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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]. Theoretically, a phylotype might have a high abundance many reads when present , even if it is very infrequent. The core biome has two relatively separate definitions.

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The Truth Is In There

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].

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. 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. 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.

Over the past six months, we have sampled over five hundred volunteers for belly button bacteria. Belly buttons were swabbed with sterile cotton tips that were then immersed in 0.

Swabbing has previously been determined to be as effective as other sampling methods for sampling of human skin bacteria 7. The primer F was appended with a TC linker and a Roche B pyrosequencing adapter, and the R primer was appended with a bp sample-specific barcode sequence, a CA linker, and a Roche A sequencing adapter. The sample-specific, error-correcting barcode allowed for pooling all amplicons in a single pyrosequencing run.

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All samples, including no-template controls, were PCR-amplified in triplicate following the protocol described in [18] , [19]. The concentration of each amplicon was determined using the Quant-iT PicoGreen dsDNA kit Invitrogen , and equimolar aliquots of all samples were pooled. The platform was chosen over other platforms, since our team has had significant success with this methodology in previous studies of human microbiome i.

Also, the reads produced by pyrosequencing are significantly longer than from most other approaches, and thus easier to analyze and interpret. The pyrosequencing output consisted of , reads that passed the first quality screen within the platform. This output was processed and analyzed using the comprehensive analysis package QIIME for barcoded amplicons of microbial communities [20]. Sequences were assigned to samples according to the bp barcode; only 50 sequences had uncorrectable barcode sequence. Read counts a proxy for abundance of identified microbial taxa across samples were exported as a matrix to be used in subsequent community analyses.

All samples were rarefied to a sequencing depth of reads per sample prior to downstream analyses. None of these twenty sequences was chimeric, thus we concluded that chimeras, even if present, were rare and inconsequential in our dataset. To test whether the frequency and abundance of bacterial phylotypes among humans are predictable, we calculated the Spearman rank correlation between the frequencies of the taxa found in both of two independent sets of individuals.

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This excludes the very rare taxa, most of which were found in only one individual and thus by definition are negatively correlated between the groups in frequency and abundance. The samples contained 35 and 25 individuals, and taxa were observed in both. This would be expected if frequent phylotypes tend to be from the narrower subset of lineages with adaptations for life on humans, whereas rare phylotypes tend to be more random samples of environmental bacteria.

Mean pairwise distance was compared to a distribution of the same measure in a randomly drawn sets of 23 phylotypes from the rest of the phylotypes. In the 60 samples of belly buttons considered here, we found phylotypes of bacteria based on , sequence reads, excluding sequences of insufficient quality see Supporting Information S1. These phylotypes likely correspond to far more than biological species.


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Also, the overall rarefaction curves for belly button bacterial phylotypes failed to level off, suggesting additional phylotypes would have been encountered were more individuals sampled, or were additional human populations considered whether from different regions or different genetic backgrounds. Even conservatively considering just the phylotypes, our diversity of bacterial phylotypes was more than twice as great as the species diversity of, for example, North American birds [24] or ants [25].

The vast majority of phylotypes were both infrequent encountered on few people and rare represented by few reads when present; Table 1. Conversely, no phylotypes were present on all individuals sampled and just eight phylotypes were present on more than seventy percent of individuals. From a taxonomic perspective, the frequent, abundant phylotypes encountered were dominated by well-known skin bacteria, specifically Staphylococci, Corynebacteria, and several genera of Actinobacteria e.

This composition corresponds to the previously reported composition of the skin microbiome in deep sequencing studies [1] , [3] , [26]. Interestingly, it is also very similar to the taxa recorded in a culture-based study of skin samples from humans in our same study region of North Carolina [26]. The most common skin bacteria in that study were lineages of Staphylococcus , Micrococcus within the group Actinobacteria above , Bacillus Bacilli above and then Acinetobacter , Klebsiella , Streptomyces and Enterobacter.

The frequently encountered genera in the culture-based study were all also frequently encountered here with the exception of Streptomyces, and Enterobacter which were present in the belly button samples but not common and Klebsiella which was absent from our samples. The quantitative dominance of Corynebacteria in bellybuttons is also in line with a previous report [4]. Of special note are three phylotypes of Archaea, a domain of life often found in extreme environments and not previously reported from human skin [1] , [27] , multiple phylotypes of which we isolated from two independent samples see online Supporting Information S1.

