In order to complete a jigsaw puzzle, the first step is to take it all apart. At least, that is what organic geochemist Nicole Bale does. The 'puzzles' are lipids, carbon-based molecules from cell membranes, found in plants, animals or microorganisms. "When we apply pressure, they break up in very specific ways, providing us with detailed information about the individual 'puzzle pieces'. In this way, we can work out the structure of the lipid.”
In particular, Nicole focuses on the lipids of bacteria and archaea (two of the three domains of life). "Compared to the tremendous progress in the genetic study of microorganisms (e.g. using DNA), our knowledge of their membrane lipids is much less. With the newest analytical methods, we are currently learning in much more detail about these molecules and therefore about the organisms themselves.”
“Apart from working out the structure of lipids we also carry out studies into their function. For example, lipids can be found in seawater or sediment, both recent and ancient. We want to know which organisms these lipids belong – or belonged to. That information can also give us clues about the environment around the organisms, such as the temperature or pH.
“Bacteria and other microorganisms are extremely flexible. When the temperature or the acidity of their environment changes, they can adapt their membrane lipids. We would like to better understand what specific adjustments enable them to live at a higher or lower temperature, or a higher or lower pH. Knowing these adjustments may provide us with so-called biomarkers, that can tell us whether a sample was derived from a warmer or a colder environment, or from an acid or alkaline environment. That way we can also gather information about the climate in past times.”Read more +
Tremendous progress has been made in the recent decades 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 are striving 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.
Biomarkers for symbiotic N2 fixing cyanobacteria in marine diatoms.
This line of research focuses on tracing marine symbiotic heterocystous cyanobacteria in present and past marine environments. Hexose-based heterocyte glycolipids (HGs) are established biomarkers for free-living, N-fixing, cyanobacteria. A focus of my work has been developing pentose-based HGs as biomarkers for cyanobacteria-diatom symbioses in the open ocean. The combination of these two types of HG biomarkers has provided 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 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.
The marine nitrogen cycle
In particular, I was involved in 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. 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).
Isoprenoidal GDGTs and GDDs associated with anoxic lacustrine environments. Danica Mitrović, Ellen C. Hopmans, Nicole J. Bale, Nora Richter, Linda A. Amaral-Zettler, Allix J. Baxter, Francien Peterse, Pedro Miguel Raposeiro, Vítor Gonçalves, Ana Cristina Costa, Stefan Schouten. Organic Geochemistry.
Dominance of mixed ether/ester, intact polar membrane lipids in five species of the order Rubrobacterales: Another group of bacteria that ignores the “lipid divide”. Jaap S. Sinninghe Damsté, W. Irene C. Rijpstra, Katharina J. Huber, Luciana Albuquerque, Conceição Egas, Nicole J. Bale. Systematic and Applied Microbiology.
Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation. Su Ding, Jan Henkel, Ellen Hopmans, Nicole Bale, Michel Koenen, Laura Villanueva, and Jaap S. Damste. ISME Communications 2022.
A window into eastern Mediterranean productivity conditions over three Pliocene precession-forced climate cycles. Anna Victoria Cutmore, Nicole Bale, Gert J De Lange, Ivar A Nijenhuis, Lucas Joost Lourens. Earth and Space Science Open Archive
Disentangling the lipid divide: Identification of key enzymes for the biosynthesis of membrane-spanning and ether lipids in Bacteria. Diana X Sahonero-Canavesi, Melvin Siliakus, Alejandro Abdala Asbun, Michel Koenen, FA Bastiaan von Meijenfeldt, Sjef Boeren, Nicole J Bale, Julia C Engelmann, Kerstin Fiege, Lora Strack van Schijndel, Jaap S Sinninghe Damste, Laura Villanueva. Science Advances 2022.
Natranaeroarchaeum sulfidigenes gen. nov., sp. nov., carbohydrate-utilizing sulfur-respiring haloarchaeon from hypersaline soda lakes, a member of a new family Natronoarchaeaceae fam. nov. in the order Halobacteriales. Dimitry Y.Sorokin, Michail Yakimov, Enzo Messina, Alexander Y. Merkel, Michel Koenen, Nicole J.Bale, Jaap S.Sinninghe Damsté. Systematic and Applied Microbiology 2022.
Natronocalculus amylovorans gen. nov., sp. nov., and Natranaeroarchaeum aerophilus sp. nov., dominant culturable amylolytic natronoarchaea from hypersaline soda lakes in southwestern Siberia. Dimitry Y.Sorokin, Alexander G. Elcheninov, Tatjana V. Khizhniak, Michel Koenen, Nicole J. Bale, Jaap S. Sinninghe Damsté, Ilya V. Kublanova. Systematic and Applied Microbiology 2022.
Acetate degradation at low pH by the moderately acidophilic sulfate reducer Acididesulfobacillus acetoxydans gen. nov. sp. nov. Irene Sánchez-Andrea, Charlotte Monique van der Graaf, Bastian Hornung, Nicole J. Bale, Monika Jarzembowska, Diana Z Sousa, W.Irene C. Rijpstra, Jaap Sinninghe Damsté and Alfons J.M. Stams. Frontiers in Microbiology 2022.
