Laura Villanueva gave her inaugural lecture 'Ocean’s hidden heroes: Adaptation and evolution of marine microorganisms' on 14 November 2024, at Utrecht University.
The “skin” of microorganisms reflect their environment
Microbiologist Laura Villanueva studies the membranes that surround microbes. ‘A microorganism’s membrane is effectively its skin. Just like our skin, the membrane responds strongly to the environment. Our skin becomes darker if more sunlight falls on it or shivers if it is cold. Similarly, changes also take place in the membranes of microorganisms. These can tell you something about the climate under which the organism is living or has lived.’
‘In particular, the possibility to derive conditions from the past based on the composition of a membrane offers many interesting possibilities. By searching for fossils of membranes in seafloors – the lipid molecules from these membranes can remain intact for millions of years – we can learn what the sea temperature was in a certain period. However, to do that we first need to investigate “modern” species to find out how their composition changes when allowed to grow at different temperatures. Ultimately, this research could contribute to understanding the earth’s climate in the past and therefore to prognoses for the climate of the future.’
Extremists
From an evolutionary viewpoint, I am particularly interested in the “archaea”, more commonly known as ancient bacteria. This is a separate domain of unicellular organisms that can survive under extreme conditions. By searching for archaea that can live at considerable depth without oxygen and under extreme pressure, or under extreme temperatures in the vicinity of hot water springs, I also hope to learn what that does to the composition of their membranes.’
‘The study of membranes also has particularly practical applications. Some medicines can only be delivered to the right location in the body if the active substances are packaged in the right membrane. So besides understanding the climate from the past and the present, membranes can also teach us something about how we can improve medicines.’
Molecular Geomicrobiology is the molecular level understanding of microbial activities both in past and present ecosystems. I combine molecular microbiology & organic biogeochemistry techniques to determine:
Biological sources of lipid biomarkers
Evolutionary acquisition of lipid biomarkers
Regulation of microbial lipid synthesis
Abundance, activity & distribution of key players of carbon, nitrogen and sulfur cycles in marine systems
Education & research experience
2023: Head of the Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research.
2020: Associate Professor (ius promovendi), Department of Earth Sciences, Faculty of Geosciences, Utrecht University
2020: Research Leader at the Department of Marine Microbiology and Biogeochemistry, NIOZ.
2013-2019: Senior Research Scientist (tenured) at the Department of Marine Microbiology and Biogeochemistry, NIOZ.
Topic: Molecular evolution of lipid synthetic pathways. Anaerobic microorganisms involved in carbon, nitrogen and sulfur cycles. Metagenomics and lipidomics.
2009-2013: Tenure-track Research Scientist (Geomicrobiology) at the Department of Marine Organic Biogeochemistry, NIOZ.
Topic: Microbial ecology of microorganisms involved in the nitrogen cycle. Lipid biomarkers marine Thaumarchaeota.
2007-2009: Postdoctoral fellow at the Center for Systems Biology at Harvard University (MA, USA).
Topic: Evolution of bacteriophage-host specificity.
2006-2007: Postdoctoral fellow at the Department of Microbiology in the University of Massachusetts (Amherst, MA, USA).
Topic: Anaerobic culturing and gene expression in Desulfovibrio
1/2002–12/2005: PhD in Microbial Ecology in the Department of Microbiology, Faculty of Biology, University of Barcelona (Spain).
Title: Ecophysiological and molecular characterization of estuarine microbial mats. Diploma of European Mention.
Research interests
Lipid biosynthetic pathways
My research is focused on lipid biomarkers of certain organisms either because they are markers of the presence of a specific group (e.g. ladderane lipids of anammox bacteria), physiological condition (e.g. ornithine lipids, thought to be formed under phosphate limitation), or mostly because they have been seen to correlate to growth temperature and thus used to estimate paleotemperature (e.g. long chain alkenones, GDGTs, and long chain diols involved in the organic paleotemperature proxies UK37, TEX86 and LDI).
