- Organic Geochemistry
- Marine Biogeochemistry
- Intact polar lipids
- Liquid Chromatography Mass Spectrometry
Dr. Nicole Bale
Research interests
Microbial lipids: The three domain “lipid divide”
Tremendous progress has been made in the last decade in the genetic characterization of microorganisms, both in culture and in the environment. However, our knowledge of microbial membrane lipids, essential building blocks of the cell, has only marginally improved. This is remarkable since there exists a dichotomy in the distribution of lipids between the three Domains of Life. Diacyl glycerols based on straight-chain fatty acids are produced by bacteria and eukaryotes, whereas archaea synthesize isoprenoidal glycerol ether lipids. From a microbial evolutionary perspectives, this ‘lipid divide’ is enigmatic since it has recently become clear that eukaryotes evolved from the archaea. When novel analytical methodology is used, there is a large hidden diversity in microbial lipid composition that may resolve this fundamental question. We propose to systematically characterize prokaryotic intact polar lipids with state-of-the-art analytical techniques based on liquid chromatography and high-resolution mass spectrometry to bring our knowledge of microbial lipids to the next level.
Novel biomarkers for symbiotic N2 fixing cyanobacteria in marine diatoms.
This research project focuses on tracing marine symbiotic heterocystous cyanobacteria in present and past marine environments. It is important to gain more knowledge about these cyanobacteria because they are sustaining marine primary production in the oligotrophic ocean. The development of a new glycolipid biomarker will allow the investigation of cyanobacteria – diatom symbioses in the natural environment and assess the importance for present day fixation of dinitrogen in the ocean. In addition, the application of this new tracer to analyze the sediment record has the unique potential to improve our knowledge of the paleo-N-cycle. Elucidating the contribution of dinitrogen-fixing cyanobacteria in the past when the atmospheric CO2 levels were high will give clues to predict changes in the nitrogen cycle during the expected high CO2 future.
You can read about the HCC research cruise as part of this project here.
Detailed study of the nitrogen cycle in the North Sea and Wadden Sea
This research formed part of a multi-disciplinary project entitled “The nitrogen cycle and changes in the carrying capacity of coastal waters (NICYCLE)”. This project, funded as part of the Dutch National Program for Sea and Coastal Research (ZKO), performed an extensive study of key nitrogen cycling microorganisms in the Netherlands’ coastal waters, the North and Wadden Seas. My strength is in analytical chemistry and my work within this project concentrated on the specific intact polar lipids (IPLs) associated with nitrogen cycling microorganisms in order to trace their activity and diversity, using organic geochemical techniques such as liquid chromatography- multistage mass spectrometry (LC-MS/MS).
Publications:
2020
A search for the membrane lipids of the uncultivated Marine Group II and III Euryarchaeota. Marc Besseling, Ellen Hopmans, Nicole Bale, Stefan Schouten, Jaap Sinninghe Damsté, Laura Villanueva. Scientific Reports.
2019
The membrane lipid composition of the moderately thermophilic ammonia-oxidizing archaeon Ca. Nitrosotenius uzonensis at different growth temperatures. Nicole J. Bale, Marton Palatinszky, W. Irene. C. Rijpstra, Craig Herbold, Michael Wagner, Jaap. S. Sinninghe Damsté. Applied and Environmental Microbiology.
Natronolimnobius sulfurireducens sp. nov., and Halalkaliarchaeum desulfuricum gen. nov., sp. nov., the first sulfur-respiring alkaliphilic haloarchaea from hypersaline alkaline lakes. Dimitry Y Sorokin; Mikhail Yakimov; Enzo Messina; Nicole J Bale; Jaap S Sinninghe Damsté; Alexander Y. Merkel.
Halococcoides cellulosivorans gen. nov., sp. nov., an extremely halophilic cellulose-utilizing haloarchaeon from hypersaline lakes. Dimitry Y Sorokin, Tatiana V Khijniak, Nadezhda A Kostrikina, Alexander G Elcheninov, Stepan V Toshchakov, Nicole J Bale, Jaap S Sinninghe Damsté, Ilya V Kublanov. International Journal of Systematic and Evolutionary Microbiology 69:1327–1335.
