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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Dynamic modelling of brewers’ yeast and Cyberlindnera fabianii co-culture behaviour for steering fermentation performance
Rijswijck, Irma M.H. van; Mastrigt, Oscar van; Pijffers, Gerco ; Wolkers–Rooijackers, Judith C.M. ; Abee, Tjakko ; Zwietering, Marcel H. ; Smid, Eddy J. - \ 2019
Food Microbiology 83 (2019). - ISSN 0740-0020 - p. 113 - 121.

Co-cultivation of brewers' yeast (Saccharomyces cerevisiae) with Cyberlindnera fabianii makes it possible to steer aroma and alcohol levels by changing the inoculation ratio of the two yeasts. A dynamic model was developed based on mono-culture performance of brewers' yeast and C. fabianii in controlled bioreactors with aerated wort as medium, describing growth rate, carbohydrate utilization, ethanol production, maintenance, oxygen consumption and ergosterol biosynthesis/use for cell membrane synthesis (the last one only for brewers' yeast). The parameters were estimated by fitting models to experimental data of both mono-cultivations. To predict the fermentation outcome of brewers' yeast and C. fabianii in co-cultivation, the two models were combined and the same parameter settings were used. The co-cultivation model was experimentally validated for the inoculum ratios 1:10 and 1:100 brewers' yeast over C. fabianii. The use of predictive modelling supported the hypothesis that performance of brewers' yeast in co-cultivation is inhibited by oxygen depletion which is required for the biosynthesis of ergosterol. This dynamic modelling approach and the parameters involved may also be used to predict the performance of brewers’ yeast in the co-cultivation with other yeast species and to give guidance to optimize the fermentation outcome.

Acetate-ester hydrolase activity for screening of the variation in acetate ester yield of Cyberlindnera fabianii, Pichia kudriavzevii and Saccharomyces cerevisiae
Rijswijck, Irma M.H. van; Kruis, Aleksander J. ; Wolkers – Rooijackers, Judith C.M. ; Abee, Tjakko ; Smid, Eddy J. - \ 2019
Food Science and Technology = Lebensmittel-Wissenschaft und Technologie 104 (2019). - ISSN 0023-6438 - p. 8 - 15.
Acetate esters - Alcohol acetyltransferase - Cyberlindnera fabianii - Pichia kudriavzevii - Saccharomyces cerevisiae

Esters constitute an important class of aroma compounds and contribute significantly to the aroma of yeast-fermented beverages. Ester formation is well studied in Saccharomyces cerevisiae, while production of aroma compounds by non-conventional yeasts has received little attention. The selection of such strains for co-culturing with S. cerevisiae offers opportunities for product innovations. Therefore, we performed a comparative analysis of the diversity in ester production by Cyberlindnera fabianii 65 (Cf65), Pichia kudriavzevii 129 (Pk129) and S. cerevisiae 131 (Sc131). For all three species distinct aroma profiles were identified, with Cf65 producing the highest amount of acetate esters. Since esters are formed from alcohols and acyl-CoA or acetyl-CoA, we analysed in vitro alcohol dehydrogenase and alcohol acetyl transferase activities in those three yeasts and found no correlation with ester formation. In contrast, a clear inverse correlation between the acetate-ester hydrolase activity and acetate ester yield was found for the three yeast species. Our study indicates that acetate-ester hydrolase activity plays a key role in determination of the final amount of acetate esters in fermentation broths.

