Lentic and Lotic Habitats as Templets for Fungal Communities: Traits, Adaptations, and Their Significance to Litter Decomposition Within Freshwater Ecosystems

Decomposition of plant matter is a key ecosystem process and considerable research has examined plant litter decay processes in freshwater habitats. Fungi are common inhabitants of the decomposer microbial community and representatives of all major fungal phyla have been identified within freshwater systems. Development and application of quantitative methods over the last several decades have firmly established that fungi are central players in the decomposition of plant litter in freshwaters and are important mediators of energy and nutrient transfer to higher trophic levels. Despite the critical roles that fungi play in carbon and nutrient cycling in freshwater ecosystems, there are notable differences in the types and adaptations of fungal communities between lotic and lentic habitats. These differences can be explained by the wide range of hydrologic, physical, chemical and biological conditions within freshwater systems, all of which can influence the presence, type, and activity of fungal decomposers and their impact on litter decomposition. This paper seeks to provide a brief overview of the types, adaptations, and role of fungi within lotic and lentic freshwater ecosystems, with a particular emphasis on their importance to litter decomposition and the key environmental conditions that impact their growth and decay activities. This discussion will specifically focus on fungal dynamics occurring on plant litter in forested headwater streams and emergent freshwater marshes, since published data concerning their role in these systems is considerably more abundant in comparison to other freshwater habitats

Algal Regulation of Extracellular Enzyme Activity in Stream Microbial Communities Associated with Inert Substrata and Detritus

We tested the hypothesis that algae influence the activities of extracellular enzymes involved in mineralization processes within microbial assemblages in streams. We tested the prediction that the factors that influence algal biomass and photosynthesis (i.e., diel fluctuations in photosynthetically active radiation [PAR], long-term variations in light regime, and community development stage) would have a corresponding effect on extracellular enzyme activities. We also tested the prediction that algae would influence enzyme activities on inorganic substrata and in detrital communities where they ultimately would influence plant litter decomposition rates. We allowed microbial communities to develop on inert substrata (glass-fiber filters) or on leaf litter in artificial streamside channels. For each community type, we examined the effects of long-term light manipulations, community development stage, and diel periodicity on the activities of P-glucosidase, alkaline phosphatase, leucine-aminopeptidase, and phenol oxidase. In addition, we measured the decomposition rates of the leaf litter substrata in the low- and high-light treatments. Our results support the prediction that factors that influence algal photosynthesis and biomass in the short (diel fluctuations in PAR) and long (shading, community development stage) term ultimately influence enzyme activities in microbial communities associated with both inorganic substrata and detritus. Furthermore, decomposition rates of organic detritus probably are enhanced by algal colonization and activity. Algal photosynthesis might enhance redox and pH conditions within microbial communities, and in turn, might increase the activities of oxidative and hydrolytic enzymes. As a consequence, photoautotrophic activities might stimulate heterotrophic pathways in stream ecosystems by creating conditions favorable for decomposition of both dissolved and particulate organic detritus

Evalution of the Efficacy of the Photosystem II Inhibitor DCMU in Periphyton and Its Effects On Nontarget Microorganisms and Extracellular Enzymatic Reactions

We examined the efficacy of the photosystem II inhibitor 3-(3,4-diclorophenyl)-1,1-dimethyl urea (DCMU) for inhibition of algal photosynthesis in periphyton associated with submerged decomposing litter of Typha angustifolia. We also investigated the possible nontarget effects of DCMU exposure on heterotrophic microorganisms (i.e., bacteria and fungi) and extracellular enzyme activity associated with decaying litter. Standing-dead Typha leaf litter was submerged for 34 and 73 d, returned to the laboratory, and used for controlled laboratory experiments that examined the effect of DCMU on algal ([14C]bicarbonate, pulse-amplitude modulated fluorometry), bacterial ([3H]leucine), and fungal ([14C]acetate) production. Simultaneous assays also were conducted to examine the effect of DCMU on the activities of 4 extracellular enzymes (β-glucosidase, β-xylosidase, leucine-aminopeptidase, and phosphatase). DCMU significantly inhibited algal photosynthesis in light-exposed periphyton (p always \u3c 0.0003), with strong inhibitory effects occurring within 5 min after exposure to DCMU. In contrast, DCMU had no significant direct effect on bacterial (p \u3e 0.5) or fungal production (p \u3e 0.3). Extracellular enzyme activities also were not significantly affected by exposure to DCMU. Heterotrophic microbial and enzyme activity assays were conducted in darkness to avoid any indirect effects of DCMU (i.e., heterotrophic responses to the inhibition of photosynthesis, rather than to DCMU itself). The apparent lack of nontarget effects of DCMU on heterotrophic microbial processes, combined with good efficacy against algal photosynthesis, suggest that DCMU may a useful selective inhibitor for investigations of interactions among litter-inhabiting microbiota

