2. Beer and its Principal Interactions with the Microbiota
2.1. The Microorganisms from Beer and Their Probiotic Potential
Beer is usually a pasteurized product, but there are crafted beers that have a potential of influencing the gut microbiota because they contain bacteria. Studies of the effect of beer consumption on the gut microbiota are few. A study from 2019 detected by sequencing of 16S rDNA eighteen genera of bacteria present in the rice beer,
Lactobacillus being the dominant group (90%). Other types were
Acetobacter,
Acinetobacter,
Bacillus,
Dickeya,
Enterococcus,
Enterobacter,
Exiguobacterium,
Gluconobacter,
Janibacteria,
Klebsiella,
Lactococcus,
Leuconostoc,
Pseudomonas,
Pediococcus,
Rothia,
Staphylococcus and
Weissella. Based on the detected bacteria and their bacterial profiles metabolic pathways were revealed as being influenced by the consumption of the rice beer, such as metabolisms of carbohydrate, amino acid, vitamins and cofactors, as well as xenobiotic biodegradation [
89].
The main effect of alcohol intake on gut microbiota is dysbiosis [
13,
31], by changing the balance of the dominant bacterial from
Phyla Bacteroidetes,
Firmicutes and
Phylum proteobacteria. However, this is not the case with usual beer, when consumed with moderation, because it contains about 5% alcohol. Low-alcohol and alcohol-free beers are popular and widely consumed. So, when considering beer, it is important to choose a type of beer with low or without alcohol, which gives the benefits of fermented foods.
Beer enriched with Saccharomyces cerevisiae strain intake may modulate gut microbiota and have beneficial influence the symptoms in Alzheimer’s disease, generating a neuroprotective effect by ameliorating cognition and increasing the concentration of anti-inflammatory cytokines, as new data revealed in 2022 [
9]. Another type of beer rich in bacterial composition is Belgian lambic beer. The different bacteria present throughout the production process result because of the spontaneous inoculation of microorganisms from the environmental air and the inner surfaces of the wooden barrels [
86]. Several new bacterial species such as
Acetobacter lambici and
Gluconobacter cerevisiae have been described in lambic beer. In the process of production of this type of beer, the following bacteria are present: Enterobacteria (
Enterobacter cloacae;
Klebsiella oxitoca), acetic acid bacteria (
Acetobacter spp.;
Gluconobacter cerevisiae) and lactic acid bacteria (
Pediacoccus spp.), along with different yeasts (
Hanseniaspora uvarum;
Saccharomyces spp.;
Brettanomyces spp.), with possible, not-yet-studied influence on gut microbiota. Crafted beers with several enhanced tastes, such as fruits, herbs, honey, spices and vegetables, have become more popular lately, but because they are not always pasteurized or sterilized by filtration they are subject to spoilage, due to the microbiota associated with the organic raw ingredients added to obtain the special tastes. Even if there is not enough knowledge available about the microbiota diversity in craft breweries it is known that some lactic acid bacteria from beer can produce biogenic amines such as histamine, tyrosine, putrescine and cadaverine, which can alter the beer and have possible toxic effects. Biogenic amines can also be found in sausages, fermented vegetables, fishery products, cheese and wine [
32]. Published studies of sixty monitored points inside the craft brewery revealed that
Lactobacillus,
Pediococcus and
Leuconostoc genera, are responsible for biogenic amines production, especially two isolates of
Lactobacillus brevis that are able to be cultured into acidic conditions, with more hop and alcohol, these isolates had presented horA, horC and hitA genes, and the highest production of biogenic amines [
90]. Corn beer has potential sources of probiotic lactic acid bacteria with cholesterol lowering activity, the strains identified by sequencing the 16S rRNA gene were
Levilactobacillus brevis and
Enterococcus faeccium, NCBI genbank accension numbers ON454506 and ON908682; isolates that effectively lowered LDL-c and increased HDL-c in rat sera, which are the main risk factors for cardiovascular diseases [
84]. Beer is a fermented beverage that has enhanced nutritional and functional properties due to transformation of substrates, formation of bioactive end-products and presence of living microorganisms, genetically similar to strains used as probiotics [
27]. Some studies revealed that beer components may have antimicrobial properties, as well as microbiological spoilage risks [
91].
The microbial community (bacteria and fungi) from beer differs in time because it is influenced by its initial composition, the quantity of alcohol and the type of barrel where it is kept. Studies that used amplicon sequencing of the V4 region of the bacterial 16S rRNA gene and the fungal ITS1 region have shown using PerMANOVA analysis that during the process of beer maturation significant higher levels in the bacterial and fungal population appeared. The lactic acid bacteria became dominant in the moderately hopped beers and remained fairly constant in high-bitterness beer; with similar composition of the traditional beers,
Pediococcus damnosus,
Lactobacillus brevis and
Acetobacter spp., and the fungi were influenced by the presence of alcohol [
85]. There are even studies that introduced the idea of non-
Saccharomyces yeast beers, and these types of beers may enter on the market in the future, after investigations and guideline for the safety assessment of yeasts are carried out [
92].
So, bacteria and fungi encountered in the beer fabrication process, enriched or crafted beer, produce an array of compounds such as vitamins, bacteriocins and organic acids which confer health benefits to the consumers and can modulate the indigenous intestinal flora of the host.
