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Genome-Based Selection and Application of Food-Grade Microbes

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Genome-Based Selection and Application of Food-Grade Microbes Tangyu et al. Microb Cell Fact (2021) 20:109 https://doi.org/10.1186/s12934-021-01595-2 Microbial Cell Factories RESEARCH Open Access Genome-based selection and application of food-grade microbes for chickpea milk fermentation towards increased L-lysine content, elimination of indigestible sugars, and improved favour Muzi Tangyu1, Michel Fritz1, Rosa Aragao‑Börner2, Lijuan Ye2, Biljana Bogicevic2, Christoph J. Bolten3 and Christoph Wittmann1* Abstract Background: Plant‑based milk alternatives are more popular than ever, and chickpea‑based milks are among the most commercially relevant products. Unfortunately, limited nutritional value because of low levels of the essential amino acid L‑lysine, low digestibility and unpleasant taste are challenges that must be addressed to improve product quality and meet consumer expectations. Results: Using in-silico screening and food safety classifcations, 31 strains were selected as potential L‑lysine pro‑ ducers from approximately 2,500 potential candidates. Benefcially, 30% of the isolates signifcantly accumulated amino acids (up to 1.4 mM) during chickpea milk fermentation, increasing the natural level by up to 43%. The best‑ performing strains, B. amyloliquefaciens NCC 156 and L. paracasei subsp. paracasei NCC 2511, were tested further. De novo lysine biosynthesis was demonstrated in both strains by 13C metabolic pathway analysis. Spiking small amounts of citrate into the fermentation signifcantly activated L‑lysine biosynthesis in NCC 156 and stimulated growth. Both microbes revealed additional benefts in eliminating indigestible sugars such as stachyose and rafnose and convert‑ ing of‑favour aldehydes into the corresponding alcohols and acids with fruity and sweet notes. Conclusions: B. amyloliquefaciens NCC 156 and L. paracasei subsp. paracasei NCC 2511 emerged as multi‑beneft microbes for chickpea milk fermentation with strong potential for industrial processing of the plant material. Given the high number of L‑lysine‑producing isolates identifed in silico, this concept appears promising to support strain selection for food fermentation. 13 Keywords: L‑lysine, Lactic acid bacteria, Lacticaseibacillus paracasei, Bacillus amyloliquefaciens, C isotope study, Chickpea, Plant‑based milk alternative, Plant milk, fermentation, Flavour, Indigestible sugar, Rafnose, Stachyose Background Plant-based milk alternatives are growing in popularity. Tey ofer attractive properties for consumers by being *Correspondence: christoph.wittmann@uni‑saarland.de ecologically more sustainable and animal-welfare-friendly 1 Institute of Systems Biotechnology, Saarland University, Saarbrücken, than dairy milks, lactose-free, and vegan. Notably, the Germany Full list of author information is available at the end of the article world market for such products is continuously increasing © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Tangyu et al. Microb Cell Fact (2021) 20:109 Page 2 of 21 and is expected to surpass US$ 26 billion by 2023 [1]. As l-lysine degradation, and pathways competing with prominent example, chickpea (Cicer arietinum L.), one of l-lysine biosynthesis for carbon precursors (Fig. 1). A the oldest and most widely consumed legumes worldwide component from the pathway architecture for bacterial [2], is regarded an attractive source of milk-alternative con- l-lysine biosynthesis, the lysA gene (encoding diami- sumer products [3, 4] with good protein quality [5, 6]. nopimelate decarboxylase) was inferred as a premium Unfortunately, suspensions of chickpea four (termed selection criterion to identify potential l-lysine produc- chickpea milk below due to their milk-like appearance) ers. Tis enzyme catalyses the terminal step of l-lysine do not match animal milk in all desired characteristics, synthesis, downstream of meso-diaminopimelate, where which is a limitation that is generally observed for plant- all synthetic routes converge (Fig. 1). Terefore, the pres- based milk alternatives [7]. Tis limitation also holds for ence of lysA was an essential (minimal) feature required the essential amino acid l-lysine, which is required for for l-lysine formation. In total, 2472 bacterial NCC