Establishment of Normal Gut Microbiota Is Compromised under Excessive Hygiene Conditions

Article (PDF Available)inPLoS ONE 6(12):e28284 · December 2011with51 Reads
DOI: 10.1371/journal.pone.0028284 · Source: PubMed
Abstract
Early gut colonization events are purported to have a major impact on the incidence of infectious, inflammatory and autoimmune diseases in later life. Hence, factors which influence this process may have important implications for both human and animal health. Previously, we demonstrated strong influences of early-life environment on gut microbiota composition in adult pigs. Here, we sought to further investigate the impact of limiting microbial exposure during early life on the development of the pig gut microbiota. Outdoor- and indoor-reared animals, exposed to the microbiota in their natural rearing environment for the first two days of life, were transferred to an isolator facility and adult gut microbial diversity was analyzed by 16S rRNA gene sequencing. From a total of 2,196 high-quality 16S rRNA gene sequences, 440 phylotypes were identified in the outdoor group and 431 phylotypes in the indoor group. The majority of clones were assigned to the four phyla Firmicutes (67.5% of all sequences), Proteobacteria (17.7%), Bacteroidetes (13.5%) and to a lesser extent, Actinobacteria (0.1%). Although the initial maternal and environmental microbial inoculum of isolator-reared animals was identical to that of their naturally-reared littermates, the microbial succession and stabilization events reported previously in naturally-reared outdoor animals did not occur. In contrast, the gut microbiota of isolator-reared animals remained highly diverse containing a large number of distinct phylotypes. The results documented here indicate that establishment and development of the normal gut microbiota requires continuous microbial exposure during the early stages of life and this process is compromised under conditions of excessive hygiene.
    • "The bacterial diversity and community in fish intestines vary greatly from herbivorous to carnivorous life styles (Table 2). In general, the balance of gut microbial composition can be altered by many factors, such as nutritional status (Turnbaugh et al. 2009), stress (Kelly 2010), degree of hygiene (Schmidt et al. 2011), antibiotics (Tanaka et al. 2009), age (Hopkins et al. 2002) and infection (Dethlefsen et al. 2006 ). However, information regarding the bacterial composition is often controversial . "
    [Show abstract] [Hide abstract] ABSTRACT: The bacterial community in the fish gut is very dense compared to surrounding water, which suggests that gastrointestinal tract (GIT) provides a favorable ecological niche for survival. GIT bacteria can be broadly divided into two groups; autochthonous (able to colonize on the mucosal surface) and allochthonous (free living). From the host’s point of view, autochthonous bacteria are considered to be more important than allochthonous, as they provide both nutritional as well as disease prevention support to the host. Among their several functions, the autochthonous bacteria are believed to produce several types of extracellular enzymes, block the attachment site for pathogens and secrete a wide range of bacteriocins. Most of the bacterial species in the gut are non-culturable and thus several types of sophisticated techniques such as Denaturing Gradient Gel Electrophoresis (DGGE), Temperature Gradient Gel Electrophoresis (TGGE) and Next Generation Sequencing (NGS) have been introduced to explore the microbial communities in gut. In this present review, we have summarized the impact of gut bacteria in fish with special emphasis on extracellular enzyme production by gut microbiota, bacterial composition, mechanism of attachment in epithelial surface and their role in disease prevention.
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    • "The four major bacteria phyla in the intestine (Actinobacteria, Bacteroides, Firmicutes, and Proteobacteria) have been found in meconium. Experimental studies in pigs indicate that the establishment and development of a normal gut microbiota and immune system require continuous microbial exposure during the first months of life, and that can be compromised by excessive hygiene (Schmidt et al., 2011). It has been suggested that the composition and diversity stabilize and reach the level of adult microbiota within the first three years of life (Yatsunenko et al., 2012). "
    [Show abstract] [Hide abstract] ABSTRACT: Food allergy has rapidly increased in prevalence, suggesting an important role for environmental factors in disease susceptibility. The immune response of food allergy is characterized by IgE production, and new findings from mouse and human studies indicate an important role of the cytokine IL-9, which is derived from both T cells and mast cells, in disease manifestations. Emerging evidence suggests that route of exposure to food, particularly peanut, is important. Exposure through the skin promotes sensitization while early exposure through the gastrointestinal tract promotes tolerance. Evidence from mouse studies indicate a role of the microbiome in development of food allergy, which is supported by correlative human studies showing a dysbiosis in food allergy. There is no approved treatment for food allergy, but emerging therapies are focused on allergen immunotherapy to provide desensitization, while pre-clinical studies are focused on using adjuvants or novel delivery approaches to improve efficacy and safety of immunotherapy.
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    • "Nevertheless, it is currently not known whether the changes in the gut microbiota in IBD are due to a disturbed local environment because of the inflammation or are a primary cause for the development of these disease entities. Like in other mammals, the human gut microbiota consists of different phyla, mainly Firmicutes, Bacteroidetes, Actinobacteria, and Proteobacteria293031. Most taxa from the intestinal microbiota belong to the phyla Firmicutes and Bacteroidetes. "
    [Show abstract] [Hide abstract] ABSTRACT: Introduction: Changes in the intestinal bacterial composition seem to play a major role in the pathogenesis and in the clinical course of inflammatory bowel diseases (IBD), which consist of Crohn's disease (CD), and ulcerative colitis (UC). Mutations in the NOD2 gene are the most important genetic risk factors for the development of CD. In this study, the association between mucosal biopsies and the mucosa-associated bacterial composition from CD and UC patients regarding their genetic risk factors (mutations in the NOD2 gene), their endoscopic activity, and their medical therapy (TNF-α blocking therapy) was examined. Material and methods: Seventy biopsies from routine colonoscopies from 33 IBD patients (26 CD and 7 UC) were obtained. Disease activity and clinical characteristics were assessed. Seven different bacterial strains (Bacteroides fragilis, Escherichia coli, Prevotella melaninogenica, Clostridium coccoides, Clostridium difficile, Bifidobacterium bifidum, and Faecalibacterium prausnitzii) were quantified using real-time PCR. NOD2 genotyping from patients with CD was performed. Results: Five of the 24 patients were positive for at least one mutation in the NOD2 gene. The bacterial composition was different in CD compared to UC, in macroscopic healthy compared to macroscopic inflamed biopsies, in NOD2 mutated compared to NOD2 wildtype patients, and in patients receiving TNF-α blocking therapy compared to patients without this treatment. Conclusion: This study further characterizes the mucosa-associated bacteria in IBD patients. Different clinical situations lead to an altered mucosa-associated bacterial composition. The analyzed bacteria could be promising targets for cost-effective surveillance or therapies in IBD patients.
    Article · Mar 2016
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