Long-term and combined heavy-metal contamination forms a unique microbiome and resistome: a case study in the sediments of a Yellow River tributary

Microorganisms have mechanisms to adapt to environmental stress, but how microbial communities adapt to long-term and combined heavy-metal contamination under natural environmental conditions remains unclear. This study is the first to investigate the characteristics of heavy metal compositions, microbial community and heavy metal resistance genes in the sediments along a tributary of the Yellow River which has over 1000 years history and heavily been polluted by industrial production for more than 40 years. The results indicated that the river was mainly polluted by Cr, Zn, Pb, Cu, As, with concentrations of 50.15~2966.9, 19.65~205.8, 7.6~63.65, 22.35~51.9, 6.05~29.7 mg/kg, respectively, among which Cu had the highest bioavailability of 74 ~ 81%. The ecological risks of combined heavy metals in the sediments of Mang River decreased gradiently from very strong risk to mild risk along the river stream, and two-thirds of the Mang River sediment samples were in above moderate risk. HMs are the main drivers of structural changes in microbial communities. The sensitivity to heavy metal contamination was archaea >bacterial >fungi. Additionally, the bacterial phyla Acidobacteria, Actinobacteria, Chloroflexi and Planctomycetes and the archaea phyla Thaumarchaeota, Crenarchaeota and Candidatus Lokiarchaeota were found to be the core functional phyla in the contaminated sediments. Cr and Zn resistant gene (e.g., ruvB, recG and troB), glycan biosynthesis and metabolism, Carbohydrate metabolism and Lipid metabolism pathways showed a higher abundance in extremely contaminated samples. In conclusion, microbiome of sediment from Mang River has evolved into an integrated system resistant to long-term heavy metal pollution.