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Intestinal Microbiota in Human Health and Disease: the Impact of Probiotics

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Intestinal Microbiota in Human Health and Disease: the Impact of Probiotics Genes Nutr (2011) 6:209–240 DOI 10.1007/s12263-011-0229-7 REVIEW Intestinal microbiota in human health and disease: the impact of probiotics Jacoline Gerritsen • Hauke Smidt • Ger T. Rijkers • Willem M. de Vos Received: 4 February 2011 / Accepted: 20 April 2011 / Published online: 27 May 2011 Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract The complex communities of microorganisms Keywords Diversity Á Dysbiosis Á Host-microbe that colonise the human gastrointestinal tract play an interactions Á Intestinal microbiota Á Probiotics important role in human health. The development of cul- ture-independent molecular techniques has provided new insights in the composition and diversity of the intestinal Introduction microbiota. Here, we summarise the present state of the art on the intestinal microbiota with specific attention for the It is known for over three decades that the human body application of high-throughput functional microbiomic contains tenfold more microbial cells (1014) than human approaches to determine the contribution of the intestinal cells (Savage 1977). These microorganisms colonise microbiota to human health. Moreover, we review the practically every surface of the human body that is exposed association between dysbiosis of the microbiota and both to the external environment, including the skin, oral cavity, intestinal and extra-intestinal diseases. Finally, we discuss respiratory, urogenital and gastrointestinal tract. Of these the potential of probiotic microorganism to modulate the body sites, the gastrointestinal (GI) tract is by far the most intestinal microbiota and thereby contribute to health and densely colonised organ. The complex community of well-being. The effects of probiotic consumption on the microorganisms residing in or passing through the GI tract intestinal microbiota are addressed, as well as the devel- is referred to as the intestinal microbiota. opment of tailor-made probiotics designed for specific The intestinal microbiota plays a role in metabolic, aberrations that are associated with microbial dysbiosis. nutritional, physiological and immunological processes in the human body. It exerts important metabolic activities by extracting energy from otherwise indigestible dietary & J. Gerritsen ( ) Á H. Smidt Á W. M. de Vos polysaccharides such as resistant starch and dietary fibres. Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, The Netherlands These metabolic activities also lead to the production of e-mail: [email protected] important nutrients, such as short-chain fatty acids (SCFA), vitamins (e.g. vitamin K, vitamin B12 and folic acid) and J. Gerritsen amino acids, which humans are unable to produce them- Winclove Bio Industries B.V., Amsterdam, The Netherlands selves (Hamer et al. 2008; Wong et al. 2006). In addition, G. T. Rijkers the intestinal microbiota participates in the defence against Department of Medical Microbiology and Immunology, pathogens by mechanisms such as colonisation resistance St. Antonius Hospital, Nieuwegein, The Netherlands and production of antimicrobial compounds. Furthermore, G. T. Rijkers the intestinal microbiota is involved in the development, Department of Operating Rooms, University Medical Center St. maturation and maintenance of the GI sensory and motoric Radboud, Nijmegen, The Netherlands functions, the intestinal barrier and the mucosal immune system. These are just a few examples of the functional W. M. de Vos Departments of Microbiology and Immunology and Veterinary contributions of the intestinal microbiota to human health, Biosciences, University of Helsinki, Helsinki, Finland a subject that is regularly reviewed (Barbara et al. 2005; 123 210 Genes Nutr (2011) 6:209–240 Cerf–Bensussan and Gaboriau–Routhiau 2010; O’Hara each species in a specific ecosystem. These definitions are and Shanahan 2006; Sekirov et al. 2010; Zoetendal et al. used to describe the microbial diversity in the GI tract. 