Substrate-restricted methanogenesis and limited volatile organic compound degradation in highly diverse and heterogeneous municipal landfill microbial communities

Microbial communities in landfills transform waste and generate methane in an environment unique from other built and natural environments. Landfill microbial diversity has predominantly been observed at the phylum level, without examining the extent of shared organismal diversity across space or time. We used 16S rRNA gene amplicon and shotgun metagenomic sequencing to examine the taxonomic and functional diversity of the microbial communities inhabiting a Southern Ontario landfill. The microbial capacity for volatile organic compound degradation in leachate and groundwater samples was correlated with geochemical conditions. Across the landfill, 25 bacterial and archaeal phyla were present at >1% relative abundance within at least one landfill sample, with Patescibacteria, Bacteroidota, Firmicutes, and Proteobacteria dominating. Methanogens were neither numerous nor particularly abundant, and were predominantly constrained to either acetoclastic or methylotrophic methanogenesis. The landfill microbial community was highly heterogeneous, with 90.7% of organisms present at only one or two sites within this interconnected system. Based on diversity measures, the landfill is a microbial system undergoing a constant state of disturbance and change, driving the extreme heterogeneity observed. Significant differences in geochemistry occurred across the leachate and groundwater wells sampled, with calcium, iron, magnesium, boron, meta and para xylenes, ortho xylenes, and ethylbenzene concentrations contributing most strongly to observed site differences. Predicted microbial degradation capacities indicated a heterogeneous community response to contaminants, including identification of novel proteins implicated in anaerobic degradation of key volatile organic compounds.