In order to improve the predictive nature of lipid biomarkers used for microbial ecology and in paleotemperature proxies it is essential to determine the following: •Their biological source/s, as well as seasonality and spatial distribution of the source/s. •How changes in physicochemical conditions influence the abundance and distribution of these biomarkers •How and when these biomarkers have been acquired through evolution and how these capacity has been spread among different biological taxa
For doing so, I combine lipid analysis with molecular techniques based on: •Analyzing lipid synthetic pathways: evolution and prediction of gene function •Targeting phylogenetic, metabolic and lipid biosynthetic genes as markers for the presence of lipid biomarker producers. •Estimating which physicochemical conditions that induce changes in the synthesis of lipid biomarkers.
Thaumarchaeota diversity and ecophysiology
Members of the Thaumarchaeota phylum have been found to be ubiquitous in marine, freshwater, soils (and others) environments. So far it has been assumed that all thaumarchaeota are chemolithoautotrophs and ammonia oxidizers based on the presence of a unique carbon fixation pathway and the gene coding for ammonia monooxygenase (amoA gene). These physiological characteristics, as well as the relative high abundance of this group in some environments, suggest an important role of Thaumarchaeota in the carbon and nitrogen cycles. In addition, it has been observed that all cultured representatives of the Thaumarchaeota uniquely synthesize the glycerol dialkyl glycerol tetraether (GDGT) crenarchaeol (with 4 cyclopentane and a cyclohexane moiety), which is considered as a biomarker for the presence of this group. The relative abundance of thaumarchaeotal membrane lipids (GDGTs with zero to 4 cyclopentane moieties, GDGT-0 to GDGT-4, and crenarchaeol) has been shown to be correlated with the temperature at which these organisms are growing. Based on this the TEX86 (TetraEther indeX of tetraethers consisting of 86 carbon atoms) paleotemperature proxy was developed and further tested to reconstruct the temperature in past environments.
Anaerobic bacteria involved in Nitrogen and Methane cycles
The re-mineralization of organic matter in anoxic sediments is mainly driven by fermentative microorganisms, sulfate reducers, and methanogens. However, there is a general lack of knowledge on the diversity, abundance and activity of the anaerobic microorganisms involved (directly or indirectly) in organic matter recycling in anoxic sediments. Methanogens (strictly anaerobic archaea) biologically produce methane, a trace greenhouse gas in the earth’s atmosphere the concentration of which has doubled since industrialization. On its way to the atmosphere, methane travels through anaerobic sediments, passing through zones dominated by different regimes of anaerobic respiration before reaching the aerobic sediment or oxic water column. Along this route methane can be oxidized, which significantly decreases/mitigates the effective emission of this greenhouse gas to the atmosphere. However, it is unclear how ecosystems to different physicochemical conditions with respect to methane production, consumption and thus ultimately emissions to the atmosphere.
Our aim is to improve our understanding of the microbial players involved in anaerobic organic matter remineralization and also specifically focus on those involved in the methane cycle. We also want to assess their individual niches, metabolic pathways, environmental significance, interactions, and their response to environmental changes. Ultimately this information will be key to explore their potential use in biotechnology and to design mitigation strategies for greenhouse gas emission.
This research is conducted in the framework of the Soehngen Institute for Anaerobic Microbiology SIAM (Gravitation grant- Zwaartekracht, from the Dutch Ministry of Education, Culture and Science, read more here) in which the Radboud University, Wageningen University, Delft University of Technology, and NIOZ Royal Netherlands Institute for Sea Research participate.
