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All Things Small and Great

It's time for a new, conservation-minded view of the microbial communities that live on and in us

Robert L. Dorit

More than a Truce

As we seek to explain the diversity and composition of the human microbiome, local environmental characteristics clearly matter: pH in the mouth is near 7, but that of the stomach is about 2. Host characteristics also matter, as age, gender and genetics all play a part. And as always in biology, an individual's life-history matters too. In fact, it matters from our very first minute: Babies delivered by caesarean section have different initial microbial communities than do vaginal-birth babies. Babies emerging from the germ-free amniotic sac into the birth canal are immediately colonized by bacteria from their mother's vaginal and fecal communities. As unsavory as these bacteria sound, they're highly desirable, as this welcome-to-the-world present is critical to the health of the newborn.

Slowly, inevitably, the growing infant's environment and genes reshape that maternal gift into the child's own microbiome. The microbiomes of identical twins resemble one another more than the microbiomes of unrelated infants—but no more than the microbiomes of fraternal twins. We can now track the ways in which this newly seeded microbial complement adapts to the newborn, adjusting first to a diet of mother's milk and later to the varied diet that accompanies weaning. Other studies show that babies born vaginally have a lower risk of developing food allergies, and this reduced risk is related to the microbial makeup of the gut and to the family history of allergy. This first gift from mom leaves a profound imprint.

As details of the partnership with our microbial friends come into focus, we are very much in Adam's position. We are seeing this world clearly for the first time and naming its inhabitants. And we should accept our role as custodians and caretakers of this unseen world. Perhaps the most important implication of this perspective involves our use of antibiotics. Over the past 60 years, broad-spectrum antibiotics have saved countless lives, and antibiotics remain a powerful weapon in our medical arsenal. But broad-spectrum antibiotics are coarse tools in an age where we are beginning to understand the subtleties of microbial environments and genomes.

Because antibiotics kill bacteria indiscriminately, collateral damage far exceeds target destruction, and our microbial supporting cast is decimated in pursuit of the pathogen. Under the old view of human-microbe interactions, we accepted this collateral damage as a small cost to pay for ridding ourselves of bacteria. Under our proposed ecological model, however, we can understand that we no longer need to destroy the village in order to save it. Broad-spectrum antibiotics are properly seen as agents of major perturbation. Recent studies make clear that antibiotic exposure reduces the diversity of resident microbial communities and makes it easier for pathogens to invade.

A clearer picture of the genetic changes that make bacteria "go bad" and become pathogens is also coming into focus. Pathogens are thugs. The lives of these bacterial delinquents are all about competing aggressively for scarce resources (iron, for instance), clinging to surfaces, and producing bacteriostatic and bactericidal molecules that clear away the established residents. Yet delinquency comes at a cost: The pathogen lifestyle is expensive and burdensome for the pathogen itself. Pathogenesis is a fringe occupation for most bacteria, and the conditions that give pathogens an opportunity are rare. Ironically, our scorched-earth approach to the microbial world increases the opportunities for pathogens to gain a foothold. Excessive antibiotic use sows chaos in our resident microbiota, and pathogens thrive on such chaos. Well-organized, stable resident communities can normally resist thugs; weakened and disrupted communities cannot.

Let me be clear—there are, of course, specific situations where bacteria are certainly not welcome. A surgical field needs to remain sterile. Catheters inserted into patients must be free of bacteria. Hands need to be washed before eating. Little dishes of unwrapped mints in restaurants should be avoided at all costs. But these scenarios, too, are better understood when framed as ecological problems: The ingestion of the overhandled mints or the presence of non-sterile instruments introduces non-native microorganisms into established communities (or into fully sterile internal environments). Just as introductions of non-native organisms perturb and can destroy ecological communities at the macroscopic level, non-native bacteria disturb the unseen world. Bacterial pathogenesis hinges on the ability of pathogens to displace established bacteria and occupy their niches, their homes: us. The indiscriminate use of broad-spectrum antibiotics and the resulting selection for antibiotic resistance (the topic of a later column) simplify the task.

Ultimately, our survival depends on following the second set of instructions issued to Adam—on thinking of ourselves as part of the living world, rather than above it. We now know that most of the living world is smaller than we are and even smaller than what we can see with our naked eye. Our size and our senses make us oddities in the living world, but they do not set us apart. The beginning of the 21st century is as good a time as any to acknowledge our deep dependence on the microbial world. Within our bodies, bacteria outnumber us, but they also support us. It is time to create rules of engagement with infectious diseases that reflect our longstanding partnership with the unseen world.

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