| Peer-Reviewed

Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus

Received: 6 November 2020    Accepted: 21 November 2020    Published: 30 November 2020
Views:       Downloads:
Abstract

Decarboxylation of tyrosine through tyrosine decarboxylase enzyme produces tyramine which may represent a serious threat to public health, as it may cause severe toxicological effects. Intake of tyramine will invariably result in acute symptoms as it can rapidly gain access to the bloodstream and to various organs where it can act as a vasoactive agent through interaction with the sympathetic noradrenergic nerve terminals innervating cardiac and vascular smooth muscle tissues. This research is focusing on tyramine as one of the indicators of inappropriate food storage and processing conditions of milk products. In the current study, 25 dairy product samples were collected from local markets in Alexandria, Egypt, and were analyzed for bacterial contamination and prevalence of tyramine-producing bacteria by PCR using degenerate primers (DEC5/DEC3). While cream was the most contaminated dairy product, balady yogurt samples were the least contaminated ones. Different types of tyraminogenic bacteria have been isolated from the collected dairy products. Cream samples were contaminated with the widest variety of tyraminogenic bacteria among the isolated samples including Bacillus pumilis, Escherichia coli, Enterococcus faecium, and Proteus mirabilis. A total of 35 strains harboring tyrosine decarboxylase gene were detected with the identification of a novel tyramine-producing strain: Rummeliibacillus pycnus. These results indicate the promising application of degenerate primers (DEC5/DEC3) to detect tyramine production in dairy products, a goal that has been regarded as a challenge by manufacturers.

Published in International Journal of Microbiology and Biotechnology (Volume 5, Issue 4)
DOI 10.11648/j.ijmb.20200504.13
Page(s) 184-192
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Tyramine, Dairy Products, Tyrosine Decarboxylase, PCR, HPLC

