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Communication

Antimicrobial Properties of Magnesium Open Opportunities to Develop Healthier Food

1
Department of Food Sciences, Institute for Postharvest Technology and Food Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion 7528809, Israel
2
The Robert H. Smith Faculty of Agriculture, Food and Environment, Institute of Biochemistry, Food Science and Nutrition, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
*
Author to whom correspondence should be addressed.
Nutrients 2019, 11(10), 2363; https://doi.org/10.3390/nu11102363
Received: 29 July 2019 / Revised: 15 September 2019 / Accepted: 21 September 2019 / Published: 3 October 2019
(This article belongs to the Special Issue Dietary Trace Minerals)

Abstract

:
Magnesium is a vital mineral that takes part in hundreds of enzymatic reactions in the human body. In the past several years, new information emerged in regard to the antibacterial effect of magnesium. Here we elaborate on the recent knowledge of its antibacterial effect with emphasis on its ability to impair bacterial adherence and formation complex community of bacterial cells called biofilm. We further talk about its ability to impair biofilm formation in milk that provides opportunity for developing safer and qualitative dairy products. Finally, we describe the pronounced advantages of enrichment of food with magnesium ions, which result in healthier and more efficient food products.

1. Introduction

Magnesium represents an essential element for life and is ubiquitously found in all organisms. This important cation plays crucial roles as an enzymatic co-factor, as well as it is involved in cellular signaling, and in stabilizing cellular components [1,2]. It is not surprising that magnesium salts are typically associated with positive effects on microbial cells. However, it appears that at elevated doses, for instance at milimolar concentrations, magnesium ions become harmful for prokaryotic cell and therefore may negatively affect important cellular processes [3,4,5,6,7]. Although, some progress has been made in investigating the effect of magnesium ions in different microorganisms, it is still not clear how these vital ions affect the cellular processes in microbial cell. Moreover, the mode of antimicrobial action of magnesium ions remains largely unknown. In the past several years, more information emerged concerning the effect of magnesium on bacterial cells. Consequently, in this mini-review, we summarize recent advances in understanding the antimicrobial properties of magnesium ions with an emphasis on their effect on biofilm formation, which became the biggest microbiological problem in clinical as well as industrial settings. We further discuss the antimicrobial potential of magnesium ions in developing novel approaches towards improving food safety and quality. Finally, we describe new perspectives in developing healthier food for human consumption by its enrichment based on magnesium ions.

2. The Antimicrobial Properties of Magnesium

Historically, back in 1915, Professor Pierre Delbet was looking for a solution to cleanse wounds that would replace the traditional antiseptics that damage tissues. After testing several solutions, he found MgCl2 solution to be most effective as it had two main advantages—it was not harmful for the tissue and it highly increased leucocyte activity and phagocytosis. Later, he found this solution to be an efficient therapy for various diseases, including diseases related to microorganisms [8]. In the past several years, new interest on this cation arose due to its antimicrobial properties. In several studies, antibiotic activity in the presence of Mg2+ ions was found to be more efficient [9,10]. It has been hypothesized that the divalent ions affect the membranes of bacterial cells. One study suggested that the curvature of the bacterial membrane is affected, and eventually the bacteria become more vulnerable, and the antibiotics are more efficient [11]. A different study showed that these cations permeabilize the membranes and cause them to be leakier [5]. Other studies tested the potential antimicrobial effect of coating different surfaces with magnesium or magnesium compounds. These surfaces were found as effective in prevention of bacteria adherence as well as biofilm formation. Some of these compounds were suggested to disrupt the membrane potential, again strengthening the idea that magnesium permeabilizes membranes and eventually cause the bacteria to be more sensitive [6,12,13,14]. Moreover, metal oxide nanoparticles of MgO were tested as antibacterial agents as well [3,6]. Indeed, these particles were found to be effective against yeast and planktonic bacteria as well as against biofilms [3]. In addition, these nanoparticles were found to be of low cytotoxicity and relatively safe. Since biofilm formation is considered as a major problem in the food industry as well as in the biomedical field, a lot of effort is put into dealing with this phenomenon [15,16]. Therefore, the effect of magnesium ions was also tested recently as a potential solution for the biofilm problem.

