Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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Ionic interaction and liquid absorption by wood in lignocellulose inorganic mineral binder composites
Doudart de la Grée, G.C.H. ; Caprai, V. ; Dam, J.E.G. van; As, H. van; Brouwers, H.J.H. ; Yu, Q.L. - \ 2019
Journal of Cleaner Production 206 (2019). - ISSN 0959-6526 - p. 808 - 818.
Alkali activated binder - Ionic behaviour - Lignocellulose - Moisture content - NMR - Reaction kinetics

This study investigates the suitability of alkali activated binders to replace Portland cement for lignocellulosic mineral-binder composite, aiming to lower the CO2 footprint. The effects of wood composition on the reaction kinetics of the binders and the formation of the reaction products are studied using isothermal calorimetry and ion chromatography. The ionic behaviour analysis of Ca2+ and Na+ ions in the binders shows that in presence of wood, a neutralisation of OH ions and reduction of Ca2+ and Na+ ions during the first 24 h of curing take place, which alters the formation of C-A-S-H and N-A-S-H gels and influences the final composite performance. Moreover, the position of water absorbed by wood with different moisture levels is investigated by using T2 relaxometry Time Domain (TD) NMR to understand the required water amount for the binder reaction as well as the liquid uptake of the wood and occurring ion migration. The results show that a hybrid binder consisting of 70% alkali activated material and 30% cement applied without NaOH pre-treatment results in a composite with excellent mechanical performances and reduced environmental impacts of 61.5% compared to a pure cement system.

Ethyl tert-butyl ether (EtBE) degradation by an algal-bacterial culture obtained from contaminated groundwater
Waals, Marcelle J. van der; Plugge, Caroline ; Meima-Franke, Marion ; Waard, Pieter de; Bodelier, Paul L.E. ; Smidt, Hauke ; Gerritse, Jan - \ 2019
Water Research 148 (2019). - ISSN 0043-1354 - p. 314 - 323.
C SIP - Algal-bacterial culture - Ethanol - Micro-oxic EtBE degradation - NMR - TBA

EtBE is a fuel oxygenate that is synthesized from (bio)ethanol and fossil-based isobutylene, and replaces the fossil-based MtBE. Biodegradation of EtBE to harmless metabolites or end products can reduce the environmental and human health risks after accidental release. In this study, an algal-bacterial culture enriched from contaminated groundwater was used to (i) assess the potential for EtBE degradation, (ii) resolve the EtBE degradation pathway and (iii) characterize the phylogenetic composition of the bacterial community involved in EtBE degradation in contaminated groundwater. In an unamended microcosm, algal growth was observed after eight weeks when exposed to a day-night light cycle. In the fed-batch reactor, oxygen produced by the algae Scenedesmus and Chlorella was used by bacteria to degrade 50 μM EtBE replenishments with a cumulative total of 1250 μM in a day/night cycle (650 lux), over a period of 913 days. The microbial community in the fed-batch reactor degraded EtBE, using a P450 monooxygenase and 2-hydroxyisobutyryl-CoA mutase, to tert-butyl alcohol (TBA), ethanol and CO2 as determined using 13C nuclear magnetic resonance spectroscopy (NMR) and gas chromatography. Stable isotope probing (SIP) with 13C6 labeled EtBE in a fed-batch vessel showed no significant difference in community profiles of the 13C and 12C enriched DNA fractions, with representatives of the families Halomonadaceae, Shewanellaceae, Rhodocyclaceae, Oxalobacteraceae, Comamonadaceae, Sphingomonadaceae, Hyphomicrobiaceae, Candidatus Moranbacteria, Omnitrophica, Anaerolineaceae, Nocardiaceae, and Blastocatellaceae. This is the first study describing micro-oxic degradation of EtBE by an algal-bacterial culture. This algal-bacterial culture has advantages compared with conventional aerobic treatments: (i) a lower risk of EtBE evaporation and (ii) no need for external oxygen supply in the presence of light. This study provides novel leads towards future possibilities to implement algal-bacterial consortia in field-scale groundwater or wastewater treatment.

