Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-23T07:37:33.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Nitrogen source: an effective component for the growth and viability of Lactobacillus delbrueckii subsp. bulgaricus

Published online by Cambridge University Press:  30 August 2022

Raphael D. Ayivi ,
Salam A. Ibrahim ,
Albert Krastanov ,
Abishek Somani  and
Shahida A. Siddiqui
Raphael D. Ayivi
Affiliation:
Department of Food and Nutritional Sciences, North Carolina A&T State University, Greensboro, NC 27411, USA Joint School of Nanoscience and Nanoengineering, University of North Carolina, Greensboro, NC 27412, USA
Salam A. Ibrahim*
Affiliation:
Department of Food and Nutritional Sciences, North Carolina A&T State University, Greensboro, NC 27411, USA
Albert Krastanov
Affiliation:
Department of Biotechnology, University of Food Technologies, Plovdiv, Bulgaria
Abishek Somani
Affiliation:
Ohly Gmbh, Wandsbeker Zollstrasse 59, 22041 Hamburg, Germany
Shahida A. Siddiqui
Affiliation:
Department of Biotechnology and Sustainability, Technical University of Munich (TUM), 94315 Straubing, Germany DIL e.V.–German Institute of Food Technologies, 49610 D-Quakenbrück, Germany
*
Author for correspondence: Salam A. Ibrahim, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In this study, we developed and optimized a growth media by evaluating various nitrogen sources for the cultivation of Lactobacillus bulgaricus, a probiotic and an important dairy starter culture. We modified the composition of deMan, Rogosa and Sharpe (MRS) culture media and substituted the nitrogen content with alternative nitrogen sources X-Seed KAT, X-Seed Carbo Max and X-Seed Nucleo Max in various blends of 5 g/l and 10 g/l respectively. Results showed that bacterial growth was significantly higher when the nitrogen source blend KCMax (10/10) was used. The optical density (OD610 nm) of the Lactobacillus bulgaricus strains were higher (1.34 and 1.79) in the KCMax (10/10) medium than in the MRS medium (0.89 and 1.42) (P < 0.05). There was no significant difference in the bacterial counts for both the MRS medium and the KCMax (10/10) medium, and all bacterial counts were estimated at 8 log CFU/ml. The buffering capacity of KCMax (10/10) was also tested and supplemented with l-histidine and was significantly different (P < 0.05) than that of the MRS control medium. Calcium supplemented in the KCMax (10/10) also served as a cryoprotectant for the cells during freezing and freeze-drying. Bacterial counts of the recovered calcium-treated freeze-dried cells were statistically significant (P < 0.05). We hypothesized that alternative nitrogen sources such as selected yeast extracts from the X-Seed brand of complex nitrogen sources could efficiently support the viability of Lb. bulgaricus. Our results thus suggested the growth of Lb. bulgaricus was efficiently supported by the X-Seed KAT, X-Seed Nucleo Max and X-Seed Carbo Max nitrogen sources. Consequently, these alternative nitrogen sources could potentially be recommended for dairy starter culture fermentations.

