13. The Human Mutualist: From Costs to Benefits

Updated: Jun 9, 2021

From the previous example of how symbioses with bacteria might form, consider the huge number of bacteria in our internal ecosystem that do not cause death or even ill health. Did they evolve from pathogenic forms into benign forms that formed a symbiotic or even mutualistic interaction with our bodies?

Let’s suppose a previously dangerous bacterium evolved another function that was useful to us. If a pathogen evolved mechanisms for defending itself from the host’s defenses, and was able to extract sufficient resources from the host to survive, then it has essentially created a niche for itself in the host’s ecosystem. Once in such a niche, the bacterium would also have to defend itself from the proliferation of other pathogens that could displace it from its niche. By doing so, it would essentially be protecting the host from those pathogens too. If the presence of one pathogen prevented the invasion by other more dangerous pathogens, the first pathogen, by default, can be viewed as a mutualist under those conditions where new infections are likely. (Nevertheless, when other external threats are not present, the resident pathogen could still exact a cost higher than the value of the benefit.)

From an evolutionary perspective this is very intriguing. Such an arrangement means that if a sub-lethal pathogen evolves a function that provides a defensive benefit to the host, the host essentially gains a new function. The new function will be derived from the pathogen’s genome, not the host’s genome. If the new function is sufficiently beneficial, it will offset the negative cost of the pathogen, that is, of having the pathogen present within the host. In such a case, the mutualism will be favored and will persist. The benefit to the host will depend on controlling but not eliminating the pathogen. The virulence of the pathogen will remain low and will probably decline over time.

If a new defensive function provided by a microbe, such as a pathogen, is superior to an existing defensive function of the host, the host’s innate defensive function is redundant and may become obsolete. How could the pathogen provide a superior defensive function? It depends largely on the difference between growth rates of human cells and bacterial cells. We know that bacteria can produce prodigious numbers of new cells in a very short amount of time and every new bacterium is a complete individual. On the other hand, human cells divide much more slowly and have limited functionality because cells in the human body represent particular tissue types.

If certain biochemical (immune) defenses of humans are dependent on cell proliferation, it is very possible that bacteria can provide a faster defensive response. We certainly know that highly virulent bacteria can overwhelm human immune defenses and this is based on cell growth rates. Thus, the very rapid response of a mutualistic bacterium to an environmental threat could outwardly appear to be a flexible defensive response of the host.

If the survival and health of the host is a highly beneficial condition to the bacterium, then protecting the health of the host becomes an evolutionary benefit and this will be expressed as a mutualistic interaction. (See the section on “Of Bigs and Bugs”)

The huge numbers of bacteria in the human microbiome did not all start as pathogens that evolved into mutualists protecting the host environment. However, it is certainly possible that initial bacterial mutualisms created an environment that was conducive to further colonization by other bacteria. That is, if the environment of the early digestive system was generally hostile for certain bacterial types, the evolution of an initial mutualism would have created a less-hostile environment in general.

An example would be the reduction of oxygen levels in the large intestine by early aerobic colonists that facilitated the survival of anaerobic bacteria as later colonists. This change in conditions has been noted in the initial colonization of newborn babies as the lactobacilli are carried by mother’s milk to the large intestine. Because the baby’s digestive system has not been activated and is incapable of breaking down lactose, that process of digesting lactose sugar is dependent on bacteria.

Lactobacilli are tolerant of low oxygen levels, but the environment in the colon becomes more anaerobic soon after bacteria take up residence and begin breaking down large food molecules, which is an oxygen consuming process. Such a modification of the internal environment could then facilitate further colonization, creating conditions favoring mutualisms with anaerobic bacteria, and thereby encouraging the eventual development of a complex internal ecosystem.

It is not necessary that all members of the ecosystem contribute equally to the health of the host and many species are likely taking advantage of the food resources in the digestive system of the host. This can be either a parasitic situation if it deprives the host of needed resources or a commensal situation if the host is unaffected by the presence of the non-mutualist. Both scenarios are very likely.

Hitchhikers are unavoidable in any large and complex system, but if the parasitic species are low in abundance and do not trigger a defensive response from the host or from the other members of the microbiome, then they can become part of the normal functioning of the ecosystem. However, this is likely to be the case only when non-beneficial species remain in relatively low abundance. From an ecological perspective, this is how bacteria such as Clostridium difficile and Staphylococcus aureas can be normal residents in the colon.

Regardless of the beneficial, commensal, or parasitic nature of the microbial inhabitants, all species gain by protecting the integrity of the system. That is, if the internal environment is threatened, then the inhabitants are threatened.[i] We should not be surprised, then, that for internal ecosystems, such as the microbiome, where the survival of the resident species is dependent on the health of the system, those species will provide defensive functions that support the integrity of the system. These defensive functions should not only favor the host, but should have a regulatory effect on the other species in the community.

In that sense, the healthy ecosystem is self-regulating though negative feedbacks that limit the growth or dominance of any one species. It’s certainly worth noting that regulation of dominance can also be accomplished merely by a change in the resource base. In other words, frequent changes in the quantity and quality of the food eaten by the host, particularly foods that favor greater microbial diversity, will prevent dominance by one or a few species. Why is this important?

In complex ecosystems, dominance by one species is rare and typically indicates an imbalance in the structure of the system. For example, dominance implies that one species is capable of being competitively superior across the range of available resources, but that would mean being able to outcompete all other species, including the specialist species. In a system with a diversity of both resources and species, this should not occur.

When the resource base is simplified or the species composition of the ecosystem has been simplified, the conditions are favorable for one or a few species to dominate and even eliminate less competitive species or those lacking sufficient resources. High species diversity typically reflects high resource diversity and should also favor both generalist and specialist species and the presence of both types will prevent any one of them from dominating the system.

One implication of this is that species diversity is probably a vital characteristic for the maintenance and stability of an internal ecosystem. In a microbiome, there is a need for the resident species to recolonize after depletion, to exchange with and stay up to date with the external ecosystems, to respond to changing conditions, to compete with other species, to specialize for resources, and to take quick advantage of new resources. All of these response functions favor species diversity and redundancy and resource specialization.

In short, a healthy and stable microbiome is a diverse microbiome that is being supported by a diverse resource base and such a microbiome will be efficient at digesting food and supportive of the host system. In addition, species diversity and redundancy means that the loss of one or more species will not greatly disrupt the system because other species are available to fill the roles of the lost species. This then leads to greater resilience in the system in the sense that the system can rebound quickly from a serious disruption. Again, for human systems that are inherently limited in their response flexibility, the presence of a mutualistic and diverse microbial community will provide necessary functions for maintaining a healthy and responsive system.

In summary, the availability of the microbial genomes for providing new abilities to the host means that humans are more complete ecosystems when we have a healthy microbiome to support us.

[i] Obviously, this is not true for pathogenic species. The integrity of the ecosystem is only relevant insofar as the transmission of the pathogen to the next host is facilitated.

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