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Food design to feed the human gut microbiota Danilo Ercolini, and Vincenzo Fogliano J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b00456 • Publication Date (Web): 22 Mar 2018 Downloaded from http://pubs.acs.org on March 22, 2018

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Journal of Agricultural and Food Chemistry

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Food design to feed the human gut microbiota

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Danilo Ercolini1, 2 & Vincenzo Fogliano*3

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Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy

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Task Force on Microbiome Studies, University of Naples Federico II, Naples, Italy

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Food Quality & Design Group Wageningen University, Wageningen, The Netherlands

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*Corresponding author

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[email protected]

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Phone/fax 0031 317 485171

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Bornse Weilanden 9, 6702AM Wageningen, NL

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Abstract

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The gut microbiome has an enormous impact on the life of the host and the diet plays a

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fundamental role in shaping microbiome composition and function. The way food is processed is a

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key factor determining the amount and the type of material reaching the gut bacteria and

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influencing their growth and the production of microbiota metabolites. In this review, the current

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possibilities to address food design toward a better feeding of gut microbiota are highlighted,

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together with a summary of the most interesting microbial metabolites that can be made from

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dietary precursors.

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Keywords: Food ingredients, Phytochemicals, Metabolism, Food processing, Mediterranean diet Melanoidins

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ACS Paragon Plus Environment


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Introduction

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Advances in food technology combined with the consumer’s preference resulted in the wide

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adoption of ultra-processed foods having high calorie density (Pellegrini & Fogliano & 2017). This is

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considered one of the causes underpinning the current epidemic obesity. Food reformulation

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strategies are currently based on sugar and fat reduction, mainly targeting food calorie reduction.

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Unfortunately, this strategy has limited efficacy as it works only for health conscious, restrained

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consumers and, more specifically, it does not take into account the needs of the gut microbiota. It

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is now firmly established that gut microbiome has an enormous functional potential for the host.

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The diet plays a fundamental role in shaping the composition of gut microbiota and thus

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determines the inter-relationship between the gut microbiome and the host (Shanahan et al.,

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2017). Microbial activities can influence the host and compelling evidence shows that microbiome

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composition and functions are responsible for human metabolism and regulate the balance

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between health and disease. In this vein, food design should take into account the needs of our

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commensal bacteria together with those of the human body. The simple concept is that microbes

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in the gut thrive on what is not bioavailable for human body. In other words, unavailable food

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components are the actual food for commensal bacteria in the gut. This concept is exemplified in

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the sketch of Figure 1. In a context of excess of macronutrient intake and high calorie dense foods

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a design that reduces the bioaccessibility is possibly beneficial for the host.

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bioavailability could raise some concerns for infants and malnourished people as in these subjects

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the priority is still host feeding.

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In the framework of microbiome-related nutrition, the attention has been mainly devoted to the

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dietary fibre, which is surely a key dietary component for the microbiome. However, the material

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reaching the gut is not limited to dietary fibre. Between 45 and 85 g of solid matter containing

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around 20-40 % of proteins can partially escape the absorption in the small intestine and reach the

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gut every day (Silvester et al., 1996). Beside proteins, a significant amount of resistant starch, fats

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and phytochemicals is also part of this material. Multiple studies showed the triglyceride

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bioavailability can be modulated by the physical structure of the foods (Capuano et al., 2018).

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Macronutrients stored inside intact plant cell wall are not accessible for the human digestive

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enzymes. In the same way, oil and protein bodies which are not damaged during food preparation

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can be degraded only at a limited extent by digestive lipase and proteases, respectively.


The reduced

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Different considerations must be drawn for most of the plant phytochemicals such as all

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poyphenols. It is well known that they have a limited bioavailability (usually only 1-5% is absorbed)

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while a large moiety is delivered to the gut. Recent evidence showed how they play multiple

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functions in the gut shaping the microbiome and triggering various biochemical pathways

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influencing inflammatory and immune status (Tomas-Barberan et al., 2017). Phytochemicals are

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extensively metabolised by the microbiota and converted in simple phenolic acids, which are

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absorbed in the body contributing to the communication between the gut and the human body.

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It is worth to notice that virtually all the undigested material can be a substrate for the community

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of the gut microbes: the higher the variability of the substrates available the higher the diversity of

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the microbiome. Mounting evidence showed that this microbiome diversity is associated with low

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inflammatory status and lean phenotype. This is not a random association: the expression of genes

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in the microbiome trigger biochemical pathways ensuring proper intestinal permeability and

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immunomodulation (Bishoff et al, 2014)

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The diet/microbiome interplay is the current basis for implementation of personalized nutrition

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(Derrien et al., 2017; Kashyap et al., 2017) and microbiota composition is a key factor affecting

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responsiveness to nutritional interventions (Shanahan et al., 2017) that will soon take into account

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initial stratification of individuals on the basis of the microbiota.