Keywords

Bacterial enumerationgrowth mediaLb. bulgaricusnitrogen sourcestarter culture
Type
Research Article
Information
Journal of Dairy Research , Volume 89 , Issue 3 , August 2022 , pp. 316 - 322
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolfsson, O, Meydani, SN and Russell, RM (2004) Yogurt and gut function. American Journal of Clinical Nutrition 80, 245–256.CrossRefGoogle ScholarPubMed
Akabanda, F, Owusu-Kwarteng, J, Tano-Debrah, K, Glover, RL, Nielsen, DS and Jespersen, L (2013) Taxonomic and molecular characterization of lactic acid bacteria and yeasts in Nunu, a Ghanaian fermented milk product. Food Microbiology 34, 277–283.CrossRefGoogle ScholarPubMed
Alazzeh, AY, Ibrahim, SA, Song, D, Shahbazi, A and AbuGhazaleh, AA (2009) Carbohydrate and protein sources influence the induction of α-and β-galactosidases in Lactobacillus reuteri. Food Chemistry 117, 654–659.CrossRefGoogle Scholar
Aponte, M, Murru, N and Shoukat, M (2020). Therapeutic, prophylactic, and functional use of probiotics: a current perspective. Frontiers in Microbiology 11, 562048.CrossRefGoogle ScholarPubMed
Atilola, OA, Gyawali, R, Aljaloud, SO and Ibrahim, SA (2015) Use of phytone peptone to optimize growth and cell density of Lactobacillus reuteri. Foods (Basel, Switzerland) 4, 318–327.Google ScholarPubMed
Aumiller, K, Stevens, E, Scheffler, R, Guvener, ZT, Tung, E, Grimaldo, AB, Carlson, HK, Deutschbauer, AM, Taga, ME, Marco, ML and Ludington, WB (2021) A chemically-defined growth medium to support Lactobacillus-Acetobacter community analysis. bioRxiv Preprint. doi: 10.1101/2021.05.12.443930CrossRefGoogle Scholar
Ayad, AA, El-Rab, DAG, Ibrahim, SA and Williams, LL (2020) Nitrogen sources effect on Lactobacillus reuteri growth and performance cultivated in date palm (Phoenix dactylifera L.) by-products. Fermentation 6, 1–10.CrossRefGoogle Scholar
Ayivi, RD, Gyawali, R, Krastanov, A, Aljaloud, SO, Worku, M, Tahergorabi, R, Silva, RC and Ibrahim, SA (2020) Lactic acid bacteria: food safety and human health applications. Dairy 1, 202–232.CrossRefGoogle Scholar
Berisvil, AP, Astesana, DM, Zimmermann, JA, Frizzo, LS, Rossler, E, Romero Scharpen, A, Olivero, CR, Zbrun, MV, Signorini Porchiett, ML, Sequeira, GJ, Drago, S and Soto, LP (2020) Low-cost culture medium for biomass production of lactic acid bacteria with probiotic potential destined to broilers. Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral. FAVE – Sección Ciencias Veterinarias 20, 1–9. https://doi.org/10.14409/favecv.v20i1.9978.CrossRefGoogle Scholar
Carvalho, AS, Silva, J, Ho, P, Teixeira, P, Malcata, FX and Gibbs, P (2004) Relevant factors for the preparation of freeze-dried lactic acid bacteria. International Dairy Journal 14, 835–847.CrossRefGoogle Scholar
Celik, OF and O'Sullivan, DJ (2013) Factors influencing the stability of freeze-dried stress-resilient and stress-sensitive strains of bifidobacteria. Journal of Dairy Science 96, 3506–3516.CrossRefGoogle ScholarPubMed
Chen, H, Huang, J, Shi, X, Li, Y and Liu, Y (2017) Effects of six substances on the growth and freeze-drying of Lactobacillus delbrueckii subsp. bulgaricus. Acta Scientiarum Polonorum Technologia Alimentaria 16, 403–412.Google ScholarPubMed
Chervaux, C, Ehrlich, SD and Maguin, E (2000) Physiological study of Lactobacillus delbrueckii subsp. bulgaricus strains in a novel chemically defined medium. Applied and Environmental Microbiology 66, 5306–5311.CrossRefGoogle Scholar
Curk, MC, Peladan, F and Hubert, JC (1993) Caractérisation biochimique des lactobacilles brassicoles. Le Lait 73, 215–231.CrossRefGoogle Scholar
