Microbiomes are a complex and dynamic network of microorganisms (bacteria, viruses, fungi, archaea) that adapt and live in a functional relationship with their specific habitats (e.g., human, soil, plant, water, animals, production sites along the food chain). Neighbouring microbiome ecosystems exert mutual influences, even when physically separated (e.g., animal and soil). In addition, microbiomes are very sensitive to environmental conditions and exposure to substances of different nature. In humans, various factors (e.g., genetics, diet, drugs, lifestyle, oxygen, pH) contribute to shaping the microbiomes’ subpopulations along the various sections of the gastrointestinal tract.
There is an increasing amount of scientific information associating – or to a lesser extent demonstrating – that the gut microbiome has the potential to influence human health. For example, the microbiome influences the development of the immune system, has a protective role (first line of defence in the gut), and synthesizes metabolites essential for maintaining human homeostasis (vitamin D and shortchain fatty acids). In addition, microbiome imbalances have also been associated with some non-communicable disorders (NCD), including inflammatory and metabolic diseases (obesity, diabetes, inflammatory bowel disease).
Non-human microbiomes have also been associated with the health status of other ecosystems, e.g., soil and plant. Such microbial populations present in the different environments along the food chain are also contributors to food quality and food safety.
Since the microbiome may play a role in human homeostasis, it can be used as a target for different dietary interventions to maintain and promote health (e.g., optimizing fibre intake, administration of pre- and probiotics). On the other hand, microbiome disruptors (e.g., imbalanced diet) are also attracting attention as they may lead to dysbiosis, which can eventually result in adverse effects on human health Much of the current interest gathers around the capacity of food additives, chemical residues (pesticides and veterinary drugs), antibiotics or other environmental pollutants to lead to biologically relevant microbiome perturbations.
Until recently, traditional microbiology has focused on the individual identification of microorganisms and related functions in, for instance, food production (e.g., fermentation), promoting health status (e.g., probiotic gut bacteria) or as contributors to disease (e.g., pathogens). New technological advances in the omics and bioinformatic fields have enabled the holistic study of microbial community structures (microbiomes) and their functional activity within a given environment. Metagenomics tools sequence the DNA material and provide information on the taxonomical composition of the microbiome and gene diversity, which provides an indication of the potential microbial functions. Other omics technologies target the microbiome activity. They indicate active metabolic pathways through the analysis of gene expression by RNA sequencing (transcriptomics and metatranscriptomics), the protein resulting from such expression (proteomics) or final end-products or metabolites (metabolomics). The science supporting the microbiome study is relatively new and still evolving. It is still lacking standardization and generates immense amounts of data that cannot yet be interpreted. Therefore, our understanding of microbiomes and interactions with their ecosystems is still limited.
The study of the microbiome from farm to fork has the potential to improve our understanding of hazards and health risks. Within the context of food safety, different microbiomes can be exploited for different purposes.
The microbiome is not a food safety risk per se. Until recently, the microbiome has been an unexplored contributor to food safety and quality. The holistic understanding of the microbiome-environment-host interactions, and their influence on human exposure to different types of biotic or abiotic factors, open a new avenue to better understand hazards and health risks, and therefore microbiological and chemical assessments.
Now that microbial populations can be evaluated in a holistic manner by using omics technologies (e.g. complete DNA or RNA analysis by culture-independent deep shotgun metagenomics or metatranscriptomics, respectively, proteomics or metabolomics), it will be possible to monitor for the full potential or the presence of microbial hazards (e.g. pathogens, pathogenic factors and antimicrobial resistance) up and downstream in food production, not only in food and food ingredients, but also in the environment of production sites. It will also improve our understanding of factors (processing steps, microbiomes in the environment, storage) influencing the pathogenic potential at a given location and the acquisition and flow of antimicrobial resistance along the production chain. Therefore, the study of the microbiomes will bring a new perspective to the characterization of microbial hazards. Moreover, it will provide the basis for the development of suitable and effective preventive measures. There are numerous scenarios where the microbiome and microbial compounds can be used as hazard indicators of food safety and quality. The following are some examples: selection of safe starter cultures and their monitoring during product manufacturing, evaluation of air microbiome in age-drying chambers to minimize the potential transfer of pathogens from the environment to the product, and the influence of storage conditions in the composition and production of compounds affecting the food safety and quality.
