The belly button is one of the habitats closest to us, and yet it remains relatively unexplored. We analyzed bacteria and arachaea from the belly buttons of humans from two different populations sampled within a nation-wide citizen science project. We examined bacterial and archaeal phylotypes present and their diversity using multiplex pyrosequencing of 16S rDNA libraries. We then tested the oligarchy hypothesis borrowed from tropical macroecology, namely that the frequency of phylotypes in one sample of humans predicts its frequency in another independent sample. We also tested the predictions that frequent phylotypes (the oligarchs) tend to be common when present, and tend to be more phylogenetically clustered than rare phylotypes. Once rarefied to four hundred reads per sample, bacterial communities from belly buttons proved to be at least as diverse as communities known from other skin studies (on average 67 bacterial phylotypes per belly button). However, the belly button communities were strongly dominated by a few taxa: only 6 phylotypes occurred on >80% humans. While these frequent bacterial phylotypes (the archaea were all rare) are a tiny part of the total diversity of bacteria in human navels (<0.3% of phylotypes), they constitute a major portion of individual reads (∼1/3), and are predictable among independent samples of humans, in terms of both the occurrence and evolutionary relatedness (more closely related than randomly drawn equal sets of phylotypes). Thus, the hypothesis that “oligarchs” dominate diverse assemblages appears to be supported by human-associated bacteria. Although it remains difficult to predict which species of bacteria might be found on a particular human, predicting which species are most frequent (or rare) seems more straightforward, at least for those species living in belly buttons.

Introduction

The skin of an average human houses trillions of individual bacteria representing hundreds or even thousands of phylotypes [1]. Most of these phylotypes or “species” (acknowledging that bacterial species definitions are vague [2]), are not yet named [3], and are often difficult to cultivate so are known only based on their nucleotide sequence. Studies have begun to characterize consistent differences in the composition of bacterial taxa across the geography of our bodies, for example, between wet (e.g., armpit) and dry (e.g., forearm) habitats [1], [4]. It is still not clear, however, how the diversity in such habitats is structured and, in particular, what makes some phylotypes common and others rare. Commonness might be the result of historically contingent or even chance processes [5], in which common phylotypes might be expected to differ among individual humans or human populations in unpredictable ways. Alternatively, common phylotypes might be predictably common, because they are from lineages with adaptations that predispose them to predictable success in the environment in which they are common [4], [6], [7].

To test whether the commonness of different phylotypes of bacteria on human bodies is predictable, we compared newly collected samples of skin bacteria and archaea from two independent samples of North Americans. The samples were collected from volunteers in a nation-wide citizen science project, Belly Button Biodiversity (http://www.wildlifeofyourbody.org/), and we assessed the microbial communities on the volunteers using multiplex pyrosequencing of 16S rDNA libraries. We tested two predictions derived from research on common and rare multicellular species, such as tropical trees or freshwater fish. The first two predictions we tested were 1) phylotypes frequent in one human population should be predictably frequent in others and 2) frequent phylotypes should also be abundant when present [7], [8]. We define frequent phylotypes as those that occur on many humans and abundant phylotypes are those that are found many times (which is to say, represented by many 16S rDNA “reads” in the pyrosequencing output) on those humans on which they are found. Theoretically, a phylotype might have a high abundance (many reads when present), even if it is very infrequent. While it has long been known that many communities (be they of fish, bacteria or something else) are composed of a few exceptionally frequent and/or abundant species and many more rare species [9], [10], few studies seem to have compared whether abundant species tend to be the same among regions or, as in our case, populations of hosts.

In the context of rain forest trees, species that are both frequent across samples and abundant when present have been referred to as “oligarchs” [6]. In the context of fish communities, they have been called “core species” (which were then contrasted with “occasional species”) [7]. The concepts of oligarchy or core species are similar to, but more specific than the microbiological concept of a “core microbiome”(note, we will focus on the term oligarchy here, rather than “core species,” to avoid confusion between the ecological term core species and the microbiological term “core microbiome”). The core biome has two relatively separate definitions. In some contexts, the core microbiome is described as a set of genes and metabolic functions that are nearly universal among individuals [11], [12], in many cases relatively independent of which phylotypes are present. In other contexts, the term core microbiome is used in a sense more directly tied to our focus, wherein a core microbiome is described as a set of phylotypes that are nearly universal among samples [13]. The oligarchy concept extends this second definition of the “core microbiome” by statistically considering whether the frequency and abundance of phylotypes is predictable or if samples are taxonomically unpredictable assemblages of strains.

Frequent phylotypes might be those phylotypes with specific adaptations for dispersal among and/or competitive success on human hosts. If success is associated with specific adaptations and those adaptations are difficult to evolve, one might expect frequent species to be phylogenetically clustered [14], [15]. Alternatively, if success is independent of specific adaptations for survival on belly buttons or bodies more generally, success may simply be a function of neutral or stochastic processes [16] or the traits necessary for success may be easily evolved. In this context, we tested a third hypothesis, namely that the most frequently encountered bacterial phylotypes (our putative oligarchs, found on greater than 50% of individuals sampled) tend to be more closely related than would be expected among phylotypes chosen randomly from those we sampled as has been suggested to be the case for rain forest trees [6].

The samples of human skin bacteria in our analyses were collected during two separate citizen-science sampling events in which two separate groups of individuals (35 in the first event, 25 in the second) volunteered to swab their own belly buttons. Citizens participated in this study not only in sampling but also in hypothesis generation (via twitter and online comments) and data visualization and were provided with images of bacterial cultures of their samples (www.wildifeofyourbody.org) and lists of the phylotypes discovered during molecular work. Bacteria are common on all parts of the skin, but the belly button offers several advantages. It is an environment that varies relatively little from person to person, in terms of morphology (compared, for example, to the belly itself). It is removed from daily scrubbing, and has the potential to host a less disturbed bacterial community particularly in contrast to frequently washed and exposed parts of the body such as the hands [4]. And last but not least, sampling from belly buttons has also proven of broad interest to the public, which has aided in drawing attention to discussions of the species with which humans are most intimately associated, a key goal of our broader work (www.yourwildlife.org).