Fecal Bacterial Communities in Insectivorous Bats from the Netherlands and Their Role as a Possible Vector for Foodborne Diseases
Wolkers-Rooijackers, Judith C.M. ; Rebmann, Katharina ; Bosch, Thijs ; Hazeleger, Wilma C. - \ 2018
Acta Chiropterologica 20 (2018)2. - ISSN 1508-1109 - p. 475 - 483.
bacteria - bats - DGGE - microbial diversity

Bats are commonly regarded as vectors for viruses, but little is known about bacterial communities in bats and the possible role of bats in the transmission cycle of foodborne diseases. To gain more insight, microbial communities in fecal samples from 37 insectivorous bats of different species from the Netherlands were investigated by polymerase chain reaction and denaturant gradient gel electrophoresis (PCR-DGGE). Subsequently, 10 samples from the following bat species: common pipistrelle (Pipistrellus pipistrellus; n = 3), Daubenton's bat (Myotis daubentonii; n = 3), serotine bat (Eptesicus serotinus; n = 1), whiskered bat (Myotis mystacinus; n = 1), Geoffroy's bat (Myotis emarginatus; n = 1) and Natterer's bat (Myotis nattereri; n = 1) were selected and used in bacterial 16S rDNA cloning and sequencing. The fecal microbiota in bats was found to be diverse with predominant bacterial genera Carnobacterium, Serratia, Pseudomonas, Enterococcus and Yersinia. The presence of opportunistic pathogens Citrobacter freundii, Escherichia coli, Enterococcus faecalis, Serratia fonticola and Rahnella aquatilis was also recorded. Based on cloning results, we found no proof that bats in the Netherlands are a major vector for the transmission of bacterial zoonotic diseases, although previous findings in literature reported isolation of foodborne pathogens from bats.

Contribution of Eat1 and other alcohol acyltransferases to ester production in Saccharomyces cerevisiae
Kruis, A.J. ; Gallone, Brigida ; Jonker, T. ; Mars, A.E. ; Rijswijck, I.M.H. van; Wolkers-Rooijackers, J.C.M. ; Smid, E.J. ; Steensels, Jan ; Verstrepen, Kevin J. ; Kengen, S.W.M. ; Oost, J. van der; Weusthuis, R.A. - \ 2018
Frontiers in Microbiology 9 (2018). - ISSN 1664-302X - 11 p.
Esters are essential for the flavor and aroma of fermented products, and are mainly produced by alcohol acyl transferases (AATs). A recently discovered AAT family named Eat (Ethanol acetyltransferase) contributes to ethyl acetate synthesis in yeast. However, its effect on the synthesis of other esters is unknown. In this study, the role of the Eat family in ester synthesis was compared to that of other Saccharomyces cerevisiae AATs (Atf1p, Atf2p, Eht1p, and Eeb1p) in silico and in vivo. A genomic study in a collection of industrial S. cerevisiae strains showed that variation of the primary sequence of the AATs did not correlate with ester production. Fifteen members of the EAT family from nine yeast species were overexpressed in S. cerevisiae CEN.PK2-1D and were able to increase the production of acetate and propanoate esters. The role of Eat1p was then studied in more detail in S. cerevisiae CEN.PK2-1D by deleting EAT1 in various combinations with other known S. cerevisiae AATs. Between 6 and 11 esters were produced under three cultivation conditions. Contrary to our expectations, a strain where all known AATs were disrupted could still produce, e.g., ethyl acetate and isoamyl acetate. This study has expanded our understanding of ester synthesis in yeast but also showed that some unknown ester-producing mechanisms still exist.
Enhancing vitamin B12 in lupin tempeh by in situ fortification
Wolkers–Rooijackers, Judith C.M. ; Endika, Martha F. ; Smid, Eddy J. - \ 2018
Food Science and Technology = Lebensmittel-Wissenschaft und Technologie 96 (2018). - ISSN 0023-6438 - p. 513 - 518.
Lupin - Propionibacterium freudenreichii - Rhizopus oryzae - Tempeh - Vitamin B