New insights into the polar lipid composition of extremely halo(alkali)philic euryarchaea from hypersaline lakes. Nicole Bale, Dimitry Y. Sorokin, Ellen C. Hopmans, Michel Koenen, W. Irene C. Rijpstra, Laura Villanueva, Hans Wienk, Jaap S. Sinninghe Damsté. Frontiers in Microbiology. 10:337, 2019.
Biomarker evidence for cyanobacterial blooms in a brackish surface layer in the Mediterranean Sea during sapropel deposition. Nicole Bale, Rick Hennekam, Ellen C. Hopmans, Denise Dorhout, Gert-Jan Reichart, Marcel van der Meer, Tracy A. Villareal, Jaap S. Sinninghe Damsté, Stefan Schouten. Geology.
Natrarchaeobius chitinivorans gen. nov., sp. nov., and Natrarchaeobius haloalkaliphilus sp. nov., alkaliphilic, chitin-utilizing haloarchaea from hypersaline alkaline lakes. Dimitry Sorokin, Alexander Elcheninov, Jaap Sinninghe Damsté, Nicole Bale, Stepan Toshchakov, Tatiana Khijniak, Ilya Kublanov. Systematic and Applied Microbiology. 42, 309-318, 2019.
Fatty acid and hopanoid adaption to cold in the methanotroph Methylovulum psychrotolerans
2018
C5 glycolipids of heterocystous cyanobacteria track symbiont abundance in the diatom Hemiaulus hauckii
across the tropical north Atlantic. Nicole J. Bale, Tracy A. Villareal, Ellen C. Hopmans, Corina P.D. Brussaard, Marc Besseling, Denise Dorhout, Jaap S. Sinninghe Damsté, Stefan Schouten. Biogeosciences. 15, 1229–1241, 2018.
A quest for the biological sources of the ubiquitous long chain alkyl diols in the marine realm. Sergio Balzano, Julie Lattaud; Laura Villanueva; Sebastiaan Rampen; Corina P Brussaard; Judith van Bleijswijk; Nicole Bale; Jaap S Sinninghe Damsté; Stefan Schouten. Biogeosciences. 15, 5951-5968, 2018
Natronobiforma cellulotropha gen. nov., sp. nov., a novel haloalkaliphilic member of the family Natrialbaceae (class Halobacteria) from hypersaline alkaline lakes. Dimitry Sorokin, Taniana Khijniak, Nadezhda Kostrikina, Alexander Elcheninov, Stepan Toshchakov, Nicole Bale, Jaap Sinninghe Damste, Ilya Kublanov. Systematic and Applied Microbiology 41, 355-362, 2018.
A novel heterocyst glycolipid detected in a pelagic N2-fixing cyanobacterium of the genus Calothrix. Nicole J. Bale, Ellen C. Hopmans, Denise Dorhout, Lucas J. Stal, Michele Grego, Judith van Bleijswijk, Jaap S. Sinninghe Damsté, Stefan Schouten. Organic Geochemistry 123, 44-47, 2018.
2017
A method for quantifying heterocyst glycolipids in biomass and sediments. Nicole Bale, Steven de Vries, Ellen C. Hopmans, Jaap S. Sinninghe Damsté, Stefan Schouten. Organic Geochemistry. 110, 33-35, 2017
The Holocene sedimentary record of cyanobacterial glycolipids in the Baltic Sea: Evaluation of their application as tracers of past nitrogen fixation. Martina Sollai, Ellen Hopmans, Nicole Bale, Anchelique Metz, Matthias Moros, and Jaap Sinninghe Damsté. Biogeosciences. 14, 5789–5804, 2017
2016
Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes. Nicole J. Bale, Ellen C. Hopmans, Petra L. Schoon, Anna de Kluijver, John A. Downing, Jack J. Middelburg, Jaap S. Sinninghe Damsté and Stefan Schouten. Limnology and Oceanography. 61, 1065–1077, 2016
Increasing P limitation and viral infection impact lipid remodeling of the picophytoplankter Micromonas pusilla. D. S. Maat, N. J. Bale, E. C. Hopmans, J. S. Sinninghe Damsté, S. Schouten and C. P. D. Brussaard. Biogeosciences. 13, 1667-1676, 2016.
