Microbial Functional Diversity Correlates with Species Diversity along a Temperature Gradient

Microbial community diversity is often correlated with physical environ-mental stresses like acidity, salinity, and temperature. For example, species diversity usually declines with increasing temperature above 20 degrees C. However, few studies have examined whether the genetic functional diversity of community metagenomes varies in a similar way as species diversity along stress gradients. Here, we investigated bacte-rial communities in thermal spring sediments ranging from 21 to 88 degrees C, representing communities of 330 to 3,800 bacterial and archaeal species based on 16S rRNA gene amplicon analysis. Metagenomes were sequenced, and Pfam abundances were used as a proxy for metagenomic functional diversity. Significant decreases in both species di-versity and Pfam diversity were observed with increasing temperatures. The relationship between Pfam diversity and species diversity followed a power function with the steep-est slopes in the high-temperature, low-diversity region of the gradient. Species addi-tions to simple thermophilic communities added many new Pfams, while species addi-tions to complex mesophilic communities added relatively fewer new Pfams, indicating that species diversity does not approach saturation as rapidly as Pfam diversity does. Many Pfams appeared to have distinct temperature ceilings of 60 to 80 degrees C. This study suggests that temperature stress limits both taxonomic and functional diversity of mi-crobial communities, but in a quantitatively different manner. Lower functional diversity at higher temperatures is probably due to two factors, including (i) the absence of many enzymes not adapted to thermophilic conditions, and (ii) the fact that high-tem-perature communities are comprised of fewer species with smaller average genomes and, therefore, contain fewer rare functions. IMPORTANCE Only recently have microbial ecologists begun to assess quantitatively how microbial species diversity correlates with environmental factors like pH, tempera -ture, and salinity. However, still, very few studies have examined how the number of distinct biochemical functions of microbial communities, termed functional diversity, varies with the same environmental factors. Our study examined 18 microbial com-munities sampled across a wide temperature gradient and found that increasing tem-perature reduced both species and functional diversity, but in different ways. Initially, functional diversity increased sharply with increasing species diversity but eventually plateaued, following a power function. This pattern has been previously predicted in theoretical models, but our study validates this predicted power function with field metagenomic data. This study also presents a unique overview of the distribution of metabolic functions along a temperature gradient, demonstrating that many functions have temperature ceilings above which they are no longer found.

Automated summary

Microbial community diversity is correlated with physical environmental stresses. This study investigated bacterial communities in thermal spring sediments and found that both species diversity and metagenomic functional diversity decrease with increasing temperatures. The relationship between the two diversities follows a power function, indicating a quantitatively different manner in which temperature stress limits both taxonomic and functional diversity of microbial communities. The study also highlights the distinct temperature ceilings of various metabolic functions.