The Ecology of the Human Microbiome
Is The Human Microbiome Structured Like an Ecosystem?
The human body is the ultimate complex system: it is composed of over a trillion human cells, while also acting as host for quadrillions of microorganisms (the “human microbiome”), all interacting in diverse ways (Bianconi et al. 2013, 463; Fierer et al. 2012, 138). The ecology of the human microbiome is largely unexplored, but potentially very similar to plant and animal (“macrobiotic”) communities. This leads to the unique situation for ecologists of needing to ask very basic questions about the human microbiome (such as whether microbial communities are indeed analogous to macrobiotic communities), while also having the last hundred years of ecological theory to provide sophisticated predictions. Here, I will take an example of an incredibly simple, almost puerile question about the human microbiome and demonstrate how, in pursuit of answers, we end up asking some of the most prominent questions, and drawing on the most sophisticated work, in ecology.
How would the human microbiome change if the human host stopped, or severely reduced, food intake?
A Test Question
How would the human microbiome change if the human host stopped, or severely reduced, food intake? First, there are many publications that support the idea that a change would indeed occur: changes in gut-microbial community composition and phylogenetic structure have been observed with diet change (Fierer et al. 2012, 143; Costello et al. 2012, 1258). But what kind of changes would be observed? We would expect a decrease in abundances of microbiota that rely on host-acquired resources (i.e. resources the host has to consume). For example, a decrease in overall food consumption probably means a decrease in lactose consumption as a result. Therefore, we would expect a decrease in the abundance of Lactobacillus, a genus of bacteria that live in the human digestive tract and convert lactose to lactic acid, because it has experienced a decrease in resources. Without competition from microbes that consume host-acquired resources, we would expect an increase in microbiota that rely on host-derived resources (i.e. compounds the host is making either way to stay alive). For example, we would expect an increase in the population size of Bacteroides (another abundant bacterial genus in the human gut), because mucosal poly- and ogligosaccharides (a resource Bacteroides consumes that Lactobacillus cannot) are still being produced by the host and Bacteroides is no longer experiencing competition for space and other resources from Lactobacillus (Sonnenburg et al. 2004, 571). So an simple (linear) expectation would be that when the host stops eating, its microbiome becomes dominated by microbes that rely on host-derived resources (Costello et al. 2012, 1260).
Human Bodies are Inhabited by Diverse Microbiotic Communities
Complex Systems Give Unexpected Outcomes
However, as previously mentioned, the human microbiome is an incredibly complex system. We know from Neo Martinez and Peter Chesson’s lectures that complex systems exhibit non-linear or even chaotic dynamics. For example, the increased competition among consumers of host-derived resources could actually suppress their population sizes, which in turn could allow invasion of, and subsequent coexistence with, the microbiome by an entirely new microbe (a well known mechanism of density-dependent invasion shown mathematically by Peter Chesson). For example, in the absence of some anaerobic microbes (the presence of which are dependent upon the diet of the human host), Clostridium perfringens is more likely to invade and grow in the human gut (Costello et al. 2012, 1260).
It would also be reasonable to expect that there is a third class of microbe consumers: consumers of microbe-derived resources. This class could certainly overlap with the classes of consumers of host-acquired or host-derived resources: a given microbe may synthesize a waste product that the host also synthesizes or acquires from food, or a microbe may “adaptively forage,” as described by Neo Martinez. Then, with an increase in microbial consumers of host-derived resources, we may observe an increase in consumers of microbe-derived resources, which we may naively have assumed were consumers of host-acquired resources. This could perhaps also result in increased competition for substrate space among the microbes.
Potential Effects of Disturbance such as Starvation on the Human Microbiota
Alternatively, or simultaneously, the stressful conditions of host starvation could encourage mutualistic or facultative interactions to arise, again resulting in the increase of microbe species we may not have originally expected. For example, Porphyomonas gingivalis uses Quorum Sensing to colonize periodontal biofilms created by Streptococcus gordonii. We could conclude that S. gordonii facilitates host invasion by P. gingivalis, and so, if conditions are right for S. gordonii to increase in population size, P. gingivitis may as well (Fierer et al. 2012, 149). But again, the increased presence of P. gingivalis may cause increased competition resulting in limitation to other microbes. Additionally, from Judie Bronstein’s species interactions lectures, we may expect to see context-dependency of interactions. With the right combination of microbe abundances and environmental conditions, a given interaction may switch from mutualism to commensalism, etc. The conceptual possibilities (and hypotheses) of non-linear dynamics are endless here, though they could be made more concrete with knowledge of a host’s specific microbes and their physiologies. From Larry Venable’s lecture, we know there is already a conceptual framework from plant population ecology to use that information: plant population ecology interfaces with physiological ecology to understand the functional traits that determine plant population abundance and community composition. Questions about the human microbiome can be informed by this work, and hopefully inform it reciprocally in the future.