2.2. Polyphenols and Microbiota
Beer is an important vehicle for polyphenols, which, together with bitter acids, form beer’s antioxidants. Most of them come from malt and only about 20% from hops. There are in vitro studies that confirm the action of polyphenols on the microbiota [
93] (
Figure 2). Animal studies support this interaction. For example, a polyphenol well represented in beer, ferulic acid, amplifies the biodiversity of the microbiota and stimulates the multiplication of bacteria that produce propionate and butyrate in the colon of rats [
36]. Although limited in number, studies on human subjects also confirm the interaction under discussion. Studies show that after the ingestion of polyphenols, the production of short chain fatty acids (SCFA) increases, with consequent local anti-inflammatory effects [
37]. The increase in SCFA synthesis confirms the action on the microbiota, an effect already demonstrated in the case of red wine consumption, which is itself a source of polyphenols. Red wine increased the levels of
Bifidobacterium in the microbiota, as well as
Faecalibacterium prausnitzii and
Roeburia. The development of
Enterobacter or
Escherichia coli strains was inhibited [
38]. These positive effects were also observed for alcohol-free wine. So, although the absorption of polyphenols from alcohol-free products (beer, wine) decreases compared to the same products with alcohol [
4,
94], polyphenols not absorbed that reach the colon have important effects in situ with multiple repercussions through the action on the intestinal microbiota. It is about oligo and polymeric polyphenols that usually do not undergo transformations until the distal intestine [
37]. Polyphenols are “activated” by certain populations of the microbiota, especially when it comes to phytoestrogens [
39,
40,
95]. Polyphenols are transformed by bacteria into absorbable products that reach through the portal blood, to the liver or into prenylated products that have important sanogenic actions, such as the antiproliferative action on some cell lines, as prenyl naringenin and xanthohumol have [
41]. The interrelation between polyphenols and microbiota is extremely complex. The microbiota increases the bioavailability of polyphenols which, in turn, modulate the composition of the populations in the colon, inhibiting pathogenic microorganisms and stimulating the development of healthy ones through a prebiotic action [
42,
43]. Quercitin, a flavonoid from beer, combated intestinal dysbiosis, improving the ratio between Firmicutes and Bacteroides populations and opposing the proliferation of microbiota species associated with excessive body weight [
48,
49]. It should be noted that by drinking non-alcoholic beer or wine, you not only avoid the negative effects determined by ethyl alcohol, including on the microbiota, but also increase the number of polyphenols that reach the intestine and which would have positive effects on the microbiota.
Figure 2. The action of polyphenols on the microbiota.
In a study conducted by Hernández-Quiroz et al. [
46], after the administration of a dose of 355 mL of beer per day for 30 days in healthy subjects, divided into a group that received beer without alcohol (
n = 35) and one that received beer with alcohol (
n = 33), a clear influence on the intestinal microbiota, as well as on the functionality of pancreatic β cells and fasting blood glucose, could be observed. The action on the microbiota consisted of increasing the diversity of the microbiota, by favoring species of the
Bacteroides type, at the expense of
Firmicutes. The authors attribute this effect to the polyphenols in beer, and it was found in beer without alcohol. Beer with alcohol did not have positive effects of the same scope and negatively impacted blood sugar and β cell functionality.
Another observational study [
47] found an increase in butyric acid, a byproduct of the intestinal microbiota, in beer consumers, but without quantifying the intake of polyphenols. Positive effects were found only with wine in a large study on twins in Great Britain, in which non-alcoholic beer was not an element of investigation [
96]. A recent clinical study by Martínez-Montoro et al. [
97] worked on adults aged 30–60, divided into two groups (with or without metabolic syndrome) who were administered beer with different concentrations of polyphenols, consumed successively, after respective washout periods. In the beginning there were no radical differences in microbiota characteristics between the two groups. During the study, the authors report significant changes in the microbiota, with substantial changes in the entire profile, all the more important as the polyphenol content of the beer was higher. The changes were also influenced by the metabolic status of the individuals, being significant in the group of subjects with metabolic syndrome, where the abundance of streptococcus was highest after consumption of dark beer. A previous study showed that certain species of streptococci interact with gallic acid and catechins, amplifying their antioxidant effects [
48]. Moreover, some streptococci can transform beer melanoidins into an isoflavone with estrogenic and antioxidant action called equol [
49]. The authors attribute the effects found in the group with metabolic syndrome to the correction of intestinal dysbiosis, which is usually present in individuals with the syndrome in question. Since the most important changes were found after the consumption of dark beer, very rich in antioxidant polyphenols, the authors explain the influence also through the respective antioxidant action on the microbiota, excluding the possible interference of alcohol, which was found in equal quantities in lager beer (with fewer polyphenols) and in the black one (with maximum level of polyphenols).
There are still open study perspectives in which to possibly follow the impact of some types of beer enriched in polyphenols, with or without alcohol, on the intestinal microbiota and from here, on the entire metabolism [
4]. An extensive review of the effects of beer polyphenols on the microbiota was carried out by Quesada-Molina et al. [
50]. The authors analyze the existing studies, noting that in principle a detailed analysis of the microbiota-polyphenols interaction is needed and that the existing results so far are based on deduction rather than on concrete quantification of the effects.