Nutrimetabolomics: An Integrative Action for Metabolomic Analyses in Human Nutritional Studies
Ulaszewska, Marynka M. ; Weinert, Christoph H. ; Trimigno, Alessia ; Portmann, Reto ; Andres Lacueva, Cristina ; Badertscher, René ; Brennan, Lorraine ; Brunius, Carl ; Bub, Achim ; Capozzi, Francesco ; Cialiè Rosso, Marta ; Cordero, Chiara E. ; Daniel, Hannelore ; Durand, Stéphanie ; Egert, Bjoern ; Ferrario, Paola G. ; Feskens, Edith J.M. ; Franceschi, Pietro ; Garcia-Aloy, Mar ; Giacomoni, Franck ; Giesbertz, Pieter ; González-Domínguez, Raúl ; Hanhineva, Kati ; Hemeryck, Lieselot Y. ; Kopka, Joachim ; Kulling, Sabine E. ; Llorach, Rafael ; Manach, Claudine ; Mattivi, Fulvio ; Migné, Carole ; Münger, Linda H. ; Ott, Beate ; Picone, Gianfranco ; Pimentel, Grégory ; Pujos-Guillot, Estelle ; Riccadonna, Samantha ; Rist, Manuela J. ; Rombouts, Caroline ; Rubert, Josep ; Skurk, Thomas ; Sri Harsha, Pedapati S.C. ; Meulebroek, Lieven Van; Vanhaecke, Lynn ; Vázquez-Fresno, Rosa ; Wishart, David ; Vergères, Guy - \ 2018
Molecular Nutrition & Food Research (2018). - ISSN 1613-4125
GC–MS - LC–MS - metabolomics - NMR - nutrition
The life sciences are currently being transformed by an unprecedented wave of developments in molecular analysis, which include important advances in instrumental analysis as well as biocomputing. In light of the central role played by metabolism in nutrition, metabolomics is rapidly being established as a key analytical tool in human nutritional studies. Consequently, an increasing number of nutritionists integrate metabolomics into their study designs. Within this dynamic landscape, the potential of nutritional metabolomics (nutrimetabolomics) to be translated into a science, which can impact on health policies, still needs to be realized. A key element to reach this goal is the ability of the research community to join, to collectively make the best use of the potential offered by nutritional metabolomics. This article, therefore, provides a methodological description of nutritional metabolomics that reflects on the state-of-the-art techniques used in the laboratories of the Food Biomarker Alliance (funded by the European Joint Programming Initiative “A Healthy Diet for a Healthy Life” (JPI HDHL)) as well as points of reflections to harmonize this field. It is not intended to be exhaustive but rather to present a pragmatic guidance on metabolomic methodologies, providing readers with useful “tips and tricks” along the analytical workflow.
Zeapyranolactone − A novel strigolactone from maize
Charnikhova, Tatsiana V. ; Gaus, Katharina ; Lumbroso, Alexandre ; Sanders, Mark ; Vincken, Jean Paul ; Mesmaeker, Alain De; Ruyter-Spira, Carolien P. ; Screpanti, Claudio ; Bouwmeester, Harro J. - \ 2018
Phytochemistry letters 24 (2018). - ISSN 1874-3900 - p. 172 - 178.
Maize (Zea mays) - NMR - Prep-HPLC–MS - Strigolactones - Zeapyranolactone
The structure of a new strigolactone present in the root exudate and root extract of maize hybrid cv NK Falkone plants was elucidated and characterized as zeapyranolactone: Methyl.(E)-3-((4-methyl-5-oxo-2,5-dihydrofuran-2-yl)oxy)-2-(4,4,5-trimethyl-2-oxo-2,3,4,6,7,7a-hexahydrocyclopenta[b]pyran-7-yl)acrylate. Unlike any other strigolactone published so far, it contains a 4,4-dimethyltetrahydropyran-2-one as A ring. The impact of the elucidation of this structure on the earlier postulated biosynthetic pathway of another maize strigolactone, zealactone, is discussed.
Age and Sex Effects on Plasma Metabolite Association Networks in Healthy Subjects
Vignoli, Alessia ; Tenori, Leonardo ; Luchinat, Claudio ; Saccenti, Edoardo - \ 2018
Journal of Proteome Research 17 (2018)1. - ISSN 1535-3893 - p. 97 - 107.
differential network analysis - metabolism - metabolomics - network inference - NMR
In the era of precision medicine, the analysis of simple information like sex and age can increase the potential to better diagnose and treat conditions that occur more frequently in one of the two sexes, present sex-specific symptoms and outcomes, or are characteristic of a specific age group. We present here a study of the association networks constructed from an array of 22 plasma metabolites measured on a cohort of 844 healthy blood donors. Through differential network analysis we show that specific association networks can be associated with sex and age: Different connectivity patterns were observed, suggesting sex-related variability in several metabolic pathways (branched-chain amino acids, ketone bodies, and propanoate metabolism). Reduction in metabolite hub connectivity was also found to be associated with age in both sex groups. Network analysis was complemented with standard univariate and multivariate statistical analysis that revealed age- and sex-specific metabolic signatures. Our results demonstrate that the characterization of metabolite-metabolite association networks is a promising and powerful tool to investigate the human phenotype at a molecular level.
Effect of theobromine consumption on serum lipoprotein profiles in apparently healthy humans with low HDL-cholesterol concentrations
Jacobs, Doris M. ; Smolders, Lotte ; Lin, Yuguang ; Roo, Niels de; Trautwein, Elke A. ; Duynhoven, John van; Mensink, Ronald P. ; Plat, Jogchum ; Mihaleva, Velitchka V. - \ 2017
Frontiers in Molecular Biosciences 4 (2017)AUG. - ISSN 2296-889X
HDL - Lipoprotein - NMR - PLS model - Theobromine
Scope: Theobromine is a major active compound in cocoa with allegedly beneficial effect on high-density-lipoprotein-cholesterol (HDL-CH). We have investigated the effect of theobromine (TB) consumption on the concentrations of triglyceride (TG) and cholesterol (CH) in various lipoprotein (LP) subclasses. Methods: In a randomized, double-blind, placebo-controlled, cross-over study, 44 apparently healthy women and men (age: 60 ± 6 years, BMI: 29 ± 3 kg/m2) with low baseline HDL-CH concentrations consumed a drink supplemented with 500 mg/d theobromine for 4 weeks. TG and CH concentrations in 15 LP subclasses were predicted from diffusion-edited 1H NMR spectra of fasting serum. Results: The LP phenotype of the subjects was characterized by low CH concentrations in the large HDL particles and high TG concentrations in large VLDL and chylomicron (CM) particles, which clearly differed from a LP phenotype of subjects with normal HDL-CH. TB only reduced CH concentrations in the LDL particles by 3.64 and 6.79%, but had no effect on TG and CH in any of the HDL, VLDL and CM subclasses. Conclusion: TB was not effective on HDL-CH in subjects with a LP phenotype characterized by low HDL-CH and high TG in VLDL.
Zealactones. Novel natural strigolactones from maize
Charnikhova, Tatsiana V. ; Gaus, Katharina ; Lumbroso, Alexandre ; Sanders, Mark ; Vincken, Jean Paul ; Mesmaeker, Alain de; Ruyter-Spira, Carolien P. ; Screpanti, Claudio ; Bouwmeester, Harro J. - \ 2017
Phytochemistry 137 (2017). - ISSN 0031-9422 - p. 123 - 131.
Maize (Zea mays) - NMR - Prep-HPLC-MS - Seed germination - Striga hermonthica (Orobanchaceae) - Strigolactones - UHPLC-MS-MS - Zealactone