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In this framework, it is timely to start re-styling the concept of food and to add the role of feeding

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the gut microbiota by providing precursors of microbial metabolites that are responsible for the

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microbiome/host relationship.

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Delivery of nutrients to the gut microbiota

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The traditional nutritional recommendation to feed human microbiota is to formulate food or

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prescribe a diet plenty of dietary fibre. Unfortunately, fibre-rich foods are often not palatable and

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not liked by many consumers. Thus, it is pragmatic to develop food design strategies able to

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properly feed the microbiota keeping the sensory characteristics making Western foods attractive

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and rewarding (Pellegrini & Fogliano 2017).

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Beside the intrinsic nature of the food component, the type and the amount of food material

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reaching the lower gut depends on how the whole food is designed: by changing the food matrix,

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it is possible to modulate the nutrients digestibility. Mounting evidence indicates that nutrient

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bioavailability is not an absolute value defined for each nutrient, but it is influenced by the food ACS Paragon Plus Environment


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matrix as the digestion and absorption process is a time-dependent function. Most of the food

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components can only be absorbed after conversion into their basic units: proteins, triglycerides

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and polysaccharides into amino acids, free fatty acids and glucose, respectively. If a food has a

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strong and entangled matrix this conversion into the basic unit becomes very slow and the

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nutrients become de facto less bioavailable. In this case they will became potential substrates for

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the gut microbiota. As illustrated in Figure 1, designing food with a limited bioaccessibility could

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result in a low bioavailability of proteins, carbohydrates, lipids and phytochemicals resulting in

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higher levels of nutrient delivery to the microbiota and less calorie absorption for the host. This is

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a win-win situation especially for subjects living in an obesogenic environment and having no

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macro or micro nutrients deficiencies.

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Also looking at phytochemicals and micronutrients the proper balance between bioavailability and

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microbiota should be taken into account: the natural low bioavailability of food phytochemicals

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favoured the evolutionary capability of several microbes to metabolize them into signaling

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molecules. There is evidence showing how the microbiome variability is responsible for the

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formation of metabolites that can be measured in human urine and plasma and correlated with

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healthy status (Tomas-Barberan et al., 2017).

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From this viewpoint, it is clear that the way a food is designed can deeply influence the

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distribution of nutrients between the human body (i.e. the bioaccessible fraction) and the

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microbiota. Delaying the digestion kinetic can be an effective strategy to deliver the gut nutrients

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and micronutrients, which could be in theory 100% bioavailable to humans. In this vein, food

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design can be a powerful tool to modulate the microbiota. This targeted delivery can be achieved

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in many different ways both at industrial level and during domestic preparation of food. Some

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examples are provided in the following paragraphs illustrating strategies that can be useful both

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for both macro and micronutrients.

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1) Food particle size and macronutrient bioavailability: the bigger the lower.

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An extensive mechanical processing is often performed to make foods highly palatable. Convert

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raw materials into “flours and juices” is the easiest starting point to design any type of foods. In

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fact, from the food designers’ perspective, to work with ultra-processed, homogeneous and

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flexible ingredients is a great advantage. The extensive processing makes all nutrients fully

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accessible to the digestive enzymes accelerating their degradation and absorption, while limiting

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mechanical processing can reduce their bioavailability. Despite the common belief that digestion ACS Paragon Plus Environment

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starts in the mouth, the human masticatory apparatus is not able to perform an extensive particle

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size reduction. The formation of the bolus is mainly designed to avoid choke, not to facilitate the

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digestion process. Mounting evidence showed that the dimension of food particle size is inversely

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related to the absorption by human body. Studies with ileostomy subjects showed that 17% of

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starch from barley was not absorbed when 3 mm flaked particles rather than flour was provided.

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Similarly, soybean protein digestibility was improved processing the seeds into a fine flour.

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Therefore, it is not surprising that a significant reduction of the overall calorie intake can be

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achieved just by avoiding fine grinding (Capuano et al., 2018). In this framework, it has been

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reported that the anti-inflammatory effects of wheat bran is dependent on their particle size, the

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bigger the better, and this could be related to the changes in caecal Enterobacteriaceae (Suriano

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et al., 2018).