2.1. The Effect of Magnesium on Bacterial Survival and Biofilm Formation

Biofilms are highly structured multicellular communities [17,18,19]. Biofilm formation is a multistage process in which bacterial cells adhere to a surface and/or to each other through production of an extracellular matrix that is typically composed of exopolymeric substances (EPS) such as polysaccharides, proteins, and nucleic acids, which surround and may protect the enclosed bacteria [19,20,21]. They form highly structured multicellular communities that are capable of coordinated and collective behavior [17,18,22]. Bacterial cells in biofilms are characterized by increased resistance to unfavorable environmental conditions, antimicrobial agents, and cleaning chemicals [19,23,24]. It appears that the major source of the contamination of food products is often associated with biofilms on the surfaces of food processing equipment [15,25,26]. Therefore, biofilm formation is considered as a major problem in the food industry [15,26,27].
Several approaches were suggested to deal with biofilm formation in the food industry [15,26]. Environmental factors such as electrolyte concentrations and medium composition were shown to have important impact on biofilm formation [28]. Divalent cations can influence biofilm formation directly through their effect on electro-static interactions and indirectly via physiology-dependent attachment processes by acting as important cellular cations and enzyme cofactors [28,29,30,31]. Due to its potentially important role, the effect of Mg2+ ions on biofilm formation has been tested. These ions are crucial for the physiology of bacterial cells, although their excess can be harmful for them. Bacterial cells maintain the tolerable concentrations of Mg2+ ions by influx and efflux strategies based on their availability. Bacteria overcome limitations in those ions or respond to excess levels, and this helps to maintain the metal homeostasis within the cell. It appears that Mg2+ ions are vital for membrane stabilization and function as a cofactor for diverse enzymatic reactions. Bacteria achieve Mg2+ homeostasis by regulating the Mg2+ transporters and sensors that coordinate the influx and efflux of Mg2+ from the bacterial cell. The Gram-negative bacterium Salmonella enterica serovar Typhimurium is one of the best-understood models for explaining the Mg2+ homeostasis [32,33]. In Staphylococcus aureus, Mg2+ was shown to increase the rigidity of cell wall by binding to teichoic acids (TA). TA, bind the positively charged Mg2+ ions to mitigate the electrostatic repulsive interactions between the negatively charged neighboring phosphates. In addition, the Mg2+ ions start a signaling cascade, which results in expression of biofilm related genes [34]. Furthermore, studies have shown that Mg2+ ions have varying effects on bacterial adhesion and biofilm formation [4,28,35,36,37] (Table 1), which could be explained by differences in bacterial species and Mg2+ concentrations used in the various studies. Since EPS possesses an anionic nature, it was proposed previously that certain Mg2+ concentration might contribute to an increase in exopolysaccharide (EPS) production and biofilm stabilization [38]. It was also reported that Mg2+ limitation is an important environmental trigger of Pseudomonas aeruginosa biofilm development [39]. However, it was found that biofilm formation decreased with increasing concentration of Mg2+ in Enterobacter cloacae [40]. Moreover, another recent study demonstrated how Mg2+ ions affected Bacillus subtilis biofilm formation by down-regulating the expression of extracellular matrix genes by more than 10-fold [4]. Taken together, the literatures up to now suggest that, in low concentrations, Mg2+ ions seem to induce adherence of bacteria to surfaces and subsequent biofilm formation, while higher concentrations seem to reduce the biofilm formation.
Thus, magnesium ions have a reasonable potential in affecting the food associated biofilm formation and by this preventing food spoilage and losses in the food industry. The exact mechanism as to how exactly the magnesium ions operate and delay biofilm formation remains unclear, yet several suggestions arise [5,11,41,42] (Figure 1). They could directly interact with the membrane and in some way prevent biofilm formation. Alternatively, they could also directly or indirectly influence the regulation of biofilm formation and delay biofilm formation. Due to the promising results obtained with magnesium ions in prevention of biofilm formation, the effect of Mg2+ ions on biofilm formation in the context of food matrices has also been recently studied.

