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.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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Author Correction: Climatic controls of decomposition drive the global biogeography of forest-tree symbioses
Steidinger, B.S. ; Crowther, T.W. ; Liang, J. ; Nuland, M.E. Van; Werner, G.D.A. ; Reich, P.B. ; Nabuurs, G.J. ; de-Miguel, S. ; Zhou, M. ; Picard, N. ; Herault, B. ; Zhao, X. ; Zhang, C. ; Routh, D. ; Peay, K.G. ; Abegg, Meinrad ; Adou Yao, C.Y. ; Alberti, Giorgio ; Almeyda Zambrano, Angelica ; Alvarez-Davila, Esteban ; Alvarez-Loayza, Patricia ; Alves, Luciana F. ; Ammer, Christian ; Antón-Fernández, Clara ; Araujo-Murakami, Alejandro ; Arroyo, Luzmila ; Avitabile, Valerio ; Aymard, Gerardo ; Baker, Timothy ; Bałazy, Radomir ; Banki, Olaf ; Barroso, Jorcely ; Bastian, Meredith ; Bastin, Jean Francois ; Birigazzi, Luca ; Birnbaum, Philippe ; Bitariho, Robert ; Boeckx, Pascal ; Bongers, Frans ; Bouriaud, Olivier ; Brancalion, Pedro H.H.S. ; Decuyper, Mathieu ; Hengeveld, Geerten ; Herold, Martin ; Lu, Huicui ; Parren, Marc ; Poorter, Lourens ; Schelhaas, Mart Jan ; Sheil, Douglas ; Zagt, Roderick - \ 2019
Nature 571 (2019)7765. - ISSN 0028-0836

In this Letter, the middle initial of author G. J. Nabuurs was omitted, and he should have been associated with an additional affiliation: ‘Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, The Netherlands’ (now added as affiliation 182). In addition, the following two statements have been added to the Supplementary Acknowledgements. (1): ‘We would particularly like to thank The French NFI for the work of the many field teams and engineers, who have made extraordinary efforts to make forest inventory data publicly available.’ (1): ‘Sergio de Miguel benefited from a Serra- Húnter Fellowship provided by the Generalitat of Catalonia.’ Finally, the second sentence of the Methods section should have cited the French NFI, which provided a national forestry database used in our analysis, to read as follows: ‘The GFBi database consists of individual-based data that we compiled from all the regional and national GFBi forest-inventory datasets, including the French NFI (IGN—French National Forest Inventory, raw data, annual campaigns 2005 and following,, site accessed on 01 January 2015)’. All of these errors have been corrected online.

Microbial production of short and medium chain esters: Enzymes, pathways, and applications
Kruis, Aleksander J. ; Bohnenkamp, Anna C. ; Patinios, Constantinos ; Nuland, Youri M. van; Levisson, Mark ; Mars, Astrid E. ; Berg, Corjan van den; Kengen, Servé W.M. ; Weusthuis, Ruud A. - \ 2019
Biotechnology Advances 37 (2019)7. - ISSN 0734-9750
Alcohol - Alcohol acyltransferase - Bulk chemical - Carboxylic acid - Ester - Metabolic engineering - Microbial synthesis

Sustainable production of bulk chemicals is one of the major challenges in the chemical industry, particularly due to their low market prices. This includes short and medium chain esters, which are used in a wide range of applications, for example fragrance compounds, solvents, lubricants or biofuels. However, these esters are produced mainly through unsustainable, energy intensive processes. Microbial conversion of biomass-derived sugars into esters may provide a sustainable alternative. This review provides a broad overview of natural ester production by microorganisms. The underlying ester-forming enzymatic mechanisms are discussed and compared, with particular focus on alcohol acyltransferases (AATs). This large and versatile group of enzymes condense an alcohol and an acyl-CoA to form esters. Natural production of esters typically cannot compete with existing petrochemical processes. Much effort has therefore been invested in improving in vivo ester production through metabolic engineering. Identification of suitable AATs and efficient alcohol and acyl-CoA supply are critical to the success of such strategies and are reviewed in detail. The review also focusses on the physical properties of short and medium chain esters, which may simplify downstream processing, while limiting the effects of product toxicity. Furthermore, the esters could serve as intermediates for the synthesis of other compounds, such as alcohols, acids or diols. Finally, the perspectives and major challenges of microorganism-derived ester synthesis are presented.