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Ding, S.; von Meijenfeldt, F. A.B.; Bale, N.J.; Sinninghe Damsté, J.S; Villanueva, L. (2024). Production of structurally diverse sphingolipids by anaerobic marine bacteria in the euxinic Black Sea water column. ISME J. 18(1). https://dx.doi.org/10.1093/ismejo/wrae153
Tamby, A.; Sahonero Canavesi, D.; Villanueva, L. (2024). Exploring robustness of hybrid membranes under high hydrostatic pressure and temperature. Front. Microbiol. 15: 1470844. https://dx.doi.org/10.3389/fmicb.2024.1470844
Yadav, S.; Koenen, M.; Bale, N.; Reitsma, W.; Engelmann, J.C.; Stefanova, K.; Sinninghe Damsté, J.S; Villanueva, L. (2024). Organic matter degradation in the deep, sulfidic waters of the Black Sea: insights into the ecophysiology of novel anaerobic bacteria. Microbiome 12(1): 98. https://dx.doi.org/10.1186/s40168-024-01816-x
Hoshino, Y.; Villanueva, L. (2023). Four billion years of microbial terpenome evolution. FEMS Microbiol. Rev. 47(2): 1-39. https://dx.doi.org/10.1093/femsre/fuad008
Pérez Gallego, R.; Bale, N.J.; Sinninghe Damsté, J.S; Villanueva, L. (2023). Developing a genetic approach to target cyanobacterial producers of heterocyte glycolipids in the environment. Front. Microbiol. 14: 1257040. https://dx.doi.org/10.3389/fmicb.2023.1257040
Pérez Gallego, R.; Bale, N.J.; Sinninghe Damsté, J.S; Villanueva, L. (2023). Developing a genetic approach to target cyanobacterial producers of heterocyte glycolipids in the environment. Front. Microbiol. 14: 1257040. https://dx.doi.org/10.3389/fmicb.2023.1257040
Pérez Gallego, R.; Bale, N.J.; Sinninghe Damsté, J.S; Villanueva, L. (2023). Developing a genetic approach to target cyanobacterial producers of heterocyte glycolipids in the environment. Front. Microbiol. 14: 1257040. https://dx.doi.org/10.3389/fmicb.2023.1257040
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
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
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
Suominen, S.; Gomez-Saez, G.V.; Dittmar, T.; Sinninghe Damsté, J.S; Villanueva, L. (2022). Interplay between microbial community composition and chemodiversity of dissolved organic matter throughout the Black Sea water column redox gradient. Limnol. Oceanogr. 67(2): 329-347. https://dx.doi.org/10.1002/lno.11995
van Kemenade, Z.R.; Villanueva, L.; Hopmans, E.C.; Kraal, P.; Witte, H.J.; Sinninghe Damsté, J.S.; Rush, D. (2022). Bacteriohopanetetrol-x: constraining its application as a lipid biomarker for marine anammox using the water column oxygen gradient of the Benguela upwelling system. Biogeosciences 19(1): 201-221. https://dx.doi.org/10.5194/bg-19-201-2022
Villanueva, L.; Coolen, M.J.L. (2022). Contributions of genomics to lipid biomarker research: From paleoclimatology to evolution. Elements 18(2): 87-92. https://dx.doi.org/10.2138/gselements.18.2.87
Baxter, A.J.; van Bree, L.G.J.; Peterse, F.; Hopmans, E.C.; Villanueva, L.; Verschuren, D.; Sinninghe Damste, J.S. (2021). Seasonal and multi-annual variation in the abundance of isoprenoid GDGT membrane lipids and their producers in the water column of a meromictic equatorial crater lake (Lake Chala, East Africa). Quat. Sci. Rev. 273: 107263. https://dx.doi.org/10.1016/j.quascirev.2021.107263
Lattaud, J.; Balzano, S.; van der Meer, M.T.J.; Villanueva, L.; Hopmans, E.C.; Sinninghe Damsté, J.S; Schouten, S. (2021). Sources and seasonality of long-chain diols in a temperate lake (Lake Geneva). Org. Geochem. 156: 104223. https://doi.org/10.1016/j.orggeochem.2021.104223
Suominen, S.; Dombrowski, N.; Sinninghe Damsté, J.S; Villanueva, L. (2021). A diverse uncultivated microbial community is responsible for organic matter degradation in the Black Sea sulphidic zone. Environ. Microbiol. 23(6): 2709-2728. https://dx.doi.org/10.1111/1462-2920.14902
