Honey is a product with low water activity because of the great amount of sugars (fructose and glucose), and also it has antimicrobial compounds derived from flowers or because of its transformation process in the beehive. Despite all the honey microorganism barriers, some species of microorganisms are able to survive and may cause damage to honeybees or consumers. Techniques of pathogenic microorganism identification by DNA using PCR are recommended and required for sanitary and customs control. It is important to know the diversity of contaminating microorganisms in honey, especially due to disseminate pathogenic microorganisms in the international traded marketing. In contrast, beneficial microorganisms such as yeasts can remain latently in this product waiting for the moment in which the environment is suitable for their development. Among the beneficial bacteria found in honeybee products, we can mention some lactic acid bacteria that act as prebiotics when ingested. The microorganisms in the digestive tract of honeybees are important for their health. Thus, we present the knowledge of microbiota associated with honey from honeybees and stingless bees (Hymenoptera, Apidae) and the techniques available for the detection of microorganisms in honey.
- pathogenic microorganisms
Honey is used as a therapeutic product since ancient times. Its properties are chemically evidenced by its composition. Among features that make this product effective against microorganisms, we can quote high osmotic pressure by low water activity (average 17.2%); low pH because of the presence of organic acids, mainly gluconic acid (average 3.9); the presence of hydrogen peroxide generated by action of enzyme glucose oxidase; low protein content; low redox potential due to the presence of reducing sugars; and chemical agents present as lysozyme, phenolic acids, pinocembrin, terpenes, benzyl alcohol, and volatile substances [1, 2].
High osmotic pressure results from its composition: 85–95% of sugar, of which it has 28–31% of glucose, 22–38% of fructose, 1–4% of sucrose, and 1–9% maltose . Isomaltose and some oligosaccharides are also present in honey and vary according to flowering, climate, and local production [4, 5]. As honey is a product developed from changes in nectar, the bees incorporate the glucose oxidase enzyme that converts glucose into hydrogen peroxide and gluconic acid; this compound is indeed important for the taste of products as well as their bioactivity [5, 6]. The presence of acids and other chemicals varies with the composition of the transformed nectar; for this reason, some honeys have higher antimicrobial activity with respect to other different blossoming .
About these conditions, few microorganisms have the capacity to develop or remain in honey. These microorganisms are derived from primary or secondary sources of contamination. The primary sources are related to digestive tract of honeybees, which have natural microorganisms and sources of material collection such as nectar, pollen and propolis, air, flowers, and the environment inside the beehive, while the secondary sources are incorporation of honey microorganisms postharvest, processing plants, and appliances .
2. Human pathogenic microorganisms found in honey
Due to characteristics cited above, only pathogenic bacteria capable of sporulation have the ability to keep in honey, but they have no reproductive capacity or vegetative cells. Fungi and yeasts are able to maintain their vegetative form .
Fungal growth is followed by the production of mycotoxins, which are secondary metabolites of filamentous fungi and toxic to humans and animals even in small concentrations. These are produced by fungi to reduce the incidence of competitors in environment . The main producers of mycotoxins are fungi of the genus
In research performed with honey samples of different blossoming, fungi of different species were isolated,
Despite of inappropriate condition found in honey for mycotoxin production, it is important to say that the presence of fungus can also cause disease in different ways, as induction of allergic responses and infections. The fungi of genus
With respect to yeasts, only
There are about 200 species of
Researchers isolated some bacteria in honey samples of different geographical and botanical origins. “They found
3. Beneficial microorganisms in honey for humans
Human metabolism is dependent of symbiotic microorganisms, known as the indigenous microflora capable of favoring the production and absorption of essential nutrients to our body such as K and B12 vitamins, pentatonic acid, pyridoxine, and biotin, and acts by modulating the immune system . This microbiota lives in the gut, due to high acidity of the stomach (pH 1.5); the most microorganisms are unable to grow, while in the gut we can found a lot of microorganisms with 500–600 different species . There is no oxygen in gut; for this reason, the gut bacteria are aero-tolerant and facultative anaerobic. We can find bacteria of genus
For honey production, honeybees ingest nectar and turn this with help of enzymes. Beyond the enzymes, they incorporate some symbiont microorganisms associated with gastrointestinal tract that can bring benefit to human health . The natural human microbiota is stable; so it is necessary for daily intake of the new symbiont to be able to populate the human body and maintain its benefits . These microorganisms are known as probiotics and, when they grow in human gut, can make nourishment benefits, like fermentation, and broke nutrients facilitating absorption of short-chain fatty acids, ions, amino acids, and vitamins; protective effect, preventing invasion of pathogenic microorganisms; and trophic effect in the gut epithelium and in the system .