In addition to macro and micronutrients, the gut microbiome can enter in contact with other compounds through food and water consumption. These can be intentionally introduced in the product formulation (i.e., food additives) or result from upstream activities in the food chain (e.g., residues of veterinary drugs and pesticides) or be present inadvertently in the diet (e.g., environmental or industrial contaminants). The gut microbiome can metabolize and transform compounds, alter their bioavailability and modify their toxic potential. Therefore, microbial activities can modify human exposure to such substances. Moreover, exogenous compounds also have the potential to induce changes in the composition and activity of the microbiome and lead to dysbiosis. Such microbial imbalance could eventually have implications for human health.
Exogenous compounds such as food additives, residues of veterinary drugs and pesticides or microplastics are very heterogeneous groups of chemical compounds. Out of this broad chemical spectrum, research has only been conducted on a limited number of compounds and show their potential to disturb the gut microbiota. Most studies, which differ in design and methodologies, are generally conducted at levels that exceed those found in a normal diet. Therefore, this information is of limited use from the perspective of food safety risk assessment as it does not reflect a realistic (low-level) dietary exposure. However, the limited number of studies specifically designed to evaluate exogenous compounds at low residue levels provides an indication that effects of exogenous compounds on the microbiome follow a dose-dependent relationship. Although some associations are made between microbiota alterations and adverse health effects observed in laboratory animals, the causal role of microbial disturbances specifically induced by these exogenous compounds on host alterations remains unclear Microbiome science is a quickly developing field of research. Food safety risk assessment bodies are closely watching the emerging research regarding its significance for food safety risk assessment. However, the science available to date does not provide enough consensus, mechanistic understanding and has not established sufficient repeatability, so that no clear conclusions can be drawn at the moment.
The gut microbiome contributes to the resistance against the colonization by foodborne pathogens and the proliferation of commensal opportunistic pathogens. Pathogen colonization does not only depend on the infective dose and the host’s immune system but also on the health status of the gut microbiota. Alterations on the structure and function of the gut microbiome, which may be caused by dietary imbalances or exposures to certain substances, can offer a window of opportunity for pathogens to break the gut barrier. Colonization resistance is one of the endpoints used to determine the microbiological Acceptable Daily Intake (mADI) in the assessment of veterinary drug residues.
Chemical risk assessments aim at evaluating the safety of food additives, chemical residues in food and environmental pollutants and contaminants, and serve as the basis to establish health-based guidance values (e.g., Acceptable Daily Intake ADI, Acute Reference Dose ARfD). With the further step of exposure assessment, a risk can be characterized, and this serves as a basis to set up regulatory levels such as, for example, Maximum Residue Limits (MRLs) for veterinary drugs and pesticides, Maximum Levels (MLs) for contaminants, and Maximum Use Level (MUL) for food additives. Although the Joint FAO/ WHO Expert Committee on Food Additives (JECFA) and the Joint Meeting on Pesticide Residues (JMPR) have advanced their procedures to complement toxicological chemical assessments with a microbiological component, there are many ongoing discussions among risk assessors about further integrating the microbiome in chemical risk assessment.
Regulatory decisions require careful consideration, given their impact on the food system. For this reason, the science supporting risk assessment needs to be robust, reproducible and based on suitable and well-defined endpoints. However, although the microbiome’s potential as a component of risk assessment is widely recognized, critical technical limitations and knowledge gaps need to be addressed before the evaluation of microbiome interactions with food additives, pesticide and veterinary drug residues and other food contaminants are incorporated into regulatory activities.
Latest trends have placed the microbiome as the target of dietary interventions to promote health or as a mediator in human disease due to alterations caused by different types of compounds (e.g., food additives, residues of veterinary drugs and pesticides, and environmental pollutants). However, the information supporting any claim requires careful and critical interpretation. While for the vast majority of cases research has only provided statistical associations between microbiome disturbances and health or disease, there is a need to prove causality (in other words, demonstrate the causal link between changes in the microbiome composition and function and physio pathological alterations in the subject). This would be the demonstration that, indeed, the microbiome contributes to either maintaining or disrupting human homeostasis. Moreover, further investigation about causal links could also indicate that microbial changes are a consequence of disease, not the cause. Once proven, it will be necessary to understand the dimension of such contribution.
Understanding the relative role and underlying mechanisms of the microbiome in health and disease will enable the update of chemical risk assessments and the development of evidence-based methodologies and frameworks to evaluate microbiome-related data.
Now that we have the possibility to evaluate the dynamics of microbial ecosystems, we also have significant potential to study the microbiome in food systems (ingredients, and foods and the different environments along the food production chain). These can include:
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