Convergent Community Assembly among Globally Separated Acidic Cave Biofilms

Acidophilic bacteria and archaea inhabit extreme geochemical “islands” that can tell us when and how geographic barriers affect the biogeography of microorganisms. Here, we describe microbial communities from extremely acidic (pH 0 to 1) biofilms, known as snottites, from hydrogen sulfide-rich caves. Given the extreme acidity and subsurface location of these biofilms, and in light of earlier work showing strong geographic patterns among snottite Acidithiobacillus populations, we investigated their structure and diversity in order to understand how geography might impact community assembly. We used 16S rRNA gene cloning and fluorescence in situ hybridization (FISH) to investigate 26 snottite samples from four sulfidic caves in Italy and Mexico. All samples had very low biodiversity and were dominated by sulfur-oxidizing bacteria in the genus Acidithiobacillus. Ferroplasma and other archaea in the Thermoplasmatales ranged from 0 to 50% of total cells, and relatives of the bacterial genera Acidimicrobium and Ferrimicrobium were up to 15% of total cells. Rare phylotypes included Sulfobacillus spp. and members of the phyla “Candidatus Dependentiae” and “Candidatus Saccharibacteria” (formerly TM6 and TM7). Although the same genera of acidophiles occurred in snottites on separate continents, most members of those genera represent substantially divergent populations, with 16S rRNA genes that are only 95 to 98% similar. Our findings are consistent with a model of community assembly where sulfidic caves are stochastically colonized by microorganisms from local sources, which are strongly filtered through environmental selection for extreme acid tolerance, and these different colonization histories are maintained by dispersal restrictions within and among caves.