Priming effect: bridging the gap between terrestrial and aquatic ecology

Abstract

Understanding how ecosystems store or release carbon is one of ecology's greatest challenges in the 21st century. Organic matter covers a large range of chemical structures and qualities, and it is classically represented by pools of different recalcitrance to degradation. The interaction effects of these pools on carbon cycling are still poorly understood and are most often ignored in global-change models. Soil scientists have shown that inputs of labile organic matter frequently tend to increase, and often double, the mineralization of the more recalcitrant organic matter. The recent revival of interest for this phenomenon, named the priming effect, did not cross the frontiers of the disciplines. In particular, the priming effect phenomenon has been almost totally ignored by the scientific communities studying marine and continental aquatic ecosystems. Here we gather several arguments, experimental results, and field observations that strongly support the hypothesis that the priming effect is a general phenomenon that occurs in various terrestrial, freshwater, and marine ecosystems. For example, the increase in recalcitrant organic matter mineralization rate in the presence of labile organic matter ranged from 10% to 500% in six studies on organic matter degradation in aquatid ecosystems. Consequently, the recalcitrant organic matter mineralization rate may largely depend on labile organic matter availability, influencing the CO2 emissions of both aquatic and terrestrial ecosystems. We suggest that (1) recalcitrant organic matter may largely contribute to the CO2 emissions of aquatic ecosystems through the priming effect, and (2) priming effect intensity may be modified by global changes, interacting with eutrophication processes and atmospheric CO2 increases. Finally, we argue that the priming effect acts substantially in the carbon and nutrient cycles in all ecosystems. We outline exciting avenues for research, which could provide new insights on the responses of ecosystems to anthropogenic perturbations and their feedbacks to climatic changes.

Functional and Structural Responses of Hyporheic Biofilms to Varying Sources of Dissolved Organic Matter

“…Despite the increased metabolism upon AU-DOM additions, there were no corresponding changes in extracellular enzyme activities measured in the outflow of the bioreactors. We expected that AU-DOM provides easily available energy that would enable microorganisms to express more extracellular enzymes enhancing AL-DOM degradation (9). The tendency of higher esterase and endopeptidase activities in the AU-DOM treatments indicates a delayed expression increase of these enzymes.…”

“…On the other hand, AL-DOM, such as leachates from decaying leaf litter, is often aged and depleted in labile compounds and may therefore be resistant (recalcitrant) to microbial degradation (8). The interaction of these different organic matter pools has potentially important implications for carbon cycling in stream ecosystems (9). For instance, labile organic matter may enhance microbial degradation of recalcitrant organic matter through priming or cometabolism (1,(9)(10)(11).…”

“…The interaction of these different organic matter pools has potentially important implications for carbon cycling in stream ecosystems (9). For instance, labile organic matter may enhance microbial degradation of recalcitrant organic matter through priming or cometabolism (1,(9)(10)(11). Therefore, knowledge of the structure and functioning of the microbial communities dwelling in the hyporheic zone and their potential response to variations in the DOM supply is important to better assess the role of the hyporheic zone for biogeochemical processes.…”

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…The release of labile DOC from POC degradation by particleassociated microorganisms may not only fuel the microbial loop (198,273,274) but also facilitate the priming effect that stimulates the degradation of recalcitrant organic matter (275,276). Furthermore, deep-water microorganisms usually have large genomes and inventories of genes contributing to surface association (199).…”

Composition of riparian litter input regulates organic matter decomposition: Implications for headwater stream functioning in a managed forest landscape

“…Such effects may be attributed to (1) a local adaptation by microbial communities, resulting in locally produced litter being more readily decomposed than litter from outside (i.e., “home‐field advantage”; Gholz, Wedin, Smitherman, Harmon, & Parton, 2000; Hunt, Ingham, Coleman, Elliott, & Reid, 1988; Jackrel & Wootton, 2014) and/or (2) a “priming effect” where higher‐quality resources, by providing more easily accessible nutrients, increase microbial biomass, which in turn accelerates the turnover of lower‐quality resources (Guenet, Danger, Abbadie, & Lacroix, 2010; Kuzyakov, Friedel, & Stahr, 2000). Independent of the mechanism, these relationships have obvious implications for management of riparian zones, but the challenge is to assess the significance of riparian composition effects across heterogeneous landscapes, where a suite of other potentially important physical and chemical factors may also vary.…”