Aquatic ecosystem enrichment can lead to distinct and irreversible changes to undesirable states. Understanding changes in active microbial community function and composition following organic-matter loading in enriched ecosystems can help identify biomarkers of such state changes. In a field experiment, we enriched replicate aquatic ecosystems in the pitchers of the northern pitcher plant, Sarracenia purpurea. Shotgun metaproteomics using a custom metagenomic database identified proteins, molecular pathways, and contributing microbial taxa that differentiated control ecosystems from those that were enriched. The number of microbial taxa contributing to protein expression was comparable between treatments; however, taxonomic evenness was higher in controls. Functionally active bacterial composition differed significantly among treatments and was more divergent in control pitchers than enriched pitchers. Aerobic and facultative anaerobic bacteria contributed most to identified proteins in control and enriched ecosystems, respectively. The molecular pathways and contributing taxa in enriched pitcher ecosystems were similar to those found in larger enriched aquatic ecosystems and are consistent with microbial processes occurring at the base of detrital food webs. Detectable differences between protein profiles of enriched and control ecosystems suggest that a time series of environmental proteomics data may identify protein biomarkers of impending state changes to enriched states.
Changes in environmental conditions can lead to rapid shifts in ecosystem state ("regime shifts"), which subsequently returns slowly to the previous state ("hysteresis"). Large spatial and temporal scales of dynamics, and the lack of frameworks linking observations to models, are challenges to understanding and predicting ecosystem responses to perturbations. The naturally-occurring microecosystem inside leaves of the northern pitcher plant (Sarracenia purpurea) exhibits oligotrophic and eutrophic states that can be induced by adding insect "prey." Here, we further develop a model for simulating these dynamics, parameterize it using data from a prey addition experiment and conduct a sensitivity analysis to identify critical zones within the parameter space. Simulations illustrate that the microecosystem model displays regime shifts and hysteresis. Parallel results were observed in the plant itself after experimental enrichment with prey. Decomposition rate of prey was the main driver of system dynamics, including the time the system remains in an anoxic state and the rate of return to an oxygenated state. Biological oxygen demand influenced the shape of the system's return trajectory. The combination of simulated results, sensitivity analysis and use of empirical results to parameterize the model more precisely demonstrates that the Sarracenia microecosystem model displays behaviors qualitatively
Changes in environmental conditions can lead to rapid shifts in the state of an ecosystem ("regime shifts"), which, even after the environment has returned to previous conditions, subsequently recovers slowly to the previous state ("hysteresis"). Large spatial and temporal scales of dynamics, and the lack of frameworks linking observations to models, are challenges to understanding and predicting ecosystem responses to perturbations. The naturallyoccurring microecosystem inside leaves of the northern pitcher plant (Sarracenia purpurea) exhibits oligotrophic and eutrophic states that can be induced by adding insect prey. Here, we further develop a model for simulating these dynamics, parameterize it using data from a prey addition experiment and conduct a sensitivity analysis to identify critical zones within the param-
Incremental increases in a driver variable, such as nutrients or detritus, can trigger abrupt shifts in aquatic ecosystems that may exhibit hysteretic dynamics and a slow return to the initial state. A model system for understanding these dynamics is the microbial assemblage that inhabits the cup-shaped leaves of the pitcher plant Sarracenia purpurea. With enrichment of organic matter, this system flips within three days from an oxygen-rich state to an oxygen-poor state. In a replicated greenhouse experiment, we enriched pitcher-plant leaves at different rates with bovine serum albumin (BSA), a molecular substitute for detritus. Changes in dissolved oxygen (DO) and undigested BSA concentration were monitored during enrichment and recovery phases. With increasing enrichment rates, the dynamics ranged from clockwise hysteresis (low), to environmental tracking (medium), to novel counterclockwise hysteresis (high). These experiments demonstrate that detrital enrichment rate can modulate a diversity of hysteretic responses within a single aquatic ecosystem, and suggest different management strategies may be needed to mitigate the effects of high vs. low rates of detrital enrichment.
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 waterfilled 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 detritalbased ecosystems.
8Incremental increases in a driver variable, such as nutrients or detritus, can trigger abrupt shifts in aquatic ecosys-9 tems. Once these ecosystems change state, a simple reduction in the driver variable may not return them to their 10 original state. Because of the long time scales involved, we still have a poor understanding of the dynamics of ecosys-11 tem recovery after a state change. A model system for understanding ecosystem recovery is the aquatic microecosystem 12 that inhabits the cup-shaped leaves of the pitcher plant Sarracenia purpurea. With enrichment of organic matter, this 13 system flips within 1 to 3 days from an oxygen-rich state to an oxygen-poor (hypoxic) state. In a replicated green-14 house experiment, we enriched pitcher plant leaves at different rates with bovine serum albumin (BSA), a molecular 15 substitute for detritus. Changes in dissolved oxygen ([O 2 ]) and undigested BSA concentration were monitored during 16 enrichment and recovery phases. At low enrichment rates, ecosystems showed a substantial lag in the recovery of [O 2 ] 17 (clockwise hysteresis). At intermediate enrichment rates, [O 2 ] tracked the levels of undigested BSA with the same 18 profile during the enrichment and recovery phases (no hysteresis). At high enrichment rates, we observed a novel 19 response: changes in [O 2 ] were proportionally larger during the recovery phase than during the enrichment phase 20 (counter-clockwise hysteresis). These experiments demonstrate that detrital enrichment rate can modulate a diversity 21 of hysteretic responses in a single aquatic ecosystem. With counter-clockwise hysteresis, rapid reduction of a driver 22variable following high enrichment rates may be a viable restoration strategy. 23Anthropogenically enriched ecosystems often exhibit complex dynamics and regime shifts 1 . Such shifts occur when in-24 cremental changes in a driver variable suddenly tip these systems from one basin of attraction to another 1-5 . Early studies 25 emphasized the importance of forecasting impending regime shifts by signature statistical changes in the autocorrelation 6 or 26 the variance 7 of a response variable. However, the lead times 8 and sampling frequencies 9 necessary to detect early warning 27 signals are usually too long to implement for practical management strategies. Equally important for management is how 28 a system recovers after a collapse. Aquatic ecosystems that collapse rapidly often recover slowly 10-12 , and may remain in 29 an altered state long after enrichment has ceased. A general mechanism that might cause such a lag is hysteresis -a phe-30 nomenon in which the relationship between a response variable and driver variable depends on the state of the system 13 . In 31 hysteretic systems, changes in the response variable lag behind those in the driver variable due to feedback loops between 32 the response variable and other components of the system. 33In spite of their potential importance to management and restoration ecology 14 , hysteretic responses of recovering en-34 ...
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