In the root exudate and root extracts of maize hybrid cv NK Falkone seven putative strigolactones were detected using UPLC-TQ-MS-MS. All seven compounds displayed MS-MS-fragmentation common for strigolactones and particularly the presence of a fragment of m/z 97 Da, which may indicate the presence of the so-called D-ring, suggests they are strigolactones. The levels of all these putative strigolactones increased upon phosphate starvation and decreased upon fluridone (carotenoid biosynthesis inhibitor) treatment, both of which are a common response for strigolactones. All seven compounds were subsequently isolated with prep-HPLC-MS. They all exhibited Striga hermonthica seed germination inducing activity just as the synthetic strigolactone analog GR24. The structure of two of the seven compounds was elucidated by NMR spectroscopy as: methyl (2E,. 3E)-4-(3,. 3-dimethyl-5-oxo-2-(prop-1-en-2-yl)tetrahydrofuran-2-yl)-2-(((4-methyl-5-oxo-2,. 5-dihydrofuran-2-yl)oxy)methylene)but-3-enoate (two diastereomers 1a and 1b). Strigolactones (1a/b) are closely related to the methyl ester of carlactonoic acid (MeCLA) and heliolactone. However, they contain a unique 4,4-dimethyltetrahydrofuran-2-one motif as the "A-ring" instead of the classical (di)methylcyclohexene. Because these compounds were isolated from maize (Zea mays) we called them "zealactone 1a and 1b". The implications of this discovery for our view on strigolactones and their biosynthesis are discussed.

