Metals alter membership but not diversity of a headwater stream microbiome

Metal contamination from mining or natural weathering is a common feature of surface waters in the American west. Traditionally, stream macroinvertebrate community metrics have been used for stream quality assessments. Advances in microbial analyses have created the potential for routine sampling of aquatic microbiomes as a tool to assess the quality of stream habitat. We sought to determine if microbiome diversity and membership were affected by metal contamination in a manner similar to what has been observed for stream macroinvertebrates, and if so, identify candidate microbial taxa to be used to indicate metal stress in stream ecosystems. We evaluated microbiome membership from sediments at multiple sites within the principal drainage of an EPA superfund site near the headwaters of the Upper Arkansas River, Leadville, CO. From each sample, we extracted DNA and sequenced the 16S rRNA gene amplicon on the Illumina MiSeq platform. We used the remaining sediments to simultaneously evaluate environmental metal concentrations. We also conducted an artificial stream mesocosm experiment using sediments collected from two of the observational study sites. The mesocosm experiment had a 2x2 factorial design: 1) location (upstream or downstream of contaminating tributary), and 2) treatment (metal exposure or control). We found no difference in diversity between upstream and downstream sites in the field. Similarly, diversity changed very little following experimental metal exposure. However, microbiome membership differed between upstream and downstream locations and experimental metal exposure changed microbiome membership in a manner that depended on origin of the sediments used in each mesocosm. ImportanceOur results suggest that microbiomes can be reliable indicators of ecosystem metal stress even when surface water chemistry and other metrics used to assess ecosystem health do not indicate ecosystem stress. Several results presented in this study are consistent with the idea that a microbial response to metals at the base of the food web may be affecting consumers one trophic level above. If effects of metals are mediated through shifts in the microbiome, then microbial metrics, as presented here, may aid in the assessment of stream ecosystems health.