Quantifying the importance of the rare biosphere for microbial community adaptation to organic pollutants in a freshwater ecosystem
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Microbial community analysis frequently focuses on abundant organisms, but natural communities commonly harbor thousands of low abundance, ‘rare’ organisms. The importance of this ‘rare biosphere’ for microbial community adaptation to environmental perturbations and pollution remains speculative. We tested whether rare species respond to changing environmental conditions by establishing 20 liter, planktonic mesocosms with water from Lake Lanier (Georgia, USA), and perturbing them with organic pollutants that are rarely detectable in the lake, such as 2,4-dichlorophenoxyacetic acid (2,4-D; a pesticide), 4-nitrophenol (4-NP; an industrial organic), and caffeine. The populations of the degraders of these compounds were initially below detection limit of qPCR or metagenomic sequencing methods (i.e., <0.001% of total community), but increased substantially in abundance after perturbation. All replicated 2,4-D mesocosms exhibited distinct degradation profiles, presumably due to the response of the rare biosphere (e.g., not all species are present in all inocula due to low abundance) and/or stochastic processes in the activation of rare species and genes. To obtain further insights into the latter, we sequenced several 2,4D-degrading isolates, and assessed their genomes against time-series metagenomic datasets from the 2,4-D replicated mesocosms. We found distinct, co-occurring alleles of degradation genes, encoded frequently on transmissible plasmids, and distinct species dominated the post-enrichment datasets from each mesocosm. Collectively, these results supported the hypothesis that the rare biosphere can serve as a genetic reservoir that enables community adaptation to changing environmental conditions, and provided insights into the size of the pool of rare genes and species for the biodegradation of important environmental pollutants.