Two of these three phylotypes were from an individual who self-reported not having showered or bathed for several years. In order to account for differences in numbers of reads from different belly buttons, we rarefied each belly button sample to reads. Rarefying the data decreased the total number of bacterial phylotypes being considered in our analyses to For this rarefied dataset, we recovered a median diversity of 67 bacterial phylotypes per reads per belly button.

The most diverse bacterial sample included phylotypes, and the least diverse included 29 phylotypes. In other words, some belly buttons appear more than three times as diverse as others. Such differences have the potential to influence human health and well-being. Several recent studies suggested that skin bacteria have a beneficial effect on skin immune function [28] , [29]. Interestingly, our results suggest that when a high diversity of phylotypes is present on the bellybutton skin, most of those phylotypes are rare, infrequent, phylotypes.

Thus, if microbial diversity on habitats like the belly button skin plays a role in allergy, the role may be contingent on the rare, infrequent, phylotypes. While the great diversity of bacterial and to a far lesser extent, archaeal phylotypes in belly buttons, like that in many samples of bacteria from humans, suggests an inscrutable complexity, we found that most of the variation in the frequency of phylotypes was predictable.

Based on the frequency of bacterial phylotypes number of hosts on which they occurred in our first sample of 35 individual humans, we were able to account statistically for much of the variation in the frequency of phylotypes in our second, independent, sample of 25 separate individual humans Figure 1. The size of circles corresponds to the number of reads of each phylotype, where reads are a proxy for abundance.

In short, a subset of bacterial phylotypes, a group we term the oligarchs, are predictably very frequent despite the great total diversity of bacteria and often abundant when present. While infrequent, rare phylotypes maybe transient, frequent, and abundant phylotypes oligarchs might be expected to be those with specific adaptations to the pH, host antimicrobial compounds and dry conditions that characterize the skin [29]. If this were the case, we would expect the oligarchs to derive from fewer lineages than do more infrequent phylotypes.

The hypothesis that frequent taxa are from a subset of lineages with adaptations for the habitat being studied whereas infrequent species draw from a broader range of lineages, many of which are not locally adapted has precedent in ecological literature. For example, a disproportionate number of common rain forest tree species are from the family of palms which possess a range of unique adaptations for tropical forest life [6]. Rare, more occasional, species might represent more random species capable of arriving in a habitat, but not necessarily succeeding. If this were the case, bacteria frequently encountered on humans should belong to fewer lineages than a random draw of the same number of less frequent species.

In our samples from belly buttons, we found the most frequently encountered bacterial phylotypes were indeed more phylogenetically clustered than random draws of the same number of representatives from the remaining bacteria. These results support the hypothesis that while human bodies encounter many thousands of bacterial phylotypes, the most successful phylotypes are from only a few lineages.

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We hypothesize that these lineages have, over evolutionary history, evolved traits that allow them to thrive on humans, a hypothesis that seems supported by older culture-based studies in which the lineages we found to be most frequent and abundant are nearly identical to those suggested to have specific adaptations for the tough, desert-like conditions found on human skin [26] , [30]. Overall, we found that while belly button bacterial phylotypes were diverse, aspects of this diversity were predictable.

The most frequent and abundant phylotypes were similar across independent populations as well as being phylogenetically clustered. Such oligarchs were represented by multiple reads in most sampled human individuals, yet not a single one of the oligarchs is present in all samples. This appears in line with the oligarchy concept or ecological core species concept, but at odds with the traditional concept of core microbiome, defined as subset of taxa that are present in all samples [13].

Such phylotypes may have been present on all of the humans in our study but were undetected. We found that while the microbial communities in human belly buttons may display some degree of flexibility in the taxonomic composition they appear much more predictable than a random assemblage from a functionally redundant metacommunity.

Importantly, this pattern of predictable taxonomic composition is borne predominantly by the oligarchs — frequent, abundant, and phylogenetically clustered symbionts, while the rest of the community appears to be much more stochastic. Don't be afraid baby, ooh no Sweet virgin of the world You know we can't help but make it 'Cause there's true love between us girl Hmmm! So let us touch that cloud That everyone dreams of Oh! We're almost there darling truly making love. What's that now baby, what's that you say Something's eating at you And it's hard to get away hard to get away Oh don't fight it baby just open up the door 'Cause that's the key to the freedom That we've both been working for Let it go baby, let it go darling, ooh Right there, right there Baby don't you move it don't you dare Go baby let it go honey oh right there baby Don't you move it anywhere.

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