Changes in the Human Microbiome Occur on a Timescale Scientists Can Observe
Changes in "macrobiotic" communities (ecosystems composed of plants and animals) can occur across decades--certainly longer than an average research grant lasts! Microbiotic communities (such as the one inhabiting our bodies) react to change on a much shorter timescale, since reproduction time for microbiota is only hours or days.
Though Complex, The Human Microbiome Provides Many Experimental Opportunities
The most exciting part about the bevy of hypotheses for how community composition would change with disturbance such as starvation is that this change would actually occur on a timescale reasonable for scientists to observe. However, an easy temporal scale is in this case at the expense of a difficult spatial scale. Nonetheless, simple experimental manipulation of the human microbiome is both possible and desirable. Fierer et al. 2012 state that “microbial communities are more amenable to experimental manipulations than plant and animal communities, where generation times are longer and logistical concerns prevent experimentation with large numbers of individuals in well-replicated studies” (149). The authors go on to suggest that microbiome experiments can be performed on non-human subjects to help with spatial scale issues (150), but consider the previously mentioned example of P. gingivalis and S. gordonii and their interactions on the human tooth. Using the same system, we can ask many questions about community and population ecology. The microbiome of the human tooth could be characterized using extremely fine spatial- and temporal-scale sampling on and between teeth in a given mouth. This same process could be repeated on cleaned teeth, teeth applied with a phylum-specific (or a finer scale of specificity, if it is available) antibiotic, and/or teeth applied with known microbiota. With characterization of the microbes of the surrounding environment (the mouth and air), such an experiment would provide a time series of abundances for microbes, which could be analyzed to determine community assembly of the microbiome of the human tooth, the influence of priority effects, successional regimes, species of microbes which have dispersal or fitness advantages to invade available niches on the human tooth (Katrina Dlugosch’s lecture, Peter Chesson’s lectures), and potential competitive and facilitative interactions which could be responsible for limitation or promotion of certain microbes.
An incredible amount of data on community dynamics would be available after only a few days of sampling, as compared to years of field work required for similar characterization of a plant or animal community. Generalization of the results on community assembly, invasion, competition, and facilitation can give testable hypotheses for macrobiotic communities, pushing forward theory on community ecology and also allowing a test for the premise that microbiotic communities are a proxy for macrobiotic communities.
Bianconi, Eva, Allison Piovesan, Federica Facchin, Alina Beraudi, Raffaella Casadei, Flavia Frabetti, Lorenza Vitale, Maria Chiara Pelleri, Simone Tassani, Francesco Piva, Soledad Perez-Amodio, Pierluigi Strippoli, and Silvia Canaider. "An Estimation of the Number of Cells in the Human Body." Ann Hum Biol Annals of Human Biology 40.6 (2013): 463-71. Web. 10 Dec. 2015.
Bronstein, Judie. "Species Interactions 1: The Classics." Tucson. 20 Oct. 2015. Lecture.
Chesson, Peter. "Density-dependent Population Dynamics." Tucson. 1 Oct. 2015. Lecture.
Chesson, Peter. "Density-independent Population Dynamics." Tucson. 29 Sept. 2015. Lecture.
Costello, E. K., K. Stagaman, L. Dethlefsen, B. J. M. Bohannan, and D. A. Relman. "The Application of Ecological Theory Toward an Understanding of the Human Microbiome." Science 336.6086 (2012): 1255-262. Web. 1 Dec. 2015.
Dlugosch, Katrina. "Ecology of Invasive Species." Tucson. 22 Sept. 2015. Lecture.
Fierer, Noah, Scott Ferrenberg, Gilberto E. Flores, Antonio González, Jordan Kueneman, Teresa Legg, Ryan C. Lynch, Daniel Mcdonald, Joseph R. Mihaljevic, Sean P. O'Neill, Matthew E. Rhodes, Se Jin Song, and William A. Walters. "From Animalcules to an Ecosystem: Application of Ecological Concepts to the Human Microbiome." Annu. Rev. Ecol. Evol. Syst. Annual Review of Ecology, Evolution, and Systematics 43.1 (2012): 137-55. Web. 1 Dec. 2015.
Martinez, Neo. "Network Analysis in Community and Ecosystem Ecology." Tucson. 17 Nov. 2015. Lecture.
Sonnenburg, Justin L., Largus T. Angenent, and Jeffrey I. Gordon. "Getting a Grip on Things: How Do Communities of Bacterial Symbionts Become Established in Our Intestine?" Nature Immunology Nat Immunol 5.6 (2004): 569-73. Web. 10 Dec. 2015.
Venable, Larry. "Historical Overview of Plant Population Ecology." Tucson. 17 Sept. 2015. Lecture.
Don't have access to a library from a research institute?
Leave a comment--and I'll send you the papers I've referenced and any supplemental reading material you are interested in! I also referenced lectures from the Ecology program at the University of Arizona. I'm happy to send you my notes or even send an introductory email to the awesome (and pretty famous) scientists I mentioned here.
© 2018 Lili Adams