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  1. Summary

    To distinguish among hypotheses on the importance of resource‐exchange ratios in outcomes of mutualisms, we measured resource (carbon (C), nitrogen (N), and phosphorus (P)) transfers and their ratios, betweenPinus taedaseedlings and two ectomycorrhizal (EM) fungal species,Rhizopogon roseolusandPisolithus arhizusin a laboratory experiment.

    We evaluated how ambient light affected those resource fluxes and ratios over three time periods (10, 20, and 30 wk) and the consequences for plant and fungal biomass accrual, in environmental chambers.

    Our results suggest that light availability is an important factor driving absolute fluxes of N, P, and C, but not exchange ratios, although its effects vary among EM fungal species. Declines in N : C and P : C exchange ratios over time, as soil nutrient availability likely declined, were consistent with predictions of biological market models. Absolute transfer of P was an important predictor of both plant and fungal biomass, consistent with the excess resource‐exchange hypothesis, and N transfer to plants was positively associated with fungal biomass.

    Altogether, light effects on resource fluxes indicated mixed support for various theoretical frameworks, while results on biomass accrual better supported the excess resource‐exchange hypothesis, although among‐species variability is in need of further characterization.

    Free, publicly-accessible full text available November 8, 2023
  2. Abstract

    Producer–decomposer interactions within aquatic biofilms can range from mutualistic associations to competition depending on available resources. The outcomes of such interactions have implications for biogeochemical cycling and, as such, may be especially important in northern peatlands, which are a global carbon sink and are expected to experience changes in resource availability with climate change. The purpose of this study was to evaluate the effects of nutrients and organic carbon on the relative proportion of primary producers (microalgae) and heterotrophic decomposers (bacteria and fungi) during aquatic biofilm development in a boreal peatland. Given that decomposers are often better competitors for nutrients than primary producers in aquatic ecosystems, we predicted that labile carbon subsidies would shift the biofilm composition towards heterotrophy owing to the ability of decomposers to outcompete primary producers for available nutrients in the absence of carbon limitation.

    We manipulated nutrients (nitrate and phosphate) and organic carbon (glucose) in a full factorial design using nutrient‐diffusing substrates in an Alaskan fen.

    Heterotrophic bacteria were limited by organic carbon and algae were limited by inorganic nutrients. However, the outcomes of competitive interactions depended on background nutrient levels. Heterotrophic bacteria were able to outcompete algae for available nutrients when organic carbon was elevated andmore »nutrient levels remained low, but not when organic carbon and nutrients were both elevated through enrichment.

    Fungal biomass was significantly lower in the presence of glucose alone, possibly owing to antagonistic interactions with heterotrophic bacteria. In contrast to bacteria, fungi were stimulated along with algae following nutrient enrichment.

    The decoupling of algae and heterotrophic bacteria in the presence of glucose alone shifted the biofilm trophic status towards heterotrophy. This effect was overturned when nutrients were enriched along with glucose, owing to a subsequent increase in algal biomass in the absence of nutrient limitation.

    By measuring individual components of the biofilm and obtaining data on the trophic status, we have begun to establish a link between resource availability and biofilm formation in northern peatlands. Our results show that labile carbon subsidies from outside sources have the potential to disrupt microbial coupling and shift the metabolic balance in favour of heterotrophy. The extent to which this occurs in the future will probably depend on the timing and composition of bioavailable nutrients delivered to surface waters with environmental change (e.g. permafrost thaw).

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  3. Abstract

    Periphyton communities associated with submerged plant detritus contain interacting autotrophic and heterotrophic microbes, and are sites of extracellular enzymatic activity. The strength and nature of these interactions might be expected to change over time as microbial communities develop on plant litter. Microbial interactions and enzymatic activity can be altered by nutrient availability, suggesting that litter stoichiometry could also affect these phenomena.

    We grew wetland plants under ambient and nutrient‐enriched conditions to generate plant litter of differing nutrient content. In two experiments, we investigated: (1) the influence of algal photosynthesis on fungal and bacterial production and the activities of four extracellular enzymes throughout a 54‐day period of microbial colonisation and growth; and (2) the influence of litter stoichiometry on these relationships.

    Ambient and nutrient‐enriched standing‐dead plant litter was collected and then submerged in wetland pools to allow for natural microbial colonisation and growth. Litter samples were periodically retrieved and transported to the laboratory for experiments manipulating photosynthesis using the photosystem II inhibitor DCMU (which effectively prevents algal photosynthetic activity). Algal (14C‐bicarbonate), bacterial (3H‐leucine), and fungal (14C‐acetate) production, and β‐glucosidase, β‐xylosidase, leucine aminopeptidase, and phosphatase activities (MUF‐ or AMC‐labelled fluorogenic substrates) were measured under conditions of active and inhibited algal photosynthesis.

