{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T06:06:05Z","timestamp":1772258765476,"version":"3.50.1"},"reference-count":38,"publisher":"Copernicus GmbH","issue":"10","license":[{"start":{"date-parts":[[2012,10,24]],"date-time":"2012-10-24T00:00:00Z","timestamp":1351036800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biogeosciences"],"abstract":"<jats:p>Abstract. Biologically produced molecular hydrogen (H2) is characterised by a very strong depletion in deuterium. Although the biological source to the atmosphere is small compared to photochemical or combustion sources, it makes an important contribution to the global isotope budget of H2. Large uncertainties exist in the quantification of the individual production and degradation processes that contribute to the atmospheric budget, and isotope measurements are a tool to distinguish the contributions from the different sources. Measurements of \u03b4 D from the various H2 sources are scarce and for biologically produced H2 only very few measurements exist.  Here the first systematic study of the isotopic composition of biologically produced H2 is presented. In a first set of experiments, we investigated \u03b4 D of H2 produced in a biogas plant, covering different treatments of biogas production. In a second set of experiments, we investigated pure cultures of several H2 producing microorganisms such as bacteria or green algae. A Keeling plot analysis provides a robust overall source signature of \u03b4 D = \u2212712\u2030 (\u00b113\u2030) for the samples from the biogas reactor (at 38 \u00b0C, \u03b4 DH2O= +73.4\u2030), with a fractionation constant &amp;amp;varepsilon;H2-H2O of \u2212689\u2030 (\u00b120\u2030) between H2 and the water. The five experiments using pure culture samples from different microorganisms give a mean source signature of \u03b4 D = \u2212728\u2030 (\u00b128\u2030), and a fractionation constant &amp;amp;varepsilon;H2-H2O of \u2212711\u2030 (\u00b134\u2030) between H2 and the water. The results confirm the massive deuterium depletion of biologically produced H2 as was predicted by the calculation of the thermodynamic fractionation factors for hydrogen exchange between H2 and water vapour. Systematic errors in the isotope scale are difficult to assess in the absence of international standards for \u03b4 D of H2.  As expected for a thermodynamic equilibrium, the fractionation factor is temperature dependent, but largely independent of the substrates used and the H2 production conditions. The equilibrium fractionation coefficient is positively correlated with temperature and we measured a rate of change of 2.3\u2030 \/ \u00b0C between 45 \u00b0C and 60 \u00b0C, which is in general agreement with the theoretical prediction of 1.4\u2030 \/ \u00b0C. Our best experimental estimate for &amp;amp;varepsilon;H2-H2O at a temperature of 20 \u00b0C is \u2212731\u2030 (\u00b120\u2030) for biologically produced H2. This value is close to the predicted value of \u2212722\u2030, and we suggest using these values in future global H2 isotope budget calculations and models with adjusting to regional temperatures for calculating \u03b4 D values.