzymatic action promotes the resuscitation of dormant mycobacteria.FEBS Journal,2015,282(13):2500–2511.
[31]Ruggiero A,Squeglia F,Romano M,Vitagliano L,de Simone A,Berisio R.Structure and dynamics of the multi-domain resuscitation promoting factor Rpf B from Mycobacterium tuberculosis.Journal of Biomolecular Structure&Dynamics,2017,35(6):1322–1330.
[32]Ruggiero A,Squeglia F,Romano M,Vitagliano L,de Simone A,Berisio R.The structure of Resuscitation promoting factor B from M.tuberculosis reveals unexpected ubiquitin-like domains.Biochimica Et Biophysica Acta(BBA)-General Subjects,2016,1860(2):445–451.
[33]Buerger S,Spoering A,Gavrish E,Leslin C,Ling L,Epstein SS.Microbial scout hypothesis,stochastic exit from dormancy,and the nature of slow growers.Applied and Environmental Microbiology,2012,78(9):3221–3228.
[34]Papenfort K,Bassler BL.Quorum sensing signal-response systems in Gram-negative bacteria.Nature Reviews Microbiology,2016,14(9):576–588.
[35]Mukamolova GV,Turapov OA,Kazarian K,Telkov M,Kaprelyants AS,Kell DB,Young M.The rpf gene of Micrococcus luteus encodes an essential secreted growth factor.Molecular Microbiology,2002,46(3):611–621.
[36]Kell DB,Young M.Bacterial dormancy and culturability:the role of autocrine growth factors:Commentary.Current Opinion in Microbiology,2000,3(3):238–243.
[37]Ayrapetyan M,Williams TC,Oliver JD.Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios.Applied and Environmental Microbiology,2014,80(8):2478–2483.
[38]Su XM,Liu YD,Hashmi MZ,Ding LX,Shen CF.Culture-dependent and culture-independent characterization of potentially functional biphenyl-degrading bacterial community in response to extracellular organic matter from Micrococcus luteus.Microbial Biotechnology,2015,8(3):569–578.
[39]Vaidya S,Jain K,Madamwar D.Metabolism of pyrene through phthalic acid pathway by enriched bacterial consortium composed of Pseudomonas,Burkholderia,andRhodococcus(PBR).3 Biotech,2017,7(1):29.
[40]Mishra S,Panda S,Pradhan N,Satapathy D,Biswal SK,Mishra BK.Insights into DBT biodegradation by a native Rhodococcus strain and its sulphur removal efficacy for two Indian coals and calcined pet coke.International Biodeterioration&Biodegradation,2017,120:124–134.
[41]Carvajal P,Alejandro Dinamarca M,Baeza P,CamúE,Ojeda J.Removal of sulfur-containing organic molecules adsorbed on inorganic supports by Rhodococcus Rhodochrous spp..Biotechnology Letters,2017,39(2):241–245.
[42]Su XM,Zhang Q,Hu JX,Hashmi MZ,Ding LX,Shen CF.Enhanced degradation of biphenyl from PCB-contaminated sediments:the impact of extracellular organic matter from Micrococcus luteus.Applied Microbiology and Biotechnology,2015,99(4):1989–2000.
[2]Epstein SS.Microbial awakenings.Nature,2009,457(7233):1083.
[3]Galloway WRJD,Hodgkinson JT,Bowden SD,Welch M,Spring DR.Quorum sensing in Gram-negative bacteria:small-molecule modulation of AHL and AI-2 quorum sensing pathways.Chemical Reviews,2011,111(1):28–67.
[4]Su XM,Liu YD,Hashmi MZ,Hu JX,Ding LX,Wu M,Shen CF.Rhodococcus biphenylivorans sp.nov.,a polychlorinated biphenyl-degrading bacterium.Antonie Van Leeuwenhoek,2015,107(1):55–63.
[5]Yu XY,Zhang L,Ren B,Yang N,Liu M,Liu XT,Zhang LX,Ding LX.Arthrobacter liuii sp.nov.,resuscitated from Xinjiang desert soil.International Journal of Systematic and Evolutionary Microbiology,2015,65(3):896–901.
