The Invisible Organ Shaping Our Lives: Milestones in Human Microbiota Research

Good overview of the "past 300 years" of microbiome research.

Humans have always been explorers. From Magellan to Columbus, from traveling the Silk Road to traversing the Amazon basin, exploration is a rich part of our history. We are driven by curiosity and a deep need to chart new frontiers and new extraterrestrial worlds. But all this time we have been looking for new civilizations far, far away, the most fascinating, complex, and sophisticated civilization ever discovered has been living within us. We just haven’t fully appreciated it.

The incredible ecosystem that we call the human microbiome is home to microscopic species that grow like we do, interact like we do, and speak different languages like we do. During their millions of years of evolution, they have studied the human host carefully and found a way to communicate with us. They understand very clearly our anatomy and physiology, our strengths and our weaknesses, and our biological necessities and goals.

Today, even with our still limited knowledge of our little tenants, we are at the dawn of a scientific revolution — one that, we believe, will lead to a paradigm shift in science and medicine, opening up new ways to treat and prevent diseases as we have never been able to do before. In revisiting the lifestyle trajectory and groundbreaking research that brought us to where we are, it becomes easier to imagine where we might be in just a few years’ time.

Our Evolutionary Journey

For most of our evolutionary journey, we lived as hunters and gatherers. We traveled in small groups, practicing a nomadic lifestyle with few chances to encounter other hominids. Then, three major lifestyle changes — agriculture, urbanization, and globalization — completely revolutionized our evolutionary plan. These changes caused a radical departure from a carefully crafted and ideal symbiotic relationship in which specific lineages of microbes coevolved with humans over millions of years, passing through hundreds of thousands of generations, shaping our biology throughout evolution until the first disruptor, agriculture, arrived.

Agriculture

The domestication of livestock and the cultivation of crops made food procurement much more predictable and less time-consuming. No longer tied to animal migrations and crop cycles, we became settlers, increasing the density of human communities and making interpersonal microbial exchanges more frequent. Living in close contact with animals led to another unplanned consequence, namely the risk of zoonosis (the passage of microorganisms from animal to human host). Combined with a higher consumption of animal protein, these changes caused a major deviation from the planned evolution of the human microbiome’s composition and function.

Urbanization

The second disruptor, urbanization, marked another major milestone in human history. It caused an even greater concentration and interconnection of people, which increased the speed at which exchanges of microorganisms occurred. When this exchange involved pathogens, it led to the spread of new infections. Fast-forward to the 20th century, when these infectious diseases were tackled by the advent and extensive use of antibiotics. The implementation of a highly sanitized environment also had a major impact on the “urban microbiota,” which became less diverse compared to the “rural microbiota” that more closely resembled our original microbiota.

Another consequence of urbanization was far-reaching changes to the global habitat, with the expansion of large cities and highly dense populations, thus limiting areas for extensive agricultural production. This posed additional challenges to human evolution in terms of food procurement and sustainability and created major environmental and social shifts, including concentration of resources — power, knowledge, wealth, and human density — that contrasted with scattered resources in rural areas.

This power differential was found between rural and urban environments. Within urban areas, the same power differential was characterized by extreme inequality between rich and poor populations living in close proximity. This dynamic caused the marginalization of part of the population due to exclusion from the production system, in which mechanization gradually replaced human labor. The segregation between highly populated cities and food supplies coming from scarcely populated rural areas created economic inequities with the multiplication of intermediaries between agricultural producers and consumers.

Globalization

The challenge of maintaining food sustainability for a disproportionately urban consumer community, supplied by a shrinking farming community, was met through globalization, the third disruptor. Now we are in a global village of communication, with the instant exchange of ideas and goods and the constant mobility of people. We can move from one end of the world to another in a matter of hours. However, globalization arrived with a high price tag.

The closer integration of the world economy has facilitated a much faster and unplanned exchange of microorganisms, including the global spread of pathogens through trade and travel. But the globalization of the food supply has had an even greater impact on shifts in microorganisms. The dominant role of the globalized, corporate food system in our modern societies implies that processed foods and, more specifically, mass-produced, empty-calorie nonfoods, like snacks, sweetened beverages, prepared frozen meals, and fast-food items, occupy an exponentially increasing part of the diet of typical consumers in these societies.

To save cost and maintain demand, processed fats, sugar, and salt are used as low-cost ingredients in these foods. The prevalence of these dietary choices means that consumers eat a large proportion of “empty calories” without fiber, high-quality fats, sufficient vitamins, and minerals. Even more worrisome is the fact that what was once an occasional choice — the consumption of unhealthy food — is now the norm as the backbone of the typical Western diet. This is especially true as consumers become more urbanized, undertaking sedentary lifestyles without time to cook from scratch using healthy ingredients.

With the appreciation that diet is the most influential factor shaping our gut microbiome, and that dysbiosis (the reduction in microbial diversity) can be associated with a variety of chronic inflammatory diseases, more affluent people are now moving away from junk food and making healthier food choices. The impact of globalization on human health has changed the landscape to the point that the old paradigm of describing noninfectious, chronic inflammatory diseases as “diseases of affluence” typical of Western societies has become misleading. In fact, it is low-income people in industrialized countries as well as in the developing world who currently face the greatest impact from these diseases.

Empty calories are often very cheap calories for people who live in poorer sectors around the world. Consumption of processed or predominantly carbohydrate diets with insufficient whole grains, fruits, and vegetables is more common among the economically disadvantaged, and these dietary traits, studies have shown, have a negative impact on microbiome composition and function. Accordingly, the “hygiene hypothesis” — the theory that increased sanitation through hand washing and water and sewage management, along with social changes like increasingly urbanized lifestyles and smaller households, led to a lower incidence of infection in early childhood that was linked to the rise in pediatric allergic disease — is now being challenged by the “microbiome hypothesis.” This postulates that by having an influence on the evolutionary, symbiotic relationship between humans and our microbiota, lifestyle changes and, most important, dietary changes are the driving force fueling the epidemics of noninfectious, chronic inflammatory diseases worldwide.

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