<\/jats:p>","DOI":"10.5194\/bg-9-4115-2012","type":"journal-article","created":{"date-parts":[[2012,10,24]],"date-time":"2012-10-24T11:41:07Z","timestamp":1351078867000},"page":"4115-4123","source":"Crossref","is-referenced-by-count":23,"title":["The stable isotopic signature of biologically produced molecular hydrogen (H\n                    <sub>2<\/sub>\n                    )"],"prefix":"10.5194","volume":"9","author":[{"given":"S.","family":"Walter","sequence":"first","affiliation":[]},{"given":"S.","family":"Laukenmann","sequence":"additional","affiliation":[]},{"given":"A. J. M.","family":"Stams","sequence":"additional","affiliation":[]},{"given":"M. K.","family":"Vollmer","sequence":"additional","affiliation":[]},{"given":"G.","family":"Gleixner","sequence":"additional","affiliation":[]},{"given":"T.","family":"R\u00f6ckmann","sequence":"additional","affiliation":[]}],"member":"3145","published-online":{"date-parts":[[2012,10,24]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"Batenburg, A. M., Walter, S., Pieterse, G., Levin, I., Schmidt, M., Jordan, A., Hammer, S., Yver, C., and R\u00f6ckmann, T.: Temporal and spatial variability of the stable isotopic composition of atmospheric molecular hydrogen: observations at six EUROHYDROS stations, Atmos. Chem. Phys., 11, 6985\u20136999, https:\/\/doi.org\/10.5194\/acp-11-6985-2011, 2011.","DOI":"10.5194\/acp-11-6985-2011"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Bottinga, Y.: Calculated fractionation factors for carbon and hydrogen isotope exchange in the system calcite-carbon dioxide-graphite-methane-hydrogen-water vapour, Geochim. Cosmochim. Ac., 33, 49\u201364, 1969.","DOI":"10.1016\/0016-7037(69)90092-1"},{"key":"ref3","doi-asserted-by":"crossref","unstructured":"Bowen, G. J. and J. Revenaugh: Interpolating the isotopic composition of modern meteoric precipitation, Water Resour. Res., 39, 1299, https:\/\/doi.org\/10.1029\/2003WR002086, 2003.","DOI":"10.1029\/2003WR002086"},{"key":"ref4","doi-asserted-by":"crossref","unstructured":"Ehhalt, D. H. and Rohrer, F.: The tropospheric cycle of H2: a critical review, Tellus B, 61, 500\u2013535, 2009.","DOI":"10.1111\/j.1600-0889.2009.00416.x"},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"Feck, T., Groo{\u00df}, J. U., and Riese, M.: Sensitivity of Arctic ozone loss to stratospheric H2O, Geophys. Res. Lett., 35, L01803, https:\/\/doi.org\/10.1029\/2007GL031334, 2008.","DOI":"10.1029\/2007GL031334"},{"key":"ref6","doi-asserted-by":"crossref","unstructured":"Feilberg, K. L., Johnson, M. S., Bacak, A., R\u00f6ckmann, T., and Nielsen, C. J.: Relative tropospheric photolysis rates of HCHO and HCDO measured at the European photoreactor facility, J. Phys. Chem. A, 111, 9034\u20139046, 2007.","DOI":"10.1021\/jp070185x"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Gerst, S. and Quay, P.: Deuterium component of the global molecular hydrogen cycle, J. Geophys. Res., 106, 5021\u20135031, 2001.","DOI":"10.1029\/2000JD900593"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Hauglustaine, D. A. and Ehhalt, D. H.: A three-dimensional model of molecular hydrogen in the troposphere, J. Geophys. Res., 107, 4330\u20134346, https:\/\/doi.org\/10.1029\/2001JD001156, 2002.","DOI":"10.1029\/2001JD001156"},{"key":"ref9","unstructured":"Haus, P., M\u00fchlethaler, T., and Verbree, C.: Wasserstoffproduktion mit Gr\u00fcnalgen, Maturarbeit, Kantonsschule Aarau, Switzerland, 2009."