Periphytic algae decouple fungal activity from leaf litter decomposition via negative priming

Abstract

1. Well-documented in terrestrial settings, priming effects describe stimulated heterotrophic microbial activity and decomposition of recalcitrant carbon by additions of labile carbon. In aquatic settings, algae produce labile exudates which may elicit priming during organic matter decomposition, yet the directions and mechanisms of aquatic priming effects remain poorly tested. 2. We tested algal-induced priming during decomposition of two leaf species of contrasting recalcitrance, Liriodendron tulipifera and Quercus nigra, in experimental streams under light or dark conditions. We measured litter-associated algal, bacterial, and fungal biomass and activity, stoichiometry, and litter decomposition rates over 43 days. 3. Light increased algal biomass and production rates and increased bacterial abundance 141–733% and fungal production rates 20–157%. Incubations with a photosynthesis inhibitor established that algal activity directly stimulated fungal production rates in the short-term. 4. Algal-stimulated fungal production rates on both leaf species were not coupled to long-term increases in fungal biomass accrual or litter decomposition rates, which were 154–157% and 164–455% greater in the dark, respectively. The similar patterns on fast- vs. slow-decomposing L. tulipifera and Q. nigra, respectively, indicated that substrate recalcitrance may not mediate priming strength or direction. 5. In this example of negative priming, periphytic algae decoupled fungal activity from decomposition, likely by providing labile carbon invested toward greater fungal growth and reproduction instead of recalcitrant carbon degradation. If common, algal-induced negative priming could stimulate heterotrophy reliant on labile carbon yet suppress decomposition of recalcitrant carbon, modifying energy and nutrients available to upper trophic levels and enhancing organic carbon storage or export in well-lit aquatic habitats.

Litter quality and site characteristics interact to affect the response of priming effect to temperature in subtropical forests

“…Conversely, at the low elevation site, AP‐tase activity increased by 36% and 22% after addition of the high‐ and low‐quality litters, respectively, and the C enz /AP of the high‐quality litter treatment was higher than the low‐quality litter treatment, suggesting that microbes under the high‐quality litter treatment invested more C towards the acquisition of P from SOM. Taken together, these results for the low elevation site indicate that high‐quality litter caused micro‐organisms to decompose more native SOM to meet microbial P demands compared with low‐quality litter (Halvorson et al, ; Rousk, Hill, & Jones, ).…”

Temporal and stoichiometric patterns of algal stimulation of litter‐associated heterotrophic microbial activity

“…Rapid photosynthetic stimulation of heterotrophic microbial activity is another interaction which can occur in periphyton. Algal photosynthesis can result in near-instantaneous stimulation of bacterial (Neely & Wetzel, 1995;Scott, Back, Taylor, & King, 2008;Kuehn, Francoeur, Findlay, & Neely, 2014) and fungal (Kuehn et al, 2014;Halvorson et al, 2019a) production and growth rates in periphyton. Photosynthesis may also cause similar rapid increases in the activity of carbon (C)-acquiring (e.g., ß-glucosidase, ß-xylosidase), nitrogen (N)-acquiring (e.g., leucineaminopeptidase), and phosphorus (P)-acquiring (phosphatase) extracellular enzymes produced…”

Algal-Mediated Priming Effects on the Ecological Stoichiometry of Leaf Litter Decomposition: A Meta-Analysis

“…Under positive priming, algae increase N and P mass loss, likely through increased heterotrophic investment in degradative enzymes and mineralization of litter N and P (Rier et al, 2007;Kuzyakov, 2010). Under negative priming, algae reduce N and P mineralization from litter, probably by suppressing heterotrophic investment in enzymes and simultaneously by immobilizing N and P (Blagodatskaya and Kuzyakov, 2008;Halvorson et al, 2019). In this way, algal priming intensity may also strongly affect the fate of endogenous litter N and P, not just litter C. The opposing algal effects on C:N and C:P versus k N and k P indicate algal effects on litter-periphyton C loss are relatively stronger than effects on N and P loss.…”

“…For a description of methods used to collect unpublished data, see Supplementary Material Appendix 1. Some of the studies in our meta-analysis included experiments using different nutrient levels (Danger et al, 2013;Halvorson et al, 2016) or contrasting leaf species (Halvorson et al, 2019) and we considered each dataset from these contrasting conditions as a separate contribution to calculate an algal effect size. Although there is a common first-author among many of these datasets (present first-author), indicating possible non-independence of the data, each of these datasets was collected by a different group of scientists in a different experimental setting.…”

“…In particular, recent research has revealed an important role of labile organic C additions, such as plant exudates or glucose, in stimulating microbial degradation of comparatively recalcitrant organic C by as much as 382% (Kuzyakov, 2010;Danger et al, 2013;Cheng et al, 2014). However, recent research in aquatic systems indicates that the presence of algal exudates (considered a source of labile C) can elicit wide-ranging effects, from significant enhancement (Danger et al, 2013) to significant inhibition (Halvorson et al, 2019), of leaf litter decomposition rates. As a consequence, the "priming effect" phenomenon appears to elicit a wide potential to alter the fate of organic C and nutrients across many ecosystems (Guenet et al, 2010(Guenet et al, , 2018, yet the interplay between priming and nutrient dynamics during organic matter decomposition remains poorly studied (Chen et al, 2014;Li et al, 2018).…”