Can heavy metal pollution stress reduce microbial carbon-use efficiencies?

The fate of soil organic matter (OM) is determined by its microbial use for growth or respiration. Many environmental factors influence microbial OM use, including the presence of contaminants and toxins in the environment, such as heavy metals. We evaluated short- and long-term responses of microbial processes to metal contamination by estimating biomass concentrations and growth rates of bacteria and fungi, respiration, and the resulting microbial carbon-use efficiencies (CUE), and microbial turnover times. We sampled O-horizon from a gradient in boreal forest soils exposed to long-term heavy metal contamination arising from industrial point source since the 1930s to assess long term effects on soil microorganisms. To estimate microbial responses to short-term metal exposure, additions of Cu were used. Bacterial growth rates and respiration rates decreased in response to long-term metal contamination, while fungal growth rates were unaffected, without changes in CUEs. Bacterial biomass concentrations were independent of soil metal concentrations while fungal and total biomass decreased. Thus, turnover times for bacteria were slowed while fungal turnover times were accelerated by metal pollution. Bacterial growth was inhibited and fungal growth stimulated by experimental Cu additions, with bigger effect sizes in contaminated sites. We interpreted the low rates of growth but high biomass in collected soil samples to indicate that the fungal community included a large mycorrhizal fraction. Although Cu additions decreased the overall microbial OM-use (i.e., the sum of fungal and bacterial growth and total respiration), they also increased the CUE. In conclusion, fungal OM-use was less sensitive than bacterial to metal pollution and the CUE was unaffected. Microbial decomposer communities in contaminated soils were also able to maintain higher CUE when challenged with new metal additions. Our results imply that microbial communities align their trait compositions to environmental challenges, and that this can mitigate the reduction in microbial carbon-use efficiencies that often is expected to occur from environmental stress.