References
[1] Ruiz-Capillas, C. and A. Herrero, (2019). Impact of Biogenic Amines on Food Quality and Safety. Foods 8, 62.
[2] Schirone, M., R. Tofalo, P. Visciano, A. Corsetti, and G. Suzzi (2012). Biogenic Amines in Italian Pecorino Cheese. Frontiers Microbiology 3, 171.
[3] Tamang, J., D. H. Shin, S. J. Jung, and S. W. Chae, (2016). Functional Properties of Microorganisms in Fermented Foods. Frontiers in Microbiology 7, 578.
[4] Marcobal, A., B. de Las Rivas, J. M. Landete, L. Tabera, and R. Muñoz (2012). Tyramine and Phenylethylamine Biosynthesis by Food Bacteria. Critical Review of Food Science and Nutrition 52, 448–467.
[5] McCabe-Sellers, B., C. G. Staggs, and M. L. Bogle (2006). Tyramine in Foods and Monoamine Oxidase Inhibitor Drugs: A Crossroad where Medicine, Nutrition, Pharmacy, and Food Industry Converge. Journal of Food Composition and Analysis 19, S58–S65.
[6] Bieck, P. R., and K. H. Antonin (1988). Oral Tyramine Pressor Tests the Safety of Monoamine Oxidase Inhibitor Drugs: Comparison of Brofaromine and Tranylcypromine in Healthy Subjects. Journal of Clinical Psycopharmacology 8, 237–245.
[7] Wunderlichová, L., L. Buňková, M. Koutný, P. Jančová, and F. Buňka (2014). Formation, Degradation, and Detoxification of Putrescine by Foodborne Bacteria: A Review. Comprehensive Reviews in Food Science and Food Safety 13, 1012-1030.
[8] Hanchi, H., W. Mottawea, K. Sebei, and R. Hammami (2018). The Genus Enterococcus: Between Probiotic Potential and Safety Concerns—An Update. Frontiers in Microbiology 9, 1791.
[9] Bover-Cid, S., M. Hugas, M. Izquierdo-Pulido, and M. C. Vidal-Carou (2000). Amino Acid-Decarboxylase Activity of Bacteria Isolated from Fermented Pork Sausages. International Journal of Food Microbiology 66, 185–189.
[10] Fernández, M., D. M. Linares, B. del Rio, V. Ladero, and M. A. Álvarez (2007). HPLC Quantification of Biogenic Amines in Cheeses: Correlation with PCR Detection of Tyramine-Producing Microorganisms. Journal of Dairy Research 74, 276–282.
[11] Russo, P., M. Fragasso, C. Berbegal, F. Grieco, G. Spano, and V. Capozzi, “Microorganisms Able to Produce Biogenic Amines and Factors Affecting Their Activity”, in Biogenic Amines in Food: Analysis, Occurrence and Toxicity, 1st Ed, B. Saad and R. Tofalo, Eds. London: Royal Society of Chemistry, 2019, pp. 18-40.
[12] Lucas, P., J. Landete, M. Coton, E. Coton, and A. Lonvaud-Funel (2003). The Tyrosine Decarboxylase Operon of Lactobacillus brevis IOEB 9809: Characterization and Conservation in Tyramine-Producing Bacteria. FEMS Microbiology letters 229, 65-71.
[13] J. W. Messer and C. H. Johnson, “Total viable counts. Pour plate technique”, in Encyclopedia of Food Microbiology, vol. III, R. K. Robinson, C. A. Batt and P. D. Patel, Eds. London: Academic Press, 2000, pp. 2154-2158.
[14] H. E. McKiernan and P. B. Danielson, “Molecular diagnostic applications in forensic science”, in Molecular diagnostics, 3rd Ed, G. P. Patrinos, Eds. New Jersey: Academic Press, 2017, pp. 371-394.
[15] Torriani, S., V. Gatto, S. Sembeni, R. Tofalo, G. Suzzi, N. Belletti, F. Gardini, and F. Bover Cid (2008). Rapid Detection and Quantification of Tyrosine Decarboxylase Gene (tdc) and its Expression in Gram-positive Bacteria Associated with Fermented Foods using PCR-based Methods. Journal of Food Protection 71, 93-101.
[16] Powers, T. W., B. A. Neely, Y. Shao, H. Tang, D. A. Troyer, A. S. Mehta, et al. (2014). MALDI Imaging Mass Spectrometry Profiling of N-Glycans in Formalin-Fixed Paraffin Embedded Clinical Tissue Blocks and Tissue Microarrays. PLoS One 9, e106255.
[17] Santos, T. M., R. V. Pereira, L. S. Caixeta, C. L. Guard, and R. C. Bicalho (2012). Microbial Diversity in Bovine Papillomatous Digital Dermatitis in Holstein Dairy Cows from Upstate New York. FEMS Microbiology Ecology 79, 518–529.
[18] Green, M., and J. Sambrook, “Analysis of DNA”, in Molecular Cloning: A Laboratory Manual, K. Janssen and J. Cuddihy, Eds. New York: Cold Spring Harbor Laboratory Press, 2012, pp. 82-85.
[19] Guo X, Li L, Chen Y, Xiao D, “Development of HPLC method for determination of the content of tyramine in rice wine” [Proceedings of the 2012 International Conference on Applied Biotechnology (ICAB 2012), Springer].
[20] da Silva, M. V., O. V. Pinho, I. Ferreira, L. Plestilová, and P. A. Gibbs (2002). Production of Histamine and Tyramine by Bacteria Isolated from Portuguese Vacuum-Packed Cold-Smoked Fish. Food Control 13, 457–461.