Suominen, S.; Doorenspleet; Sinninghe Damsté, J.S; Villanueva, L. (2021). Microbial community development on model particles in the deep sulfidic waters of the Black Sea. Environ. Microbiol. 23(6): 2729-2746. https://dx.doi.org/10.1111/1462-2920.15024
Suominen, S.; van Vliet, D.M.; Sánchez-Andrea, I.; van der Meer, M.T.J.; Sinninghe Damsté, J.S; Villanueva, L. (2021). Organic matter type defines the composition of active microbial communities originating from anoxic Baltic Sea sediments. Front. Microbiol. 12: 628301. https://doi.org/10.3389/fmicb.2021.628301
Villanueva, L.; von Meijenfeldt, F.A.B.; Westbye, A.B.; Yadav, S.; Hopmans, E.C.; Dutilh, B.E.; Sinninghe Damsté, J.S (2021). Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids. ISME J. 15: 168-182. https://dx.doi.org/10.1038/s41396-020-00772-2
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
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
Carreira, C.; Lønborg, C.; Kühl, M.; Lillebø, A.I.; Sandaa, R.-A.; Villanueva, L.; Cruz, S. (2020). Fungi and viruses as important players in microbial mats. FEMS Microbiol. Ecol. 96(11): fiaa187. https://doi.org/10.1093/femsec/fiaa187
van Bree, L.G.J.; Peterse, F.; Baxter, A.J.; De Crop, W.; van Grinsven, S.; Villanueva, L.; Verschuren, D.; Sinninghe Damsté, J.S (2020). Seasonal variability and sources of in situ brGDGT production in a permanently stratified African crater lake. Biogeosciences 17(21): 5443-5463. https://doi.org/10.5194/bg-17-5443-2020
van Grinsven, S.; Sinninghe Damsté, J.S.; Harrison, J.; Polerecky, L.; Villanueva, L. (2021). Nitrate promotes the transfer of methane‐derived carbon from the methanotroph Methylobacter sp. to the methylotroph Methylotenera sp. in eutrophic lake water. Limnol. Oceanogr. 66(3): 878-891. https://doi.org/10.1002/lno.11648
van Grinsven, S.; Sinninghe Damsté, J.S; Abdala Asbun, A.; Engelmann, J.C.; Harrison, J.; Villanueva, L. (2020). Methane oxidation in anoxic lake water stimulated by nitrate and sulfate addition. Environ. Microbiol. 22(2): 766-782. https://dx.doi.org/10.1111/1462-2920.14886
van Grinsven, S.; Sinninghe Damsté, J.S; Harrison, J.; Villanueva, L. (2020). Impact of electron acceptor availability on methane-influenced microorganisms in an enrichment culture obtained from a stratified lake. Front. Microbiol. 11: article 715. https://dx.doi.org/10.3389/fmicb.2020.00715
van Grinsven, S.; Sinninghe Damsté, J.S; Villanueva, L. (2020). Assessing the effect of humic substances and Fe(III) as potential electron acceptors for anaerobic methane oxidation in a marine anoxic system. Microorganisms 8(9): 1288. https://doi.org/10.3390/microorganisms8091288
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
Balzano, S.; Villanueva, L.; de Bar, M.; Sahonero Canavesi, D.X.; Yildiz, C.; Engelmann, J.C.; Maréchal, E.; Lupette, J.; Sinninghe Damsté, J.S.; Schouten, S. (2019). Biosynthesis of long chain alkyl diols and long chain alkenols in Nannochloropsis spp. (Eustigmatophyceae). Plant Cell Physiol. 60(8): 1666-1682. https://dx.doi.org/10.1093/pcp/pcz078
Besseling, M.A.; Hopmans, E.C.; Koenen, M.; van der Meer, M.T.J.; Vreugdenhil, S.; Schouten, S.; Sinninghe Damsté, J.S; Villanueva, L. (2019). Depth-related differences in archaeal populations impact the isoprenoid tetraether lipid composition of the Mediterranean Sea water column. Org. Geochem. 135: 16-31. https://dx.doi.org/10.1016/j.orggeochem.2019.06.008
Sollai, M.; Villanueva, L.; Hopmans, E.C.; Keil, R.G.; Sinninghe Damsté, J.S. (2019). Archaeal sources of intact membrane lipid biomarkers in the oxygen deficient zone of the eastern tropical South Pacific. Front. Microbiol. 10: 765. https://dx.doi.org/10.3389/fmicb.2019.00765
Sollai, M.; Villanueva, L.; Hopmans, E.C.; Reichart, G.-J.; Sinninghe Damsté, J.S. (2019). A combined lipidomic and 16S rRNA gene amplicon sequencing approach reveals archaeal sources of intact polar lipids in the stratified Black Sea water column. Geobiol. 17(1): 91-109. https://doi.org/10.1111/gbi.12316