Tempeh is a traditional, fungal fermented Indonesian product, usually made from soybeans. Tempeh is known to contain vitamin B12 which is essential for a healthy human diet. Therefore, tempeh is of particular interest for vegan diets since B12 is normally found only in animal derived products. The vitamin B12 in tempeh is associated with the presence of opportunistic pathogens like Klebsiella pneumoniae. Levels of B12 in tempeh do not sustain the recommended daily intake though. In addition, the use of a food-grade bacterium instead of K. pneumoniae is preferred. Lupin can serve as alternative substrate for soybeans due to its similar protein content, resulting in ‘lupin tempeh’. In this study, Propionibacterium freudenreichii, a food-grade, vitamin B12 producing bacterium, was used in co-culture with Rhizopus oryzae to produce B12-enriched lupin tempeh. A significant increase of vitamin B12 content (up to 0.97 μg/100 g) was achieved by fermenting lupin using a mixed starter of R. oryzae and P. freudenreichii. Other parameters, such as texture and volatile organic compounds, were not affected by the bacterial co-inoculation. Therefore, these results are promising for in situ vitamin B12 fortification of lupin tempeh making it a sustainable protein source for a healthy human diet.

Elevated vitamin B12 levels in lupin tempeh by in situ fortification
Wolkers-Rooijackers, J.C.M. ; Endika, M.F. ; Smid, E.J. - \ 2017
In situ vitamin B12 fortification of lupin tempeh
Wolkers-Rooijackers, J.C.M. ; Endika, M.F. ; Smid, E.J. - \ 2017
In: 12th International Symposium on Lactic Acid Bacteria. - LABsymposium - p. 120 - 120.
Performance of non-conventional yeasts in co-culture with brewers’ yeast for steering ethanol and aroma production
Rijswijck, Irma M.H. van; Wolkers - Rooijackers, Judith C.M. ; Abee, Tjakko ; Smid, Eddy J. - \ 2017
Microbial Biotechnology 10 (2017)6. - ISSN 1751-7907 - p. 1591 - 1602.

Increasing interest in new beer types has stimulated the search for approaches to extend the metabolic variation of brewers’ yeast. Therefore, we tested two approaches using non-conventional yeast to create a beer with lower ethanol content and a complex aroma bouquet. First, the mono-culture performance was monitored of 49 wild yeast isolates of Saccharomyces cerevisiae (16 strains), Cyberlindnera fabianii (9 strains) and Pichia kudriavzevii (24 strains). Interestingly, both C. fabianii and P. kudriavzevii isolates produced relatively more esters compared with S. cerevisiae isolates, despite their limited fermentation capacity. Next, one representative strain of each species (Sc131, Cf65 and Pk129) was applied as co-culture with brewers’ yeast (ratio 1:1). Co-cultures with Cf65 and Pk129 resulted in a beer with lower alcohol content (3.5, 3.8 compared with 4.2% v/v) and relatively more esters. At higher inoculum ratios of Cf65 over brewers’ yeast, growth inhibition of brewers’ yeast was observed, most likely caused by competition for oxygen between brewers’ yeast and Cf65 resulting in a reduced level of ethanol and altered aroma profiles. With this study, we demonstrate the feasibility of using non-conventional yeast species in co-cultivation with traditional brewers’ yeast to tailor aroma profiles as well as the final ethanol content of beer.

Bacterial concentration and diversity in fresh tropical shrimps (Penaeus notialis) and the surrounding brackish waters and sediment
Dabade, S. ; Wolkers-Rooijackers, J.C.M. ; Azokpota, P. ; Hounhouigan, D.J. ; Zwietering, M.H. ; Nout, R. ; Besten, H.M.W. den - \ 2016
International Journal of Food Microbiology 218 (2016). - ISSN 0168-1605 - p. 96 - 104.
Clone libraries analysis - Invertebrates microbiota - PCR-DGGE - Tropical fishery products

This study aimed at determining bacterial concentration and diversity in fresh tropical shrimps (. Penaeus notialis) and their surrounding brackish waters and sediment. Freshly caught shrimp, water and sediment samples were collected in Lakes Nokoue and Aheme in Benin (West Africa) during two periods with different water salinity and temperature. We used complementary culture-dependent and culture-independent methods for microbiota analysis. During both sampling periods, total mesophilic aerobic counts in shrimp samples ranged between 4.4 and 5.9 log CFU/g and were significantly higher than in water or sediment samples. In contrast, bacterial diversity was higher in sediment or water than in shrimps. The dominant phyla were Firmicutes and Proteobacteria in shrimps, Firmicutes, Proteobacteria, and Actinobacteria in water, and Proteobacteria and Chloroflexi in sediment. At species level, distinct bacterial communities were associated with sediment, water and shrimps sampled at the same site the same day. The study suggests that the bacterial community of tropical brackish water shrimps cannot be predicted from the microbiota of their aquatic environment. Thus, monitoring of microbiological quality of aquatic environments might not reflect shrimp microbiological quality.