Seasonal changes in the D/H ratio of fatty acids of pelagic microorganisms in the coastal North Sea. S. Heinzelmann, N. Bale, L. Villanueva, D. Sinke-Schoen, K. Philippart, J. Sinninghe Damsté, S. Schouten, and M. van der Meer. Biogeosciences. 13, 5527–5539, 2016
2015
Fatty acid dynamics during viral infection of Phaeocystis globosa. N. J. Bale, D. S. Maat, C. P. D. Brussaard, E. C. Hopmans, A. Mets, J. S. Sinninghe Damsté, S. Schouten. Aquatic Microbial Ecology. 74, 85–94. 2015
Long-chain glycolipids with pentose head groups as biomarkers for marine endosymbiotic heterocystous cyanobacteria. Nicole J. Bale, Ellen C. Hopmans, Claudia Zell, Rodrigo Sobrinho, Jung-Hyun Kim, Jaap S. Sinninghe Damsté, Tracy Villareal, Stefan Schouten. Organic Geochemistry. 81, 1-7. 2015
Chlorophyll-a transformations associated with sinking diatoms during termination of a North Atlantic spring bloom. Nicole J. Bale, Ruth L. Airs, Patrick Martin, Richard S. Lampitt, Carole A. Llewellyn. Marine Chemistry. 172, 23-33. 2015
2014
Diversity and distribution of a key sulpholipid biosynthetic gene in marine microbial assemblages. Laura Villanueva, Nicole Bale, Ellen C. Hopmans, Stefan Schouten and Jaap S. Sinninghe Damsté. Environmental Microbiology. 16, 774-787. 2014
Acquisition of intact polar lipids from the Prymnesiophyte Phaeocystis globosa by its lytic virus PgV-07T. D.S. Maat, N.J. Bale, E.C. Hopmans, A-C. Baudoux, J.S. Sinninghe Damsté, S. Schouten, and C.P.D. Brussaard. Biogeosciences. 11, 185-194. 2014
Occurrence and activity of anammox bacteria in oxygenated, sandy sediments of the southern North Sea. Nicole J. Bale, Laura Villanueva, Haoxin Fan, Lucas J. Stal, Ellen C. Hopmans, Stefan Schouten, Jaap S. Sinninghe Damsté. FEMS Microbiology Ecology. 89, 99 - 110. 2014
Critical assessments of glyco- and phospholipid separation using silica chromatography. Sandra M. Heinzelmann, Nicole J. Bale, Ellen C. Hopmans, Jaap S. Sinninghe Damsté, Stefan Schouten, Marcel T. J. van der Meer. Applied and Environmental Microbiology. 80: 360-365. 2014
Seasonality and depth distribution of the abundance and activity of ammonia oxidizing microorganisms in marine coastal sediments (North Sea). Yvonne A. Lipsewers, Nicole J. Bale, Ellen C. Hopmans, Stefan Schouten, Jaap S. Sinninghe Damsté and Laura Villanueva. Frontiers in Microbiology. 5, article 472. 2014
2013
The fate of chlorophyll-a during a viral infection of Emiliania huxleyi. Bale, N.J., Airs, R.L., KimmanceS.K., Llewellyn, C.A. Aquatic Microbial Ecology. 69, 205-210. 2013
Different seasonality of pelagic and benthic Thaumarchaeota in the North Sea. N. J. Bale, L. Villanueva, E. C. Hopmans, S. Schouten, and J. S. Sinninghe Damsté. Biogeosciences. 10, 7195-7206. 2013
2007 - 2011
The response of carotenoids and chlorophylls during virus infection of Emiliania huxleyi (Prymnesiophyceae). Llewellyn, C. A., Evans, C., Airs, R. L., Cook, I., Bale, N., Wilson, W. H. Journal of Experimental Marine Biology and Ecology. 344 (1): 101-112. 2007
Organic geochemical changes in Pliocene sediments of ODP Site 1083 (Benguela Upwelling System). Richard D. Pancost, Christopher S. Boot, Giovanni Aloisi, Mark Maslin, Claire Bickers,Virginia Ettwein, Nicole Bale, Luke Handley. Palaeogeography, Palaeoclimatology, Palaeoecology. 280 119–131. 2009
Atmospheric pressure chemical ionisation liquid chromatography/mass spectrometry of Type II chlorophyll-a alteration products: Diagnostic fragmentation patterns. Bale, N., Llewellyn, C. A., Airs, R. L. Organic Geochemistry 41, 473-481. 2010
Type I and Type II chlorophyll-a transformation products associated with algal senescence. Bale, N.J., Airs, R.L., Llewellyn, C.A. Organic Geochemistry. 42, 451–464. 2011
Previous employment and study
2005-2009
PhD, Pigment derived biomarkers of phytoplankton fate processes. Plymouth Marine Laboratory & University of Bristol. Supervisors: Dr C. A. Llewellyn, Dr R. L. Airs and Prof. R. D. Pancost.
