Opinion
The emerging medical ecology of the human gut microbiome

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It is increasingly clear that the human gut microbiome has great medical importance, and researchers are beginning to investigate its basic biology and to appreciate the challenges that it presents to medical science. Several striking new empirical results in this area are perplexing within the standard conceptual framework of biomedicine, and this highlights the need for new perspectives from ecology and from dynamical systems theory. Here, we discuss recent results concerning sources of individual variation, temporal variation within individuals, long-term changes after transient perturbations and individualized responses to perturbation within the human gut microbiome.

Section snippets

A new scientific connection: medicine meets ecological theory

The complex ecology of the human gut microbiome is of great medical importance, but researchers are only beginning to investigate its basic biology and to appreciate the challenges that it presents to medical science. The gut bacterial community has been implicated in a range of human health issues extending far beyond the gastrointestinal (GI) tract. Those issues that do directly involve the GI tract include inflammatory bowel disease [1], gastric ulcers [2], obesity and diabetes 3, 4, and

Sources of individual variation

Gut bacterial communities are highly variable among individuals, and apparently vary in ways that are important to health outcomes. Therefore, it is crucial to understand what determines the make-up and characteristics of individual gut microbiomes. The potential causes of individual variation that have received the most consideration can be classified into two categories, involving either local differences in the founding bacterial species that individuals are exposed to, or differing

Temporal variation within individuals

In the absence of any conspicuously varying external influences, human gut microbiomes show considerable temporal variation, both in the ileum [20] and colon [14]. Depending on the detail and the duration of observation, human gut microbiomes may appear stable, but similar to many others, these ecosystems are fundamentally dynamic, fluctuating such that only their average state is stable [14]. This is consistent with theory-based expectations of asymptotic dynamic stability, as opposed to

Long-term changes in gut microbiomes after transient perturbations

It is typical of complex dynamical systems, such as ecosystems, that perturbation may dislodge the system from its current basin of attraction, causing it to settle into an alternative stable state after the perturbation 18, 19. This type of behavior has been observed after perturbation of human gut microbiomes by a short course of antibiotics [14]. This observation has led to concerns that antibiotic treatment could accidentally cause an unexpected shift to an alternative stable state in a

Individualized responses to perturbation of gut microbiomes

In the standard paradigm of simple causation, a system can not be understood until experiments can be replicated and repeatable results produced. Thus, it is perplexing that different individuals responded differently to the same experimental treatment of perturbing their gut microbiome. A key consequence of multistability is that different instances of the same type of system, such as different individual gut microbiomes, may show very different responses to the same perturbation. Even within

Concluding remarks

Biologists have often been tasked with the difficult problem of managing complex ecosystem dynamics. Medical professionals have not been in the past, but that is rapidly changing. Because of the broad health importance of the human gut microbiome, all available conceptual tools must be used to understand and manage it. This is a pressing concern for public health as well as medicine. Beyond the issue of perturbing a single individual's microbiota, extensive antibiotic use, along with other

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