2.2. The Effect of Magnesium on Microbiological and Technological Properties of Milk

Milk is highly nutritious as it contains abundant water and nutrients, such as lactose, proteins, and lipids, and has a nearly neutral pH. This makes it an ideal medium for the growth of different microorganisms. Since microorganisms in milk may hold spoilage and health risks, milk manufacturing is subject to extremely stringent regulations. These regulations include pasteurization at high temperatures, which kills most bacteria, and milk storage at low temperatures, which limits the growth of many bacteria. It has been shown that in several Bacillus strains, milk triggers the formation of biofilm [43], and this might make the bacteria more resistant to pasteurization. A recent study has shown that supplementation of milk by 5mM MgCl2 and above is capable of impairment of biofilm formation [44]. The impairment of the biofilm eventually results in about a two-log reduction in survival rate of bacterial cells once exposed to heat-pasteurization [44]. Accordingly, enrichment of milk and its products with magnesium would eventually result in safer dairy products as well as this would enable a longer shelf life of the products. In addition, enrichment of food with Mg2+ ions may also influence its technological properties as well [44,45]. It was also suggested that in the presence of Mg2+ ions the milk clotting starts significantly earlier, and the obtained curd is notably firmer [44]. This finding indicates that the curdling process appears to be improved in the presence of Mg2+ ions; i.e., in order to obtain cheeses in a desired hardness, the curdling process in the presence of Mg2+ ions is shorter. In another study in which magnesium lactate was added to fat free milk to produce yogurts, the hardness of the yogurts was increased [45]. Moreover, it was also demonstrated that fortified cheeses with Mg2+ ions had higher protein quantity [44]. Therefore, enrichment of milk with magnesium not only makes the dairy products healthier, but also improves their technological properties and increases potential availability of this essential mineral for absorption from the magnesium-enriched products. Taking into account also the antimicrobial effect of magnesium, which results in longer shelf life, enrichment of food with magnesium would result in healthier and inexpensive food (Figure 2).

3. The Existing Need for the Enrichment of Food with Magnesium

Magnesium is a vital mineral that takes part in hundreds of enzymatic activities, and consumption of a sufficient amount magnesium is highly important for human health. This vital cation also plays important roles in the physiological functioning of the brain, heart, and skeletal muscles and has anti-inflammatory properties. Low levels of magnesium are associated with a wide range of diseases such as migraine, Alzheimer’s disease, hypertension, insulin resistance, pre-eclampsia and cardiovascular diseases [1,46]. The recommended daily allowance of Mg2+ according to the US Food and Nutrition Board is 420 mg for men and 320 mg for women. However, it is estimated that most people do not consume the recommended daily allowance of magnesium [2,47,48], and about 10% to 30% of a given population are in a condition of Mg2+ deficiency (MGD) [49]. MGD as a result of low intake of magnesium could potentially increase risks for various diseases. Hence, finding new means to supply magnesium to humans is essential. According to [44] an evaluation of the bioavailability potential of magnesium in milk enriched with 5–10 mM MgCl2, is ~75–90 mg/L. Hence, one needs to consume over 3.5 L of fortified milk to reach the lower limit of the recommended daily allowance. Nevertheless, consumption of milk fortified with Mg2+ will enable to increase the daily consumption of magnesium. Enrichment of food products with magnesium may provide a novel mean to deliver this important mineral to humans and other mammals [50].

4. Discussion

As mentioned above, magnesium plays a vital role as a cofactor in numerous enzymatic reactions in the cell [1,2,51]. These include phosphorylation and catalytic reactions, carbohydrate metabolism, lipid metabolism, as well as protein and nucleic acid synthesis. It also plays a role in the active transport of calcium and potassium ions across cell membranes. This vital cation is highly important for the human health [2,52,53]. Here, we elaborated on magnesium in the aspect of its antimicrobial effects. At high concentrations, magnesium ions decrease adherence of bacteria to surfaces and impair biofilm assembly. This makes the bacterial cells more sensitive to heat treatments. In dairy products, lower concentrations (~5mM) are required, maybe due to additional antimicrobial molecules found in the milk. Therefore, addition of magnesium ions to food and especially to dairy products would result in safer food with a longer shelf-life. Moreover, the magnesium ions also improve the technological properties of the products, which eventually results in cheaper production costs. Most importantly, enrichment of food products with magnesium ions would enable a new efficient source of consumption of this important mineral.