2001-2005
MSci (Hons) Chemistry with Study in Continental Europe. University of Bristol. Final year research project and dissertation: “The Identification of Maleimides in Marine Sediments from the Benguela and Peru Upwelling Zones”. Supervisor: Prof. R. D. Pancost
2002-2003
Participation in European Erasmus programme, Université Montpellier II, France
Other websites
http://www.linkedin.com/profile/view?id=200231255&trk=nav_responsive_tab_profile
https://www.facebook.com/pages/Marine-Organic-Biogeochemistry/562010007261199?fref=ts
https://www.researchgate.net/profile/Nicole_Bale
https://scholar.google.co.uk/citations?user=8QaryooAAAAJ&hl=en
NIOZ publications
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2020
Besseling, M.A.; Hopmans, E.C.; Bale, N.J.; Schouten, S.; Sinninghe Damsté, J.S.; Villanueva, L. (2020). The absence of intact polar lipid-derived GDGTs in marine waters dominated by Marine Group II: Implications for lipid biosynthesis in Archaea. NPG Scientific Reports 10(1): 10 pp. https://dx.doi.org/10.1038/s41598-019-57035-0
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2019
Bale, N.J.; Hennekam, R.; Hopmans, E.C.; Dorhout, D.; Reichart, G.-J.; Van der Meer, M.T.J.; Villareal, T.A.; Sinninghe Damsté, J.S; Schouten, S. (2019). Biomarker evidence for nitrogen-fixing cyanobacterial blooms in a brackish surface layer in the Nile River plume during sapropel deposition. Geology (Boulder Colo.) 47(11): 1088-1092. https://dx.doi.org/10.1130/g46682.1Bale, N.J.; Palatinszky, M.; Rijpstra, W.I.C.; Herbold, C.W.; Wagner, M.; Sinninghe Damsté, J.S (2019). Membrane lipid composition of the moderately thermophilic ammonia-oxidizing archaeon “Candidatus Nitrosotenuis uzonensis” at different growth temperatures. Appl. Environ. Microbiol. 85(20). https://dx.doi.org/10.1128/aem.01332-19Bale, N.J.; Rijpstra, W.I.C.; Sahonero Canavesi, D.X.; Oshkin, I.Y.; Belova, S.E.; Dedysh, S.N.; Sinninghe Damsté, J.S (2019). Fatty acid and hopanoid adaption to cold in the methanotroph Methylovulum psychrotolerans. Front. Microbiol. 10: article 589. https://dx.doi.org/10.3389/fmicb.2019.00589Bale, N.J.; Sorokin, D.Y.; Hopmans, E.C.; Koenen, M.; Rijpstra, W.I.C.; Villanueva, L.; Wienk, H.; Sinninghe Damsté, J.S. (2019). New insights into the polar lipid composition of extremely halo(alkali)philic euryarchaea from hypersaline lakes. Front. Microbiol. 10: article 377. https://dx.doi.org/10.3389/fmicb.2019.00377Sorokin, D.Y.; Elcheninov, A.G.; Toshchakov, S.V.; Bale, N.J.; Sinninghe Damsté, J.S.; Khijniak, T.V.; Kublanov, I.V. (2019). Natrarchaeobius chitinivorans gen. nov., sp. nov., and Natrarchaeobius halalkaliphilus sp. nov., alkaliphilic, chitin-utilizing haloarchaea from hypersaline alkaline lakes. Syst. Appl. Microbiol. 42(3): 309-318. https://dx.doi.org/10.1016/j.syapm.2019.01.001Sorokin, D.Y.; Khijniak, T.V.; Elcheninov, A.G.; Toshchakov, S.V.; Kostrikina, N.A.; Bale, N.J.; Sinninghe Damsté, J.S; Kublanov, I.V. (2019). Halococcoides cellulosivorans gen. nov., sp. nov., an extremely halophilic cellulose-utilizing haloarchaeon from hypersaline lakes. Int. J. Syst. Evol. Microbiol. 