Review
Interactions of gut microbiota with functional food components and nutraceuticals

https://doi.org/10.1016/j.phrs.2009.11.001Get rights and content

Abstract

The human gut is populated by an array of bacterial species, which develop important metabolic and immune functions, with a marked effect on the nutritional and health status of the host. Dietary component also play beneficial roles beyond basic nutrition, leading to the development of the functional food concept and nutraceuticals. Prebiotics, polyunsaturated fatty acids (PUFAs) and phytochemicals are the most well characterized dietary bioactive compounds. The beneficial effects of prebiotics mainly relay on their influence on the gut microbiota composition and their ability to generate fermentation products (short-chain fatty acids) with diverse biological roles. PUFAs include the ω-3 and ω-6 fatty acids, whose balance may influence diverse aspects of immunity and metabolism. Moreover, interactions between PUFAs and components of the gut microbiota may also influence their biological roles. Phytochemicals are bioactive non-nutrient plant compounds, which have raised interest because of their potential effects as antioxidants, antiestrogenics, anti-inflammatory, immunomodulatory, and anticarcinogenics. However, the bioavailability and effects of polyphenols greatly depend on their transformation by components of the gut microbiota. Phytochemicals and their metabolic products may also inhibit pathogenic bacteria while stimulate the growth of beneficial bacteria, exerting prebiotic-like effects. Therefore, the intestinal microbiota is both a target for nutritional intervention and a factor influencing the biological activity of other food compounds acquired orally. This review focuses on the reciprocal interactions between the gut microbiota and functional food components, and the consequences of these interactions on human health.

Graphical abstract

The reciprocal interactions between the gut microbiota and functional food components influence their effects on human health. The gut microbiota transforms dietary compounds into different bioactive metabolites in vivo and, in turn, food bioactive compounds might influence the gut microbiota composition and its physiological effects on mammalian tissues.

  1. Download : Download full-size image

Introduction

The intestinal tract harbours a complex bacterial community (microbiota), integrated by more than 800 different bacterial species, which have an enormous impact on the nutritional and health status of the host. The metabolic activity developed by the gut microbiota contributes to the digestion of dietary compounds, salvage of energy, supply of (micro)nutrients and transformation of xenobiotics. Overall, a balanced gut microbiota composition confers benefits to the host, while microbial imbalances are associated with metabolic and immune-mediated disorders [1], [2]. The composition of the gut microbiota is influenced by endogenous and environmental factors (diet, antibiotic intake, xenobiotics, etc.). Of these factors, the diet is considered a major driver for changes in gut bacterial diversity that may affect its functional relationships with the host [3]. In fact, the microbiome of the adult-type and infant-type microbiota has distinct gene contents to accommodate nutrient acquisition strategies to different diets [4].

The primary role of diet is providing sufficient nutrients to meet the basic nutritional requirements for maintenance and growth, while giving the consumer a feeling of satisfaction and well-being. In addition, some food components exert beneficial effects beyond basic nutrition, leading to the concept of functional foods and nutraceuticals [5]. Functional foods are those foods that provide benefits beyond basic nutrition when consumed as part of the regular diet. Nutraceuticals are extracts containing the biologically active food components supplied in other than a food form. Dietary components with biological effects are susceptible to be metabolized by intestinal bacteria during the gastrointestinal passage, prior being absorbed. The colon has the highest bacterial load and constitutes an active site of metabolism rather than a simple excretion route [6]. The metabolic activity of the gut microbiota on bioactive food components can modify the host exposure to these components and their potential healthy effects. Furthermore, some functional food components influence the growth and/or metabolic activity of the gut microbiota and, thereby, its composition and functions [7], [8]. Therefore, the intestinal microbiota is both a target for nutritional intervention to improving health and a factor influencing the biological activity of other food compounds acquired orally. This review focuses on the reciprocal interactions between the gut microbiota and functional food components, and the consequences of these interactions on human health (Fig. 1).

Section snippets

Gut microbial ecology

The human gut is populated by a vast number of bacterial species (more than 800) that reach the highest concentrations in the colon (up to 1012 cells per gram of faeces). The gut colonization process starts immediately after birth and the development and establishment of the infant's microbiota highly depend on environmental factors. The infant's microbiota initially shows low diversity and instability, but evolves into a more stable adult-type microbiota over the first 24 months of life [9].