Climatic controls of decomposition drive the global biogeography of forest-tree symbioses
Steidinger, B.S. ; Crowther, T.W. ; Liang, J. ; Nuland, M.E. Van; Werner, G.D.A. ; Reich, P.B. ; Nabuurs, G. ; de-Miguel, S. ; Zhou, M. ; Picard, N. ; Herault, B. ; Zhao, X. ; Zhang, C. ; Routh, D. ; Peay, K.G. ; Herold, M. ; Decuyper, M. ; Avitabile, V. ; DeVries, B.R. ; Hengeveld, G.M. ; Poorter, L. ; Schelhaas, M. ; Bongers, F. - \ 2019
Nature 569 (2019)7756. - ISSN 0028-0836 - p. 404 - 408.
The identity of the dominant root-associated microbial symbionts in a forest determines the ability of trees to access limiting nutrients from atmospheric or soil pools1,2, sequester carbon3,4 and withstand the effects of climate change5,6. Characterizing the global distribution of these symbioses and identifying the factors that control this distribution are thus integral to understanding the present and future functioning of forest ecosystems. Here we generate a spatially explicit global map of the symbiotic status of forests, using a database of over 1.1 million forest inventory plots that collectively contain over 28,000 tree species. Our analyses indicate that climate variables—in particular, climatically controlled variation in the rate of decomposition—are the primary drivers of the global distribution of major symbioses. We estimate that ectomycorrhizal trees, which represent only 2% of all plant species7, constitute approximately 60% of tree stems on Earth. Ectomycorrhizal symbiosis dominates forests in which seasonally cold and dry climates inhibit decomposition, and is the predominant form of symbiosis at high latitudes and elevation. By contrast, arbuscular mycorrhizal trees dominate in aseasonal, warm tropical forests, and occur with ectomycorrhizal trees in temperate biomes in which seasonally warm-and-wet climates enhance decomposition. Continental transitions between forests dominated by ectomycorrhizal or arbuscular mycorrhizal trees occur relatively abruptly along climate-driven decomposition gradients; these transitions are probably caused by positive feedback effects between plants and microorganisms. Symbiotic nitrogen fixers—which are insensitive to climatic controls on decomposition (compared with mycorrhizal fungi)—are most abundant in arid biomes with alkaline soils and high maximum temperatures. The climatically driven global symbiosis gradient that we document provides a spatially explicit quantitative understanding of microbial symbioses at the global scale, and demonstrates the critical role of microbial mutualisms in shaping the distribution of plant species.
Coproductie van monochloorazijnzuur en energiedragers uit biomassa : : Openbaar eindrapport van project TEBE116198
Baal, Olaf van; Dirix, Karin ; Foukaraki, Marlia ; Kruis, Alex ; Mars, Astrid ; Meesters, Koen ; Nuland, Youri van; Strassberger, Zea ; Weusthuis, Ruud ; Wolbert, Emil - \ 2019
Wageningen : Wageningen Food & Biobased Research (Wageningen Food & Biobased Research rapport 1900) - 3
Diterminal oxidation of alkanes
Nuland, Y.M. van; Weusthuis, R.A. ; Eggink, G. - \ 2018
Octrooinummer: WO2018172331, verleend: 2018-09-27.
A method for the preparation of amono- and/or di-esterified aliphatic α,ω-diol, a mono- and/or di-esterified aliphatic α,ω-dicarboxylic acidora mono-and/ordi-esterified aliphatic ω-hydroxycarboxylic acid by conversion of a substrate selected from an alkane, 1-alkanol, alkanal, alkanoateand/or an alkyl alkanoate, e.g. an ethyl alkanoate or a propylalkanoate, is provided.
Bacterie maakt alkaandiolen
Nuland, Youri van; Weusthuis, Ruud - \ 2017
Production of esterified α,ω‐diols from n‐alkanes with E. coli
Nuland, Y.M. van - \ 2017
Modified bacterium converts petroleum directly into building blocks for plastics
Nuland, Youri van - \ 2017
Bacterie maakt diolen van alkanen
Nuland, Youri van; Weusthuis, Ruud - \ 2017
Bacterie verduurzaamt kunststofproductie
Nuland, Youri van - \ 2017
Bacterie maakt groenere bouwstenen voor plastic
Nuland, Youri van - \ 2017
Deze bacterie maakt plastic van aardolie
