Of microbes and men: Testing the neutral theory with the human microbiome

There is no doubt that one of the hottest current topics in microbiology revolves around the human microbiome. There have been a suite of recent studies we’ve highlighted, on organisms ranging from bees and mice, to humans. A quick google scholar search identifies over 12,000 studies on the human microbiome from 2016 alone.

Figure 2. Human Microbiome Project Consortium, 2012


There are various efforts to characterize the human microbiome, such as the one run by the NIH, established in 2008, with various ambitious goals including determining how disease affects our microbial fauna and the development of a microbial reference genome data set. They also published a nice summary back in the day on the structure and diversity of a healthy human microbiome.

Figure 4. Human Microbiome Project Consortium, 2012.


Although, interestingly enough – it’s not just scientific journals that are focusing on these bacterial communities. I finally ordered my copy of I Contain Multitudes, by Ed Yong (which you’ve likely either read, plan to read, or heard about), that discusses how our microbiome is a big part of who we are.
Microbiomes associated with select organisms represent model systems that will allow us to ultimately unravel the complex interactions among microbes in the environment. If you’re interested in keeping up with the Joneses concerning microbiome studies, you might want to check out Elisabeth Bik’s blog on the topic. It has proven to be (quite understandably) interesting and difficult to figure out how microbes interact in their natural habitats, understanding microbial community ecology is important, but definitely not easy.

What forces shape microbial community evolution? In a recent study by Li and Ma published recently in Scientific Reports, they decided to test the neutral theory and how it relates to microbial biodiversity using previously published human microbiome datasets. As the authors discuss, the neutral theory set forth by Stephen Hubbell, suggests that communities are random assortments drawn from regional pools of microbes.
This is unlike what is proposed in the traditional niche theory, that states microbes inhabit specific niches linked to the role that they play as a species. Essentially, the neutral theory suggests that any differences among microbes playing similar roles in a natural community have nothing to do with how successful they are in the environment, and the abundance of a microbe in a community reflects its relative abundance in the region.
There is no doubt that sequence-based approaches have provided a new window on what microbes exist in an environment as well as what roles they might have. While the authors theorize that it is likely both the niche and the neutral theories play a part in microbial evolution, to what extent different forces shape the human microbiome is largely unknown.
In order to determine to what extent “Everything is everywhere and the environment selects” (as Baas Becking famously proposed) in respect to the human microbiome, Li and Ma compiled an extremely extensive set of data that included 7,437 microbial communities of 242 individuals that included five major sites on the body (gut, oral, skin, vaginal, and nasal). The authors focused on the V1-V3 and V3-V5 variable regions of the 16s rRNA sequence to identify community members.

Figure 1.


The authors concluded that the vast majority (99.5%) of human microbial communities do not fit the neutral community model. In total, actually, there were only 23 communities that passed the neutrality exact test, more than half of which are on our skin. Taking into account previous results as well as addressing that “everything is everywhere” quote – the authors write that it is likely a relationship between dispersal and selection that influences influence of neutral and niche-based ecological theories on microbial communities.
The availability of large datasets is setting the stage for the further examination of microbial community ecology. While there are a variety of currently used bioinformatics tools to study these communities, the overwhelming amount of data is driving the development of new methods and tools for data analysis. Personally, I’m looking forward to reading Yong’s book, while I wait for that next nice microbiome study to come out.
References
Li, L. and Ma, Z. (S.) Testing the Neutral Theory of Biodiversity with Human Microbiome Datasets. Sci. Rep. 6, 31448; doi: 10.1038/srep31448 (2016).
Baas-Becking, L. G. M. Geobiologie; of inleiding tot de milieukunde.(eds W. P. Van Stockum & Zoon N. V., Den Haag [Netherlands], 1934).
Human Microbiome Project Consortium. “Structure, function and diversity of the healthy human microbiome.” Nature 486.7402 (2012): 207-214.
Hubbell, S. P. Neutral theory and the evolution of ecological equivalence. Ecology 87, 1387–1398 (2006).

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