69(5): 1327-1335. https://dx.doi.org/10.1099/ijsem.0.003312Sorokin, D.Y.; Yakimov, M.; Messina, E.; Merkel, A.Y.; Bale, N.J.; Sinninghe Damsté, J.S. (2019). Natronolimnobius sulfurireducens sp. nov. and Halalkaliarchaeum desulfuricum gen. nov., sp. nov., the first sulfur-respiring alkaliphilic haloarchaea from hypersaline alkaline lakes. Int. J. Syst. Evol. Microbiol. 69(9): 2662-2673. https://dx.doi.org/10.1099/ijsem.0.003506
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2018
Bale, N.J.; Hopmans, E.C.; Dorhout, D.; Stal, L.J.; Grego, M.; van Bleijswijk, J.D.L.; Sinninghe Damsté, J.S.; Schouten, S. (2018). A novel heterocyst glycolipid detected in a pelagic N2 -fixing cyanobacterium of the genus Calothrix. Org. Geochem. 123: 44-47. https://doi.org/10.1016/j.orggeochem.2018.06.009Bale, N.J.; Villareal, T.A.; Hopmans, E.C.; Brussaard, C.P.D.; Besseling, M.; Dorhout, D.; Sinninghe Damsté, J.S.; Schouten, S. (2018). C5 glycolipids of heterocystous cyanobacteria track symbiont abundance in the diatom Hemiaulus hauckii across the tropical North Atlantic. Biogeosciences 15(4): 1229-1241. https://dx.doi.org/10.5194/bg-15-1229-2018Balzano, S.; Lattaud, J.; Villanueva, L.; Rampen, S.W.; Brussaard, C.P.D.; van Bleijswijk, J.; Bale, N.; Sinninghe Damsté, J.S.; Schouten, S. (2018). A quest for the biological sources of long chain alkyl diols in the western tropical North Atlantic Ocean. Biogeosciences 15(19): 5951-5968. https://doi.org/10.5194/bg-15-5951-2018Sorokin, D.Y.; Khijniak, T.V.; Kostrikina, N.A.; Elcheninov, A.G.; Toshchakov, S.V.; Bale, N.J.; Sinninghe Damsté, J.S; Kublanov, I.V. (2018). Natronobiforma cellulositropha gen. nov., sp. nov., a novel haloalkaliphilic member of the family Natrialbaceae (class Halobacteria) from hypersaline alkaline lakes. Syst. Appl. Microbiol. 41(4): 355-362. https://dx.doi.org/10.1016/j.syapm.2018.04.002
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2017
Bale, N.; de Vries, S.; Hopmans, E.C.; Sinninghe Damsté, J.S.; Schouten, S. (2017). A method for quantifying heterocyst glycolipids in biomass and sediments. Org. Geochem. 110: 33-35. https://dx.doi.org/10.1016/j.orggeochem.2017.04.010Sollai, M.; Hopmans, E.C.; Bale, N.J.; Mets, A.; Warden, L.; Moros, M.; Sinninghe Damsté, J.S. (2017). The Holocene sedimentary record of cyanobacterial glycolipids in the Baltic Sea: an evaluation of their application as tracers of past nitrogen fixation. Biogeosciences 14(24): 5789-5804. https://doi.org/10.5194/bg-14-5789-2017
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2016