},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Hoffmann, G., Werner, M., and Heimann, M.: The water isotope module of the ECHAM atmospheric general circulation model \u2013 A study on time scales from days to several years, J. Geophys. Res., 103, 16871\u201316896, 1998.","DOI":"10.1029\/98JD00423"},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"Jacobson, M. Z.: Effects of wind-powered hydrogen fuel cell vehicles on stratospheric ozone and global climate, Geophys. Res. Lett., 35, L19803, https:\/\/doi.org\/10.1029\/2008GL035102, 2008.","DOI":"10.1029\/2008GL035102"},{"key":"ref12","doi-asserted-by":"crossref","unstructured":"Jacobson, M. Z., Colella, W. G., and Golden, D. M.: Cleaning the air and improving health with hydrogen fuel-cell vehicles, Science, 308, 1901\u20131905, 2005.","DOI":"10.1126\/science.1109157"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"Kaiser, J., Engel, A., Borchers, R., and R\u00f6ckmann, T.: Probing stratospheric transport and chemistry with new balloon and aircraft observations of the meridional and vertical N2O isotope distribution, Atmos. Chem. Phys., 6, 3535\u20133556, https:\/\/doi.org\/10.5194\/acp-6-3535-2006, 2006.","DOI":"10.5194\/acp-6-3535-2006"},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Laube, J. C., Engel, A., B\u00f6nisch, H., M\u00f6bius, T., Worton, D. R., Sturges, W. T., Grunow, K., and Schmidt, U.: Contribution of very short-lived organic substances to stratospheric chlorine and bromine in the tropics \u2013 a case study, Atmos. Chem. Phys., 8, 7325\u20137334, https:\/\/doi.org\/10.5194\/acp-8-7325-2008, 2008.","DOI":"10.5194\/acp-8-7325-2008"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"Laube, J. C., Martinerie, P., Witrant, E., Blunier, T., Schwander, J., Brenninkmeijer, C. A. M., Schuck, T. J., Bolder, M., R\u00f6ckmann, T., van der Veen, C., B\u00f6nisch, H., Engel, A., Mills, G. P., Newland, M. J., Oram, D. E., Reeves, C. E., and Sturges, W. T.: Accelerating growth of HFC-227ea (1,1,1,2,3,3,3-heptafluoropropane) in the atmosphere, Atmos. Chem. Phys., 10, 5903\u20135910, https:\/\/doi.org\/10.5194\/acp-10-5903-2010, 2010.","DOI":"10.5194\/acp-10-5903-2010"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Nilsson, E. J. K., Johnson, M. S., Taketani, F., Matsumi, Y., Hurley, M. D., and Wallington, T. J.: Atmospheric deuterium fractionation: HCHO and HCDO yields in the CH2DO + O2 reaction, Atmos. Chem. Phys., 7, 5873\u20135881, https:\/\/doi.org\/10.5194\/acp-7-5873-2007, 2007.","DOI":"10.5194\/acp-7-5873-2007"},{"key":"ref17","doi-asserted-by":"crossref","unstructured":"Nilsson, E. J. K., Andersen, V. F., Skov, H., and Johnson, M. S.: Pressure dependence of the deuterium isotope effect in the photolysis of formaldehyde by ultraviolet light, Atmos. Chem. Phys., 10, 3455\u20133462, https:\/\/doi.org\/10.5194\/acp-10-3455-2010, 2010.","DOI":"10.5194\/acp-10-3455-2010"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Nimcevic, D., Schuster, M., and Gapes, J. R.: Solvent production by Clostridium beijerinckii NRRL B592 growing on different potato media, Appl. Microbiol. Biot., 50, 426\u2013428, 1998.","DOI":"10.1007\/s002530051315"},{"key":"ref19","doi-asserted-by":"crossref","unstructured":"Novelli, P. C., Lang, P. M., Masarie, K. A., Hurst, D. F., Myers, R., and Elkins, J. W.: Molecular hydrogen in the troposphere: Global distribution and budget, J. Geophys. Res., 104, 30427\u201330444, 1999.","DOI":"10.1029\/1999JD900788"},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Pieterse, G., Krol, M. C., and R\u00f6ckmann, T.: A consistent molecular hydrogen isotope chemistry scheme based on an independent bond approximation, Atmos. Chem. Phys., 9, 8503\u20138529, https:\/\/doi.org\/10.5194\/acp-9-8503-2009, 2009.","DOI":"10.5194\/acp-9-8503-2009"},{"key":"ref21","doi-asserted-by":"crossref","unstructured":"Pieterse, G., Krol, M. C., Batenburg, A. M., Steele, L. P., Krummel, P. B., Langenfelds, R. L., and