Besides these microorganisms is necessary consumption of substances that promote their development, known as prebiotics. These prebiotics are components, like oligosaccharides, that are not digested by humans, but they serve as a substrate for the growth and performance of probiotics [28, 31]. Currently, there is a great interest in combining probiotics with oligosaccharides acting like prebiotic. There are studies with probiotic
The most-studied prebiotics are fructo-oligosaccharides, inulin, and oligofructose especially [33, 34]. However, there are others recognized as prebiotic, like galacto-oligosaccharides, trans-galactosylated oligosaccharide, isomalto-oligosaccharides, lactulose, pyrodextrin, and soy-oligosaccharides . In honey we can find malto-oligosaccharides , specifically in Brazilian honey samples that were found in isomaltose, cellobiose, panose, maltotriose, melezitose, raffinose, maltose, turanose, and maltotriose, which are characterized as prebiotics .
In addition to probiotics, there are microorganisms associated with honey that can produce bacteriocins, which are substances able to reduce or eliminate competing microorganisms. These are peptides produced by bacteria producers of lactic acid, to reduce competition for nutrients, making inappropriate environment for development of other bacteria; for this reason, they are studied as an option for replacing antibiotics, and as usual these can cause harsh effects to humans also. Bacteriocins have high potency in vivo and in vitro and have low toxicity, and they can be produced in situ through consumption of probiotics or purified through bioengineering . In 2013, a study was conducted with a new bacterium strain isolated from honey, able to produce bacteriocins fungicides called
Studies suggested that the antimicrobial character of honey is attributed to activity of these bacteria in honey; these are also present in the stomach of honeybees.
Besides the microbiota associated with honey, it is worth mentioning that this product alone is highly beneficial by features from its composition. This makes the honey effective activity like antimicrobial, antioxidant, anti-inflammatory, anticancer, antihyperlipidemic, cardioprotective properties, for ocular treatment, gastrointestinal tract disorders, neurological disorders and wound healing . Honey has a series of phenolic acids like caffeic, ellagic, ferulic, and p-coumaric acids; flavonoids, such as apigenin, chrysin, galangin, hesperetin, kaempferol, pinocembrin, and quercetin; and antioxidants, such as tocopherols, ascorbic acid, superoxide dismutase, catalase, and reduced glutathione . These compounds are known for their ability to reduce free radicals; this composition may vary depending on floral source that honeybees have visited for honey production . Its antimicrobial activity makes it an important substance for the treatment of wounds as a result of carbon, lipids, amino acids, proteins, vitamins, and minerals active in healing. Components such as hydrogen peroxide, high osmolarity, acidity, non-peroxide factors, nitric oxide, and phenols are active in their healing effect. It also promotes growth of tissue in the human body, and it has anti-inflammatory activity . However, it is important to note that honey directed to the treatment of wounds and inflammation should undergo irradiation treatment, so that microbiota will not interfere negatively on treatment .
Finally, it is important to note that consumption of foods able to bring health benefits, beyond nutrition, is a current practice that should be encouraged; honey is characterized as such, and it should be ingested daily.
4. Microorganisms in honey for industrial use
The yeasts that were found in honey are able to withstand high concentrations of acids and sugar, and it can be a problem for the honey processing industry; however, they are promising for fermentative processes. Furthermore, the low concentrations of these nutrients in honey characterize yeasts as nutritionally less demanding.
Besides yeast, filamentous fungi are also significant because they are known for their ability to produce extracellular substances such as enzymes and acids; they must be studied, as they are able to produce substances of industrial interest in osmotic stress condition. The genera
5. The gut microbiota as an environmental factor for honeybee health
Honeybees have a beneficial anaerobic and micro-aerobic natural microbiota acquired and installed in their body. This includes Gram-negative groups like species
The microbiota associated to the honeybee
There are several bacterial species negatively affecting honeybee health—
Gilliam reported that these bacteria could be endemic of the digestive tract of adult honeybees and independent of seasons and nutritional factors . They are different depending on the sources of nectar and the presence of other bacterial genera in the stomach of the honeybee. It seems that bees and lactic acid bacteria developed mutualism. Lactic acid bacteria prepare the environment to make nutrients available for honeybees; on the other hand, intestinal tract of honeybees is protected from harmful microorganisms. The honeybee regurgitates the nectar stocked in the crop in the hive honeycomb that has an optimum temperature of 35°C  for the development of lactic acid bacteria.
The honeybee larvae probably are sterile initially, but as feed on honey from nurse workers, honeybees gain over time this intestinal flora before completing their life cycle . Honeybees harbor a number of commensal or beneficial bacteria distributed throughout the different compartments of their gastrointestinal tract. Each compartment of the honeybee gastrointestinal tract has a distinct environment favoring specific microorganisms . Several findings have indicated that the honeybee gut is colonized by a distinctive set of bacterial species designated as the core gut microbiota . Because the community composition changes through the life cycle of honeybee, the colonization of the gut is believed to be influenced by the age . During the course of their life span, worker honeybee performs many different tasks that can contribute to these variations. Newly emerged worker honeybees nurse larvae within the hive, whereas older worker honeybees build and maintain the wax combs, defend the colony, and receive and process food that is collected by foragers. In addition to the microbiota in the gut, a novel lactic acid bacterial flora composed of 13 taxonomically well-defined
Lactic acid bacteria are found in two distinct phyla:
Lactic acid bacteria are important inhabitants of the intestinal tract of man and other mammalian and vertebrate animals.