2008). Up till recently, conventional culture-based methods In recent years, a sharp increase is seen in the number of were used to assess the intestinal microbial diversity. Over publications addressing the intestinal microbiota. They 400 bacterial species have been successfully isolated, cul- have provided various lines of evidence supporting a close tured and characterised from the human GI tract (Rajilic´- link between the intestinal microbiota and human health. Stojanovic´ et al. 2007). However, these culture-based This review aims to summarise the current knowledge on methods have proven to be inadequate in determining the the composition and diversity of the intestinal microbiota. true microbial diversity of the intestinal microbiota since a In addition, it is discussed how new molecular approaches large fraction of the microbiota remains uncultivated. For a have provided novel insights towards the phylogenetic and more accurate analysis of the compositional diversity of the functional characterisation of the intestinal microbiota. intestinal microbiota culture-independent approaches have Furthermore, recent insights on the link between the been developed and it has been revealed that the human intestinal microbiota and human health are provided. intestinal microbiota is an even more complex ecosystem Finally, an overview is presented of ways to modulate the than previously expected. Most of these techniques target intestinal microbiota with specific attention for the use of the highly conserved 16S ribosomal RNA (rRNA) gene probiotics, defined as live microorganisms which, when sequences of bacterial and archaeal microorganisms. administered in adequate amounts, confer a health benefit Molecular techniques that are used to study the diversity of on the host (FAO/WHO 2002). the intestinal microbiota include quantitative polymerase chain reaction (qPCR), temperature or denaturing gradient gel electrophoresis (TGGE or DGGE), terminal-restriction Microbial diversity in the GI tract fragment length polymorphism (T-RFLP) and fluorescent in situ hybridisation (FISH). The latest developments in The GI tract is a complex and dynamic ecosystem con- high-throughput technologies, such as next generation taining a diverse collection of microorganisms. These sequencing and phylogenetic micro-arrays, now allow microorganisms are either resident members of the intes- more in-depth analysis of the complete phylogenetic tinal microbiota or transient passengers introduced from diversity of the intestinal microbiota (Van den Bogert et al. the environment, for example by the regularly influx of 2011; Zoetendal et al. 2008). Moving beyond the analysis microorganisms by the intake of food. of the variation in the sequence of a single marker gene, it is currently also possible to characterise the complete Compositional diversity of the intestinal microbiota genetic material obtained from environmental samples such as the GI tract. With the aid of large-scale sequencing The intestinal microbiota can be described in richness approaches these so called metagenomes can be studied (‘who is present’) and evenness (‘with how many are they and so far several metagenomic inventories of the intestinal present’) that together form the ecological terms of diver- microbiota have been reported (Table 1). sity. If applied at the species-level, richness describes the Since the first application of culture-independent meth- number of species present in a specific ecosystem, not ods to determine diversity, it has been shown that the taking into account their relative abundance. This contrasts composition of the intestinal microbiota varies substan- with evenness, which represents the relative abundance of tially amongst individuals (Zoetendal et al. 1998). At least Table 1 Overview of metagenomic studies of the human intestinal microbiota Nationality of Number of Sequencing technology Total length of References individuals individuals sequences obtained (Gb) American 2 Sanger 0.2 Gill et al. (2006) Japanese 13 Sanger 0.727 Kurokawa et al. (2007) American 18 454 FLX Titanium 2.14 Turnbaugh et al. (2009) European (Danish or Spanish) 124 Solexa (Illumina) 576.7 MetaHIT Qin et al. (2010) European 20 Sanger 2.6 Genescope French 49 SoliD 200 INRA 123 Genes Nutr (2011) 6:209–240 211 part of this diversity can be attributed to genetic differences GI tract, with the methanogens, Methanobrevibacter smi- amongst hosts. A positive relation between similarity in thii and Methanosphaera stadtmanae being by far the most dominant faecal microbial communities and genetic related- dominant archaeal groups (Gill et al. 2006; Mihajlovski ness of the hosts has been observed (Stewart et al. 2005; et al. 2008). While it was previously assumed that these Turnbaugh et al. 2009; Zoetendal et al. 2001). It is esti- methanogens were only present in a minor fraction of mated that more than 1,000 species-level phylotypes can be healthy subjects, application of new DNA isolation meth- found in the GI tract of the total human population (Qin ods has led to the observation that they are in fact highly et al. 2010; Rajilic´-Stojanovic´ et al. 2007). However, the prevalent (Dridi et al. 2009; Salonen et al. 2010b). In phylogenetic diversity in one individual is much lower, addition to bacteria and archaea, eukaryotic micro- since the intestinal microbiota of each individual only organisms can also be members of the intestinal micro- consists of approximately 160 different bacterial species biota. Culture-independent analysis of the fungal
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