Priming in the Microbial Landscape: Periphytic Algal Stimulation of Litter-Associated Microbial Decomposers

Microbial communities associated with submerged detritus in aquatic ecosystems often comprise a diverse mixture of autotrophic and heterotrophic microbes, including algae, bacteria, protozoa, and fungi. Recent studies have documented increased rates of plant litter mass loss when periphytic algae are present. We conducted laboratory and field experiments to assess potential metabolic interactions between natural autotrophic and heterotrophic microbial communities inhabiting submerged decaying plant litter of Typha angustifolia and Schoenoplectus acutus. In the field, submerged plant litter was either exposed to natural sunlight or placed under experimental canopies that manipulated light availability and growth of periphytic algae. Litter was collected and returned to the laboratory, where algal photosynthesis was manipulated (light/dark incubation), while rates of bacterial and fungal growth and productivity were simultaneously quantified. Bacteria and fungi were rapidly stimulated by exposure to light, thus establishing the potential for algal priming of microbial heterotrophic decay activities. Experimental incubations of decaying litter with 14C‐ and 13C‐bicarbonate established that inorganic C fixed by algal photosynthesis was rapidly transferred to and assimilated by heterotrophic microbial decomposers. Periphytic algal stimulation of microbial heterotrophs, especially fungal decomposers, is an important and largely unrecognized interaction within the detrital microbial landscape, which may transform our current conceptual understanding of microbial secondary production and organic matter decomposition in aquatic ecosystems

Physical Processes Dictate Early Biogeochemical Dynamics of Soil Pyrogenic Organic Matter in a Subtropical Forest Ecosystem

Quantifying links between pyOM dynamics, environmental factors and processes is central to predicting ecosystem function and response to future perturbations. In this study, changes in carbon (TC), nitrogen (TN), pH, and relative recalcitrance (R50) for pineand cordgrass-derived pyOM were measured at 3–6 weeks intervals throughout the first year of burial in the soil. Objectives were to (1) identify key environmental factors and processes driving early-stage pyOM dynamics, and (2) develop quantitative relationships between environmental factors and observed changes in pyOM properties. The study was conducted in sandy soils of a forested ecosystem within the Longleaf pine range of the United States with a focus on links between changes in pyOM properties, fire history (FH), cumulative precipitation (Pcum), average temperature (Tavg) and soil residence time (SRT). Pcum, SRT and Tavg were the main factors controlling TC and TN accounting for 77–91% and 64–96% of their respective variability. Fire history, along with Pcum, SRT and Tavg, exhibited significant controlling effects on pyOM pH and R50—accounting for 48–91% and 88–93% of respective variability. Volatilization of volatiles and leaching of water-soluble components (in summer) and the sorption of exogenous organic matter (fall through spring) were most plausibly controlling pyOM dynamics in this study. Overall, our results point to climatic and land management factors and physicochemical process as the main drivers of pyOM dynamics in the pine ecosystems of the Southeastern U

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

In aquatic settings, periphytic algae exude labile carbon (C) that can significantly suppress or stimulate heterotrophic decomposition of recalcitrant C via priming effects. The magnitude and direction of priming effects may depend on the availability and stoichiometry of nutrients like nitrogen (N) and phosphorus (P), which can constrain algal and heterotrophic activity; in turn, priming may affect heterotrophic acquisition not only of recalcitrant C, but also N and P. In this study, we conducted a meta-analysis of algal-mediated priming across leaf litter decomposition experiments to investigate (1) bottom-up controls on priming intensity by dissolved N and P concentrations, and (2) effects of algal-mediated priming on the fate of litter-periphyton N and P during decomposition. Across a total of nine datasets, we quantified priming intensity and tested algal effects on litter-periphyton C:N, C:P, and N- and P-specific mass loss rates. Algal effect sizes did not significantly differ from zero, indicating weak or inconsistent algal effects on litter-periphyton stoichiometry and nutrient loss. These findings were likely due to wide variation in algal priming intensity across a limited number of experiments, ranging from strongly negative (410% reduced decomposition) to strongly positive (104% increased decomposition). Correlation and response surface analyses showed that priming intensity switched from negative to positive with increasing dissolved inorganic N:P across datasets. Algal effects on litter-periphyton stoichiometry and nutrient loss further co-varied with dissolved N:P across datasets, suggesting algae most strongly influence the stoichiometry of decomposition under imbalanced N:P, when priming is most intense. Our findings from this limited meta-analysis support the need for additional tests of aquatic priming effects, especially across gradients of N and P availability, with consideration of coupled C and nutrient dynamics during priming of organic matter decomposition

Brown Meets Green: Light and Nutrients Alter Detritivore Assimilation of Microbial Nutrients From Leaf Litter