5. Conclusions

Magnesium is a vital mineral, which is not consumed to a sufficient quantity. Addition of magnesium to food matrices, for instance, to dairy products has several added benefits. First, the antibacterial effect of Mg2+ ions enables development of the safer and healthier food. Second, improvements in the technological properties of the magnesium supplemented food enables shorter production time and high protein content of the food products. Finally, enrichment of the food with Mg2+ ions provides a new source for the delivery of this vital mineral to humans.

Author Contributions

K.D. and M.S. originated the draft. K.D. prepared the illustrations for the manuscript. M.S. and K.D. developed the section on the antimicrobial and technological properties of magnesium ions. K.D. and R.R. discussed and elaborated on the role of magnesium in human health. All authors approved the final version of the manuscript.

Funding

This work was partially funded by the Nitzan Grant No. 4210342 of the Chief Scientist of the Ministry of Agriculture and Rural Development (Israel). This work was also supported by the Copia Agro & Food Technologies Fund, grant number 4210360.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Glasdam, S.M.; Glasdam, S.; Peters, G.H. The Importance of Magnesium in the Human Body: A Systematic Literature Review. Adv. Clin. Chem. 2016, 73, 169–193. [Google Scholar] [CrossRef] [PubMed]
  2. De Baaij, J.H.; Hoenderop, J.G.; Bindels, R.J. Magnesium in man: Implications for health and disease. Physiol. Rev. 2015, 95, 1–46. [Google Scholar] [CrossRef] [PubMed]
  3. Nguyen, N.T.; Grelling, N.; Wetteland, C.L.; Rosario, R.; Liu, H. Antimicrobial Activities and Mechanisms of Magnesium Oxide Nanoparticles (nMgO) against Pathogenic Bacteria, Yeasts, and Biofilms. Sci. Rep. 2018, 8, 16260. [Google Scholar] [CrossRef]
  4. Oknin, H.; Steinberg, D.; Shemesh, M. Magnesium ions mitigate biofilm formation of Bacillus species via downregulation of matrix genes expression. Front. Microbiol. 2015, 6, 907. [Google Scholar] [CrossRef] [PubMed]
  5. Xie, Y.; Yang, L. Calcium and Magnesium Ions Are Membrane-Active against Stationary-Phase Staphylococcus aureus with High Specificity. Sci. Rep. 2016, 6, 20628. [Google Scholar] [CrossRef]
  6. Hayat, S.; Muzammil, S.; Rasool, M.H.; Nisar, Z.; Hussain, S.Z.; Sabri, A.N.; Jamil, S. In vitro antibiofilm and anti-Adhesion effects of magnesium oxide nanoparticles against antibiotic resistant bacteria. Microbiol. Immunol. 2018, 62, 211–220. [Google Scholar] [CrossRef] [PubMed]
  7. Oyarzua Alarcon, P.; Sossa, K.; Contreras, D.; Urrutia, H.; Nocker, A. Antimicrobial properties of magnesium chloride at low pH in the presence of anionic bases. Magnes. Res. 2014, 27, 57–68. [Google Scholar] [CrossRef] [PubMed]
  8. Delbet, P. Politique Préventive du Cancer: Cytophylaxie; Denoël: Paris, France, 1944. [Google Scholar]
  9. Houlihan, A.J.; Russell, J.B. The effect of calcium and magnesium on the activity of bovicin HC5 and nisin. Curr. Microbiol. 2006, 53, 365–369. [Google Scholar] [CrossRef]
  10. Khan, F.; Patoare, Y.; Karim, P.; Rayhan, I.; Quadir, M.A.; Hasnat, A. Effect of magnesium and zinc on antimicrobial activities of some antibiotics. Pak. J. Pharm. Sci. 2005, 18, 57–61. [Google Scholar]