Dąbrowska, A, Babij, K, Szołtysik, M and Chrzanowska, J (2017) Viability and growth promotion of starter and probiotic bacteria in yogurt supplemented with whey protein hydrolysate during refrigerated storage. Advances in Hygiene & Experimental Medicine/Postepy Higieny i Medycyny Doswiadczalnej 71, 952–959.Google ScholarPubMed
Degeest, B and De Vuyst, L (1999) Indication that the nitrogen source influences both amount and size of exopolysaccharides produced by Streptococcus thermophilus LY03 and modelling of the bacterial growth and exopolysaccharide production in a complex medium. Applied and Environmental Microbiology 65, 2863–2870.CrossRefGoogle Scholar
Dixon, MJL, Flint, SH, Palmer, JS, Love, R, Chabas, C and Beuger, AL (2018) The effect of calcium on biofilm formation in dairy wastewater. Water Practice & Technology 13, 400–409.CrossRefGoogle Scholar
Fenster, K, Freeburg, B, Hollard, C, Wong, C, Rønhave Laursen, R and Ouwehand, AC (2019) The production and delivery of probiotics: a review of a practical approach. Microorganisms 7(83), 1–17.CrossRefGoogle ScholarPubMed
Grześkowiak, Ł, Endo, A, Collado, MC, Pelliniemi, LJ, Beasley, S and Salminen, S (2013) The effect of growth media and physical treatments on the adhesion properties of canine probiotics. Journal of Applied Microbiology 115, 539–545.CrossRefGoogle ScholarPubMed
Gyawali, R, Oyeniran, A, Zimmerman, T, Aljaloud, SO, Krastanov, A and Ibrahim, SA (2020) A comparative study of extraction techniques for maximum recovery of β-galactosidase from the yogurt bacterium Lactobacillus delbrueckii ssp. bulgaricus. Journal of Dairy Research 87, 123–126.CrossRefGoogle ScholarPubMed
Hayek, SA and Ibrahim, SA (2013) Current limitations and challenges with lactic acid bacteria: a review. Food Science and Nutrition 4, 73–87.Google Scholar
Hayek, SA, Gyawali, R, Aljaloud, SO, Krastanov, A and Ibrahim, SA (2019) Cultivation media for lactic acid bacteria used in dairy products. Journal of Dairy Research 86, 490–502.CrossRefGoogle ScholarPubMed
Hossain, MN, Akter, A, Humayan, S, Mohanto, LC, Begum, S and Ahmed, MM (2020) Edible growth medium: a new window for probiotic research. Advances in Microbiology 10, 39–51.CrossRefGoogle Scholar
Isshiki, K and Azuma, K (1995) Microbial growth suppression in food using calcinated calcium. Japan Agricultural Research Quarterly 29, 269–274.Google Scholar
Klotz, S, Kuenz, A and Prüße, U (2017) Nutritional requirements and the impact of yeast extract on the d-lactic acid production by Sporolactobacillus inulinus. Green Chemistry 19, 4633–4641.CrossRefGoogle Scholar
Lamberti, C, Purrotti, M, Mazzoli, R, Fattori, P, Barello, C, Coïsson, JD, Guinta, C and Pessione, E (2011) ADI pathway and histidine decarboxylation are reciprocally regulated in Lactobacillus hilgardii ISE 5211: proteomic evidence. Amino Acids 41, 517–527.CrossRefGoogle ScholarPubMed
Li, C, Liu, LB and Liu, N (2012) Effects of carbon sources and lipids on freeze-drying survival of Lactobacillus bulgaricus in growth media. Annals of Microbiology 62, 949–956.CrossRefGoogle Scholar
Liu, W, Yu, J, Sun, Z, Song, Y, Wang, X, Wang, H, Wuren, T, Zha, M, Menghe, B and Heping, Z (2016) Relationships between functional genes in Lactobacillus delbrueckii ssp. bulgaricus isolates and phenotypic characteristics associated with fermentation time and flavor production in yogurt elucidated using multilocus sequence typing. Journal of Dairy Science 99, 89–103.CrossRefGoogle ScholarPubMed
