Metagenomics analysis reveals landscape patterns of oxygen-sensitive respiratory processes in temperate rainforest soils

The North Pacific Coastal Temperate Rain forest (PCTR) of Southeast Alaska is one of Earth's most carbon-rich ecosystems. Recognizing that different modes of energy metabolism are directly related to the antecedent oxygen (O2) levels and available electron donors, this study used soil metagenomics to assess differences in PCTR soil microbial communities with special attention to genes associated with the reduction of O2 and nitrogen oxide (N-oxide) compounds which are key for the biogeochemical oxidation of carbon (C). Occurrence of reads in the metagenomes was used as a proxy to quantify the abundance of genes across an ecohydrologic gradient. We tested the hypothesis that the master variables that define the PCTR ecosystems, i.e., hydrology and vegetation, also correlate with the distribution of genes involved in aerobic and anaerobic respiration. Consistent with predominant ecosystem classifications, gene-read occurrence across ecosystems identified distinct microbial fingerprints differentiating the driest (upland forest) and wettest ecosystem (scrub-shrub and emergent wetland) types. There was little gene-based differentiation between scrub-shrub wetland and emergent wetland ecosystem classes. The forested wetland showed substantial metagenomic variability and, consequently, overlapped all three of the other ecosystem classes. Additional insight into ecosystem conditions was gained by taking advantage of the known oxygen-affinities of the various terminal reductases involved in aerobic respiration. As expected, hydrology, e.g., depth to water table, was a predictor of terminal reductase preference. However, two plant species, Tsuga heterophylla (TSHE) and Pinus contorta spp. contorta (PICO) also correlated with respiratory pathway preference. With regional temperatures rising and predicted shifts in precipitation patterns, this information is critically important for understanding how spatial shifts in soil hydrologic conditions will influence microbially mediated soil C and N storage, transformation, and greenhouse gas production across the PCTR.