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

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 t...

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Veröffentlicht in:Functional ecology 2019-01, Vol.33 (1), p.188-201
Hauptverfasser: Halvorson, Halvor M., Barry, Jacob R., Lodato, Matthew B., Findlay, Robert H., Francoeur, Steven N., Kuehn, Kevin A.
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container_issue 1
container_start_page 188
container_title Functional ecology
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creator Halvorson, Halvor M.
Barry, Jacob R.
Lodato, Matthew B.
Findlay, Robert H.
Francoeur, Steven N.
Kuehn, Kevin A.
description 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. 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. Light increased algal biomass and production rates, in turn increasing 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. 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. In this example of negative priming, periphytic algae decoupled fungal activity from decomposition, likely by providing labile carbon invested towards 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. plain language summary is available for this article. Plain Language Summary
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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. 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. Light increased algal biomass and production rates, in turn increasing 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. 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. In this example of negative priming, periphytic algae decoupled fungal activity from decomposition, likely by providing labile carbon invested towards 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. plain language summary is available for this article. Plain Language Summary</description><identifier>ISSN: 0269-8463</identifier><identifier>EISSN: 1365-2435</identifier><identifier>DOI: 10.1111/1365-2435.13235</identifier><identifier>PMID: 31673197</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Algae ; aquatic habitat ; Aquatic habitats ; bacteria ; Biodegradation ; Biological activity ; Biomass ; Carbon ; Carbon sequestration ; Decomposition ; detritus ; ecological stoichiometry ; ECOSYSTEM ECOLOGY ; energy ; exports ; Exudates ; Exudation ; fungal biomass ; fungal growth ; Fungi ; Heterotrophy ; labile carbon ; Leaf litter ; Leaves ; light ; Liriodendron tulipifera ; Microbial activity ; microbial heterotrophs ; Microorganisms ; Nutrient availability ; Nutrients ; Organic carbon ; Organic matter ; periphyton ; Photosynthesis ; plant litter ; Priming ; priming effects ; Quercus nigra ; reproduction ; Stoichiometry ; streams ; Substrates ; Terrestrial environments ; Trophic levels</subject><ispartof>Functional ecology, 2019-01, Vol.33 (1), p.188-201</ispartof><rights>2018 The Authors. © 2018 British Ecological Society</rights><rights>2018 The Authors. 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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. 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. Light increased algal biomass and production rates, in turn increasing 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. 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. In this example of negative priming, periphytic algae decoupled fungal activity from decomposition, likely by providing labile carbon invested towards 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. plain language summary is available for this article. 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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. 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. Light increased algal biomass and production rates, in turn increasing 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. 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. In this example of negative priming, periphytic algae decoupled fungal activity from decomposition, likely by providing labile carbon invested towards 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. plain language summary is available for this article. 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subjects Algae
aquatic habitat
Aquatic habitats
bacteria
Biodegradation
Biological activity
Biomass
Carbon
Carbon sequestration
Decomposition
detritus
ecological stoichiometry
ECOSYSTEM ECOLOGY
energy
exports
Exudates
Exudation
fungal biomass
fungal growth
Fungi
Heterotrophy
labile carbon
Leaf litter
Leaves
light
Liriodendron tulipifera
Microbial activity
microbial heterotrophs
Microorganisms
Nutrient availability
Nutrients
Organic carbon
Organic matter
periphyton
Photosynthesis
plant litter
Priming
priming effects
Quercus nigra
reproduction
Stoichiometry
streams
Substrates
Terrestrial environments
Trophic levels
title Periphytic algae decouple fungal activity from leaf litter decomposition via negative priming
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