  11. Som, A.; Yang, L.; Wong, G.C.; Tew, G.N. Divalent metal ion triggered activity of a synthetic antimicrobial in cardiolipin membranes. J. Am. Chem. Soc. 2009, 131, 15102–15103. [Google Scholar] [CrossRef]
  12. Zaatreh, S.; Haffner, D.; Strauss, M.; Dauben, T.; Zamponi, C.; Mittelmeier, W.; Quandt, E.; Kreikemeyer, B.; Bader, R. Thin magnesium layer confirmed as an antibacterial and biocompatible implant coating in a coculture model. Mol. Med. Rep. 2017, 15, 1624–1630. [Google Scholar] [CrossRef] [PubMed]
  13. Zaatreh, S.; Haffner, D.; Strauss, M.; Wegner, K.; Warkentin, M.; Lurtz, C.; Zamponi, C.; Mittelmeier, W.; Kreikemeyer, B.; Willumeit-Romer, R.; et al. Fast corroding, thin magnesium coating displays antibacterial effects and low cytotoxicity. Biofouling 2017, 33, 294–305. [Google Scholar] [CrossRef] [PubMed]
  14. Lellouche, J.; Kahana, E.; Elias, S.; Gedanken, A.; Banin, E. Antibiofilm activity of nanosized magnesium fluoride. Biomaterials 2009, 30, 5969–5978. [Google Scholar] [CrossRef] [PubMed]
  15. Alvarez-Ordonez, A.; Coughlan, L.M.; Briandet, R.; Cotter, P.D. Biofilms in Food Processing Environments: Challenges and Opportunities. Ann. Rev. Food Sci. Technol. 2019, 10, 173–195. [Google Scholar] [CrossRef] [PubMed]
  16. Bridier, A.; Sanchez-Vizuete, P.; Guilbaud, M.; Piard, J.C.; Naitali, M.; Briandet, R. Biofilm-Associated persistence of food-Borne pathogens. Food Microbiol. 2015, 45, 167–178. [Google Scholar] [CrossRef]
  17. Hall-Stoodley, L.; Costerton, J.W.; Stoodley, P. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004, 2, 95–108. [Google Scholar] [CrossRef] [PubMed]
  18. Kolter, R.; Greenberg, E.P. Microbial sciences: The superficial life of microbes. Nature 2006, 441, 300–302. [Google Scholar] [CrossRef]
  19. Saxena, P.; Joshi, Y.; Rawat, K.; Bisht, R. Biofilms: Architecture, Resistance, Quorum Sensing and Control Mechanisms. Indian J. Microbiol. 2019, 59, 3–12. [Google Scholar] [CrossRef]
  20. Allison, D.G. The biofilm matrix. Biofouling 2003, 19, 139–150. [Google Scholar] [CrossRef]
  21. Shemesh, M.; Kolter, R.; Losick, R. The biocide chlorine dioxide stimulates biofilm formation in Bacillus subtilis by activation of the histidine kinase KinC. J. Bacteriol. 2010, 192, 6352–6356. [Google Scholar] [CrossRef]
  22. Kalamara, M.; Spacapan, M.; Mandic-Mulec, I.; Stanley-Wall, N.R. Social behaviours by Bacillus subtilis: Quorum sensing, kin discrimination and beyond. Mol. Microbiol. 2018, 110, 863–878. [Google Scholar] [CrossRef] [PubMed]
  23. Checinska, A.; Paszczynski, A.; Burbank, M. Bacillus and other spore-Forming genera: Variations in responses and mechanisms for survival. Ann. Rev. Food Sci. Technol. 2015, 6, 351–369. [Google Scholar] [CrossRef] [PubMed]
  24. Shaheen, R.; Svensson, B.; Andersson, M.A.; Christiansson, A.; Salkinoja-Salonen, M. Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks. Food Microbiol. 2010, 27, 347–355. [Google Scholar] [CrossRef] [PubMed]
  25. Flint, S.H.; Bremer, P.J.; Brooks, J.D. Biofilms in dairy manufacturing plant—description, current concerns and methods of control. Biofouling 1997, 11, 81–97. [Google Scholar] [CrossRef]
  26. Yuan, L.; Hansen, M.F.; Roder, H.L.; Wang, N.; Burmolle, M.; He, G. Mixed-Species biofilms in the food industry: Current knowledge and novel control strategies. Crit. Rev. Food Sci. Nutr. 2019, 1–17. [Google Scholar] [CrossRef] [PubMed]