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Thermal treatments increases nutrients bioavailability

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Industrial and domestic cooking induce severe modifications in food, resulting in a generalized

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increase of macro and micro nutrient bioavailability. The most relevant effect is starch

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gelatinization: thermal treatment induces physical modifications of starch granules which are not

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well digestible to humans. Gelatinized starch becomes a good substrate for human amylases and

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starch is rapidly converted into glucose. Also heat-induced protein denaturation usually facilitates

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their digestion especially for plant proteins; however, in some cases thermal protein aggregation

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or thermally induced protein crosslinking can reduce or even revert this effect. Thermal treatment

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causes the swelling of plant food matrix which is a prerequisite for small molecules

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bioaccessibility. Solid evidence has been provided on the positive effect of domestic cooking on

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phytochemicals bioaccessibility especially using steaming and microwave (Palermo et al., 2014). In

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this respect, the effect of thermal treatment on carotenoids bioavailability can be used as the gold

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standard: processed tomatoes, especially in presence of oil, provide three times more bioavailable

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lycopene than the corresponding raw one (Rao, 2004). All together the amount of phytochemicals

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reaching the microbiota in a cooked food diet is lower than the corresponding raw one. Moreover,

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the opening of the vegetable food matrix makes the gut biotransformation of all food components

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more pronounced (Juaniz et al, 2017)

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2) Intactness of plant food tissue: plant cell walls can reduce nutrients bioavailability

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Intact plant cells are not a good substrate for the human digestion system: amylase, lipase and

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proteases cannot trespass the intact cell wall barrier and reach their substrates present in the ACS Paragon Plus Environment


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cytoplasm (Capuano et al., 2018). A large moiety of all macronutrients can reach the microbiota if

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the plant cell structure have not been destroyed by mechanical and thermal process. This effect is

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well known in raw almonds: up to 30% of lipids travels through the gastro intestinal tract

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entrapped within intact cells limiting the extent of lipids digestion (Grassby et al., 2017). On one

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hand, fine milling and extrusion cooking process combining heating, pressure and mechanical

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sheering to produce plasticized, expanded and cooked products disrupt all the barrier and

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organelles of the original plant material maximizing starch and lipid digestibility. On the other

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hand, it is possible to design food process to keep the cell wall intact and deliver more material to

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the gut microbiota as recently showed in beans cotyledon cells by Rovalino and coworkers

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(Rovalino et al., 2018).

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3) Designing a stronger food matrix to reduce macronutrient bioavailability

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There are different ways to design a strong food matrix favouring the delivery of nutrients into the

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gut. A network of highly crosslinked proteins is poorly bioavailable and it can delay the digestibility

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of the starch as observed in pasta. A network of proteins can delay the accessibility of lipid

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droplets to lipase: in cheese, it was found that the structure of the casein network and the size of

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the fat globules, which can be both modulated during cheese processing, are the main factors

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determining the lipid degradation kinetics into fatty acids (Capuano et al., 2018). Also strong non-

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covalent interactions formed in the gastro intestinal environment can result in massive

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aggregation limiting the bioaccessibility of proteins, lipids and starch. Protein gels obtained by

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cross linking or ionic gelation have different structural properties and different digestibility (Rui et

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al., 2016). Finally, the Maillard Reaction (MR) is a potent tool to strengthen the food matrix and

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reduce the protein digestibility as it happen in pasta dried at high temperature. MR promotes the

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formation of high molecular weight protein aggregates called melanoidins whose formation can

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well explain the decrease of protein digestibility observed in several roasted products. Also in this

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case the processing conditions of products like bread, bakery coffee, cocoa, roasted nuts can be

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designed to promote the formation of melanoidins and bring them to the gut microbiota (Delgado

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Andrade & Fogliano 2018). A limitation of this approach is that often the formation of melanoidins

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parallels that of potentially toxic compounds such as acrylamide. However, in these cases it is

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possible to implement strategies able to disentangle the formation of melanoidins from those of

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hazardous products (Palermo et al., 2016).

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4) Micronutrients and phytochemicals: naturally delivered to the gut ACS Paragon Plus Environment

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The low bioavailability of many micronutrients and phytochemicals was considered for many years

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a barrier to exploit their potential benefit on human health. This is actually a true concern for

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some vitamins such as Vitamin A and some minerals such as iron, zinc and calcium. However, for

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most of the phytochemicals the low bioavailability implies they are actually well available for the

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commensal bacteria, which can metabolize them and also produce new metabolites that are

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beneficial for human health. As highlighted in the following paragraph, the ability of human

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microbiota to convert specific phytochemicals into metabolites that can be absorbed in the body is

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highly variable. It is dependent on the presence of specific bacteria functions which are in turn

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dependent on the dietary exposure as well as on interaction with the host (Tomas-Barberan et al.,

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2017). The ultimate goal of food design should be to favour the delivery of phytochemicals to the

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gut by preserving their degradation during food processing and their excessive exposure during

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the passage in the upper part of gastrointestinal tract where they can be oxidized by the radicals

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formed during the digestion process.