[21] Landete, J. M., I. Pardo, and S. Ferrer (2007). Tyramine and Phenylethylamine Production Among Lactic Acid Bacteria Isolated from Wine. International Journal of Food Microbiology 115, 364-368.
[22] Benkerroum, N. (2016). Biogenic Amines in Dairy Products: Origin, Incidence, and Control Means. Comprehensive Reviews in Food Science and Food Safety 15, 801-826.
[23] Deosarkar, S. S., C. D. Khedkar, and S. D. Kalyankar, “Cream: Types of cream” in Reference module in food & health (Encyclopedia of food & health), Volume 1, B. Caballero, P. Finglas, and F. Toldrá, Eds. London: Elsevier, 2016, pp. 331-337.
[24] Sarkar, S. 2015. Microbiological Considerations: Pasteurized Milk. International Journal of Dairy Science 10, 206-218.
[25] Verraes, C., G. Vlaemynck, S. Van Weyenberg, L. De Zutter, G. Daube, M. Sindic, et al. (2015). A Review of the Microbiological Hazards of Dairy Products Made from Raw Milk. International Dairy Journal 50, 32-44.
[26] Vrdoljak, J., V. Dobranić, I. Filipović, and N. Zdolec (2016). Microbiological Quality of Soft, Semi-Hard and Hard Cheeses During the Shelf-Life. Macedonian Veterinary Review 39, 59-64.
[27] Lenze, S., A. Wolfschoon-Pombo, K. Schrader, and U. Kulozik (2019) Effect of the Compositional Factors and Processing Conditions on the Creaming Reaction During Process Cheese Manufacturing. Food and Bioprocess Technology 12, 575-586.
[28] Phelan, J., J. Renaud, and P. Fox, “Some non-European cheese varieties” in Cheese: Chemistry, Physics and Microbiology, Volume 2, P. F. Fox, Eds. New York: Springer, 1993, pp. 421-465.
[29] Bover-Cid, S., and W. H. Holzapfel (1999). Improved Screening Procedure for Biogenic Amine Production by Lactic Acid Bacteria. International Journal of Food Microbiology 53, 33-41.
[30] Papageorgiou, M., D. Lambropoulou, C. Morrison, E. Kłodzińska, J. Namieśnik, and J. Płotka-Wasylka (2018). Literature Update of Analytical Methods for Biogenic Amines Determination in Food and Beverages. Trends in Analytical Chemistry 98, 128-142.
[31] Ladero, V., N. Martínez, M. C. Martín, M. Fernández, and M. A. Alvarez (2010). qPCR for Quantitative Detection of Tyramine-Producing Bacteria in Dairy Products. Food Research International 43, 289-295.
[32] Novella-Rodríguez, S., M. T. Veciana-Nogués, A, X. Roig-Sagués, A. J. Trujillo-Mesa, and M. C. Vidal-Carou (2004). Evaluation of Biogenic Amines and Microbial Counts Throughout the Ripening of Goat Cheeses from Pasteurized and Raw Milk. Journal of Dairy Research 71, 245-252.
[33] Ma, J. K., A. Raslan, S. Elbadry, W. El-Ghareeb, Z. Mulla, M. Bin-Jumah, et al (2020). Levels of Biogenic Amines in Cheese: Correlation to Microbial Status, Dietary Intakes, and Their Health Risk Assessment. Environmental Science and Pollution Research, 10401-10402.
[34] Lanciotti, R., F. Patrignani, L. Iucci, M. E. Guerzoni, G. Suzzi, N. Belletti, and F. Gardini (2007). Effects of Milk High-Pressure Homogenization on Biogenic Amine Accumulation During Ripening of Ovine and Bovine Italian Cheeses. Food Chemistry 104, 639-701.
[35] Elsanhoty, R. M., H. Mahrous, and A. G. Ghanaimy (2009). Chemical, Microbial Counts and Evaluation of Biogenic Amines During the Ripening of Egyptian Soft Domiati Cheese Made from Raw and Pasteurized Buffaloes Milk. International Journal of Dairy Science 4, 80-90.
[36] Martín-Platero, A. M., E. Valdivia, M. Maqueda, and M. Martínez-Bueno (2009). Characterization and Safety Evaluation of Enterococci Isolated from Spanish Goats' Milk Cheeses. International Journal of Food Microbiology 132, 24-32.
[37] Roig-Sagués, A. X., A. P. Molina, and M. Hernández-Herrero (2002). Histamine and Tyramine-Forming Microorganisms in Spanish Traditional Cheeses. European Food Research and Technology 215, 96-100.
[38] Suzzi, G., M. Caruso, F. Gardini, A. Lombardi, L. Vannini, M. Guerzoni et al. (2000). A Survey of the Enterococci Isolated from an Artisanal Italian Goat's Cheese (Semicotto Caprino). Journal of Applied Microbiology 89, 267-274.
[39] Shalaby, M. A., M. A. Kassem, O. Morsy, and N. M. Mohamed (2020). Anti-tyramine Potential of Lactobacillus rhamnosus (LGG®) in Cheese Samples Collected from Alexandria, Egypt. Food Biotechnology 34, 243-261.
Cite This Article
  • APA Style