Nuland, Youri van - \ 2017
Aangepaste bacterie zet aardolie rechtstreeks om in bouwstenen voor kunststoffen
Nuland, Youri van - \ 2017
Aardolie omzetten in bouwstenen voor kunststoffen met bacterie
Nuland, Youri van - \ 2017
Solving the diterminal alkane oxidation puzzle
Nuland, Youri van - \ 2017
Combination of ester biosynthesis and ω-oxidation for production of mono-ethyl dicarboxylic acids and di-ethyl esters in a whole-cell biocatalytic setup with Escherichia coli
Nuland, Youri M. van; Eggink, Gerrit ; Weusthuis, Ruud A. - \ 2017
Microbial Cell Factories 16 (2017). - ISSN 1475-2859
Adipic acid - Esters - Monooxygenases - Whole-cell biocatalysis - α,ω-dicarboxylic acids
Background: Medium chain length (C6-C12) α,ω-dicarboxylic acids (DCAs) and corresponding esters are important building blocks for the polymer industry. For DCAs of 12 carbon atoms and longer, a sustainable process based on monooxygenase catalyzed ω-oxidation of fatty-acids has been realized. For medium-chain DCAs with a shorter chain length however, such a process has not been developed yet, since monooxygenases poorly ω-oxidize medium-chain fatty acids (MCFAs). On the contrary, esterified MCFAs are ω-oxidized well by the AlkBGTHJ proteins from Pseudomonas putida GPo1. Results: We show that MCFAs can be efficiently esterified and subsequently ω-oxidized in vivo. We combined ethyl ester synthesis and ω-oxidation in one-pot, whole-cell biocatalysis in Escherichia coli. Ethyl ester production was achieved by applying acyl-CoA ligase AlkK and an alcohol acyltransferase, either AtfA or Eeb1. E. coli expressing these proteins in combination with the ω-oxidation pathway consisting of AlkBGTHJ, produced mono-ethyl DCAs directly from C6, C8 and C9 fatty acids. The highest molar yield was 0.75, for mono-ethyl azelate production from nonanoic acid. Furthermore, di-ethyl esters were produced. Diethyl suberate was produced most among the di-ethyl esters, with a molar yield of 0.24 from octanoic acid. Conclusion: The results indicate that esterification of MCFAs and subsequent ω-oxidation to mono-ethyl DCAs via whole-cell biocatalysis is possible. This process could be the first step towards sustainable production of medium-chain DCAs and medium-chain di-ethyl esters.
Biocatalytic, one-pot diterminal oxidation and esterification of n-alkanes for production of α,ω-diol and α,ω-dicarboxylic acid esters
Nuland, Youri M. van; Vogel, Fons A. de; Scott, Elinor L. ; Eggink, Gerrit ; Weusthuis, Ruud A. - \ 2017
Metabolic Engineering 44 (2017). - ISSN 1096-7176 - p. 134 - 142.
Alkanes - Monooxygenases - Whole-cell biocatalysis - α,ω-dicarboxylic acids - α,ω-diols
Direct and selective terminal oxidation of medium-chain n-alkanes is a major challenge in chemistry. Efforts to achieve this have so far resulted in low specificity and overoxidized products. Biocatalytic oxidation of medium-chain n-alkanes – with for example the alkane monooxygenase AlkB from P. putida GPo1- on the other hand is highly selective. However, it also results in overoxidation. Moreover, diterminal oxidation of medium-chain n-alkanes is inefficient. Hence, α,ω-bifunctional monomers are mostly produced from olefins using energy intensive, multi-step processes. By combining biocatalytic oxidation with esterification we drastically increased diterminal oxidation upto 92 mol% and reduced overoxidation to 3% for n-hexane. This methodology allowed us to convert medium-chain n-alkanes into α,ω-diacetoxyalkanes and esterified α,ω-dicarboxylic acids. We achieved this in a one-pot reaction with resting-cell suspensions of genetically engineered Escherichia coli. The combination of terminal oxidation and esterification constitutes a versatile toolbox to produce α,ω-bifunctional monomers from n-alkanes.
Production of medium-chain, a, omega-bifunctional monomers from fatty acids and n-alkanes
Nuland, Youri M. - \ 2017
Wageningen University. Promotor(en): G. Eggink; J.P.M. Sanders, co-promotor(en): R.A. Weusthuis. - Wageningen : Wageningen University - ISBN 9789463436809 - 161

