Long-term industrial metal contamination unexpectedly shaped diversity and activity response of sediment microbiome

[Display omitted] •Combined DNA/RNA sequencing and FRGs accurately predicted microbial lifestyles.•Metal pollution in sediment resulted in unexpected higher microbial diversity.•Community coalescence, HGT and microbial facilitation explained this higher diversity. Metal contamination poses serious biotoxicity and bioaccumulation issues, affecting both abiotic conditions and biological activity in ecosystem trophic levels, especially sediments. The MetalEurop foundry released metals directly into the French river “la Deûle” during a century, contaminating sediments with a 30-fold increase compared to upstream unpolluted areas (Férin, Sensée canal). Previous metaproteogenomic work revealed phylogenetically analogous, but functionally different microbial communities between the two locations. However, their potential activity status in situ remains unknown. The present study respectively compares the structures of both total and active fractions of sediment prokaryotic microbiomes by coupling DNA and RNA-based sequencing approaches at the polluted MetalEurop site and its upstream control. We applied the innovative ecological concept of Functional Response Groups (FRGs) to decipher the adaptive tolerance range of the communities through characterization of microbial lifestyles and strategists. The complementing use of DNA and RNA sequencing revealed indications that metals selected for mechanisms such as microbial facilitation via “public-good” providing bacteria, Horizontal Gene Transfer (HGT) and community coalescence, overall resulting in an unexpected higher microbial diversity at the polluted site.