van Vliet, D.M.; Palakawong Na Ayudthaya, S.; Diop, S.; Villanueva, L.; Stams, A.J.M.; Sánchez-Andrea, I. (2019). Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from Black Sea sediment. Front. Microbiol. 10: 253. https://dx.doi.org/10.3389/fmicb.2019.00253
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
Sinninghe Damsté, J.S.; Rijpstra, W.I.C.; Foesel, B.U.; Huber, K.J.; Overmann, J.; Nakagawa, S.; Kim, J.J.; Dunfield, P.F.; Dedysh, S.N.; Villanueva, L. (2018). An overview of the occurrence of ether- and ester- linked iso-diabolic acid membrane lipids in microbial cultures of the Acidobacteria: Implications for brGDGT paleoproxies for temperature and pH. Org. Geochem. 124: 63-76. https://doi.org/10.1016/j.orggeochem.2018.07.006
Villanueva, L. (2018). Engineering E. coli to have a hybrid Archaeal/Bacterial membrane. Trends microbiol. (Regul. ed.) 26(7): 559-560. https://dx.doi.org/10.1016/j.tim.2018.05.003
Balzano, S.; Villanueva, L.; de Bar, M.; Sinninghe Damsté, J.S.; Schouten, S. (2017). Impact of culturing conditions on the abundance and composition of long chain alkyl diols in species of the genus Nannochloropsis. Org. Geochem. 108: 9-17. https://dx.doi.org/10.1016/j.orggeochem.2017.02.006
Sinninghe Damsté, J.S.; Rijpstra, W.I.C.; Dedysh, S.N.; Foesel, B.U.; Villanueva, L. (2017). Pheno- and Genotyping of Hopanoid Production in Acidobacteria. Front. Microbiol. 8: 968. https://dx.doi.org/10.3389/fmicb.2017.00968
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
Lipsewers, Y.A.; Hopmans, E.C.; Meysman, F.J.R.; Sinninghe Damsté, J.S.; Villanueva, L. (2016). Abundance and diversity of denitrifying and anammox bacteria in seasonally hypoxic and sulfidic sediments of the saline Lake Grevelingen. Front. Microbiol. 7: 1661. https://dx.doi.org/10.3389/fmicb.2016.01661
Heinzelmann, S.M.; Chivall, D.; M'boule, D.; Sinke-Schoen, D.; Villanueva, L.; Sinninghe Damsté, J.S.; Schouten, S.; van der Meer, M.T.J. (2015). Comparison of the effect of salinity on the D/H ratio of fatty acids of heterotrophic and photoautotrophic microorganisms. FEMS Microbiol. Lett. 362(10). dx.doi.org/10.1093/femsle/fnv065
Heinzelmann, S.M.; Villanueva, L. ; Sinke-Schoen, D.; Sinninghe Damsté, J.S.; Schouten, S.; Van der Meer, M.T.J. (2015). Impact of metabolism and growth phase on the hydrogen isotopic composition of microbial fatty acids. Front. Microbiol. 6: 408. dx.doi.org/10.3389/fmicb.2015.00408
Villanueva, L. ; Schouten, S.; Sinninghe Damsté, J.S. (2015). Depth-related distribution of a key gene of the tetraether lipid biosynthetic pathway in marine Thaumarchaeota. Environ. Microbiol. 17(10): 3527–3539. dx.doi.org/10.1111/1462-2920.12508
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
Schouten, S.; Villanueva, L.; Hopmans, E.C.; van der Meer, M.T.J.; Sinninghe Damsté, J.S. (2014). Are Marine Group II Euryarchaeota significant contributors to tetraether lipids in the ocean? Proc. Natl. Acad. Sci. U.S.A. 111(41): e4285. dx.doi.org/10.1073/pnas.1416176111
Buckles, L.K.; Villanueva, L.; Weijers, J.W.H.; Verschuren, D.; Sinninghe Damsté, J.S. (2013). Linking isoprenoidal GDGT membrane lipid distributions with gene abundances of ammonia-oxidizing Thaumarchaeota and uncultured crenarchaeotal groups in the water column of a tropical lake (Lake Challa, East Africa). Environ. Microbiol. 15(9): 2445-2462. dx.doi.org/10.1111/1462-2920.12118
Schouten, S.; Pitcher, A.; Hopmans, E.C.; Villanueva, L.; van Bleijswijk, J.; Sinninghe Damsté, J.S. (2012). Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone: I. Selective preservation and degradation in the water column and consequences for the TEX86. Geochim. Cosmochim. Acta 98: 228-243. https://dx.doi.org/10.1016/j.gca.2012.05.002