Quite recently fructophilic lactic acid bacteria were found in the gastrointestinal tract of several flower- or fructose-related insects, including honeybees, tropical fruit flies, and giant ants [86–88], whose diets are fructose rich. Of these insects, honeybees are economically and agriculturally important for honey production and especially for crop pollination, which links to human food production. However, despite the importance of these insects in nature and in our lives, populations of honeybees are reported to have decreased considerably during the last decade and to be still decreasing worldwide, mainly by colony collapse disorder . To understand and to prevent the disorder, microbial interactions, both symbiotic and pathogenic, have recently been studied [90, 91], and findings have indicated that honeybees carry specific microbiota dissimilar to other animals, including humans. Fructophilic lactic acid bacteria, especially
Symbiosis is common in nature, in which symbionts as commensals or mutualists evolved to benefit each other. Culture-independent studies of the human microbiota identified recently a complex symbiotic environment with more than 1000 bacterial phylotypes representing more than 7000 strains . The composition of this microbiota has been suggested to be a result of a highly coevolved symbiosis and commensalism influenced by nutrition, physiology, and immunological factors. It varied with the sources of nectar and the presence of other bacterial genera within the honeybee and ended up eventually in the honey (Figure 1).
6. Microorganisms in stingless bee honey
Products of stingless bees are consumed since before the discovery of the Americas to the present day. Honey of these bees has activities against microorganisms, having importance in the colony maintenance as a microbiologically stable environment . Stingless bee honey has characteristics that confer antimicrobial character, i.e., activity against Gram-negative and Gram-positive bacteria such as
About fungi, the interesting fact is that bees cultivate them as food  and protection against other pathogenic microorganisms , i.e.,
Little is known about pathogens in stingless bees; however, there are no pathogen transfer record from
7. Microorganism detection methodologies in honey and honeybee products
7.1. Microbial diversity
Much has been discussed about the succession of gut microbiota among queens, workers, and larvae and the role of the diversity on the quality of honey, safety, and health of the colony [11, 53, 114–117]. New methodologies have made it possible to access information about the differences in the profile of this microbiota in different apiculture sources [118–121], species [53, 122] and genetic diversity  of honeybees, development stages [53, 68, 117, 122–126], nutrition [116, 127], location inside the gut [49, 53, 68] and digestive system , ontogenetic stage and geographic location [118, 122, 125], environmental conditions , health control , and individual [116, 125].
This access has been carried out mainly by sequencing the coding region of the 16S subunit of the bacterial ribosome [53, 121, 130], both from genomic DNA from microorganisms growing on selective media as Man-Rogosa-Sharpe agar, Sabouraud dextrose agar, and
Several microorganisms present in the honey and in the gut of honeybees have antagonistic effects on honeybees and human pathogens, especially of
7.2. Monitoring of the microbiological honey quality
Traditional methods are often still used for monitoring the microbiological quality of honey used for human consumption, even as the rates established by the laws use these methods. Potato dextrose agar and yeast extract glucose chloramphenicol agar are media normally used for aerobic count and the total fungi (yeasts and molds), while Violet Red Bile and MacConkey medium agars are normally used for counting coliforms, which can also be done by the most probable number technique [119, 141, 142]. These media have recently been used to monitor the efficiency of a new filter-based method based in reducing the microbial burden and to improve the microbiological quality of honey . Potato glucose agar in Brazil was also used for monitoring the honey contamination by yeast and fungi . Standard plate count agar is used for monitoring of mesophilic bacteria, such as that was done in honey samples of Portugal [141, 142] and Argentina [119, 145].
7.3. Detection of honeybee pathogens in honey
The honey is an important route of contamination of honeybees, spreading many microorganisms, particularly pathogens that infect the honeybees. Several molecular techniques have been developed for the detection of pathogens like
The use of these techniques and the detection of this pathogen have allowed the control of mortality of honeybee populations around the world, restricting the dissemination of pathogens in bee products. For example, the diagnosis of American foulbrood and European foulbrood usually occurs through visual inspection of brood combs and detection of diseased larvae, subjective criteria that could be confused with other beehive conditions [155, 156]. The traditional methods of detection of these pathogens include the visualization by microscopy and detection in tissues ; culture on selective medium [151, 155, 156], including
RT-PCR has been used to simultaneously detect multiple viruses such as in cases of honeybee parasitic mite syndrome where five out of seven viruses were detected in sample mite in Thailand . Also, different multiplex RT-PCR were developed for the simultaneous detection of i) black queen cell virus (BQCV), deformed wing virus (DWV), Kashmir bee virus (KBV) and Sacbrood virus (SV) , ii) acute bee paralysis virus (ABPV), BQCV and SV , iii) ABPV and SV  iv) ABPV, chronic bee paralysis virus (CBPV), BQCV, DWV, KBV, and SV . The effectiveness of this method in the detection of these pathogens was demonstrated in the simultaneous detection of these viruses in colonies [159, 160] and queens , where up to 93% of the queens have multiple infections .
Even more efficiently nine viruses (ABPV, BQCV, CBPV, DWV, KBV, SV, Israel acute paralysis virus (IAPV),
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