Bale, N.J.; Hopmans, E.C.; Schoon, P.; de Kluijver, A.; Downing, J.A.; Middelburg, J.J.; Sinninghe Damsté, J.S.; Schouten, S. (2016). Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes. Limnol. Oceanogr. 61(3): 1065–1077. dx.doi.org/10.1002/lno.10274Heinzelmann, S.M.; Bale, N.J.; Villanueva, L.; Sinke-Schoen, D.; Philippart, C.J.M.; Sinninghe Damsté, J.S.; Schouten, S.; Van der Meer, M.T.J. (2016). Seasonal changes in the D / H ratio of fatty acids of pelagic microorganisms in the coastal North Sea. Biogeosciences 13: 5527-5539. dx.doi.org/10.5194/bg-13-5527-2016Maat, D.; Bale, N.J.; Hopmans, E.C.; Sinninghe Damsté, J.S.; Schouten, S.; Brussaard, C.P.D. (2016). Increasing P limitation and viral infection impact lipid remodeling of the picophytoplankter Micromonas pusilla. Biogeosciences 13(5): 1667-1676. http://dx.doi.org/10.5194/bg-13-1667-2016
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2015
Bale, N.; Hopmans, E.C.; Zell, C.; Sobrinho, R.; Kim, J.H.; Sinninghe Damsté, J.S.; Villareal, T.A.; Schouten, S. (2015). Long chain glycolipids with pentose head groups as biomarkers for marine endosymbiotic heterocystous cyanobacteria. Org. Geochem. 81: 1-7. https://dx.doi.org/10.1016/j.orggeochem.2015.01.004Bale, N.J.; Maat, D.S.; Hopmans, E.C.; Mets, A.; Sinninghe Damsté, J.S.; Brussaard, C.P.D.; Schouten, S. (2015). Fatty acid dynamics during viral infection of Phaeocystis globosa. Aquat. Microb. Ecol. 74: 85–94. dx.doi.org/10.3354/ame01730
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2014
Bale, N.; Villanueva, L.; Fan, H.; Hopmans, E.C.; Schouten, S.; Sinninghe Damsté, J.S.; Stal, L.J. (2014). Occurrence and activity of anammox bacteria in surface sediments of the southern North Sea. FEMS Microbiol. Ecol. 89(1): 99–110. hdl.handle.net/10.1111/1574-6941.12338Bale, N.J. (2014). Cruise report HCC cruise: R/V Pelagia 64PE393, 26th August – 21st September 2014 . NIOZ: Texel. 77 pp.Heinzelmann, S.M.; Bale, N.J.; Hopmans, E.C.; Sinninghe Damsté, J.S.; Schouten, S.; van der Meer, M.T.J. (2014). Critical Assessment of Glyco- and Phospholipid Separation by Using Silica Chromatography. Appl. Environ. Microbiol. 80(1): 360-365. dx.doi.org/10.1128/AEM.02817-13Lipsewers, Y.A.; Bale, N.J.; Hopmans, E.C.; Schouten, S.; Sinninghe Damsté, J.S.; Villanueva, L. (2014). Seasonality and depth distribution of the abundance and activity of ammonia oxidizing microorganisms in marine coastal sediments (North Sea). Front. Microbiol. 5: 471 1-12. dx.doi.org/10.3389/fmicb.2014.00472Maat, D.S.; Bale, N.J.; Hopmans, E.C.; Baudoux, A.C.; Sinninghe Damsté, J.S.; Schouten, S.; Brussaard, C.P.D. (2014). Acquisition of intact polar lipids from the prymnesiophyte Phaeocystis globosa by its lytic virus PgV-07T. Biogeosciences 11(1): 185-194. dx.doi.org/10.5194/bg-11-185-2014Villanueva, L.; Hopmans, E.C.; Bale, N.; Schouten, S.; Sinninghe Damsté, J.S. (2014). Diversity and distribution of a key sulpholipid biosynthetic gene in marine microbial assemblages. Environ. Microbiol. 16(3): 774-787. dx.doi.org/10.1111/1462-2920.12202
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2013
Bale, N.J.; Hopmans, E.C.; Schouten, S.; Sinninghe Damsté, J.S. (2013). Different seasonality of pelagic and benthic Thaumarchaeota in the North Sea. Biogeosciences 10: 7195–7206. hdl.handle.net/10.5194/bg-10-7195-2013
Linked projects
