Spatiotemporal profiling and succession of microbial communities in landfills based on a cross-kingdom abundance quantification method

Abstract

Landfill provides a unique niche for both prokaryotic and eukaryotic microorganisms, in which organic matter and physiochemical conditions continuously change with the landfill age and drive the succession of landfill microbiomes. Nonetheless, information on the spatiotemporal changes of landfill microbiomes, particularly the prokaryotic and eukaryotic communities and their interactions, remain scarce. In this study, a new cross-kingdom abundance quantification method was devised to obtain cell abundance of both prokaryotes and eukaryotes based on high-throughput sequencing, and employed to elucidate microbiomes of leachate samples collected from nationwide landfills in China. Results showed the clustering of landfills into two groups primarily based on microbial community compositions, being in line with the change in their landfill ages (i.e., Group-I, <10 years; Group-II, ≧10 years), and 1320.9 and 88.0 times of abundance difference between prokaryotes and eukaryotes in the Group-I and –II communities, respectively. Reducing equivalent was determined as a primary factor governing the landfill microbial abundance, assembly and interactions. In contrast to Group-I characterized by the extensive organic matter fermentation and multi-pathway methanogenesis driven by fermenters and methanogenic archaea, aerobic heterotrophs played a primary role in element cycling and archaea-mediated methanogenic activities were diminished in Group-II communities, in which heterotrophic bacteria and fungi might synergistically degrade recalcitrant organic matter. Interestingly, protozoa and metazoa as bacteria/fungi predators decreased the stability of Group-II communities in a top-down manner. Based on these observations, a scenario was proposed for the energy-driven succession of landfill microbiomes and mediated biogeochemical processes. Our study provided the first large-scale and comprehensive insight into the landfill microbiomes for their future sustainable management.