Humboldt's spa: microbial diversity is controlled by temperature in geothermal environments

Abstract

Over 200 years ago Alexander von Humboldt (1808) observed that plant and animal diversity peaks at tropical latitudes and decreases toward the poles, a trend he attributed to more favorable temperatures in the tropics. Studies to date suggest that this temperature-diversity gradient is weak or nonexistent for Bacteria and Archaea. To test the impacts of temperature as well as pH on bacterial and archaeal diversity, we performed pyrotag sequencing of 16S rRNA genes retrieved from 165 soil, sediment and biomat samples of 36 geothermal areas in Canada and New Zealand, covering a temperature range of 7.5-99 °C and a pH range of 1.8-9.0. This represents the widest ranges of temperature and pH yet examined in a single microbial diversity study. Species richness and diversity indices were strongly correlated to temperature, with R(2) values up to 0.62 for neutral-alkaline springs. The distributions were unimodal, with peak diversity at 24 °C and decreasing diversity at higher and lower temperature extremes. There was also a significant pH effect on diversity; however, in contrast to previous studies of soil microbial diversity, pH explained less of the variability (13-20%) than temperature in the geothermal samples. No correlation was observed between diversity values and latitude from the equator, and we therefore infer a direct temperature effect in our data set. These results demonstrate that temperature exerts a strong control on microbial diversity when considered over most of the temperature range within which life is possible.

Figure 1

Scatter plots of total OTUs detected (a) and Shannon diversity index (b) versus sample pH. Dashed lines represent the best-fit linear model to the data. Diversity indices were calculated using 2730 sequences per spring sample. Symbol shape indicates Canada (○) or New Zealand (Δ).

Figure 2

Nonmetric multidimensional scaling plot of geothermal spring microbial communities based on Bray–Curtis similarity showing separation of sites based on temperature and pH. Shade coding indicates temperature (a) or pH (b). Symbols in (b) indicate location: Canada (○) or New Zealand (Δ).

Figure 3

Scatter plots of total OTUs detected (a) and Shannon diversity index (b) versus temperature for neutral–alkaline springs (pH >5) included in the current study, plus additional sites from previous studies (Cole et al., 2013; Hou et al., 2013). Solid lines represent the best-fit Gaussian four-parameter model to the data. The dashed line represents the best-fit linear model to the data. Diversity indices for our study were calculated using 2730 sequences per spring sample. Symbol shape indicates Canada (○), New Zealand (Δ), China (□) (Hou et al., 2013) or the United States (◊) (Cole et al., 2013).