Why are we seeing these changes in the human microbiota? Studies show that the western lifestyle promotes a suboptimal phenotype, in the sense that highly processed diets, sedentary living, lack of sun exposure, etc., results in a gene expression that leads to poor health and disease (1,2). However, we’re now learning that this gene-environment mismatch in many ways also involves the second genome in our bodies, in the sense that the western lifestyle is a master manipulator of the microbial communities in and on our bodies. Basically, we’re not providing the types of inputs that promote a healthy microbiome.
Widespread use of antibiotics, increased rates of caesarean sections, certain aspects of modern hygiene, highly processed diets, and indoor living are just some of the factors that alter the gut microbiome, and some researchers have now begun talking about a westernized microbiota, a microbial rainforest that has lost key species and lacks the resilience of the ancestral microbiome (3,4,5,6). This statement is also consistent with recent studies which show that hunter-gatherer populations and rural communities have vastly more diverse microbiomes than westerners (7,8). Some researchers have even attempted to analyze the microbiome of our forefathers (~8000-1400 years B.P.) by looking at coprolites, and what they found indicate that the modern cosmopolitan lifestyle lead to a dramatic change to the human gut microbiome (9).
As antibiotics, highly processed foods, and other factors associated with the western lifestyle are very recent introductions in the human evolutionary history, it could be argued that the hunter-gatherer/ancestral microbiome represents the default/natural state of the human microbiome. It’s believed, and generally accepted, that this increased microbial diversity in non-westernized populations stems from the fact that these traditional peoples don’t have access to antibiotics, hand sanitizers, and other products that decrease microbial diversity. Also, they generally eat diets that are rich in whole foods and have an increased exposure to microorganisms from dirt, untreated water, soil, and the rest of the environment. Some hunter-gatherer populations, such as the Hadza of Northern Tanzania, even eat the intestines of some of the animals they kill, thereby consuming a wide range of microbes (10).
We’ve lost contact with some old microbial friends
“The hygiene hypothesis” suggests that the primary reason we’re seeing a steady increase in incidence of autoimmune disorders in the industrialized world is that we’ve become too clean and hygienic and therefore lost some of the microbial exposures that helped train our immune system. This hygiene hypothesis has now expanded into the “old friends hypothesis”, a hypothesis that is based on the idea that the combination of widespread use of broad spectrum antibiotics, modern hygiene, “clean” and processed diets, sanitary practices, and a general disconnect from the natural environment has resulted in the loss of some old microbial friends that used to be a part of the paleolithic microbiota. These old friends that co-evolved with our species include some types of helminths, parasites, and many other organisms that are a part of the natural environment.
The old friends hypothesis is based on the idea that our immune system doesn’t develop normally in the absence of “adequate” microbial input, and that the decrease in microbial exposures from the natural environment is one of the primary reasons the westernized microbiome is much less diverse than the microbiome of hunter-gatherers and people who live in rural settings. There’s now more and more supporting evidence for this hypothesis, and several reports suggest that the loss of microbial old friends could be one of the keys to understanding the rapid rise in inflammation-associated illnesses in high-income urban environments (11,12,13,14).
This high exposure to microorganisms from the environment might seem unhealthy and dangerous to many people who live in the “clean” modern world, but we have to remember that this is the way humans have lived throughout most of our evolution. It’s only recently that we’ve disconnected ourselves from the vast bacterial communities found in nature by moving into clean homes, processing, washing, and cooking most of our food, chlorinating our water supply, and regularly washing our hands and body. Nobody’s denying that these practices decrease our exposure to potential pathogenic microbes and that modern technology and science have helped us overcome many types of infectious diseases. However, we’re now learning that many aspects of our modern lifestyle also come with some, up until now, hidden costs.
The fact that hunter-gatherer tribes which have been studied during the last several centuries are virtually free from the so-called diseases of civilization has largely been attributed to their ancestral diets and physical activity patterns. However, with the emerging field of microbiome science we’re learning that part of the protective factor of the hunter-gatherer lifestyle has to do with the diverse and resilient hunter-gatherer microbiome.
We receive microbes from animals and other humans
So, science has shown us that although we don’t know exactly how the healthiest state of the microbiome looks like (if such a thing exists), we do know that many aspects of our western lifestyle have a detrimental effect on the microbial communities in our body. But let’s backtrack a little to really understand how the microbiome is shaped and how we acquire these microbes in the first place. While we’ve always thought that the uterus is a sterile environment, we’re now learning that the human microbiota is probably seeded before birth (15). This seeding continues as the child travels through the birth canal, and the microbiota is slowly established as the child receives microbes from breast milk, the skin and mouth of mum, dad, and other family members, and the rest of the environment. From then, the microbiome is, as we already talked about, shaped by lifestyle and environment throughout life.