Roles of the gut microbiota in host physiology and health

The gut microbiota develops a number of protective, immune and metabolic functions, which altogether have an enormous impact on the nutritional and health status of the host. The indigenous gut microbiota and transient bacteria (food-associated and probiotics) are known to influence the development and regulation of the host's defences, of immune and non-immune nature, via interaction with the epithelium and the gut-associated lymphoid tissue [13]. The intestinal epithelium constitutes a

Prebiotics and gut microbiota

Prebiotics are non-digestible food ingredients, mostly oligosaccharides, which beneficially affect the host by stimulating growth, activity or both of specific intestinal bacteria [38]. The criteria that have to fulfil a prebiotic include, (1) resistance to gastric acidity and mammalian enzymes; (2) susceptibility to be fermented by gut microbiota; and (3) ability to stimulate the growth and/or activity of beneficial intestinal bacteria. The possible beneficial effects of prebiotics include the

Polyunsaturated fatty acids (PUFAs) and gut microbiota

PUFA are fatty acids that contain more than one double bond, which are separated from each other by a single methylene group. The ω-3 fatty acids (linolenic, ecosapentaenoic and docosahexaenoic acids) and ω-6 fatty acids (linoleic and arachidonic acids) are the best characterized so far. The biological effects of the ω-3 and ω-6 fatty acids are largely mediated by their mutual interactions. The possible underlying mechanisms by which PUFA exert their beneficial effects on health are diverse,

Phytochemicals and gut microbiota

Phytochemicals are defined as bioactive non-nutrient plant compounds present in fruits, vegetables, grains, and other plant foods, whose ingestion has been linked to reductions in risk of major chronic diseases [70]. The different compounds included in this group can be classified according to common structural features into carotenoids, phenolics, alkaloids and nitrogen-containing and organosulfur compounds. Phenolics, flavonoids and phytoestrogens have raised particular interest because of

Conclusions and future perspectives

The gut microbiota exerts an enormous impact on the nutritional and health status of the host via modulation of the immune and metabolic functions. The microbiome provides additional enzymatic activities involved in the transformation of dietary compounds. Food bioactive compounds also exert significant effects on the intestinal environment, modulating the gut microbiota composition and probably its functional effects on mammalian tissues. This evidence is changing the way the biological roles

Acknowledgements

This work was supported by grants AGL2008-01440/ALI and Consolider Fun-C-Food CSD2007-00063 from the Spanish Ministry of Science and Innovation (MICINN, Spain) and PIF08-010-4 form CSIC. J.M. Laparra has a postdoctoral contract of the programme “Juan de la Cierva” (MICINN, Spain).

References (94)

  • V. Marcil et al.

    Butyrate impairs lipid transport by inhibiting microsomal triglyceride transfer protein in Caco-2 cells

    J Nutr

    (2003)
  • A. Napolitano et al.

    Potential prebiotic activity of oligosaccharides obtained by enzymatic conversion of durum wheat insoluble dietary fibre into soluble dietary fibre

    Nutr Metab Cardiovasc Dis

    (2009)
  • M.D. Howard et al.

    Dietary fructooligosaccharide, xylooligosaccharide and gum arabic have variable effects on cecal and colonic microbiota and epithelial cell proliferation in mice and rats

    J Nutr

    (1995)
  • U.N. Das

    Beneficial effect(s) of n-3 fatty acids in cardiovascular diseases: but, why and how?

    Prostaglandins Leukot Essent Fatty Acids

    (2000)
  • S. Straniero et al.

    Deficiency and supplementation of PUFA in the diet have similar effects on the age-associated changes in rat-plasma cholesterol levels

    Mech Ageing Dev

    (2008)
  • P.E. Kankaanpää et al.

    The influence of polyunsaturated fatty acids on probiotic growth and adhesion

    FEMS Microbiol Lett

    (2001)
  • P.E. Kankaanpää et al.