Impact of Compost Application during 5 Years on Crop Production, Soil Microbial Activity, Carbon Fraction, and Humification Process
Jindo, K. ; Chocano, C. ; Melgares de Aguilar, J. ; González, D. ; Hernandez, T. ; García, C. - \ 2016
Communications in Soil Science and Plant Analysis 47 (2016)16. - ISSN 0010-3624 - p. 1907 - 1919.
Compost - FT-IR - humic acid - NMR - organic farming

Compost amendment is considered as a practical tool to increase the soil organic matter (SOM), which contributes to agricultural sustainability. The objective of the present work was to evaluate the impacts of organic soil management over 5 years on orchard prune production (Prunus salicina), microbial activity, soil carbon (C) fraction, and stabilization degrees of soil humification. Plot experiment was designed with two different soil managements: i) for minimizing anthropogenic disturbances, only mulching of orchard residues derived from prune tree plot area was applied to soil surface (S + V); and ii) the amendment of composted manure was annually practiced in addition to the utilization of orchard residues inside the plot area (S + V + C). After 5 years, the soil with the continuous compost application (S + V + C) showed higher productivity of Prunus salicina (21.4%), greater fruit diameter (7.8%), and heavier fruit weight (22.4%) than the soil without compost application (S + V). Nutrient content in foliar analysis showed no difference between the two treatments (S + V and S + V + C). By contrast, the amended soil by compost (S + V + C) increased the SOM and water-soluble C fraction in parallel with the increase of microbial parameters (microbial biomass C, adenosine triphosphate (ATP), basal respiration, and dehydrogenase). Analyzing soil humic acid character by chemical spectra techniques of Fourier-transform infrared (FT-IR) spectra and 13C nuclear magnetic resonance (13C-NMR), gradual reformation of a more stabilized structure was shown in both soils (S + V and S + V + C), due to the selective biodegradation and humification process after the amendments over 5 years. Especially, in the soil treated with compost application (S + V + C), the increase of functional C groups (aromatic and carboxylic groups), which reinforce the recalcitrant character of soil humified fraction, was clearly observed. The continuous application of composted manure for the duration of 5 years improved the orchard soil fertility as well as productivity. Abbreviations: ATP, adenosine triphosphate; CPMAS, cross-polarization magic angle spinning; EC, electrical conductivity; FT-IR, Fourier-transform infrared; HA, humic acid; HS, humic substance; INTF, iodonitrotetrazolium formazan; K, Potassium; LSD, least significant differences, N, nitrogen; NMR, nuclear magnetic resonance; O, oxygen; OM, organic matter; MBC, microbial biomass C; P, phosphorous; SD, standard deviation; SE, standard error; SOM, soil organic matter; TOC, total organic carbon; WSC, water-soluble C; WS-Ch, water-soluble carbohydrate

Assessment of dietary exposure and effect in humans : The role of NMR
Duynhoven, John P.M. Van; Jacobs, Doris M. - \ 2016
Progress in Nuclear Magnetic Resonance Spectroscopy 96 (2016). - ISSN 0079-6565 - p. 58 - 72.
Dietary effect - Dietary exposure - Metabolite identification - Metabolomics - NMR

