The human intestine is home to trillions of bacteria. Investigation of the colonization of the infant gut by these microorganisms is a prelude to understanding how they may act in both health and disease.
At birth, babies emerge from a sterile environment into one that is laden with microbes. The infant's intestine then rapidly becomes home to one of the densest populations of bacteria on Earth. Writing in PLoS Biology, Palmer et al.1 report the most comprehensive analysis to date of the bacteria that first take up residence in the human intestine.
Interest in this ecosystem stems in part from the discovery of numerous benefits that arise from our intestinal microbiota: these bacteria help in extracting nutrients from food, and are instrumental in the development of the gut2,3 and the immune system4 after birth. However, gut microbes have also been linked to several disease states, including inflammatory bowel diseases and colon cancer, and less directly to maladies such as asthma, rheumatoid arthritis, atopic dermatitis and even autism5,6. An accurate and comprehensive analysis of the microbes present in the developing microbiota of the infant is an essential first step towards understanding which of them may affect the health of the host.
Palmer et al.1 analysed the microbial composition of the intestinal ecosystem of 14 infants by sampling their faeces. Sampling began with the first stool after birth, and was followed by 25 further samples from each infant over their first year of life. The authors' method of quantifying the bacterial composition avoided the need to culture the bacteria. It involved use of a comprehensive DNA microarray that differentiated and quantified the distinct taxonomic groups present in the samples.
There are 22 broad taxonomic groupings, or phyla, of bacteria, but the bacteria abundant in the infant intestine fell into only three of them: the Gram-positive bacteria (Firmicutes and Actinobacteria), the Bacteroidetes and the Proteobacteria. Given the broad nature of these taxonomic groupings, the results are not entirely surprising — most of the bacteria known to associate with humans fall into these three major groupings. A previous analysis of the intestinal microbiota of healthy adults demonstrated the abundance of only two of these three phyla7, with members of the Proteobacteria being only minor components. Proteobacteria are facultative anaerobes — that is, they can grow in the presence or absence of oxygen. They may be early settlers that are necessary to create the reduced environment required for the ensuing colonization by obligate anaerobes, which require oxygen-free conditions.
Contrasting with the similarity in the infants' microbiota at the phylum level, Palmer et al. found a remarkable degree of species-level variation, especially during the first few months. Some species appeared only transiently; others persisted for weeks to months. In general, there was no discernible pattern of abundant species or temporal mode of acquisition of particular organisms in different individuals. The two infants whose microbiotas were the most similar to each other were fraternal twins. These babies share both similar genetics and a similar environment. But their microbial profiles were no more like those of their own parents than they were to those of the parents of the other infants, implying that environment may play a greater role than genetics.
To try to identify the origin of the early colonizers, Palmer et al. investigated two relevant sources — the microbiotas of maternal vaginal fluid and of breast milk. The lactobacilli that predominate in the vaginal microbiota were not abundant in the early faecal samples, and the bacterial sample of only one infant 'clustered' with the vaginal microbiota of its mother, and then only during the first day after birth. So it seems that vaginal birth does not make a lasting contribution to an infant's intestinal microbiota. All babies in this study were breast-fed to some extent, but their intestinal microbiotas did not cluster with those of their mother's milk. Surprisingly, bifidobacterial species turned out to be only minor components: it is generally accepted that these bacteria are abundant in the stool samples of breast-fed infants, and that they are beneficial to their host.
Although the early microbiota of the gut seems largely to result from chance microbial encounters, by one year old there was a consistent convergence towards that of an adult-like microbiota, often coinciding with the introduction of solid food. Therefore, despite the absence of a programmed succession of early organisms, factors such as diet, gut development and environmental changes (possibly induced by the early colonizers) eventually result in the stable colonization of characteristic members of the adult microbiota. A notable exception was the lack of methanogenic archaea in the one-year samples. These organisms are abundant in the adult intestinal microbiota7, where they consume methane produced by bacterial members.
Palmer and colleagues' methods1 could be used to identify differences in the microbiotas of specific groups of infants and young children. A couple of examples suggest themselves.
First, an aspect only briefly mentioned in this paper is the effect of antibiotic treatment on microbial composition: although some antibiotics severely reduced the microbial load, the authors did not identify any consistent consequences of such treatment. Given the frequent use of antibiotics in children, this is a topic well worth following up with more focused and comprehensive analyses.
Second, it has been proposed that the increased prevalence of chronic inflammatory disorders in industrialized countries is associated with improved sanitation resulting in a reduced microbial burden, or with reduced exposure to particular microbes that regulate the host's immune response8. The DNA microarray technique could be used to examine the microbiotas of infants in developing countries where the incidence of chronic inflammatory diseases is low compared with that in developed countries. The analysis of different cohorts of at-risk populations, followed over time, may eventually allow us to predict whether specific microbes increase the likelihood of a person developing a particular disease, or, conversely, whether the lack of a protective species leads to immune dysregulation.
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