Mani-Lopez, E, Palou, E and Lopez-Malo, A (2014) Probiotic viability and storage stability of yogurts and fermented milks prepared with several mixtures of lactic acid bacteria. Journal of Dairy Science 97, 2578–2590.CrossRefGoogle ScholarPubMed
Manzoor, A, Qazi, JI, ul Haq, I, Mukhtar, H and Rasool, A (2017) Significantly enhanced biomass production of a novel bio-therapeutic strain Lactobacillus plantarum (AS-14) by developing low-cost media cultivation strategy. Journal of Biological Engineering 11, 1–10.CrossRefGoogle ScholarPubMed
Norton, S, Lacroix, C and Vuillemard, JC (1994) Kinetic study of continuous whey permeate fermentation by immobilized Lactobacillus helveticus for lactic acid production. Enzyme and Microbial Technology 16, 457–466.CrossRefGoogle Scholar
Papizadeh, M, Rohani, M, Hosseini, SN, Shojaosadati, SA, Nahrevanian, H, Talebi, M and Pourshafie, MR (2020) Screening for efficient nitrogen sources for overproduction of the biomass of the functionally probiotic L. plantarum strain RPR42 in a cane molasses-based medium. AMB Express 10, 1–14.CrossRefGoogle Scholar
Petry, S, Furlan, S, Crepeau, MJ, Cerning, J and Desmazeaud, M (2000) Factors affecting exocellular polysaccharide production by Lactobacillus delbrueckii subsp. bulgaricus grown in a chemically defined medium. Applied and Environmental Microbiology 8, 3427–3431.CrossRefGoogle Scholar
Polak-Berecka, M, Waśko, A, Kordowska-Wiater, M, Podleśny, MARCIN, Targoński, Z and Kubik-Komar, A (2010) Optimization of medium composition for enhancing growth of Lactobacillus rhamnosus PEN using response surface methodology. Polish Journal of Microbiology 59, 113–118.CrossRefGoogle ScholarPubMed
Ponomarova, O, Gabrielli, N, Sévin, DC, Mülleder, M, Zirngibl, K, Bulyha, K, Andrejev, S, Kafkia, E, Typas, A, Sauer, U, Ralser, M and Patil, KR (2017) Yeast creates a niche for symbiotic lactic acid bacteria through nitrogen overflow. Cell Systems 5, 345–357.CrossRefGoogle ScholarPubMed
Saguir, FM and de Nadra, MCM (2007) Improvement of a chemically defined medium for the sustained growth of Lactobacillus plantarum: nutritional requirements. Current Microbiology 54, 414–418.CrossRefGoogle ScholarPubMed
Savijoki, K, Suokko, A, Palva, A and Varmanen, P (2006) New convenient defined media for [35S] methionine labelling and proteomic analyses of probiotic lactobacilli. Letters in Applied Microbiology 42, 202–209.CrossRefGoogle ScholarPubMed
Sieuwerts, S (2016) Microbial interactions in the yoghurt consortium: current status and product implications. SOJ Microbiology and Infectious Diseases 4, 1–5.CrossRefGoogle Scholar
Suzuki, K, Ishii, M, Li, M, Kawai, Y, Masuda, T and Oda, M (2014) Inhibitory eŠects of cysteine and serine on the growth of lactobacilli. Milk Science 63, 1–7.Google Scholar
Wright, CT and Klaenhammer, TR (1981) Calcium-induced alteration of cellular morphology affecting the resistance of Lactobacillus acidophilus to freezing. Applied and Environmental Microbiology 41, 807–815.CrossRefGoogle ScholarPubMed
Wright, CT and Klaenhammer, TR (1983) Survival of Lactobacillus bulgaricus during freezing and freeze-drying after growth in the presence of calcium. Journal of Food Science 48, 773–777.CrossRefGoogle Scholar
Zeidan, MB, Zara, G, Viti, C, Decorosi, F, Mannazzu, I, Budroni, M, Giovannetti, L and Zara, S (2014) l-Histidine inhibits biofilm formation and FLO11-associated phenotypes in Saccharomyces cerevisiae flor yeasts. PLoS One 9, e112141, 1–10.CrossRefGoogle Scholar
Supplementary material: PDF

Ayivi et al. supplementary material

Ayivi et al. supplementary material

Download Ayivi et al. supplementary material(PDF)
PDF 517.5 KB