In human nutritional science progress has always depended strongly on analytical measurements for establishing relationships between diet and health. This field has undergone significant changes as a result of the development of NMR and mass spectrometry methods for large scale detection, identification and quantification of metabolites in body fluids. This has allowed systematic studies of the metabolic fingerprints that biological processes leave behind, and has become the research field of metabolomics. As a metabolic profiling technique, NMR is at its best when its unbiased nature, linearity and reproducibility are exploited in well-controlled nutritional intervention and cross-sectional population screening studies. Although its sensitivity is less good than that of mass spectrometry, NMR has maintained a strong position in metabolomics through implementation of standardisation protocols, hyphenation with mass spectrometry and chromatographic techniques, accurate quantification and spectral deconvolution approaches, and high-throughput automation. Thus, NMR-based metabolomics has contributed uniquely to new insights into dietary exposure, in particular by unravelling the metabolic fates of phytochemicals and the discovery of dietary intake markers. NMR profiling has also contributed to the understanding of the subtle effects of diet on central metabolism and lipoprotein metabolism. In order to hold its ground in nutritional metabolomics, NMR will need to step up its performance in sensitivity and resolution; the most promising routes forward are the analytical use of dynamic nuclear polarisation and developments in microcoil construction and automated fractionation.

Poly(hydroxy urethane)s based on renewable diglycerol dicarbonate
Velthoven, Juliën L.J. van; Gootjes, Linda ; Es, Daan S. van; Noordover, Bart A.J. ; Meuldijk, Jan - \ 2015
European Polymer Journal 70 (2015). - ISSN 0014-3057 - p. 125 - 135.
Biobased - Diglycerol dicarbonate - Isocyanate-free - NMR - Poly(hydroxy urethane) - Thermal properties

Abstract In this paper, we present a series of amorphous non-isocyanate poly(hydroxy urethane)s (PHU) synthesized from diglycerol dicarbonate in bulk conditions at mild temperatures, without using a catalyst. Diglycerol dicarbonate has been synthesized from diglycerol and dimethyl carbonate and was subsequently reacted with various diamines to form PHUs. These fully bio-based PHUs were amorphous and displayed a broad range of Tg values i.e. from -7 to 66 °C. 1D and 2D NMR techniques were used to determine the ratio between primary and secondary hydroxyl groups formed along the PHU backbone, which was found to be 31:69 for all compositions. The number-average molecular weights were calculated from NMR data and range from 4100 to 9400 g/mol. In FTIR spectra, residual cyclic carbonate groups were observed, which is in agreement with the loss of diamine as detected by NMR. TGA analysis indicated that the polymers are stable up to 200 °C. The polymers synthesized are expected to perform well in e.g. coating applications, given their molecular and thermal properties as well as the abundance of reactive hydroxyl functionalities present along the PHU backbone, which can be used for curing purposes and/or further functionalization.

Taste detection of the non-volatile isothiocyanate moringin results in deterrence to glucosinolate-adapted insect larvae
Müller, Caroline ; Loon, Joop Van; Ruschioni, Sara ; Nicola, Gina Rosalinda De; Olsen, Carl Erik ; Iori, Renato ; Agerbirk, Niels - \ 2015
Phytochemistry 118 (2015). - ISSN 0031-9422 - p. 139 - 148.
Brassicales - Deterrent - Glucosinolate - HPLCMS/MS - Isothiocyanate - Neuron - NMR - Sensory physiology - Specialist herbivores - Stimulant - Taste

Isothiocyanates (ITCs), released from Brassicales plants after hydrolysis of glucosinolates, are known for their negative effects on herbivores but mechanisms have been elusive. The ITCs are initially present in dissolved form at the site of herbivore feeding, but volatile ITCs may subsequently enter the gas phase and all ITCs may react with matrix components. Deterrence to herbivores resulting from topically applied volatile ITCs in artificial feeding assays may hence lead to ambiguous conclusions. In the present study, the non-volatile ITC moringin (4-(α-l-rhamnopyranosyloxy)benzyl ITC) and its glucosinolate precursor glucomoringin were examined for effects on behaviour and taste physiology of specialist insect herbivores of Brassicales. In feeding bioassays, glucomoringin was not deterrent to larvae of Pieris napi (Lepidoptera: Pieridae) and Athalia rosae (Hymenoptera: Tenthredinidae), which are adapted to glucosinolates. Glucomoringin stimulated feeding of larvae of the related Pieris brassicae (Lepidoptera: Pieridae) and also elicited electrophysiological activity from a glucosinolate-sensitive gustatory neuron in the lateral maxillary taste sensilla. In contrast, the ITC moringin was deterrent to P. napi and P. brassicae at high levels and to A. rosae at both high and low levels when topically applied to cabbage leaf discs (either 12, 120 or 1200 nmol moringin per leaf disc of 1 cm diameter). Survival of A. rosae was also significantly reduced when larvae were kept on leaves treated with moringin for several days. Furthermore, moringin elicited electrophysiological activity in a deterrent-sensitive neuron in the medial maxillary taste sensillum of P. brassicae, providing a sensory mechanism for the deterrence and the first known ITC taste response of an insect. In simulated feeding assays, recovery of moringin was high, in accordance with its non-volatile nature. Our results demonstrate taste-mediated deterrence of a non-volatile, natural ITC to glucosinolate-adapted insects.

