Royal Netherlands Institute for Sea Research
A A
Royal Netherlands
Institute for Sea Research
Phone number
+31 (0)222 36 9525
Location
Texel
Department
Microbiology & Biogeochemistry (MMB)
Function
Head of Analytical Laboratory
Expertise
  • Organic Geochemistry
  • Marine Biogeochemistry
  • Intact polar lipids
  • Liquid Chromatography Mass Spectrometry

Dr. Nicole Bale

Head of Analytical Laboratory

Molecular jigsaw

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.”

Flexible organisms

“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.”

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Research interests

Microbial lipids

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).

Publications:

2023

A Taxonomically-informed Mass Spectrometry Search Tool for Microbial Metabolomics Data. Simone Zuffa et al. Submitted to Nature Microbiology.

Acetic acid stress response of the acidophilic sulfate reducer Acididesulfobacillus acetoxydans. Egas, Reinier A.; Sahonero-Canavesi, Diana X.; Bale, Nicole; Koenen, Michel; Yildiz, Çağlar; Villanueva, L; Sousa, Diana; Sanchez-Andrea, Irene. Submitted to Environmental Microbiology.

Developing a genetic approach to target cyanobacterial producers of heterocyte glycolipids in the environment. Ruth Pérez Gallego, Nicole J. Bale, Jaap S. Sinninghe Damste, Laura Villanueva. Submitted to Frontiers in Microbiology.

Marine nitrogen cycling dynamics under altering redox conditions: insights from deposition of sapropels S1 and the ambiguous S2 in the Eastern Mediterranean Sea. Zoë van Kemenade, Anna Cutmore, Rick Hennekam, Ellen Hopmans, Marcel van der Meer, Meryem Moijtahid, Frans Jorissen, Nicole Bale, Gert-Jan Reichart, Jaap Sinninghe Damsté, Darci Rush. Geochimica et Cosmochimica Acta.

A window into eastern Mediterranean productivity conditions over three Pliocene precession-forced climate cycles. Anna V. Cutmore, Nicole Bale, Gert J. De Lange, Ivar A. Nijenhuis, Lucas J. Lourens. Paleoceanography and Paleoclimatology.

 

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.

2022

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.

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.

2021

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.

Archaeal Intact Polar Lipids in Polar Waters: A Comparison Between the Amundsen and Scotia Seas.
Charlotte L. Spencer-Jones, Erin L. McClymont, Nicole J. Bale, Ellen C. Hopmans, Stefan Schouten, Juliane Müller, E. Povl Abrahamsen, Claire Allen, Torsten Bickert, Claus-Dieter Hillenbrand, Elaine Mawbey, Victoria Peck, Aleksandra Svalova, and James A. Smith. Biogeosciences, 2021.
 
2020
 

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.

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. 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.

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

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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

https://twitter.com/NicoleBale3

 

Linked news

Thursday 06 April 2023
Lauded microbiologist Jill Banfield visits NIOZ
Earth scientist Professor Jill Banfield of the University of California at Berkeley received the Van Leeuwenhoek Medal yesterday, during the annual meeting of the Royal Dutch Society for Microbiology. This award for influential (micro)biologists has…
Read more
Monday 19 December 2022
Linking fossil climate proxies to living bacteria helps climate predictions
Microbes have skins that react to the environment, much in the same way that our skin sweats when it is hot , or shivers when it is cold outside. Fossilized microbial skins can give us a glimpse of how the climate was in the deep geological past. By…
Read more
Monday 28 November 2022
NWO grant for research project to understand Sargassum inundations in the Caribbean
Climate change or Natural Range Expansion? As of 2011, the Caribbean Sea regularly suffers from washed-up masses of seaweed, called Sargassum, that rot if left to accumulate on beaches and in harbors. As part of an international call, a Dutch-led…
Read more

