Niche differentiation in microbial communities with stable genomic traits over time in engineered systems

Abstract

Microbial communities in full-scale engineered systems undergo dynamic compositional changes. However, mechanisms governing assembly of such microbes and succession of their functioning and genomic traits under various environmental conditions are unclear. In this study, we used the activated sludge and anaerobic treatment systems of four full-scale industrial wastewater treatment plants as models to investigate the niches of microbes in communities and the temporal succession patterns of community compositions. High-quality representative metagenome-assembled genomes revealed that taxonomic, functional, and trait-based compositions were strongly shaped by environmental selection, with replacement processes primarily driving variations in taxonomic and functional compositions. Plant-specific indicators were associated with system environmental conditions and exhibited strong determinism and trajectory directionality over time. The partitioning of microbes in a co-abundance network according to groups of plant-specific indicators, together with significant between-group differences in genomic traits, indicated the occurrence of niche differentiation. The indicators of the treatment plant with rich nutrient input and high substrate removal efficiency exhibited a faster predicted growth rate, lower guanine-cytosine content, smaller genome size, and higher codon usage bias than the indicators of the other plants. In individual plants, taxonomic composition displayed a more rapid temporal succession than functional and trait-based compositions. The succession of taxonomic, functional, and trait-based compositions was correlated with the kinetics of treatment processes in the activated sludge systems. This study provides insights into ecological niches of microbes in engineered systems and succession patterns of their functions and traits, which will aid microbial community management to improve treatment performance.

Keywords: genome-resolved metagenomics; genomic traits; microbial succession; niche differentiation; plant-specific indicators; process kinetics.