  27. Maukonen, J.; Matto, J.; Wirtanen, G.; Raaska, L.; Mattila-Sandholm, T.; Saarela, M. Methodologies for the characterization of microbes in industrial environments: A review. J. Ind. Microbiol. Biotechnol. 2003, 30, 327–356. [Google Scholar] [CrossRef] [PubMed]
  28. Song, B.; Leff, L.G. Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol. Res. 2006, 161, 355–361. [Google Scholar] [CrossRef]
  29. Fletcher, M. Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium-Substratum separation distance. J. Bacteriol. 1988, 170, 2027–2030. [Google Scholar] [CrossRef]
  30. Mhatre, E.; Sundaram, A.; Holscher, T.; Muhlstadt, M.; Bossert, J.; Kovacs, A.T. Presence of Calcium Lowers the Expansion of Bacillus subtilis Colony Biofilms. Microorganisms 2017, 5. [Google Scholar] [CrossRef] [PubMed]
  31. Polyudova, T.V.; Eroshenko, D.V.; Korobov, V.P. Plasma, serum, albumin, and divalent metal ions inhibit the adhesion and the biofilm formation of Cutibacterium (Propionibacterium) acnes. AIMS Microbiol. 2018, 4, 165–172. [Google Scholar] [CrossRef]
  32. Cromie, M.J.; Shi, Y.; Latifi, T.; Groisman, E.A. An RNA sensor for intracellular Mg2+. Cell 2006, 125, 71–84. [Google Scholar] [CrossRef] [PubMed]
  33. Groisman, E.A.; Hollands, K.; Kriner, M.A.; Lee, E.J.; Park, S.Y.; Pontes, M.H. Bacterial Mg2+ homeostasis, transport, and virulence. Ann. Rev. Genet. 2013, 47, 625–646. [Google Scholar] [CrossRef] [PubMed]
  34. Garcia-Betancur, J.C.; Goni-Moreno, A.; Horger, T.; Schott, M.; Sharan, M.; Eikmeier, J.; Wohlmuth, B.; Zernecke, A.; Ohlsen, K.; Kuttler, C.; et al. Cell differentiation defines acute and chronic infection cell types in Staphylococcus aureus. eLife 2017, 6. [Google Scholar] [CrossRef] [PubMed]
  35. Dunne, W.M., Jr.; Burd, E.M. The effects of magnesium, calcium, EDTA, and pH on the in vitro adhesion of Staphylococcus epidermidis to plastic. Microbiol. Immunol. 1992, 36, 1019–1027. [Google Scholar] [CrossRef] [PubMed]
  36. Marcus, H.; Austria, A.; Baker, N.R. Adherence of Pseudomonas aeruginosa to tracheal epithelium. Infect. Immun. 1989, 57, 1050–1053. [Google Scholar]
  37. Tamura, G.S.; Kuypers, J.M.; Smith, S.; Raff, H.; Rubens, C.E. Adherence of group B streptococci to cultured epithelial cells: Roles of environmental factors and bacterial surface components. Infect. Immun. 1994, 62, 2450–2458. [Google Scholar]
  38. Costerton, J.W.; Lewandowski, Z.; Caldwell, D.E.; Korber, D.R.; Lappin-Scott, H.M. Microbial biofilms. Ann. Rev. Microbiol. 1995, 49, 711–745. [Google Scholar] [CrossRef]
  39. Mulcahy, H.; Lewenza, S. Magnesium limitation is an environmental trigger of the Pseudomonas aeruginosa biofilm lifestyle. PLoS ONE 2011, 6, e23307. [Google Scholar] [CrossRef]
  40. Zhou, G.; Li, L.J.; Shi, Q.S.; Ouyang, Y.S.; Chen, Y.B.; Hu, W.F. Efficacy of metal ions and isothiazolones in inhibiting Enterobacter cloacae BF-17 biofilm formation. Can. J. Microbiol. 2014, 60, 5–14. [Google Scholar] [CrossRef]
  41. Gao, X.; Mukherjee, S.; Matthews, P.M.; Hammad, L.A.; Kearns, D.B.; Dann, C.E. Functional characterization of core components of the Bacillus subtilis cyclic-di-GMP signaling pathway. J. Bacteriol. 2013, 195, 4782–4792. [Google Scholar] [CrossRef]