In chapter 1, we give an introduction to bifunctional monomers that play an important role in the chemical industry. Briefly, the conventional production processes of α,ω-dicarboxylic acids and α,ω-diols are discussed. Strategies for more sustainable alternatives for production of medium-chain bifunctional monomers are discussed. Monooxygenase-based processes seem promising, if the problem of poor diterminal oxidation capacities of monooxygenases is solved. Esterification could be a tool to solve this problem.

In chapter 2 we have investigated the ω-oxidation activities of E. coli expressing AlkBGT or AlkBGTL, with various esters having an alkyl chain >1. These strains were able to ω-oxidize ethyl, propyl and butyl esters of C6-C10 fatty acids. Using esters with a longer alkyl chain enhanced ω-oxidation activities for C6 and C7 fatty acids. The major products were ω-hydroxy fatty acid esters, but over oxidation to the aldehyde and carboxylic acid also occurred. AlkL improved whole-cell ω-oxidation activities for substrates with a logPo/w above 4.

Since the major products were ω-hydroxy fatty acid esters in chapter 2, we investigated further conversion of these compounds to mono-esterified dicarboxylic acids in chapter 3. Alcohol dehydrogenase AlkJ and aldehyde dehydrogenase AlkH were functionally expressed in E. coli. AlkJ is functional with 9-hydroxy ethyl nonanoate as substrate, AlkH is functional with 9-oxo methyl nonanoate. Expansion of the AlkBGTL system with AlkJ and AlkH yielded strain E. coli AlkBGTHJL. This strain accumulated mono-ethyl azelate exclusively from ethyl nonanoate. Adding the substrate dissolved in a carrier solvent increased final product titers.

Subsequently, we investigated if in vivo esterification could enhance the ω-oxidation of AlkB in chapter 4. E. coli expressing AlkBGTHJL can ω-oxidize octanoate and nonanoate, but not efficiently. When acyl-CoA ligase AlkK and acyltransferase AtfA or Eeb1 were also expressed, ω-oxidation was more efficient. Furthermore, complete oxidation to the carboxylic acid was much more efficient when also in vivo esterification was achieved. Also di-ethyl esters were produced, meaning that esterification occurred twice.

Since ω-oxidation of fatty acids was improved with in vivo esterification in chapter 4, we were interested to investigate whether this system could also work with n-alkanes in chapter 5. Mono-esters of dicarboxylic acids were produced from n-alkanes by E. coli expressing AlkBGTHJKL and either AtfA or Eeb1. Starting from n-alkanes would also allow production of alcohols if overoxidation could be prevented. Application of a different alcohol acyltransferase (Atf1), limited the overoxidation by AlkB. ω-Oxidation of the formed ester resulted in the production of ω-alcohols, which were again esterified by Atf1.

