Metaproteomics reveals biomarkers of system collapse in a dynamic aquatic ecosystem

Abstract

Forecasting and preventing rapid ecosystem state changes is important but hard to achieve without functionally relevant early warning indicators. Here we use metaproteomic analysis to identify protein biomarkers indicating a state change in an aquatic ecosystem resulting from detrital enrichment. In a 14-day field experiment, we used detritus (arthropod prey) to enrich replicate aquatic ecosystems formed in the water-filled pitcher-shaped leaves of the northern pitcher plant, Sarracenia purpurea. Shotgun metaproteomics using a translated, custom metagenomic database identified proteins, molecular pathways, and microbial taxa that differentiated control oligotrophic ecosystems that captured only ambient prey from eutrophic ecosystems that were experimentally enriched. The number of microbial taxa was comparable between treatments; however, taxonomic evenness was higher in the oligotrophic controls. Aerobic and facultatively anaerobic bacteria dominated control and enriched ecosystems, respectively. The molecular pathways and taxa identified in the enriched treatments were similar to those found in a wide range of enriched or polluted aquatic ecosystems and are derived from microbial processes that occur at the base of most detrital food webs. We encourage the use of metaproteomic pipelines to identify better early-warning indicators of impending changes from oligotrophic to eutrophic states in aquatic and other detrital-based ecosystems.