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Impact of the hydrogen partial pressure on lactate degradation in a coculture of Desulfovibrio sp. G11 and Methanobrevibacter arboriphilus DH1

  • Environmental biotechnology
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Abstract

In this study, the impact of the hydrogen partial pressure on lactate degradation was investigated in a coculture of Desulfovibrio sp. G11 and Methanobrevibacter arboriphilus DH1. To impose a change of the hydrogen partial pressure, formate was added to the reactor. Hydrogen results from the bioconversion of formate besides lactate in the liquid phase. In the presence of a hydrogen-consuming methanogen, this approach allows for a better estimation of low dissolved hydrogen concentrations than under conditions where hydrogen is supplied externally from the gas phase, resulting in a more accurate determination of kinetic parameters. A change of the hydrogen partial pressure from 1,200 to 250 ppm resulted in a threefold increase of the biomass-specific lactate consumption rate. The 50 % inhibition constant of hydrogen on lactate degradation was determined as 0.692 ± 0.064 μM dissolved hydrogen (831 ± 77 ppm hydrogen in the gas phase). Moreover, for the first time, the maximum biomass-specific lactate consumption rate of Desulfovibrio sp. G11 (0.083 ± 0.006 mol-Lac/mol-XG11/h) and the affinity constant for hydrogen uptake of Methanobrevibacter arboriphilus DH1 (0.601 ± 0.022 μM dissolved hydrogen) were determined. Contrary to the widely established view that the biomass-specific growth rate of a methanogenic coculture is determined by the hydrogen-utilizing partner; here, it was found that the hydrogen-producing bacterium determined the biomass-specific growth rate of the coculture grown on lactate and formate.

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References

  • Archer DB, Powell GE (1985) Dependence of the specific growth-rate of methanogenic mutualistic cocultures on the methanogen. Arch Microbiol 141(2):133–137. doi:10.1007/Bf00423273

    Article  CAS  Google Scholar 

  • Brill WJ, Wolin EA, Wolfe RS (1964) Anaerobic formate oxidation: a ferredoxin-dependent reaction. Science 144(3616):297–298. doi:10.1126/science.144.3616.297

    Article  CAS  PubMed  Google Scholar 

  • Cussler EL (1997) Mass Transfer in Fluid Systems, 2nd edn. Cambridge University Press, New York

    Google Scholar 

  • de Kok S, Meijer J, van Loosdrecht MCM, Kleerebezem R (2013) Impact of dissolved hydrogen partial pressure on mixed culture fermentations. Appl Microbiol Biot 97(6):2617–2625. doi:10.1007/s00253-012-4400-x

    Article  CAS  Google Scholar 

  • Dolfing J, Jiang B, Henstra AM, Stams AJ, Plugge CM (2008) Syntrophic growth on formate: a new microbial niche in anoxic environments. Appl Environ Microbiol 74(19):6126–6131. doi:10.1128/AEM. 01428-08

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fitz RM, Cypionka H (1991) Generation of a proton gradient in Desulfovibrio vulgaris. Arch Microbiol 155(5):444–448. doi:10.1007/bf00244959

    Article  CAS  Google Scholar 

  • Goodwin S, Giraldogomez E, Mobarry B, Switzenbaum MS (1991) Comparison of diffusion and reaction-rates in anaerobic microbial aggregates. Microbial Ecol 22(2):161–174. doi:10.1007/Bf02540221

    Article  CAS  Google Scholar 

  • Junicke H, Abbas B, Oentoro J, van Loosdrecht M, Kleerebezem R (2014) Absolute quantification of individual biomass concentrations in a methanogenic coculture. AMB Express 4:35. doi:10.1186/s13568-014-0035-x

    Article  PubMed Central  PubMed  Google Scholar 

  • Kleerebezem R, Stams AJM (2000) Kinetics of syntrophic cultures: a theoretical treatise on butyrate fermentation. Biotechnol Bioeng 67(5):529–543. doi:10.1002/(Sici)1097-0290(20000305)67:5<529::Aid-Bit4>3.0.Co;2-Q

    Article  CAS  PubMed  Google Scholar 

  • Kleerebezem R, Van Loosdrecht MCM (2010) A generalized method for thermodynamic state analysis of environmental systems. Crit Rev Env Sci Tec 40(1):1–54. doi:10.1080/10643380802000974

    Article  Google Scholar 

  • Kristjansson JK, Schonheit P, Thauer RK (1982) Different Ks-values for hydrogen of methanogenic bacteria and sulfate reducing bacteria—an explanation for the apparent inhibition of methanogenesis by sulfate. Arch Microbiol 131(3):278–282. doi:10.1007/Bf00405893

    Article  CAS  Google Scholar 

  • Leadbetter JR, Breznak JA (1996) Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Appl Environ Microbiol 62(10):3620–3631

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li X, McInerney MJ, Stahl DA, Krumholz LR (2011) Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate. Microbiology 157(10):2912–2921. doi:10.1099/mic. 0.051284-0

    Article  CAS  PubMed  Google Scholar 

  • McCarty PL, Bae J (2011) Model to couple anaerobic process kinetics with biological growth equilibrium thermodynamics. Environ Sci Technol 45(16):6838–6844. doi:10.1021/Es2009055

    Article  CAS  PubMed  Google Scholar 

  • Meyer B, Kuehl J, Deutschbauer AM, Price MN, Arkin AP, Stahl DA (2013) Variation among Desulfovibrio species in electron transfer systems used for syntrophic growth. J Bacteriol 195(5):990–1004. doi:10.1128/JB.01959-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noguera DR, Brusseau GA, Rittmann BE, Stahl DA (1998) A unified model describing the role of hydrogen in the growth of Desulfovibrio vulgaris under different environmental conditions. Biotechnol Bioeng 59(6):732–746

