High-Altitude Living Shapes the Skin Microbiome in Humans and Pigs

The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.

Human skin pigmentation is the product of two clines produced by natural selection to adjust levels of constitutive pigmentation to levels of UV radiation (UVR). One cline was generated by high UVR near the equator and led to the evolution of dark, photoprotective, eumelanin-rich pigmentation. The other was produced by the requirement for UVB photons to sustain cutaneous photosynthesis of vitamin D(3) in low-UVB environments, and resulted in the evolution of depigmented skin. As hominins dispersed outside of the tropics, they experienced different intensities and seasonal mixtures of UVA and UVB. Extreme UVA throughout the year and two equinoctial peaks of UVB prevail within the tropics. Under these conditions, the primary selective pressure was to protect folate by maintaining dark pigmentation. Photolysis of folate and its main serum form of 5-methylhydrofolate is caused by UVR and by reactive oxygen species generated by UVA. Competition for folate between the needs for cell division, DNA repair, and melanogenesis is severe under stressful, high-UVR conditions and is exacerbated by dietary insufficiency. Outside of tropical latitudes, UVB levels are generally low and peak only once during the year. The populations exhibiting maximally depigmented skin are those inhabiting environments with the lowest annual and summer peak levels of UVB. Development of facultative pigmentation (tanning) was important to populations settling between roughly 23 degrees and 46 degrees , where levels of UVB varied strongly according to season. Depigmented and tannable skin evolved numerous times in hominin evolution via independent genetic pathways under positive selection.

Skin-associated bacteria of amphibians are increasingly recognized for their role in defence against pathogens, yet we have little understanding of their basic ecology. Here, we use high-throughput 16S rRNA gene sequencing to examine the host and environmental influences on the skin microbiota of the cohabiting amphibian species Anaxyrus boreas, Pseudacris regilla, Taricha torosa and Lithobates catesbeianus from the Central Valley in California. We also studied populations of Rana cascadae over a large geographic range in the Klamath Mountain range of Northern California, and across developmental stages within a single site. Dominant bacterial phylotypes on amphibian skin included taxa from Bacteroidetes, Gammaproteobacteria, Alphaproteobacteria, Firmicutes, Sphingobacteria and Actinobacteria. Amphibian species identity was the strongest predictor of microbial community composition. Secondarily, within a given amphibian species, wetland site explained significant variation. Amphibian-associated microbiota differed systematically from microbial assemblages in their environments. Rana cascadae tadpoles have skin bacterial communities distinct from postmetamorphic conspecifics, indicating a strong developmental shift in the skin microbes following metamorphosis. Establishing patterns observed in the skin microbiota of wild amphibians and environmental factors that underlie them is necessary to understand skin symbiont community assembly, and ultimately, the role skin microbiota play in the extended host phenotype including disease resistance. © 2013 John Wiley & Sons Ltd.