[6]Su XM,Sun FQ,Wang YL,Hashmi MZ,Guo L,Ding LX,Shen CF.Identification,characterization and molecular analysis of the viable but nonculturable Rhodococcus biphenylivorans.Scientific Reports,2015,5:18590.
[7]Epstein SS.The phenomenon of microbial uncultivability.Current Opinion in Microbiology,2013,16(5):636–642.
[8]Winterberg H.Zur Methodik der Bakterienz?hlung.Zeitschrift für Hygiene und Infektionskrankheiten,1898,29(1):75–93.
[9]Amann J.Die direkte Z?hlung der Wasserbakterien mittels des Ultramikroskops.Centralbl Bakteriol,1911,29:381–384.
[10]Staley JT,Konopka A.Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats.Annual Review of Microbiology,1985,39(1):321–346.
[11]Vartoukian SR,Palmer RM,Wade WG.Strategies for culture of‘unculturable’bacteria.FEMS Microbiology Letters,2010,309(1):1–7.
[12]Eichorst SA,Breznak JA,Schmidt TM.Isolation and characterization of soil bacteria that define Terriglobus gen.nov.,in the phylum Acidobacteria.Applied and Environmental Microbiology,2007,73(8):2708–2717.
[13]Miller MB,Bassler BL.Quorum sensing in bacteria.Annual Review in Microbiology,2001,55(1):165–199.
[14]Cano RJ,Borucki MK.Revival and identification of bacterial spores in 25-to 40-million-year-old dominican amber.Science,1995,268(5213):1060–1064.
[15]Colwell RR,Brayton PR,Grimes DJ,Roszak DB,Huq SA,Palmer LM.Viable but non-culturable Vibrio cholerae and related pathogens in the environment:implications for release of genetically engineered microorganisms.Nature Biotechnology,1985,3(9):817–820.
[16]Signoretto C,Burlacchini G,del Mar LleòM,Pruzzo C,Zampini M,Pane L,Franzini G,Canepari P.Adhesion of Enterococcus faecalis in the nonculturable state to plankton is the main mechanism responsible for persistence of this bacterium in both lake and seawater.Applied and Environmental Microbiology,2004,70(11):6892–6896.
[17]Signoretto C,Burlacchini G,Pruzzo C,Canepari P.Persistence of Enterococcus faecalis in aquatic environments via surface interactions with copepods.Applied and Environmental Microbiology,2005,71(5):2756–2761.
[18]Whitesides MD,Oliver JD.Resuscitation of Vibrio vulnificusfrom the viable but nonculturable state.Applied and Environmental Microbiology,1997,63(3):1002–1005.
[19]Du M,Chen JX,Zhang XH,Li AJ,Li Y.Characterization and resuscitation of viable but nonculturable Vibrio alginolyticusVIB283.Archives of Microbiology,2007,188(3):283–288.
[20]Mc Dougald D,Rice SA,Weichart D,Kjelleberg S.Nonculturability:adaptation or debilitation?FEMS Microbiology Ecology,1998,25(1):1–9.
[21]Nystr?m T.Conditional senescence in bacteria:death of the immortals.Molecular Microbiology,2003,48(1):17–23.
[22]Nystr?m T.Not quite dead enough:on bacterial life,culturability,senescence,and death.Archives of Microbiology,2001,176(3):159–164.
[23]Kaprelyants AS,Mukamolova GV,Kell DB.Estimation of dormant Micrococcus luteus cells by penicillin lysis and by resuscitation in cell-free spent culture medium at high dilution.FEMS Microbiology Letters,1994,115(2-3):347–352.
[24]Mukamolova GV,Kaprelyants AS,Kell DB.Secretion of an antibacterial factor during resuscitation of dormant cells in Micrococcus luteus cultures held in an extended stationary phase.Antonie Van Leeuwenhoek,1995,67(3):289–295.
[25]Mukamolova GV,Kaprelyants AS,Young DI,Young M,Kell DB.A bacterial cytokine.Proceedings of the National Academy of Sciences of the United States of America,1998,95(15):8916–8921.