    Photosynthesis stimulated overallmore »fungal and bacterial production in both experiments, although the strength of stimulation varied amongst sampling dates. Phosphatase activity was stimulated by photosynthesis during the first, but not the second, experiment. No other enzymatic responses to short‐term photosynthesis manipulations were observed.

    Microbial communities on high‐nutrient litter occasionally showed increased extracellular enzyme activity, fungal growth rates, and bacterial production compared to communities on non‐enriched litter, but algal and fungal production were not affected. Litter stoichiometry had no effects on fungal, bacterial, or enzymatic responses to photosynthesis, but the mean enzyme vector analysis angle (a measure of P‐ versus N‐acquiring enzyme activity) was positively correlated to litter N:P, suggesting that elevated litter N:P led to an increase in the relative activity of P‐acquiring enzymes.

    These results supported the hypothesis that algal photosynthesis strongly influences heterotrophic microbial activity on macrophyte leaf litter, especially that of fungi, throughout microbial community development. However, the strength of this photosynthetic stimulation does not generally depend on small differences in litter nutrient content.

    Stimulation of microbial heterotrophs by algal photosynthesis could drive diurnal shifts in periphyton community and aquatic ecosystem function, as well as linkinggreen(photoautotroph‐based) andbrown(detrital‐based) food webs.

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  4. Abstract

    In aquatic detrital‐based food webs, research suggests that autotroph‐heterotroph microbial interactions exert bottom‐up controls on energy and nutrient transfer. To address this emerging topic, we investigated microbial responses to nutrient and light treatments duringLiriodendrontulipiferalitter decomposition and fed litter to the caddisfly larvaePycnopsychesp. We measured litter‐associated algal, fungal, and bacterial biomass and production. Microbes were also labeled with14C and33P to trace distinct microbial carbon (C) and phosphorus (P) supportingPycnopsycheassimilation and incorporation (growth). Litter‐associated algal and fungal production rates additively increased with higher nutrient and light availability. Incorporation of microbial P did not differ across diets, except for higher incorporation efficiency of slower‐turnover P on low‐nutrient, shaded litter. On average,Pycnopsycheassimilated fungal C more efficiently than bacterial or algal C, andPycnopsycheincorporated bacterial C more efficiently than algal or fungal C. Due to high litter fungal biomass, fungi supported 89.6–93.1% ofPycnopsycheC growth, compared to 0.2% to 3.6% supported by bacteria or algae. Overall,Pycnopsycheincorporated the most C in high nutrient and shaded litter. Our findings affirm others' regarding autotroph‐heterotroph microbial interactions and extend into the trophic transfer of microbial energy and nutrients through detrital food webs.

  5. Abstract

    Recent evidence suggests that periphytic algae stimulate plant litter heterotrophs (fungi and bacteria) in the presence of light, but few studies have tested whether this stimulation varies across gradients of light, which may covary with temperature.

    We exposed field‐conditionedTypha domingensislitter to fully‐crossed, short‐term gradients of temperature (15, 20, 25, and 30°C) and light (0, 25, 53, 123, and 388 µmol quanta m−2 s−1) and measured responses of litter‐associated algal, fungal, and bacterial production rates and β‐glucosidase, β‐xylosidase, and phenol oxidase enzyme activities in the laboratory.

    Increased light stimulated algal production rates, from immeasurable production under darkness to >200 µg algal C g−1detrital C hr−1at the highest light level, with the greatest light sensitivity and maximal photosynthetic rates at 25°C. In turn, increased light stimulated fungal production rates, especially at the two highest temperatures and most strongly at 25°C where light stimulated fungal production by a mean of 65 µg C g−1detrital C hr−1, indicating 2.1‐fold stimulation by light. Bacterial production rates also responded to light, indicated by stimulation of a mean of 16 µg C g−1detrital C hr−1(1.6‐fold) at 15°C, but stimulation was weaker at higher temperatures. Enzyme activities increased strongly with elevated temperature but were not affected by light.

    Our experimental evidence suggests algae differentially stimulate litter‐associated bacteria and fungi in amore »light‐dependent manner that further depends on temperature. These findings advance understanding of the onset of algal stimulation of heterotrophy, including algal‐induced priming effects during litter decomposition, in response to common covarying environmental gradients subject to global change.

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  6. Abstract

    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 tulipiferaandQuercus 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‐decomposingL. tulipiferaandQ. 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 recalcitrantmore »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 summaryis available for this article.

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