Wild yeasts: the key to beer innovation?
Rijswijck, I.M.H. van; Zweers, Saskia ; Ploeg, R. van der; Wolkers-Rooijackers, J.C.M. ; Abee, T. ; Smid, E.J. - \ 2015
Wild yeasts: the key to beer innovation?
Rijswijck, I.M.H. van; Zweers, Saskia ; Ploeg, R. van der; Wolkers-Rooijackers, J.C.M. ; Abee, T. ; Smid, E.J. - \ 2015
Biodiversity of wild yeast isolates and their potential in brewing
Wolkers-Rooijackers, J.C.M. ; Rijswijck, I.M.H. van; Mik, Ivana ; Abee, T. ; Smid, E.J. - \ 2015
Strain diversity and phage resistance in complex dairy starter cultures
Spus, M. ; Alexeeva, S.V. ; Wolkers-Rooijackers, J.C.M. ; Zwietering, M.H. ; Abee, T. ; Smid, E.J. - \ 2015
Journal of Dairy Science 98 (2015)8. - ISSN 0022-0302 - p. 5173 - 5182.
streptococcus-cremoris - lactic streptococci - lactococcus-lactis - food fermentations - bacteriophages - competition - products - genomics - bacteria - plasmid
The compositional stability of the complex Gouda cheese starter culture Ur is thought to be influenced by diversity in phage resistance of highly related strains that co-exist together with bacteriophages. To analyze the role of bacteriophages in maintaining culture diversity at the level of genetic lineages, simple blends of Lactococcus lactis strains were made and subsequently propagated for 152 generations in the absence and presence of selected bacteriophages. We first screened 102 single-colony isolates (strains) from the complex cheese starter for resistance to bacteriophages isolated from this starter. The collection of isolates represents all lactococcal genetic lineages present in the culture. Large differences were found in bacteriophage resistance among strains belonging to the same genetic lineage and among strains from different lineages. The blends of strains were designed such that 3 genetic lineages were represented by strains with different levels of phage resistance. The relative abundance of the lineages in blends with phages was not stable throughout propagation, leading to continuous changes in composition up to 152 generations. The individual resistance of strains to phage predation was confirmed as one of the factors influencing starter culture diversity. Furthermore, loss of proteolytic activity of initially proteolytic strains was found. Reconstituted blends with only 4 strains with a variable degree of phage resistance showed complex behavior during prolonged propagation. Key words: starter culture; bacteriophage; diversity; proteolytic activity
Nutrient limitation leads to penetrative growth into agar and affects aroma formation in Pichia fabianii, P. kudriavzevii and Saccharomyces cerevisiae
Rijswijck, I.M.H. van; Dijksterhuis, J. ; Wolkers-Rooijackers, J.C.M. ; Abee, T. ; Smid, E.J. - \ 2015
Yeast 32 (2015)1. - ISSN 0749-503X - p. 89 - 101.
ziziphus-mauritiana fruits - filamentous growth - yeast - alcohols - wine - catabolism - fungi
Among fermentative yeast species, Saccharomyces cerevisiae is most frequently used as a model organism, although other yeast species may have special features that make them interesting candidates to apply in food-fermentation processes. In this study, we used three yeast species isolated from fermented masau (Ziziphus mauritiana) fruit, S. cerevisiae 131, Pichia fabianii 65 and Pichia kudriavzevii 129, and determined the impact of nitrogen and/or glucose limitation on surface growth mode and the production of volatile organic compounds (VOCs). All three species displayed significant changes in growth mode in all nutrient-limited conditions, signified by the formation of metafilaments or pseudohyphae. The timing of the transition was found to be species-specific. Transition in growth mode is suggested to be linked to the production of certain fusel alcohols, such as phenylethyl alcohol, which serve as quorum-sensing molecules. Interestingly, we did not observe concomitant increased production of phenylethyl alcohol and filamentous growth. Notably, a broader range of esters was found only for the Pichia spp. grown on nitrogen-limited agar for 21¿days compared to nutrient-rich agar, and when grown on glucose- and glucose- plus nitrogen-limited agar. Our data suggest that for the Pichia spp., the formation of esters may play an important role in the switch in growth mode upon nitrogen limitation. Further biological or ecological implications of ester formation are discussed.