hormone formation, catalytic and structural proteins, and genomes contained an annotated lysA gene, and most of immune system support and is therefore one of the most them belonged to the orders Lactobacillales, Bacillales, impacting nutrients [8]. Critically, it exhibits much lower Bifdobacteriales, and Corynebacteriales. Fewer than half abundance in chickpea-based milk than in animal milk, of the genomes (1,117) additionally included a dapF gene, approximately half of the amount in a typical 10% dry mat- potentially indicating the succinylase and/or acetylase ter formulation [9, 10]). Moreover, chickpea milk contains route to synthesize l-lysine (Fig. 1). Only 14 strains con- elevated levels of indigestible sugars such as rafnose and tained the ddh gene (encoding diaminopimelate dehydro- stachyose, which cause fatulence, diarrhoea, and other dis- genase) as a key step of the dehydrogenase pathway. comfort upon consumption [11]. In addition, it exhibits a Te selection was narrowed down by considering grassy and beany taste that does not meet consumer expec- only strains approved for use in the food and feed chain tations [12]. according to the European Food Safety Authority [22]. Microbial fermentation is a well-established way to Among all potential l-lysine producers, i. e. all strains improve the nutritional quality of plant-based milk alterna- that contained lysA plus either dapF or ddh, 945 strains tives [1]. For example, fermentation of milks from peanut, exhibited the qualifed presumption of safety (QPS) sta- soy, cowpea, and mung bean increased protein quality and tus and therefore fulflled this extra requirement. Tey digestibility and occasionally also the l-lysine content [13– belonged to fve diferent families (Lactobacillaceae, 19]. Admittedly, only selected microbial strains improve Bacillaceae, Bifdobacteriaceae, Corynebacteraceae, desired features [20]. For example, natural microbes rarely Carnobacteriaceae), including 12 genera and 33 difer- overproduce l-lysine [21]. ent species. None of the strains that contained a ddh Here, we present a systematic workfow to fortify a gene met the food safety constraint. Carnobacterium and chickpea milk using fermentation with natural food-grade Pediococcus were not further considered because they are microbes. To improve upon the low level of l-lysine, more mainly associated with producing bacteriocins for food than 30 strains were selected as candidates based on their preservation [23, 24], and the fermentation of materials genomic repertoire related to l-lysine metabolism (Fig. 1). other than milk such as wine, cheese, sausage, and cab- A screening round revealed that one-third (9) of the tested bage [25], leaving Lactobacillaceae (757), Bacillaceae strains signifcantly accumulated l-lysine during chick- (34), Bifdobacteriaceae (119), and Corynebacteraceae (2) pea milk fermentation. 13C isotope studies showed that for the fnal selection. Accordingly, 31 potential produc- the two best-performing strains, Lacticaseibacillus para- ers (all containing lysA and dapF that covered the iden- casei subsp. paracasei Nestlé Culture Collection (NCC) tifed taxonomic diversity were selected for experimental 2511 and Bacillus amyloliquefaciens NCC 156, synthetize studies. Te selected strains represented 10 genera and l-lysine de novo. Both microbes were used for a more 19 diferent species (Additional fle 1: Table S1): (i) Lac- detailed investigation of the fermentation process. Tey tobacillus helveticus (3), Lactobacillus johnsonii (3), Lac- benefcially altered the amino acid and protein profle, uti- tobacillus acidophilus (1), Lactobacillus delbrueckii (1), lized (indigestible) carbohydrates, and formed desired fa- Limosilactobacillus reuteri (3), Limosilactobacillus pontis vour molecules, which highlights them as microbes well (1), Lacticaseibacillus paracasei (2), Lactiplantibacillus suited for chickpea milk fermentation. plantarum (1), Fructilactobacillus sanfranciscensis (3), Levilactobacillus brevis (1), Lentilactobacillus hilgardii Results (1); (ii) Bifdobacterium longum (1) and Bifdobacterium Genome‑based selection of food‑grade microbes infantis (1); (iii) Bacillus amyloliquefaciens (2), Bacillus for L‑lysine production fexus (2), Bacillus licheniformis (1), Bacillus pumilus (1), Bacterial genomes of the NCC were analysed for their fea- and
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