NIOZ publications

  • 2023
    Cutmore, A.; Bale, N.; de Lange, G.J.; Nijenhuis, I. A.; Lourens, L.J. (2023). A Window Into Eastern Mediterranean Productivity Conditions Over Three Pliocene Precession‐Forced Climate Cycles. Paleoceanography and Paleoclimatology 38(4). https://dx.doi.org/10.1029/2022pa004550
    View complete reference
    Mitrovic, D.; Hopmans, E.C.; Bale, N.J.; Richter, N.; Amaral-Zettler, L.; Baxter, A.J.; Peterse, F; Miguel Raposeiro, P.; Gonçalves, V.; Cristina Costa, A.; Schouten, S. (2023). Isoprenoidal GDGTs and GDDs associated with anoxic lacustrine environments. Org. Geochem. 178: 104582. https://dx.doi.org/10.1016/j.orggeochem.2023.104582
    View complete reference
    Sinninghe Damsté, J.S; Rijpstra, W.I.C.; Huber, K.J.; Albuquerque, L.; Egas, C.; Bale, N. (2023). Dominance of mixed ether/ester, intact polar membrane lipids in five species of the order Rubrobacterales: Another group of bacteria not obeying the “lipid divide”. Syst. Appl. Microbiol. 46(2): 126404. https://dx.doi.org/10.1016/j.syapm.2023.126404
    View complete reference
    van Kemenade, Z.R.; Cutmore, A.; Hennekam, R.; Hopmans, E.C.; van der Meer, M.T.J.; Mojtahid, M.; Jorissen, F.; Bale, N.; Reichart, G.-J.; Sinninghe Damsté, J.S; Rush, D. (2023). Marine nitrogen cycling dynamics under altering redox conditions: Insights from deposition of sapropels S1 and the ambiguous S2 in the Eastern Mediterranean Sea. Geochim. Cosmochim. Acta 354: 197-210. https://dx.doi.org/10.1016/j.gca.2023.06.018
    View complete reference
  • 2022
    Ding, S.; Henkel, J.V.; Hopmans, E.C.; Bale, N.J.; Koenen, M.; Villanueva, L.; Sinninghe Damsté, J.S. (2022). Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation. ISME Commun. 2: 121. https://dx.doi.org/10.1038/s43705-022-00207-3
    View complete reference
    Sahonero Canavesi, D.X.; Siliakus, M.F.; Abdala Asbun, A.; Koenen, M.; von Meijenfeldt, F. A.B.; Boeren, S.; Bale, N.J.; Engelmann, J.C.; Fiege, K.; Strack van Schijndel, L.; Sinninghe Damsté, J.S.; Villanueva, L. (2022). Disentangling the lipid divide: Identification of key enzymes for the biosynthesis of membrane-spanning and ether lipids in bacteria. Science Advances 8(50). https://dx.doi.org/10.1126/sciadv.abq8652
    View complete reference
    Sahonero Canavesi, D.X.; Villanueva, L.; Bale, N.J.; Bosviel, J.; Koenen, M.; Hopmans, E.C.; Sinninghe Damsté, J.S. (2022). 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. Appl. Environ. Microbiol. 88(2). https://dx.doi.org/10.1128/aem.01763-21
    View complete reference
    Sánchez-Andrea, I.; van der Graaf, C.M.; Hornung, B.; Bale, N.J.; Jarzembowska, M.; Sousa, D.Z.; Rijpstra, W.I.C.; Sinninghe Damsté, J.S.; Stams, A.J.M. (2022). Acetate degradation at low pH by the moderately acidophilic sulfate reducer Acididesulfobacillus acetoxydans gen. nov. sp. nov. Front. Microbiol. 13: 816605. https://dx.doi.org/10.3389/fmicb.2022.816605
    View complete reference
    Sorokin, D.Y.; Elcheninov, A.G.; Khizhniak, T.V.; Koenen, M.; Bale, N.J.; Sinninghe Damsté, J.S.; Kublanov, I.V. (2022). Natronocalculus amylovorans gen. nov., sp. nov., and Natranaeroarchaeum aerophilus sp. nov., dominant culturable amylolytic natronoarchaea from hypersaline soda lakes in southwestern Siberia. Syst. Appl. Microbiol. 45(4): 126336. https://dx.doi.org/10.1016/j.syapm.2022.126336
    View complete reference
    Sorokin, D.Y.; Yakimov, M.; Messina, E.; Merkel, A.Y.; Koenen, M.; Bale, N.J.; Sinninghe Damsté, J.S. (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. Syst. Appl. Microbiol. 45(6): 126356. https://dx.doi.org/10.1016/j.syapm.2022.126356
    View complete reference
  • 2021
    Bale, N.J.; Ding, S.; Hopmans, E.C.; Arts, M.G.I.; Villanueva, L.; Boschman, C.; Haas, A.F.; Schouten, S.; Sinninghe Damsté, J.S (2021). Lipidomics of environmental microbial communities. I: visualization of component distributions using untargeted analysis of high-resolution mass spectrometry data. Front. Microbiol. 12. https://dx.doi.org/10.3389/fmicb.2021.659302
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    Ding, S.; Bale, N.J.; Hopmans, E.C.; Villanueva, L.; Arts, M.G.I.; Schouten, S.; Sinninghe Damsté, J.S (2021). Lipidomics of environmental microbial communities. II: characterization using molecular networking and information theory. Front. Microbiol. 12: 659315. https://dx.doi.org/10.3389/fmicb.2021.659315
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    Sorokin, D.Y.; Diender, M.; Merkel, A.Y.; Koenen, M.; Bale, N.J.; Pabst, M.; Sinninghe Damsté, J.S.; Sousa, D.Z. (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’. Environ. Microbiol. 23(7): 3460-3476. https://doi.org/10.1111/1462-2920.15241
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    Sorokin, D.Y.; Yakimov, M.M.; Messina, E.; Merkel, A.Y.; Koenen, M.; Bale, N.J.; Sinninghe Damsté, J.S (2021). Halapricum desulfuricans sp. nov., carbohydrate-utilizing, sulfur-respiring haloarchaea from hypersaline lakes. Syst. Appl. Microbiol. 44(6): 126249. https://dx.doi.org/10.1016/j.syapm.2021.126249
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    Spencer-Jones, C.L.; McClymont, E.L.; Bale, N.J.; Hopmans, E.C.; Schouten, S.; Müller, J.; Abrahamsen, E.Povl; Allen, C.; Bickert, T.; Hillenbrand, C.-D.; Mawbey, E.M.; Peck, V.; Svalova, A.; Smith, J.A. (2021). Archaeal intact polar lipids in polar waters: a comparison between the Amundsen and Scotia seas. Biogeosciences 18(11): 3485-3504. https://dx.doi.org/10.5194/bg-18-3485-2021