  42. Chen, Y.; Chai, Y.; Guo, J.H.; Losick, R. Evidence for cyclic Di-GMP-Mediated signaling in Bacillus subtilis. J. Bacteriol. 2012, 194, 5080–5090. [Google Scholar] [CrossRef] [PubMed]
  43. Pasvolsky, R.; Zakin, V.; Ostrova, I.; Shemesh, M. Butyric acid released during milk lipolysis triggers biofilm formation of Bacillus species. Int. J. Food Microbiol. 2014, 181, 19–27. [Google Scholar] [CrossRef]
  44. Ben-Ishay, N.; Oknin, H.; Steinberg, D.; Berkovich, Z.; Reifen, R.; Shemesh, M. Enrichment of milk with magnesium provides healthier and safer dairy products. NPJ Biofilms Microb. 2017, 3, 24. [Google Scholar] [CrossRef] [PubMed]
  45. Szajnar, K.; Znamirowska, A.; Kalicka, D.; Kuzniar, P.; Najgebauer-Lejko, D. Quality of yogurt fortified with magnesium lactate. Acta Sci. Pol. Technol. Aliment. 2018, 17, 247–255. [Google Scholar] [CrossRef] [PubMed]
  46. Grober, U.; Schmidt, J.; Kisters, K. Magnesium in Prevention and Therapy. Nutrients 2015, 7, 8199–8226. [Google Scholar] [CrossRef][Green Version]
  47. King, D.E.; Mainous, A.G., III; Geesey, M.E.; Woolson, R.F. Dietary magnesium and C-Reactive protein levels. J. Am. Coll. Nutr. 2005, 24, 166–171. [Google Scholar] [CrossRef]
  48. Razzaque, M.S. Magnesium: Are We Consuming Enough? Nutrients 2018, 10, 1863. [Google Scholar] [CrossRef]
  49. Costello, R.B.; Elin, R.J.; Rosanoff, A.; Wallace, T.C.; Guerrero-Romero, F.; Hruby, A.; Lutsey, P.L.; Nielsen, F.H.; Rodriguez-Moran, M.; Song, Y. Perspective: The Case for an Evidence-Based Reference Interval for Serum Magnesium: The Time Has Come. Adv. Nutr. 2016, 15, 977–993. [Google Scholar] [CrossRef]
  50. Sacco, J.E.; Tarasuk, V. Discretionary addition of vitamins and minerals to foods: Implications for healthy eating. Eur. J. Clin. Nutr. 2011, 65, 313–320. [Google Scholar] [CrossRef]
  51. Uwitonze, A.M.; Razzaque, M.S. Role of Magnesium in Vitamin D Activation and Function. J. Am. Osteopath. Assoc. 2018, 118, 181–189. [Google Scholar] [CrossRef][Green Version]
  52. Gant, C.M.; Soedamah-Muthu, S.S.; Binnenmars, S.H.; Bakker, S.J.L.; Navis, G.; Laverman, G.D. Higher Dietary Magnesium Intake and Higher Magnesium Status Are Associated with Lower Prevalence of Coronary Heart Disease in Patients with Type 2 Diabetes. Nutrients 2018, 10, 307. [Google Scholar] [CrossRef] [PubMed]
  53. DiNicolantonio, J.J.; Liu, J.; O’Keefe, J.H. Magnesium for the prevention and treatment of cardiovascular disease. Open Heart 2018, 5, e000775. [Google Scholar] [CrossRef] [PubMed][Green Version]
Figure 1. Possible mechanisms for the influence of Mg2+ ions on biofilm formation. A: Mg2+ can affect the membranes curvature, which results in a more sensitive bacterial population. B: Elevation of c-di-GMP levels leads to inhibition of the swarming motility and increased biofilm formation. The activity of PdeH, the enzyme that degrades c-di-GMP, is Mg2+ dependent. Therefore, Mg2+ ions could possibly enhance c-di-GMP degradation and hence decrease biofilm formation that results in heat sensitive bacteria. C: A third possible explanation is that the Mg2+ ions directly regulate the pathway leading to biofilm formation, which would again result in heat sensitive bacteria.
