Article Cite This: J. Phys. Chem. C 2017, 121, 27493−27503
pubs.acs.org/JPCC
Experimental and Molecular Dynamics Investigation Proves That Montmorillonite Traps the Biogenic Amines Histamine and Tyramine Daniele Malferrari,*,† Fabrizio Bernini,† Francesco Tavanti,† Luca Tuccio,† and Alfonso Pedone† †
Department of Chemical and Geological Sciences, University of Modena and Reggio Emilia, Via Campi 103, I-41125 Modena, Italy S Supporting Information *
ABSTRACT: Biogenic amines present in high concentrations in foods obtained through fermentation could have toxic effects and contribute to the arising of allergies. For this reason, their removal is of great importance. In this work, we used an experimental and computational approach to investigate the interaction between a calcium montmorillonite, a layered silicate very common in clays, and the two biogenic amines histamine and tyramine, obtaining deep insight into their binding modalities and structural organization. Calcium montmorillonite can exchange almost all its interlayer Ca2+ with the protonated histamine and tyramine, thus reducing their concentration in water solution. The adopted multianalytical approach allowed classification of the interaction mechanism as an intercalation. Molecular dynamics simulations showed that the intercalated histamine and tyramine preferentially interact, through the protonated amino nitrogen, with tetrahedral aluminum bearing a net negative charge, whereas interactions with neutral tetrahedral silica is less favorable. We observed that most of histamine molecules bind in the center and above the 6T net of the silica sheet, but for electrostatic constraints they cannot occupy the center of two adjacent 6T nets as occurs for tyramine.
1. INTRODUCTION Biogenic amines (BA) are low molecular weight nitrogen compounds that can be produced either through microbial decarboxylation of free amino acids by the specific decarboxylase enzyme that characterizes some microbial strains1−3 or by amination and transamination of aldehydes and ketones.4,5 As bacteria are ubiquitous, BA may be enclosed in various proteins and amino acids containing foods, and, generally, their concentration is greater in foods obtained through fermentation such as meats, fruit juices, dairy products, cheese, beer, and wine.6,7 Biogenic amines are widely studied not only as they can be employed as quality markers associated with the degree of degradation and fermentation of foods8,9 but also because of their potential toxic effects on human health.10−12 Biogenic amines, at low concentrations, are essential for normal metabolic and physiological functions in living organisms. On the other hand, high (or abnormal) concentration and mixture of BA can lead to the development of allergies and physiological disorders which may be more severe in individuals having a reduced serum monoamine oxidase (MAO) and diamine oxidase (DAO) activity and result in adverse health effects such as neurological disorders, headaches, hypo- or hypertension, nausea, cardiac palpitations, and renal intoxication.6,10 Currently, against a qualified scientific literature relating to the origin and presence of BA in foods, to their effects on health (see reference above), and to the analytical methods for BA quantitative determination,13−16 only a few research studies © 2017 American Chemical Society
have attempted to tune methods for BA removal, in particular involving the use of natural inorganic materials. An encouraging solution seems to come from bentonite, a clay with an high content of the layered silicate montmorillonite. For example, it was demonstrated that treating wine with bentonite drives a significant lowering of BA (mostly histamine) concentration.17 In fact, BA are organic bases in which alkyl groups replace one or more hydrogens of ammonia. The lone pair of electrons on the nitrogen atom allows their protonation at weakly acidic pH values (i.e., between 4 and 5). Protonated BA should thus interact with montmorillonite through adsorption mechanism (i.e., through the process of attraction and adherence of cations from a solution to the surface) and/or through cation exchange reactions that drive the intercalation (i.e., to the movement of ions or molecules into the layered host structure) of the BA in montmorillonite interlayer. In fact, montmorillonite possesses free negative charges that make it a well-known ionic/molecular exchanger; furthermore, it can swell to host in the interlayer molecules larger than the original cation.18 Moreover, in the last five decades natural and synthetic montmorillonites have been exploited in many application fields not only for their high cation exchange capacity (CEC) also with organic molecules and swelling behavior but also for their ubiquitous distribution, safety, and cheapness. Classic examples of such versatility are represented by the obtainment of polymeric nanocomposites Received: October 3, 2017 Revised: November 17, 2017 Published: November 21, 2017 27493
DOI: 10.1021/acs.jpcc.7b09804 J. Phys. Chem. C 2017, 121, 27493−27503
Article
The Journal of Physical Chemistry C Table 1. Histamine and Tyramine Concentration (mol/100 g) in Mt−His and Mt−Tyra Mt Mt−His Mt−Tyr
histamine
tyramine
% CEC
Ca
K
Na
− 0.03429 −
− − 0.06501
− 103.8 98.3
0.02836 0.00169 0.00313
0.00510 0.00416 0.00402
0.00323