Systematic approach in resolving stability of complex starter culture in the context of bacteriophage predation
Spus, M. ; Wolkers-Rooijackers, J.C.M. ; Abee, T. ; Smid, E.J. - \ 2014
In: Book of abstracts Phages 2014: Bacteriophage in Medicine, Food and Biotechnology. - Oxfordshire : LibPubMedia - p. 14 - 14.
Systematic approach in resolving stability of complex starter culture in the context of bacteriophage predation
Spus, M. ; Wolkers-Rooijackers, J.C.M. ; Abee, T. ; Smid, E.J. - \ 2014
In: Abstract book 11th International Symposium on Lactic Acid Bacteria. - - p. C002 - C002.
Previous studies have shown that complex cheese starter cultures are extremely stable in its composition. This compositional stability of these cultures results from a combination of factors like genetic repertoire, plasmid content and bacteriophage sensitivity and was achieved by the course of evolution during long term use in dairy industry [1]. The main focus of this study was on the role of bacteriophages in the maintenance of functional stability. Many single colony isolates of a complex starter culture were isolated and characterized regarding bacteriophage sensitivity and plasmid content. This information was used in designing defined blends of those single colony isolates. Blends consisting of different numbers of colony isolates were exposed (or not) to bacteriophage predation and sequentially propagated in milk (back-slopping) for many generations. The functionality and population dynamics of the blends were monitored at specified time points. A systematic approach (from simple to more complex) in defined blends design allowed control over the applied level of diversity. Three different levels of diversity were gradually applied to defined blends: 1) isolates from two different genetic lineages: sensitive and resistant, 2) different levels of bacteriophage sensitivity: sensitive, moderately resistant and resistant among isolates from one of the two genetic lineages used, 3) many isolates (different levels of sensitivity) of all genetic lineages found in the complex starter. Comparative characterization of isolates from initial and end time point of sequential propagation of defined blends was performed to understand the mechanisms controlling compositional stability and maintaining culture complexity. 1 Multifactorial diversity sustains microbial community stability Oylum Erkus, Victor CL de Jager, Maciej Spus, Ingrid J van Alen-Boerrigter, Irma MH van Rijswijck, Lucie Hazelwood, Patrick WM Janssen, Sacha AFT van Hijum, Michiel Kleerebezem and Eddy J Smid; ISME Journal (2013), 1751-7362/13
Engineering functionality of complex starter cultures
Wolkers-Rooijackers, J.C.M. ; Groof, B.M.J. de; Spus, M. ; Smid, E.J. - \ 2014
In: Abstract book 11th International Symposium on Lactic Acid Bacteria. - - p. E047 - E047.
The use of starter cultures is an essential aspect in cheese manufacturing. Starter cultures may consist of single strains or mixtures of different strains and species of mainly lactic acid bacteria. An undefined mixture of different strains and species can be regarded as a complex ecosystem. Starter culture “Ur”, used for the production of Gouda cheese is an example of a complex starter culture and it contains 7 genetic lineages of Lactococcus lactis and 1 of Leuconostoc mesenteroides [1]. Complex ecosystems are known for their stability in composition, even during the process of back-slopping, where new milk is inoculated with whey from the previous batch. We set out to investigate the compositional stability of starter culture Ur during propagation at different temperatures. In addition, Ur was reconstituted from the 8 