[26]Mukamolova GV,Kormer SS,Kell DB,Kaprelyants AS.Stimulation of the multiplication of Micrococcus luteus by an autocrine growth factor.Archives of Microbiology,1999,172(1):9–14.
[27]Cohen-Gonsaud M,Keep NH,Davies AP,Ward J,Henderson B,Labesse G.Resuscitation-promoting factors possess a lysozyme-like domain.Trends in Biochemical Sciences,2004,29(1):7–10.
[28]Cohen-Gonsaud M,Barthe P,Bagnéris C,Henderson B,Ward J,Roumestand C,Keep NH.The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes.Nature Structural&Molecular Biology,2005,12(3):270–273.
[29]Mukamolova GV,Murzin AG,Salina EG,Demina GR,Kell DB,Kaprelyants AS,Young M.Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation.Molecular Microbiology,2006,59(1):84–98.
[30]Nikitushkin VD,Demina GR,Shleeva MO,Guryanova SV,Ruggiero A,Berisio R,Kaprelyants AS.A product of Rpf B and Rip A joint enzymatic action promotes the resuscitation of dormant mycobacteria.FEBS Journal,2015,282(13):2500–2511.
[31]Ruggiero A,Squeglia F,Romano M,Vitagliano L,de Simone A,Berisio R.Structure and dynamics of the multi-domain resuscitation promoting factor Rpf B from Mycobacterium tuberculosis.Journal of Biomolecular Structure&Dynamics,2017,35(6):1322–1330.
[32]Ruggiero A,Squeglia F,Romano M,Vitagliano L,de Simone A,Berisio R.The structure of Resuscitation promoting factor B from M.tuberculosis reveals unexpected ubiquitin-like domains.Biochimica Et Biophysica Acta(BBA)-General Subjects,2016,1860(2):445–451.
[33]Buerger S,Spoering A,Gavrish E,Leslin C,Ling L,Epstein SS.Microbial scout hypothesis,stochastic exit from dormancy,and the nature of slow growers.Applied and Environmental Microbiology,2012,78(9):3221–3228.
[34]Papenfort K,Bassler BL.Quorum sensing signal-response systems in Gram-negative bacteria.Nature Reviews Microbiology,2016,14(9):576–588.
[35]Mukamolova GV,Turapov OA,Kazarian K,Telkov M,Kaprelyants AS,Kell DB,Young M.The rpf gene of Micrococcus luteus encodes an essential secreted growth factor.Molecular Microbiology,2002,46(3):611–621.
[36]Kell DB,Young M.Bacterial dormancy and culturability:the role of autocrine growth factors:Commentary.Current Opinion in Microbiology,2000,3(3):238–243.
[37]Ayrapetyan M,Williams TC,Oliver JD.Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios.Applied and Environmental Microbiology,2014,80(8):2478–2483.
[38]Su XM,Liu YD,Hashmi MZ,Ding LX,Shen CF.Culture-dependent and culture-independent characterization of potentially functional biphenyl-degrading bacterial community in response to extracellular organic matter from Micrococcus luteus.Microbial Biotechnology,2015,8(3):569–578.
[39]Vaidya S,Jain K,Madamwar D.Metabolism of pyrene through phthalic acid pathway by enriched bacterial consortium composed of Pseudomonas,Burkholderia,andRhodococcus(PBR).3 Biotech,2017,7(1):29.
[40]Mishra S,Panda S,Pradhan N,Satapathy D,Biswal SK,Mishra BK.Insights into DBT biodegradation by a native Rhodococcus strain and its sulphur removal efficacy for two Indian coals and calcined pet coke.International Biodeterioration&Biodegradation,2017,120:124–134.
[41]Carvajal P,Alejandro Dinamarca M,Baeza P,CamúE,Ojeda J.Removal of sulfur-containing organic molecules adsorbed on inorganic supports by Rhodococcus Rhodochrous spp..Biotechnology Letters,2017,39(2):241–245.
[42]Su XM,Zhang Q,Hu JX,Hashmi MZ,Ding LX,Shen CF.Enhanced degradation of biphenyl from PCB-contaminated sediments:the impact of extracellular organic matter from Micrococcus luteus.Applied Microbiology and Biotechnology,2015,99(4):1989–2000.