R\u00f6ckmann, T.: Global modelling of H2 mixing ratios and isotopic compositions with the TM5 model, Atmos. Chem. Phys., 11, 7001\u20137026, https:\/\/doi.org\/10.5194\/acp-11-7001-2011, 2011.","DOI":"10.5194\/acp-11-7001-2011"},{"key":"ref22","doi-asserted-by":"crossref","unstructured":"Prather, M. J.: An environmental experiment with H2?, Science, 302, 581\u2013582, 2003.","DOI":"10.1126\/science.1091060"},{"key":"ref23","doi-asserted-by":"crossref","unstructured":"Price, H., Jaegle, L., Rice, A., Quay, P., Novelli, P. C., and Gammon, R.: Global budget of molecular hydrogen and its deuterium content: Constraints from ground station, cruise, and aircraft observations, J. Geophys. Res., 112, D22108, https:\/\/doi.org\/10.1029\/2006JD008152, 2007.","DOI":"10.1029\/2006JD008152"},{"key":"ref24","doi-asserted-by":"crossref","unstructured":"Rahn, T., Kitchen, N., and Eiler, J. M.: D\/H ratios of atmospheric H2 in urban air: Results using new methods for analysis of nano-molar H2 samples, Geochim. Cosmochim. Acta, 66, 2475\u20132481, 2002.","DOI":"10.1016\/S0016-7037(02)00858-X"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"Rahn, T., Eiler, J. M., Boering, K. A., Wennberg, P. O., McCarthy, M. C., Tyler, S., Schauffler, S., Donnelly, S., and Atlas, E.: Extreme deuterium enrichment in stratospheric hydrogen and the global atmospheric budget of H2, Nature, 424, 918\u2013921, 2003.","DOI":"10.1038\/nature01917"},{"key":"ref26","doi-asserted-by":"crossref","unstructured":"Rhee, T. S., Mak, J., R\u00f6ckmann, T., and Brenninkmeijer, C. A. M.: Continuous-flow isotope analysis of the deuterium\/hydrogen ratio in atmospheric hydrogen, Rapid Commun. Mass Sp., 18, 299\u2013306, 2004.","DOI":"10.1002\/rcm.1309"},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"Rhee, T. S., Brenninkmeijer, C. A. M., and R\u00f6ckmann, T.: The overwhelming role of soils in the global atmospheric hydrogen cycle, Atmos. Chem. Phys., 6, 1611\u20131625, https:\/\/doi.org\/10.5194\/acp-6-1611-2006, 2006.","DOI":"10.5194\/acp-6-1611-2006"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"Rice, A., Quay, P., Stutsman, J., Gammon, R., Price, H., and Jaegle, L.: Meridional distribution of molecular hydrogen and its deuterium content in the atmosphere, J. Geophys. Res., 115, D12306, https:\/\/doi.org\/10.1029\/2009JD012529, 2010.","DOI":"10.1029\/2009JD012529"},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"R\u00f6ckmann, T., Rhee, T. S., and Engel, A.: Heavy hydrogen in the stratosphere, Atmos. Chem. Phys., 3, 2015\u20132023, https:\/\/doi.org\/10.5194\/acp-3-2015-2003, 2003.","DOI":"10.5194\/acp-3-2015-2003"},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"R\u00f6ckmann, T., G\u00f3mez \u00c1lvarez, C. X., Walter, S., Veen, C. V., Wollny, A. G., Gunthe, S. S., Helas, G., P\u00f6schl, U., Keppler, F., Greule, M., and Brand, W. A.: The isotopic composition of H2 from wood burning - dependency on combustion efficiency, moisture content and \u03b4 D of local precipitation, J. Geophys. Res., 115, D17308, https:\/\/doi.org\/10.1029\/2009JD013188, 2010a.","DOI":"10.1029\/2009JD013188"},{"key":"ref31","doi-asserted-by":"crossref","unstructured":"R\u00f6ckmann, T., Walter, S., Bohn, B., Wegener, R., Spahn, H., Brauers, T., Tillmann, R., Schlosser, E., Koppmann, R., and Rohrer, F.: Isotope effect in the formation of H2 from H2CO studied at the atmospheric simulation chamber SAPHIR, Atmos. Chem. Phys., 10, 