defined genetic lineages in 1:1 starting ratio. Propagation was carried out in fat free milk and the inoculated milk was incubated at 20°C, 25°C and 30°C. These temperatures were selected to possibly favor strains that have different optimum growth temperatures. After 28 transfers (~200 generations) the composition of Ur and the reconstituted mixtures was determined using qPCR with lineage specific primers. Sequential propagation of Ur in milk at different temperatures induced changes in the relative abundance of different genomic lineages, but none of the lineages were lost. We also demonstrated that reconstituted Ur, in comparison with original Ur, leads to a similar end-point composition after 28 transfers as Ur. This demonstrates the robustness of the original Ur culture and suggests interactions between the different lineages. 1. Erkus O, de Jager VC, Spus M, van Alen-Boerrigter IJ, van Rijswijck IM, Hazelwood L, Janssen PW, van Hijum SA, Kleerebezem M, Smid EJ: Multifactorial diversity sustains microbial community stability. ISME J 2013, 7:2126-2136.
Bugs in bats 2: Analysis of microbial communities in faecal samples obtained from bats in the Netherlands
Wolkers-Rooijackers, J.C.M. ; Rebmann, K. ; Bosch, T. ; Hazeleger, W.C. - \ 2014
Little is known about bacterial communities in bats and about a possible role of bats in the transmission cycle of foodborne diseases. Different wildlife species have already been associated with the transmission of foodborne diseases and previous research at the Laboratory of Food Microbiology of Wageningen University revealed the presence of Campylobacter in 2.7% of 632 investigated bat faeces samples (bugs in bats 1: Bats may be vectors for Campylobacter). Based on these findings, the microbial communities in 37 bat faecal samples, were investigated by polymerase chain reaction and denaturant gradient gel electrophoresis (PCR-DGGE). Subsequently, 10 faecal samples from the following bat species: Common pipistrelle (3 samples), Daubenton’s bat (3 samples) and one sample each from Serotine, Whiskered bat, Geoffroy’s bat and Natterer’s bat were selected and used in bacterial 16s rDNA cloning and sequencing. The molecular approach did not reveal the presence of obligate foodborne pathogens. The microflora in bats was found to be highly diverse with major bacterial genera Carnobacterium, Enterococcus and Serratia. A relation between the members of the microflora and the bat species could not be proven. The results can be used to gain a deeper understanding of the intestinal communities in bats.
Functional implications of the microbial community structure of undefined mesophilic starter cultures
Smid, E.J. ; Erkus, O. ; Spus, M. ; Wolkers-Rooijackers, J.C.M. ; Alexeeva, S.V. ; Kleerebezem, M. - \ 2014
Microbial Cell Factories 13 (2014)suppl. 1. - ISSN 1475-2859
lactic-acid bacteria - lactococcus-lactis - subsp lactis - listeria-monocytogenes - biovar diacetylactis - metabolic models - cheddar cheese - diversity - cremoris - dairy
This review describes the recent advances made in the studies of the microbial community of complex and undefined cheese starter cultures. We report on work related to the composition of the cultures at the level of genetic lineages, on the presence and activity of bacteriophages and on the population dynamics during cheese making and during starter culture propagation. Furthermore, the link between starter composition and starter functionality will be discussed. Finally, recent advances in predictive metabolic modelling of the multi-strain cultures will be discussed in the context of microbe-microbe interactions.
Population dynamics in an undefined mixed starter culture - the role of bacteriophages
Spus, M. ; Alexeeva, S.V. ; Wolkers-Rooijackers, J.C.M. ; Erkus, O. ; Alen, I. van; Smid, E.J. - \ 2013
In: Poster abstracts Summer Conference 2013 of Sociedy for Applied Microbiology, Cardiff, Wales, 04 - 04 July. - Society for Applied Microbiology - p. 36 - 37.
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