Structural and functional response of soil microbiota to addition of plant substrate are moderated by soil Cu levels

Abstract

In soils, the microbially mediated decomposition of plant residue is a key process with wide ranging effects on ecosystem functioning and stability. Understanding the impact of contamination on this process is of high importance. We investigated the effects of long-term (6 years) copper exposure on the capacity of soil microbiota to decompose newly added resources; dried and ground Medicago truncatula stubble. In addition, the effects on the microbial community structure across the three domains were explored using polymerase chain reaction–denaturing gradient gel electrophoresis rRNA gene profiling. Ecological distances in community structure between treatments was calculated (Kulczynski) and effects tested using PERMANOVA. Clear dose–response relationships were present between microbial respiration (CO2 evolution) and soil Cu level in soils receiving medic, but not under basal conditions (i.e., no medic added). These show that relatively labile forms of C are needed to drive microbial ecotoxicological responses and that microbial adaptation to the presence of Cu in the soils—after >6 years exposure—was functionally limited. Bacterial, archaeal and fungal communities showed significant (P < 0.05) levels of structural change in soils across the Cu gradient, demonstrating that species replacement had occurred following strong selective pressure. Addition of medic resources to the soils caused significant shifts in the bacterial and archaeal community structure (P < 0.001), which occurred across the entire range of soil Cu levels. For the fungal community, a significant interaction effect was present between Cu and medic addition (P = 0.002). At low Cu levels, medic addition caused large shifts in community structure, but this was negligible under high Cu levels. This was reflected in significant changes in the level of community structural dispersion at low compared with high Cu levels. As such, we show that Cu limits the capacity of soil fungal communities to rapidly respond to new resource capture. Given the primary role of soil fungi in plant material decomposition, this may have wide ranging impacts on wider ecosystem processes including nutrient cycling, trophic interactions, food web stability and energy transfer.