5343\u20135357, https:\/\/doi.org\/10.5194\/acp-10-5343-2010, 2010b.","DOI":"10.5194\/acp-10-5343-2010"},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"Schultz, M. G., Diehl, T., Brasseur, G. P., and Zittel, W.: Air pollution and climate-forcing impacts of a global hydrogen economy, Science, 302, 624\u2013627, 2003.","DOI":"10.1126\/science.1089527"},{"key":"ref33","doi-asserted-by":"crossref","unstructured":"Stams, A. J. M., van Dijk, J. B., Dijkema, C., and Plugge, C. M.: Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria, Appl. Environ. Microbiol., 59, 1114\u20131119, 1993.","DOI":"10.1128\/aem.59.4.1114-1119.1993"},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"Stams, A. J. M. and Plugge, C. M.: Electron transfer in syntrophic communities of anaerobic bacteria and archaea, Nat. Rev. Microbiol., 7, 568\u2013577, https:\/\/doi.org\/10.1038\/nrmicro2166, 2009.","DOI":"10.1038\/nrmicro2166"},{"key":"ref35","doi-asserted-by":"crossref","unstructured":"Tromp, T. K., Shia, R.-L., Allen, M., Eiler, J. M., and Yung, Y. L.: Potential environmental impact of a hydrogen economy on the stratosphere, Science, 300, 1740\u20131742, 2003.","DOI":"10.1126\/science.1085169"},{"key":"ref36","doi-asserted-by":"crossref","unstructured":"Vollmer, M. K., Walter, S., Bond, S. W., Soltic, P., and R\u00f6ckmann, T.: Molecular hydrogen (H2) emissions and their isotopic signatures (H\/D) from a motor vehicle: implications on atmospheric H2, Atmos. Chem. Phys., 10, 5707\u20135718, https:\/\/doi.org\/10.5194\/acp-10-5707-2010, 2010.","DOI":"10.5194\/acp-10-5707-2010"},{"key":"ref37","doi-asserted-by":"crossref","unstructured":"Warwick, N. J., Bekki, S., Nisbet, E. G., and Pyle, J. A.: Impact of a hydrogen economy on the stratosphere and troposphere studied in a 2-D model, Geophys. Res. Lett., 31, L05107, https:\/\/doi.org\/10.1029\/2003GL019224, 2004.","DOI":"10.1029\/2003GL019224"},{"key":"ref38","doi-asserted-by":"crossref","unstructured":"Yver, C. E., Pison, I. C., Fortems-Cheiney, A., Schmidt, M., Chevallier, F., Ramonet, M., Jordan, A., S\u00f8vde, O. A., Engel, A., Fisher, R. E., Lowry, D., Nisbet, E. G., Levin, I., Hammer, S., Necki, J., Bartyzel, J., Reimann, S., Vollmer, M. K., Steinbacher, M., Aalto, T., Maione, M., Arduini, J., O'Doherty, S., Grant, A., Sturges, W. T., Forster, G. L., Lunder, C. R., Privalov, V., Paramonova, N., Werner, A., and Bousquet, P.: A new estimation of the recent tropospheric molecular hydrogen budget using atmospheric observations and variational inversion, Atmos. Chem. Phys., 11, 3375\u20133392, https:\/\/doi.org\/10.5194\/acp-11-3375-2011, 2011.","DOI":"10.5194\/acp-11-3375-2011"}],"container-title":["Biogeosciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/bg.copernicus.org\/articles\/9\/4115\/2012\/bg-9-4115-2012.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,15]],"date-time":"2025-02-15T06:02:50Z","timestamp":1739599370000},"score":1,"resource":{"primary":{"URL":"https:\/\/bg.copernicus.org\/articles\/9\/4115\/2012\/"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,10,24]]},"references-count":38,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2012]]}},"URL":"https:\/\/doi.org\/10.5194\/bg-9-4115-2012","relation":{"has-preprint":[{"id-type":"doi","id":"10.5194\/bgd-8-12521-2011","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bgd-8-12521-2011","asserted-by":"object"}]},"ISSN":["1726-4189"],"issn-type":[{"value":"1726-4189","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,10,24]]}}}