Application of 1D 1H NMR for fast non-targeted screening and compositional analysis of steroid cocktails and veterinary drug formulations administered to livestock
Lommen, A. ; Schilt, R. ; Weseman, J. ; Roos, A.H. ; Velde, J.W. van; Nielen, M.W.F. - \ 2002
Journal of pharmaceutical and biomedical analysis 28 (2002)1. - ISSN 0731-7085 - p. 87 - 96.
NMR - screening - steroid - anabolic - veterinary drug
Partially folded conformation of the (30-51) intermediate in the disulphide folding pathway of bovine pancreatic trypsin inhibitor : 1H and 15N resonance assignments and determination of backbone dynamics from 15N relaxation measurements
Mierlo, Carlo P.M. van; Darby, Nigel J. ; Keeler, James ; Neuhaus, David ; Creighton, Thomas E. - \ 1993
Journal of Molecular Biology 229 (1993)4. - ISSN 0022-2836 - p. 1125 - 1146.
Bovine pancreatic trypsin inhibitor (BPTI) - Disulphide bonds - Folding intermediate - NMR - Protein folding

An analogue of the important folding intermediate of BPTI with only the disulphide bond between Cys30 and Cys51 has been characterized by 1H and 15N NMR techniques. In particular, the dynamics of the polypeptide backbone were characterized using (1H)-15N NOE and 15N T1 and T2 relaxation data. The intermediate is partially folded, with part of the polypeptide chain stably folded and the remainder flexible or unfolded. The folded portion consists of the major elements of native-like secondary structure interacting through the hydrophobic core of the molecule. The 15N relaxation data show that the N-terminal 15 residues are very flexible, and the (1H,1H) NOESY data show that these residues have no NOE interactions with the remainder of the molecule. The segment of residues 37 to 41 is also flexible. These observations explain why during folding this intermediate most readily forms any of the possible disulphide bonds between Cys5, Cys14 and Cys38, including the non-native 5-14 and 5-38 bonds. The native-like folded portion of the molecule limits the possible disulphide bonds that can be formed to those in the remainder of the polypeptide chain. Also, forming the non-native disulphide bonds need not involve any disruption of that folded structure, as the Cys residues involved are in flexible regions of the molecule.

Local structure due to an aromatic-amide interaction observed by 1H-nuclear magnetic resonancespectroscopy in peptides related to the N terminus of bovine pancreatic trypsin inhibitor
Kemmink, Johan ; Mierlo, Carlo P.M. van; Scheek, Ruud M. ; Creighton, Thomas E. - \ 1993
Journal of Molecular Biology 230 (1993)1. - ISSN 0022-2836 - p. 312 - 322.
Aromatic hydrogen bonds - Aromatic-amide interaction - Bovine pancreatic trypsin inhibitor (BPTI) - NMR - Peptide conformation

A synthetic peptide corresponding to the 15 N-terminal residues of bovine pancreatic trypsin inhibitor, with serine replacing the two cysteine residues, has been characterized by 1H-nuclear magnetic resonance spectroscopy. This peptide has a very disordered conformation that is essentially the same when it is part of the analogue of the (30-51) one-disulphide intermediate in folding. This confirms the conclusion of a previous paper, that the (30-51) intermediate is partially folded, with the N-terminal segment disordered. Local elements of non-randomconformation were observed in the peptide. Especially prominent was an apparently electrostaticinteraction between the face of the aromatic ringof Tyr10 and the amide group of Gly12, which caused the latter to have a very anomalous chemicalshift. A similar interaction was observed in shorter peptides, especially in tetrapeptides with the sequences Tyr/Phe-X-Gly-Y. The local nature of this interaction indicates that it should be a general feature in peptides and in unfolded proteins with such a sequence.

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