Chapter 6 is the general discussion of this thesis, which evaluates the combination of esterification and terminal oxidation. Suggestions for improvements of the biocatalytic pathway are provided and critical factors for experiments in bioreactors are identified.

Expansion of the ω-oxidation system AlkBGTL of Pseudomonas putida GPo1 with AlkJ and AlkH results in exclusive mono-esterified dicarboxylic acid production in E. coli
Nuland, Youri M. van; Vogel, Fons A. de; Eggink, Gerrit ; Weusthuis, Ruud A. - \ 2017
Microbial Biotechnology 10 (2017)3. - ISSN 1751-7907 - p. 594 - 603.
The AlkBGTL proteins coded on the alk operon from Pseudomonas putida GPo1 can selectively ω-oxidize ethyl esters of C6 to C10 fatty acids in whole-cell conversions with Escherichia coli. The major product in these conversions is the ω-alcohol. However, AlkB also has the capacity to overoxidize the substrate to the ω-aldehyde and ω-acid. In this study, we show that alcohol dehydrogenase AlkJ and aldehyde dehydrogenase AlkH are able to oxidize ω-alcohols and ω-aldehydes of esterified fatty acids respectively. Resting E. coli expressing AlkBGTHJL enabled exclusive mono-ethyl azelate production from ethyl nonanoate, with an initial specific activity of 61 U gcdw -1. Within 2 h, this strain produced 3.53 mM mono-ethyl azelate, with a yield of 0.68 mol mol-1. This strain also produced mono-ethyl dicarboxylic acids from ethyl esters of C6 to C10 fatty acids and mono-methyl azelate from methyl nonanoate. Adding ethyl nonanoate dissolved in carrier solvent bis-(2-ethylhexyl) phthalate enabled an increase in product titres to 15.55 mM in two-liquid phase conversions. These findings indicate that E. coli expressing AlkBGTHJL is an effective producer of mono-esterified dicarboxylic acids from fatty acid esters.
Application of AlkBGT and AlkL from Pseudomonas putida GPo1 for selective alkyl ester ω-oxyfunctionalization in Escherichia coli
Nuland, Youri M. van; Eggink, Gerrit ; Weusthuis, Ruud A. - \ 2016
Applied and Environmental Microbiology 82 (2016)13. - ISSN 0099-2240 - p. 3801 - 3807.

The enzyme system AlkBGT from Pseudomonas putida GPo1 can efficiently ω-functionalize fatty acid methyl esters. Outer membrane protein AlkL boosts this ω-functionalization. In this report, it is shown that whole cells of Escherichia coli expressing the AlkBGT system can also ω-oxidize ethyl nonanoate (NAEE). Coexpression of AlkBGT and AlkL resulted in 1.7-fold-higher ω-oxidation activity on NAEE. With this strain, initial activity on NAEE was 70 U/g (dry weight) of cells (gcdw), 67% of the initial activity on methyl nonanoate. In time-lapse conversions with 5mMNAEE the main product was 9-hydroxy NAEE (3.6 mM), but also 9-oxo NAEE (0.1 mM) and 9-carboxy NAEE (0.6 mM) were formed. AlkBGT also ω-oxidized ethyl, propyl, and butyl esters of fatty acids ranging from C6 to C10. Increasing the length of the alkyl chain improved the ω-oxidation activity of AlkBGT on esters of C6 and C7 fatty acids. From these esters, application of butyl hexanoate resulted in the highest ω-oxidation activity, 82 U/gcdw. Coexpression of AlkL only had a positive effect on ω-functionalization of substrates with a total length of C11 or longer. These findings indicate that AlkBGT(L) can be applied as a biocatalyst for ω-functionalization of ethyl, propyl, and butyl esters of medium-chain fatty acids.

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