    Omnia Morsy, Mervat Amin Kassem, Abeer Elsayed Abd El-Wahab, Nelly Mostafa Mohamed. (2020). Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus. International Journal of Microbiology and Biotechnology, 5(4), 184-192. https://doi.org/10.11648/j.ijmb.20200504.13

    Copy | Download

    ACS Style

    Omnia Morsy; Mervat Amin Kassem; Abeer Elsayed Abd El-Wahab; Nelly Mostafa Mohamed. Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus. Int. J. Microbiol. Biotechnol. 2020, 5(4), 184-192. doi: 10.11648/j.ijmb.20200504.13

    Copy | Download

    AMA Style

    Omnia Morsy, Mervat Amin Kassem, Abeer Elsayed Abd El-Wahab, Nelly Mostafa Mohamed. Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus. Int J Microbiol Biotechnol. 2020;5(4):184-192. doi: 10.11648/j.ijmb.20200504.13

    Copy | Download

  • @article{10.11648/j.ijmb.20200504.13,
      author = {Omnia Morsy and Mervat Amin Kassem and Abeer Elsayed Abd El-Wahab and Nelly Mostafa Mohamed},
      title = {Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus},
      journal = {International Journal of Microbiology and Biotechnology},
      volume = {5},
      number = {4},
      pages = {184-192},
      doi = {10.11648/j.ijmb.20200504.13},
      url = {https://doi.org/10.11648/j.ijmb.20200504.13},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ijmb.20200504.13},
      abstract = {Decarboxylation of tyrosine through tyrosine decarboxylase enzyme produces tyramine which may represent a serious threat to public health, as it may cause severe toxicological effects. Intake of tyramine will invariably result in acute symptoms as it can rapidly gain access to the bloodstream and to various organs where it can act as a vasoactive agent through interaction with the sympathetic noradrenergic nerve terminals innervating cardiac and vascular smooth muscle tissues. This research is focusing on tyramine as one of the indicators of inappropriate food storage and processing conditions of milk products. In the current study, 25 dairy product samples were collected from local markets in Alexandria, Egypt, and were analyzed for bacterial contamination and prevalence of tyramine-producing bacteria by PCR using degenerate primers (DEC5/DEC3). While cream was the most contaminated dairy product, balady yogurt samples were the least contaminated ones. Different types of tyraminogenic bacteria have been isolated from the collected dairy products. Cream samples were contaminated with the widest variety of tyraminogenic bacteria among the isolated samples including Bacillus pumilis, Escherichia coli, Enterococcus faecium, and Proteus mirabilis. A total of 35 strains harboring tyrosine decarboxylase gene were detected with the identification of a novel tyramine-producing strain: Rummeliibacillus pycnus. These results indicate the promising application of degenerate primers (DEC5/DEC3) to detect tyramine production in dairy products, a goal that has been regarded as a challenge by manufacturers.},
     year = {2020}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Isolation and Molecular Identification of a Novel Tyramine-producing Bacterium, Rummeliibacillus pycnus
    AU  - Omnia Morsy
    AU  - Mervat Amin Kassem
    AU  - Abeer Elsayed Abd El-Wahab
    AU  - Nelly Mostafa Mohamed
    Y1  - 2020/11/30
    PY  - 2020
    N1  - https://doi.org/10.11648/j.ijmb.20200504.13
    DO  - 10.11648/j.ijmb.20200504.13
    T2  - International Journal of Microbiology and Biotechnology
    JF  - International Journal of Microbiology and Biotechnology
    JO  - International Journal of Microbiology and Biotechnology
    SP  - 184
    EP  - 192
    PB  - Science Publishing Group
    SN  - 2578-9686
    UR  - https://doi.org/10.11648/j.ijmb.20200504.13
    AB  - Decarboxylation of tyrosine through tyrosine decarboxylase enzyme produces tyramine which may represent a serious threat to public health, as it may cause severe toxicological effects. Intake of tyramine will invariably result in acute symptoms as it can rapidly gain access to the bloodstream and to various organs where it can act as a vasoactive agent through interaction with the sympathetic noradrenergic nerve terminals innervating cardiac and vascular smooth muscle tissues. This research is focusing on tyramine as one of the indicators of inappropriate food storage and processing conditions of milk products. In the current study, 25 dairy product samples were collected from local markets in Alexandria, Egypt, and were analyzed for bacterial contamination and prevalence of tyramine-producing bacteria by PCR using degenerate primers (DEC5/DEC3). While cream was the most contaminated dairy product, balady yogurt samples were the least contaminated ones. Different types of tyraminogenic bacteria have been isolated from the collected dairy products. Cream samples were contaminated with the widest variety of tyraminogenic bacteria among the isolated samples including Bacillus pumilis, Escherichia coli, Enterococcus faecium, and Proteus mirabilis. A total of 35 strains harboring tyrosine decarboxylase gene were detected with the identification of a novel tyramine-producing strain: Rummeliibacillus pycnus. These results indicate the promising application of degenerate primers (DEC5/DEC3) to detect tyramine production in dairy products, a goal that has been regarded as a challenge by manufacturers.
    VL  - 5
    IS  - 4
    ER  - 

    Copy | Download

Author Information
  • Department of Medical Biotechnology, Institute of Genetic Engineering, City of Scientific Research and Technological Applications, Alexandria, Egypt

  • Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, Alexandria, Egypt

  • Department of Medical Biotechnology, Institute of Genetic Engineering, City of Scientific Research and Technological Applications, Alexandria, Egypt

  • Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, Alexandria, Egypt

  • Sections