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 during Liriodendron tulipifera litter decomposition and fed litter to the caddisfly larvae Pycnopsyche sp. We measured litter-associated algal, fungal, and bacterial biomass and production. Microbes were also labeled with 14C and 33P to trace distinct microbial carbon (C) and phosphorus (P) supporting Pycnopsyche assimilation 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, Pycnopsyche assimilated fungal C more efficiently than bacterial or algal C, and Pycnopsyche incorporated bacterial C more efficiently than algal or fungal C. Due to high litter fungal biomass, fungi supported 89.6–93.1% of Pycnopsyche C growth, compared to 0.2% to 3.6% supported by bacteria or algae. Overall, Pycnopsyche incorporated the most C in high nutrient and shaded litter. Our findings affirm others\u27 regarding autotroph-heterotroph microbial interactions and extend into the trophic transfer of microbial energy and nutrients through detrital food webs

Contribution of Surface Leaf-Litter Breakdown and Forest Composition to Benthic Oxygen Demand and Ecosystem Respiration in a South Georgia Blackwater River

Many North American blackwater rivers exhibit low dissolved O2 (DO) that may be the result of benthic respiration. We examined how tree species affected O2 demand via the quantity and quality of litter produced. In addition, we compared areal estimates of surface leaf-litter microbial respiration to sediment O2 demand (SOD) and ecosystem respiration (ER) in stream and swamp reaches of a blackwater river to quantify contributions of surface litter decomposition to O2 demand. Litter inputs averaged 917 and 678 g m−2 y−1 in the swamp and stream, respectively. Tree species differentially affected O2 demand via the quantity and quality of litter produced. Bald cypress (Taxodium distichum) contributed most litter inputs because of its dominance and because it produced more litter per tree, thereby making greater relative contributions to O2 demand in the swamp. In the stream, water oak (Quercus nigra) produced litter supporting lower fungal biomass and O2 uptake rates, but produced more litter than red maple (Acer rubrum). Breakdown rates in the swamp were faster, whereas standing stock decreases were lower than in the stream, indicating greater organic matter retention. Surface litter microbial respiration accounted for 89% of SOD (6.37 g O2 m−2 d−1), and 57 to 89% of ER in the swamp. Our findings suggest that surface litter drives the majority of O2 demand in some blackwater swamps, and tree species with higher rates of litterfall may make larger contributions to ER. Forested swamps may be hotspots of O2 demand in blackwater rivers because low water velocities enhance retention

Periphytic Algae Decouple Fungal Activity From Leaf Litter Decomposition Via Negative Priming

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, 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. 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 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

Leaf litter nutrient uptake in an intermittent blackwater river : influence of tree species and associated biotic and abiotic drivers

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of British Ecological Society for personal use, not for redistribution. The definitive version was published in Functional Ecology 29 (2015): 849-860, doi:10.1111/1365-2435.12399.Organic matter may sequester nutrients as it decomposes, increasing in total N and P mass via multiple uptake pathways. During leaf litter decomposition, microbial biomass and accumulated inorganic materials immobilize and retain nutrients, and therefore both biotic and abiotic drivers may influence detrital nutrient content. We examined the relative importance of these types of nutrient immobilization and compared patterns of nutrient retention in recalcitrant and labile leaf litter. Leaf packs of water oak (Quercus nigra), red maple (Acer rubrum) and Ogeechee tupelo (Nyssa ogeche) were incubated for 431 days in an intermittent blackwater stream and periodically analyzed for mass loss, nutrient and metal content, and microbial biomass. These data informed regression models explaining temporal changes in detrital nutrient content. Informal exploratory models compared estimated biologically-associated nutrient stocks (fungal, bacterial, leaf tissue) to observed total detrital nutrient stocks. We predicted that (1) labile and recalcitrant leaf litter would act as sinks at different points in the breakdown process, (2) plant and microbial biomass would not account for the entire mass of retained nutrients, and (3) total N content would be more closely approximated than total P content solely from nutrients stored in leaf tissue and microbial biomass, due to stronger binding of P to inorganic matter. Labile litter had higher nutrient concentrations throughout the study. However, lower mass loss of recalcitrant litter facilitated greater nutrient retention over longer incubations, suggesting that it may be an important long-term sink. N and P content were significantly related to both microbial biomass and metal content, with slightly stronger correlation to metal content over longer incubations.This work was funded by the USDA-CSREES Integrated Research, Education, and Extension Competitive Grants Program’s National Integrated Water Quality Program (Award No. 2004-5113002224), Hatch & State funds allocated to the Georgia Agricultural Experiment Stations, USDA-ARS CRIS project funds, and a Student Research Grant awarded to Andrew Mehring from the Odum School of Ecology, University of Georgia.2016-01-2