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Nutrients for a profitable feeding of the gut microbiota

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The gut microbiota is characterized by a huge microbial diversity and its members can have

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different feeding requirements. It is known that an abundant supply of diverse foods promotes the

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biodiversity in the microbiota and also the variety of the microbial genes expressed that can be

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triggers of a health status. The next step is to obtain details on the specific conversion pathways of

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the various species: different precursors supplied through diet can be converted to beneficial or

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detrimental metabolites by members of the gut microbiota as schematized in Figure 2.

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The main food component to impact gut microbiota composition and activity is certainly fibre.

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Ancient dietary regimes in agrarian populations could reach 100 g intake per day while urban

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western populations eat only 15 g per day of fibre, while the recommended intake is above 25 g

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per day. By definition the dietary fibre goes through the small intestine, it reaches the colon and

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can be used by fibre-degrading members of the microbiota. The main results of such metabolism

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are short chain fatty acids (SCFAs), namely acetate, propionate and butyrate which have

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recognized health-promoting activities, such as anti-inflammatory, anti-carcinogenic and immune-

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regulatory functions (Louis et al., 2014; O’Keefe, 2016). The production of such beneficial

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molecules depends on the composition of the gut microbiota, but also on the quantity of

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consumed dietary fibre. Accordingly, increased levels of SCFAs were found in vegan, vegetarians

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and also in omnivore subjects with high-level adherence to the Mediterranean diet having a ACS Paragon Plus Environment


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remarkable daily intake of plant-based foods such as fruit vegetables and legumes (De Filippis et

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al., 2016). In addition, dietary fiber supplementation has been recently demonstrated to select

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specific groups of fibre-degrading bacteria and to increase SCFAs levels with beneficial effects on

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type 2 diabetes patients (Zhao et al., 2018). It is well known that the equilibrium of the gut

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bacteria is modulated by the dietary components reaching the gut and the metabolic degradation

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pathways of several specific class of macro and micronutrients has been elucidated. However, the

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inter-individual variability is very high and in many cases prolonged dietary exposure is the key

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factor underpinning the microbiota metabolic capacity. Some examples both of positive and

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negative consequences of microbiota action are provided in the following lines.

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Phytoestrogens are plant-derived polyphenols with a chemical structure similar to human

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estrogens that are associated to multiple health benefits. They occur at high levels in soya, seeds,

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fruits, vegetables, cereals, and also in coffee, tea and chocolate. Ingested polyphenols are poorly

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absorbed in the small intestine and remarkable quantities may be available in the colon. The gut

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microbiota can convert isoflavones, ellagitannins, and lignans to equol, urolithins, and

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enterolignans, respectively, which are recognized to have anti-inflammatory effects and induce

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anti-proliferative activities. These compounds are more bioavailable and display a higher level of

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estrogenic/antiestrogenic and antioxidant activities compared to their precursors (Gaya et al.

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2016). The polyphenol converting bacteria belong to the dominant phyla of the human intestine

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(Braune and Blaut, 2016), although the knowledge on the capability to metabolize polyphenols by

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gut bacteria is currently far from exhaustive. The individual gut microbiota seems to play an

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important role on the potential for colon activation of phytoestrogens. Equol is formed from

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isoflavones present in soy-based foods particularly daidzein. The introduction of soy-based foods

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in a diet does not necessarily determine equol production (Atkinson et al., 2005) suggesting an

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important role of the individual composition of the gut microbiota and its functional capability on

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equol production. Interestingly, more than 60% of Asian residents were found as equol producers

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from soy isoflavones, while only 30% of the Western populations display the same functionality

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(Magee, 2011). Indeed, westernization could be the cause of the loss of the equol producing

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ability as a consequence of different gut microbiome structure and different dietary patterns

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consumed. Accordingly, Wu et al. (2016), found that less than 50% of recruited western vegans

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produced equol.