    Article  CAS  PubMed  Google Scholar 

  • Pankhania IP, Spormann AM, Hamilton WA, Thauer RK (1988) Lactate conversion to acetate, Co2 and H-2 in cell-suspensions of Desulfovibrio vulgaris (Marburg)—indications for the involvement of an energy driven reaction. Arch Microbiol 150(1):26–31. doi:10.1007/Bf00409713

    Article  CAS  Google Scholar 

  • Payot S, Guedon E, Cailliez C, Gelhaye E, Petitdemange H (1998) Metabolism of cellobiose by Clostridium cellulolyticum growing in continuous culture: evidence for decreased NADH reoxidation as a factor limiting growth. Microbiol-Uk 144:375–384

    Article  CAS  Google Scholar 

  • Pieulle L, Guigliarelli B, Asso M, Dole F, Bernadac A, Hatchikian EC (1995) Isolation and characterization of the pyruvate-ferredoxin oxidoreductase from the sulfate-reducing bacterium Desulfovibrio africanus. BBA-Protein Struct M 1250(1):49–59. doi:10.1016/0167-4838(95)00029-t

    Article  Google Scholar 

  • Plugge CM (2005) Anoxic media design, preparation, and considerations. Methods Enzymol 397:3–16. doi:10.1016/S0076-6879(05)97001-8

    Article  CAS  PubMed  Google Scholar 

  • Robinson JA, Tiedje JM (1984) Competition between sulfate-reducing and methanogenic bacteria for H-2 under resting and growing conditions. Arch Microbiol 137(1):26–32. doi:10.1007/Bf00425803

    Article  CAS  Google Scholar 

  • Rodriguez J, Kleerebezem R, Lema JM, van Loosdrecht MCM (2006) Modeling product formation in anaerobic mixed culture fermentations. Biotechnol Bioeng 93(3):592–606. doi:10.1002/Bit.20765

    Article  CAS  PubMed  Google Scholar 

  • Schauer NL, Brown DP, Ferry JG (1982) Kinetics of formate metabolism in Methanobacterium formicicum and Methanospirillum hungatei. Appl Environ Microbiol 44(3):549–554

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol R 61(2):262

    CAS  Google Scholar 

  • Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–452. doi:10.1146/annurev-micro-090110-102844

    Article  CAS  PubMed  Google Scholar 

  • Snoep JL, Joost M, Demattos T, Neijssel OM (1991) Effect of the energy-source on the NADH/NAD ratio and on pyruvate catabolism in anaerobic chemostat cultures of Enterococcus-faecalis NCTC-775. Fems Microbiol Lett 81(1):63–66

    Article  CAS  Google Scholar 

  • Traore AS, Fardeau ML, Hatchikian CE, Legall J, Belaich JP (1983) Energetics of growth of a defined mixed culture of Desulfovibrio vulgaris and Methanosarcina barkeri—interspecies hydrogen transfer in batch and continuous cultures. Appl Environ Microbiol 46(5):1152–1156

    PubMed Central  CAS  PubMed  Google Scholar 

  • Uyeda K, Rabinowitz JC (1971) Pyruvate-ferredoxin oxidoreductase. 3. Purification and properties of the enzyme. J Biol Chem 246(10):3111–3119

    CAS  PubMed  Google Scholar 

  • Walker CB, He Z, Yang ZK, Ringbauer JA Jr, He Q, Zhou J, Voordouw G, Wall JD, Arkin AP, Hazen TC, Stolyar S, Stahl DA (2009) The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191(18):5793–5801. doi:10.1128/JB.00356-09

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warikoo V, McInerney MJ, Robinson JA, Suflita JM (1996) Interspecies acetate transfer influences the extent of anaerobic benzoate degradation by syntrophic consortia. Appl Environ Microbiol 62(1):26–32

    PubMed Central  CAS  PubMed  Google Scholar 

  • Weghoff MC, Bertsch J, Muller V (2014) A novel mode of lactate metabolism in strictly anaerobic bacteria. Environ Microbiol. doi:10.1111/1462-2920.12493

    PubMed  Google Scholar 

  • Willquist K, Nkemka VN, Svensson H, Pawar S, Ljunggren M, Karlsson H, Murto M, Hulteberg C, van Niel EWJ, Liden G (2012) Design of a novel biohythane process with high H2 and CH4 production rates. Int J Hydrogen Energy 37(23):17749–17762. doi:10.1016/j.ijhydene.2012.08.092

    Article  CAS  Google Scholar 

  • Zeikus JG, Henning DL (1975) Methanobacterium arbophilicum sp. nov—obligate anaerobe isolated from wetwood of living trees. A Van Leeuw J Microb 41(4):543–552. doi:10.1007/Bf02565096

    Article  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank Prof. Dr. AJM Stams and the Laboratory of Microbiology at Wageningen University for the supply of microbial cultures. The financial support of the Stichting voor de Technische Wetenschappen (STW, project number 11603) and Veolia Water is gratefully acknowledged.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC, Delft, The Netherlands

    H. Junicke, H. Feldman, M. C. M. van Loosdrecht & R. Kleerebezem

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  1. H. Junicke
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  2. H. Feldman
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  3. M. C. M. van Loosdrecht
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  4. R. Kleerebezem
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Correspondence to H. Junicke.

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Junicke, H., Feldman, H., van Loosdrecht, M.C.M. et al. Impact of the hydrogen partial pressure on lactate degradation in a coculture of Desulfovibrio sp. G11 and Methanobrevibacter arboriphilus DH1. Appl Microbiol Biotechnol 99, 3599–3608 (2015). https://doi.org/10.1007/s00253-014-6241-2

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