    Influence of probiotic supplemented infant formula on composition of plasma lipids in atopic infants

    J Nutr Biochem

    (2002)
  • R.H. Liu

    Potential synergy of phytochemicals in cancer prevention: mechanism of action

    J Nutr

    (2004)
  • M.G. Hertog et al.

    Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen elderly study

    Lancet

    (1993)
  • P.A. Ruiz et al.

    Functional diversity of flavonoids in the inhibition of the proinflammatory NF-kappaB, IRF, and Akt signaling pathways in murine intestinal epithelial cells

    J Nutr

    (2006)
  • P.A. Ruiz et al.

    Quercetin inhibits TNF-induced NF-kappaB transcription factor recruitment to proinflammatory gene promoters in murine intestinal epithelial cells

    J Nutr

    (2007)
  • E. Ramiro-Puig et al.

    Intestinal immune system of young rats influenced by cocoa-enriched diet

    J Nutr Biochem

    (2008)
  • S.J. Zunino et al.

    Resveratrol alters proliferative responses and apoptosis in human activated B lymphocytes in vitro

    J Nutr

    (2009)
  • A. Scalbert et al.

    Absorption and metabolism of polyphenols in the gut and impact on health

    Biomed Pharmacother

    (2002)
  • E. Bowey et al.

    Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human associated rats

    Food Chem Toxicol

    (2003)
  • H.C. Lee et al.

    Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota

    Res Microbiol

    (2006)
  • S.G. Parkar et al.

    The potential influence of fruit polyphenols on colonic microflora and human gut health

    Int J Food Microbiol

    (2008)
  • I. Nadal et al.

    Imbalance in the composition of the duodenal microbiota of children with coeliac disease

    J Med Microbiol

    (2007)
  • A. Santacruz et al.

    Interplay between weight loss and gut microbiota composition in overweight adolescents

    Obesity

    (2009)
  • R.E. Ley et al.

    Worlds within worlds: evolution of the vertebrate gut microbiota

    Nat Rev Microbiol

    (2008)
  • K. Kurokawa et al.

    Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes

    DNA Res

    (2007)
  • A.M. Aura

    Microbial metabolism of dietary phenolic compounds in the colon

    Phytochem Rev

    (2008)
  • G.R. Gibson et al.

    Prebiotics and resistance to gastrointestinal infections

    Br J Nutr

    (2005)
  • E.G. Zoetendal et al.

    Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria

    Appl Environ Microbiol

    (1998)
  • M. Gueimonde et al.

    Presence of specific antibiotic (tet) resistance genes in infant faecal microbiota

    FEMS Immunol Med Microbiol

    (2006)
  • J. Xu et al.

    Evolution of symbiotic bacteria in the distal human intestine

    PLoS Biol

    (2007)
  • Y. Sanz et al.

    Indigenous gut microbiota, probiotics, and coeliac disease

  • Y. Sanz et al.

    Gut microbiota and probiotics in modulation of epithelium and gut-associated lymphoid tissue function

    Int Rev Immunol

    (2009)
  • L.V. Hooper et al.

    How host-microbial interactions shape the nutrient environment of the mammalian intestine

    Annu Rev Nutr

    (2002)
  • S.R. Gill et al.

    Metagenomic analysis of the human distal gut microbiome

    Science

    (2006)
  • I.D. Wilson et al.

    The role of gut microbiota in drug response

    Curr Pharm Des

    (2009)
  • P.J. Turnbaugh et al.

    The human microbiome project

    Nature

    (2007)
  • M.A. Schell et al.

    The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract

    Proc Natl Acad Sci USA

    (2002)
  • M. Dabek et al.

    Distribution of beta-glucosidase and beta-glucuronidase activity and of beta-glucuronidase gene gus in human colonic bacteria

    FEMS Microbiol Ecol

    (2008)
  • H.J. Flint et al.

    Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis

    Nat Rev Microbiol

    (2008)
  • H.M. Hamer et al.

    The role of butyrate on colonic function

    Aliment Pharmacol Ther

    (2008)
  • M. Gueimonde et al.

    Induction of alpha-l-arabinofuranosidase activity by monomeric carbohydrates in Bifidobacterium longum and ubiquity of encoding genes

    Arch Microbiol

    (2007)
  • Cited by (550)

    View all citing articles on Scopus
    View full text