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The aryl hydrocarbon receptor (AhR) is an important factor in intestinal homeostasis. AhR is not

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only able to respond to exogenous stimuli but also to endogenous ligands that are generated from

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host-cell interactions, diet and microbiota metabolism. Therefore, AhR is considered as a sensor

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that connects the gut lumen environment with cellular processes with consequences for immune

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functioning (Zelante et al, 2013). Microbes-mediated metabolism of polyphenols, glucosinolates

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and tryptophan can generate ligands for AhR thus contributing to homeostasis. Glucosinolates are

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supplied by vegetables foods and can be also converted by gut microbes to isothiocyanates, which

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are able to activate cytoprotective, antioxidant responses (Dinkova-Kostova and Kostov, 2012).

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Interestingly, also compounds only present in processed foods such as the Maillard Reaction

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products can be metabolised by specific members of the microbiota, as demonstrated for a strain

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of Intestinimonas that was proven able to convert fructoselysine into butyrate (Bui et al. 2015).

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Moreover, the capability of human microbiota to use melanoidins as preferential substrate for

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bifidobacteria is documented especially for those present in coffee and bread crust (Delgado-

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Andrade & Fogliano 2018)

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Some other microbial metabolism of dietary components leads to the production of detrimental

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molecules. Choline and carnitine are particularly abundant in foods of animal origin such as meat,

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poultry and eggs. They are precursors of trimethylamine (TMA) that is produced from choline and

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carnitine by some members of the gut microbiota. Once absorbed, TMA is oxidized to

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trimethylamine oxide (TMAO) in the liver and TMAO is has been associated to cardiovascular risk.

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The most recent studies are targeting the discovery of yet not well known members of the gut

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microbiota that are able to degrade TMA and thus to contrast the activity of TMA producers

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(Borrel et al., 2017). In addition, a fat-rich diet determines higher levels of bile in the colon, where

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members of the microbiota may turn bile acids into secondary bile acids, mainly deoxycholic and

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lithocholic acids. These can be involved in processes linked to colorectal carcinogenesis, such as

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apoptosis, cell proliferation and DNA damage induction (Ou et al., 2013).

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In summary, mounting evidence indicates the way a food is designed will ultimately define the

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diversity of microbial metabolites released in the gut. This is not only relevant for the microbiota

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wellness but also for the host health through a number of physical connections and biochemical

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signalling indicated as gut-organ axis.

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The gut-organ axis



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The connection of microbiota wellness with the functioning of the liver is obvious: microbiota

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metabolites are carried to the liver through the portal vein: microbial dysbiosis are often the cause

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of liver inflammatory status. Similarly for all the parameters connected to the cardio circulatory

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system: mounting evidence indicates that the signal triggered by the gut microbes and their

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metabolites are directly responsible of the LDL and endothelium functionality as well as of many

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factors connected to the glucose managing capability. Finally, current trends in gut-brain axis

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science recognizes a role of the gut microbiome to interact with the brain. Psychobiotics have

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been recently defined as “any substance that exerts a microbiome-mediated psychological effect”

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and that are thus not limited to probiotics and prebiotics (Sarkar et al., 2016). Psychobiotics exert

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anxiolytic and antidepressant effects characterised by changes in emotional, cognitive, systemic,

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and neural indices (Sarkar et al., 2016). For example, bacteria crucially affect the metabolism of

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tryptophan into serotonin, whose effect on mood is recognized. In addition, the potential anti-

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inflammatory activity of gut microbes upon fibre degradation and SCFA production can stimulate

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positive responses at systemic level and be involved in emotional responses. In light of this, it is

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tantalizing to imagine food designed to act as psychobiotic, because is maybe enriched with

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prebiotic fibre or probiotics with recognized effect on human behaviour. Indeed, in a first evidence

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on humans, supplying B-GOS determined a significant reduction of waking-cortisol response, with

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a possible consequent decrease in emotional disturbances (Schmidt et al., 2015).

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In summary, the recipe to design of the perfect food is not available. However, the message we

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can take from the available knowledge is that beyond having the desired nutritional, technological,

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sensory and healthy properties, the design of novel foods should take care of the nutrients’

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availability for the host and its microbes. Ingredients formulation and processing technology

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tailoring the bioavailability of nutrients on the specific need of each individual and especially of

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our powerful symbionts will be the starting point to enter the new era of personalized nutrition.

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Figure Legend Figure 1: The way food is design has a pivotal role in defining the quantity and type of material reaching the gut microbiota. More abundant and diverse feeding material favour its health status

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Figure 2: Dietary precursors and possible beneficial and/or detrimental metabolites produced by the gut microbiota.

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Figure 2


Food Design To Feed the Human Gut Microbiota - Journal of

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