Figure 1. Possible mechanisms for the influence of Mg2+ ions on biofilm formation. A: Mg2+ can affect the membranes curvature, which results in a more sensitive bacterial population. B: Elevation of c-di-GMP levels leads to inhibition of the swarming motility and increased biofilm formation. The activity of PdeH, the enzyme that degrades c-di-GMP, is Mg2+ dependent. Therefore, Mg2+ ions could possibly enhance c-di-GMP degradation and hence decrease biofilm formation that results in heat sensitive bacteria. C: A third possible explanation is that the Mg2+ ions directly regulate the pathway leading to biofilm formation, which would again result in heat sensitive bacteria.
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Figure 2. Enrichment of food products, for instance, dairy products, with magnesium would provide pronounced advantages and eventually result in healthier and efficient food products.
Figure 2. Enrichment of food products, for instance, dairy products, with magnesium would provide pronounced advantages and eventually result in healthier and efficient food products.
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Table 1. Varying effects of magnesium ions on bacterial adhesion and biofilm formation.
Table 1. Varying effects of magnesium ions on bacterial adhesion and biofilm formation.
BacteriaInfluence of Magnesium IonsReference
Staphylococcus aureusHigh concentrations of magnesium bind TA, which increases cell wall rigidity and results in better adherence.[30]
Pseudomonas aeruginosaAdherence of two of three tested P. aeruginosa strains was enhanced by magnesium ions[32]
Magnesium ions limitation represses the expression of retS which leads to increased aggregation, exopolysaccharide (EPS) production and biofilm formation[36]
Diverse effect of divalent ions on Pseudomonas aeruginosa strains of various origins[38]
Staphylococcus epidermidisAdherence of all tested strains was enhanced in low concentrations of magnesium[31]
Group b streptococciMagnesium had no effect on adherence at physiologic concentrations[33]
Pseudomonas fluorescensMagnesium ions increased initial attachment and altered subsequent biofilm formation and structure[24]
Bacillus speciesMagnesium ions are significantly inhibited biofilm formation of Bacillus species at 50 mM concentration and higher. The expression of the two matrix operons was reduced drastically in response to magnesium ions [34]
Fortification of milk with magnesium mitigated biofilm formation by Bacillus species[39]
Enterobacter cloacaeBiofilm formation decreased with increasing concentration of magnesium ions[37]
Arthrobacter sp.Mg2+ induced biofilm development through the removal of toxic hexavalent chromium[40,41]

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Demishtein, K.; Reifen, R.; Shemesh, M. Antimicrobial Properties of Magnesium Open Opportunities to Develop Healthier Food. Nutrients 2019, 11, 2363. https://doi.org/10.3390/nu11102363

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Demishtein K, Reifen R, Shemesh M. Antimicrobial Properties of Magnesium Open Opportunities to Develop Healthier Food. Nutrients. 2019; 11(10):2363. https://doi.org/10.3390/nu11102363

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Demishtein, Keren, Ram Reifen, and Moshe Shemesh. 2019. "Antimicrobial Properties of Magnesium Open Opportunities to Develop Healthier Food" Nutrients 11, no. 10: 2363. https://doi.org/10.3390/nu11102363

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