Since we, to a great degree, receive the microbiome of our mother, and to a certain degree father and other family members, the second genome should also be considered when discussing genetics and heredity. Just like the 23 pairs of human DNA we receive from our parents determine our physiology and disease susceptibility, the microbial communities and the genetic material they hold, also have a significant impact our health. While more research in this area is needed, it’s likely that part of the hereditary component of health disorders that are characterized by alterations in the human microbiome stems from the transfer of microbes from mother to child.
It’s well established that diet, pharmaceutical use, birth method, etc. have a direct impact on the gut microbiome. However, the relationship between environment and lifestyle and the gut microbiome doesn’t stop there. Our own microbiome is also influenced by the microbiome of animals and other people. This contagious health might sound far-fetched to many, but it has been shown that household members, particularly couples, share more of their microbiota than individuals from different households (16). It has also been shown that children who grow up with animals are healthier than children who grow up without pets and that this beneficial effect stems from the transfer of microbes (17).
While it has long been known that the human body is not sterile, recent discoveries about the human microbiome have taken the idea of the human body as an ecosystem to a whole new level. Just like other ecosystems in nature, the microbial communities that live in and on this superorganism are shaped by other microbial ecosystems we encounter. This is relevant in terms of health and disease, as it could mean that disorders, such as obesity, that are generally considered non-communicable, actually are communicable in the sense that microbes are transferred between humans. To which extent the microbiome is able to affect the microbial communities of other humans is still unclear, but likely depends on several factors, such as the proximity of contact (e.g., husband and wife share more bacteria) and the original resilience of the microbiome. Is it possible that the skyrocketing rates of diseases of civilization are partly driven by the transfer of westernized microbiota between people? We don’t know. Nobody’s denying that diet and lifestyle factors play the most important roles, but it’s certainly possible that “contagious health” could also be contributing.
The obese microbiome
One of the disorders that we now know is associated with an altered gut microbiota is obesity. Almost a decade ago, researchers at Jeffrey Gordon’s lab at Washington University showed that sterile mice – mice without a microbiome – who received microbiota from lean mice stayed lean, while germ-free mice who received microbiota from obese mice gained weight (18). These were some of the first studies showing a causal relationship between gut microbes and body fat regulation, and in the decade that has passed since then, these results have been replicated and numerous other reports have investigated this relationship further. By now it’s well established that obesity is characterized by an obese microbiota and that gut microbes can influence fat storage through a variety of mechanisms (19,20,21). We’ve also learned that changes in the gut microbiota contribute to reduced host weight after gastric bypass surgery, that perturbations in the bacterial communities (e.g., from antibiotics) can cause weight gain, and that transfer of intestinal microbiota from lean human donors increases insulin sensitivity in individuals with metabolic syndrome (22,23,24).
At this point we don’t know enough to say exactly what characterizes the obese microbiota and which species are important. Some studies show a shift in the balance between the two major phylums of gut microbes, the bacteroidetes and the firmicutes, while others point to specific strains of bacteria that can initiate weight gain (25,26). However, what we do know is that there’s probably more a question of the overall community structure, rather than a few specific types of microbes. Just like the causes of obesity are considered to be both genetic and environmental, the obese microbiota is also shaped by both hereditary and environmental factors. At this point there isn’t much concrete data on the transfer of gut microbes from obese mothers to their child and the impact this inoculation has one the child’s body weight, but it’s very likely that part of the genetic component of obesity stems from the transfer of an obese microbiome.
Since we know that the human microbiome harbors 99% of the unique genetic material in the human body and that gut microbes play an important role in regulating fat storage, the role of this gene transfer from mother to child shouldn’t be underestimated. If the transfer of the microbiome from mother to child is as important as some scientists think, it’s clear that we have to rethink our perspective on obesity and genetics. While it’s well established that several genes in the human genome play a key role in obesity, we’re now learning that microbes/genes in our second genome also impact how likely we are to gain and store fat. This is also where microbiome science has a long way to go. While a lot of the studies have focused on specific bacterial strains and general community structure, the genetic material could be more important than the specific types of bacteria.
Microbes transfer DNA through other means than traditional reproduction, and in the gut it probably goes on all the time (27). This horizontal gene transfer means that gut microbes are able to pick up genes from other critters, and new species, with a somewhat different genetic material, are therefore created all of the time. This complexity and dynamic nature of the gut microbiome can help explain why it’s often estimated that humans are 99% alike in terms of our human genome, but very different in terms of our microbial inhabitants (28). It can also help explain why it’s so difficult to accurately characterize an unique makeup of the obese microbiota.
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