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    Yadav, S.; Koenen, M.; Bale, N.; Sinninghe Damsté, J.S.; Villanueva, L. (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. Environmental Microbiology Reports 13(6): 899-910. https://dx.doi.org/10.1111/1758-2229.13012
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  • 2020
    Bale, N.J.; Koenen, M.; Yadav, S.; Hopmans, E.C.; Villanueva, L.; Sinninghe Damsté, J.S.; Schouten, S. (2020). Diagnostic amide products of amino lipids detected in the microaerophilic bacteria Lutibacter during routine fatty acid analysis using gas chromatography. Org. Geochem. 144: 104027. https://doi.org/10.1016/j.orggeochem.2020.104027
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    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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    de Bar, M.W.; Weiss, G.M.; Yildiz, C.; Rampen, S.W.; Lattaud, J.; Bale, N.J.; Mienis, F.; Brummer, G.-J. A.; Schulz, H.; Rush, D.; Kim, J.-H.; Donner, B.; Knies, J.; Lückge, A.; Stuut, J.-B.W.; Sinninghe Damsté, J.S; Schouten, S. (2020). Global temperature calibration of the Long chain Diol Index in marine surface sediments. Org. Geochem. 142: 103983. https://doi.org/10.1016/j.orggeochem.2020.103983
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    van der Graaf, C.M.; Sánchez-España, J.; Yusta, I.; Ilin, A.; Shetty, S.A.; Bale, N.J.; Villanueva, L.; Stams, A.J.M.; Sánchez-Andrea, I. (2020). Biosulfidogenesis mediates natural attenuation in acidic mine pit lakes. Microorganisms 8(9): 1275. https://doi.org/10.3390/microorganisms8091275
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    van der Graaf; Sánchez-España; Yusta; Ilin; Shetty; Bale, N.J.; Villanueva, L.; Stams, A.J.M.; Sánchez-Andrea, I. (2020). Biosulfidogenesis mediates natural attenuation in acidic mine pit lakes. Microorganisms 8(9): 1275. https://doi.org/10.3390/microorganisms8091275
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    van Vliet, D.M.; Lin; Bale, N.J.; Koenen, M.; Villanueva, L.; Stams, A.J.M.; Sánchez-Andrea, I. (2020). Pontiella desulfatans gen. nov., sp. nov., and Pontiella sulfatireligans sp. nov., two marine anaerobes of the Pontiellaceae fam. nov. producing sulfated glycosaminoglycan-like exopolymers. Microorganisms 8(6): 920. https://dx.doi.org/10.3390/microorganisms8060920
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    Yadav, S.; Villanueva, L.; Bale, N.; Koenen, M.; Hopmans, E.C.; Sinninghe Damsté, J.S (2020). Physiological, chemotaxonomic and genomic characterization of two novel piezotolerant bacteria of the family Marinifilaceae isolated from sulfidic waters of the Black Sea. Syst. Appl. Microbiol. 43(5): 126122. https://doi.org/10.1016/j.syapm.2020.126122
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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/g46682.1
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    Bale, 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.01332-19
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    Bale, 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.2019.00589
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    Bale, 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.2019.00377
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    Sorokin, 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.2019.01.001
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    Sorokin, 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.0.003312
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    Sorokin, 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.2018.06.009
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    Bale, 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-15-1229-2018
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    Balzano, 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-15-5951-2018
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    Sorokin, 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.2017.04.010
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    Sollai, 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.10274
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    Heinzelmann, 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. https://dx.doi.org/10.5194/bg-13-5527-2016
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    Maat, 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.2015.01.004
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    Bale, 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/10.1111/1574-6941.12338
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    Bale, N.J. (2014). Cruise report HCC cruise: R/V Pelagia 64PE393, 26th August – 21st September 2014 . NIOZ: Texel. 77 pp.
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    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.02817-13
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    Lipsewers, 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.2014.00472
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    Maat, 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-11-185-2014
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    Villanueva, 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
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UUNIOZ_Harmful Algal Blooms
Supervisor
Laura Villanueva
Funder
Utrecht University
Project duration
1 Jan 2021 - 31 Dec 2025

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