Mineral Microniches Control the Diversity of Subsurface Microbial Populations

Abstract

Rocks and minerals surround the subsurface microbial habitat, yet mineralogy and rock chemistry are rarely considered when characterizing microbial diversity and the microbial ecosystem. Using laboratory biofilm reactors with both a pure culture of Thiothrix unzii and a mixed environmental sulfur-metabolizing community we found that the combination of buffering-capacity, cell wall electronegativity, nutrient content of the rock, and competitive exclusion of some populations control biomass density, α-diversity (local diversity), and β-diversity (global diversity) of the attached communities on mineral and rock surfaces. This suggests that different populations are better adapted to, and more competitive on, specific rock types. The primary influence on rock/mineral colonization by sulfur-oxidizing organisms is the acid-buffering capacity of the mineral substratum, with neutrophiles preferentially colonizing highly buffering carbonate rocks, while acidophiles select nonbuffering quartz. Beyond chemical controls, Thiothrix (often found in mid-ocean ridge environments) demonstrates an affinity for basalt, where it excludes other sulfur-oxidizers. A pure culture of T. unzii preferentially colonizes carbonates while all very closely related Thiothrix spp. are excluded from these same rock samples in a mixed culture. We report here experimental evidence that microorganisms colonize rock surfaces according to the rock's chemistry and the organism's metabolic requirements and tolerances. These results suggest that adaptations to specific rocks are retained even when the organism is displaced in time and space from an ancestral rock habitat.

Keywords:

• caves
• community structure
• microbe-mineral interactions
• pyrosequencing
• sulfur-oxidizing bacteria

Acknowledgments

We thank A.S. Engel (University of Tennessee), C. Omelon (University of Texas), and C. Bell (University of Texas) for valuable critique and discussion.