Halapricum desulfuricans sp. nov., carbohydrate-utilizing sulfur-respiring haloarchaea from hypersaline lakes. Dimitry Y Sorokin; Michail M. Yakimov; Enzo Messina; Alexander Y. Merkel; Michel Koenen; Nicole J. Bale; Jaap Sinninghe-Damste. International Journal of Systematic and Evolutionary Microbiology 2021.
Changes in the distribution of membrane lipids during growth of Thermotoga maritima at different temperatures: Indications for the potential mechanism of biosynthesis of ether-bound diabolic acid (membrane-spanning) lipids. Diana X Sahonero-Canavesi, Laura Villanueva, Nicole J Bale, Jade Bosviel, Michel Koenen, Ellen C Hopmans and Jaap S Sinninghe Damsté. Applied and Environmental Microbiology 2021.
The physiology and metabolic properties of a novel, low-abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role. Subhash Yadav, Michel Koenen, Nicole Bale, Jaap S. Sinninghe Damsté, and Laura Villanueva. Environmental Microbiology Reports 2021.
Lipidomics of environmental microbial communities. I: Visualization of specific niches using untargeted analysis of high-resolution mass spectrometry data. Nicole J. Bale, Su Ding, Ellen C. Hopmans, Laura Villanueva, Christine Boschman, Milou G.I. Arts, Andreas F. Haas, Stefan Schouten, Jaap S. Sinninghe Damsté. Frontiers in Microbiology 2021.
Lipidomics of environmental microbial communities. II: Characterization using molecular networking and information theory. Su Ding, Nicole J. Bale, Ellen C. Hopmans, Laura Villanueva, Milou G.I. Arts, Stefan Schouten, Jaap S. Sinninghe Damsté. Frontiers in Microbiology 2021.
Natranaerofaba carboxydovora gen. nov., sp. nov., an extremely haloalkaliphilic CO-utilizing acetogen from a hypersaline soda lake representing a novel deep phylogenetic lineage in the class "Natranaerobiia". Dimitry Y. Sorokin, Martijn Diender, Alexander Y. Merkel, Michel Koenen, Nicole J. Bale, Martin Pabst, Jaap S. Sinninghe Damsté, and Diana Z. Sousa. Environmental Microbiology, 2020.
Biosulfidogenesis mediates natural attenuation in acidic mine pit lakes. Charlotte M. van der Graaf, Javier Sánchez-España, Iñaki Yusta, Andrey Ilin, Nicole J. Bale, Sudarshan Shetty, Laura Villanueva, Alfons J. M. Stams, Irene Sánchez-Andrea. Microorganism 2020, 8, 1275.
Pontiella desulfatans gen. nov., sp. nov., and Pontiella sulfatireligans sp. nov., Two Marine Anaerobes of the Pontiellaceae fam. nov. Producing Sulfated Glycosaminoglycan-like Exopolymers. Daan M. van Vliet, Yuemei Lin, Nicole J. Bale, Michel Koenen, Laura Villanueva, Alfons J. M. Stams and Irene Sánchez-Andrea. Microorganisms 2020, 8, 920.
Global temperature calibration of the Long chain Diol Index in marine surface sediments. Marijke W. de Bar, Gabriella Weiss, Caglar Yildiz, Sebastiaan Rampen, Julie Lattaud, Nicole J. Bale, Furu Mienis, Geert-Jan A. Brummer, Hartmut Schulz, Darci Rush , Jung-Hyun Kim, Barbara Donner, Jochen Knies, Andreas Lückge, Jan-Berend W. Stuut, Jaap S. Sinninghe Damsté, Stefan Schouten. Organic Geochemistry.
Diagnostic amide products of amino lipids detected in the microaerophilic bacteria Lutibacter during routine fatty acid analysis using gas chromatography. Nicole J. Bale, Michel Koenen, Yadav Subhash, Ellen C. Hopmans, Laura Villanueva, Jaap S. Sinninghe Damsté, Stefan Schouten. Organic Geochemistry.
Physiological, chemotaxonomic and genomic characterization of two novel piezotolerant bacteria of the family Marinifilaceae isolated from sulfidic waters of the Black Sea. Subhash Yadav, Laura Villanueva, Nicole Bale, Michel Koenen, Ellen C. Hopmans, Jaap S. Sinninghe Damsté. Systematic and Applied Microbiology
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.
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. International Journal of Systematic and Evolutionary Microbiology 69:2662–2673.
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. Nicole J. Bale, W. Irene C. Rijpstra, Igor Y. Oshkin, Svetlana E. Belova, Svetlana N. Dedysh, Jaap S. Sinninghe Damsté. Frontiers in Microbiology. 10:589, 2019.
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.
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
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
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
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
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
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.
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
Participation in European Erasmus programme, Université Montpellier II, France