skip to main content


Title: Temporal and stoichiometric patterns of algal stimulation of litter‐associated heterotrophic microbial activity
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 overall 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.

 
more » « less
NSF-PAR ID:
10458089
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Freshwater Biology
Volume:
65
Issue:
7
ISSN:
0046-5070
Page Range / eLocation ID:
p. 1223-1238
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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 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 summaryis available for this article.

     
    more » « less
  2. 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 a 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.

     
    more » « less
  3. Abstract

    The potential for animals to modify spatial patterns of nutrient limitation for autotrophs and habitat availability for other members of their communities is increasingly recognized. However, net trophic effects of consumers acting as ecosystem engineers remain poorly known. The American AlligatorAlligator mississippiensisis an abundant predator capable of dramatic modifications of physical habitat through the creation and maintenance of pond‐like basins, but its role in influencing community structure and nutrient dynamics is less appreciated.

    We investigated if alligators engineer differences in nutrient availability and changes to community structure by their creation of ‘alligator ponds’ compared to the surrounding phosphorus (P)‐limited oligotrophic marsh.

    We used a halo sampling design of three distinct habitats extending outward from 10 active alligator ponds across a hydrological gradient in the Everglades, USA. We performed nutrient analysis on basal food‐web resources and quantitative community analyses, and stoichiometric analyses on plants and animals.

    Our findings demonstrate that alligators act as ecosystem engineers and enhance food‐web heterogeneity by increasing nutrient availability, manipulating physical structure and altering algal, plant and animal communities. Flocculent detritus, an unconsolidated layer of particulate organic matter and soil, showed strong patterns of P enrichment in ponds. Higher P availability in alligator ponds also resulted in bottom‐up trophic transfer of nutrients as evidenced by higher growth rates (lower N:P) for plants and aquatic consumers. Edge habitats surrounding alligator ponds contained the most diverse communities of invertebrates and plants, but low total abundance of fishes, likely driven by high densities of emergent macrophytes. Pond communities exhibited higher abundance of fish compared to edge habitat and were dominated by compositions of small invertebrates that track high nutrient availability in the water column. Marshes contained high numbers of animals that are closely tied to periphyton mats, which were absent from other habitats.

    Alligator‐engineered habitats are ecologically important by providing nutrient‐enriched ‘hotspots’ in an oligotrophic system, habitat heterogeneity to marshes, and refuges for other fauna during seasonal disturbances. This work adds to growing evidence that efforts to model community dynamics should routinely consider animal‐mediated bottom‐up processes like ecosystem engineering.

     
    more » « less
  4. Summary

    The biological and functional diversity of ectomycorrhizal (ECM) associations remain largely unknown in South America. In Patagonia, theECMtreeNothofagus pumilioforms monospecific forests along mountain slopes without confounding effects of vegetation on plant–fungi interactions.

    To determine how fungal diversity and function are linked to elevation, we characterized fungal communities, edaphic variables, and eight extracellular enzyme activities along six elevation transects in Tierra del Fuego (Argentina and Chile). We also tested whether pairingITS1rDNAIllumina sequences generated taxonomic biases related to sequence length.

    Fungal community shifts across elevations were mediated primarily by soilpHwith the most species‐rich fungal families occurring mostly within a narrowpHrange. By contrast, enzyme activities were minimally influenced by elevation but correlated with soil factors, especially total soil carbon. The activity of leucine aminopeptidase was positively correlated withECMfungal richness and abundance, and acid phosphatase was correlated with nonECM fungal abundance. Several fungal lineages were undetected when using exclusively paired or unpaired forwardITS1 sequences, and these taxonomic biases need reconsideration for future studies.

    Our results suggest that soil fungi inN. pumilioforests are functionally similar across elevations and that these diverse communities help to maintain nutrient mobilization across the elevation gradient.

     
    more » « less
  5. Abstract

    Many soils are deep, yet soil below 20 cm remains largely unexplored. Exotic plants can have shallower roots than native species, so their impact on microorganisms is anticipated to change with depth. Using environmentalDNAand extracellular enzymatic activities, we studied fungal and bacterial community composition, diversity, function, and co‐occurrence networks between native and exotic grasslands at soil depths up to 1 m. We hypothesized (1) the composition and network structure of both fungal and bacterial communities will change with increasing depth, and diversity and enzymatic function will decrease; (2) microbial enzymatic function and network connectedness will be lower in exotic grasslands; and (3) irrigation will alter microbial networks, increasing the overall connectedness. Microbial diversity decreased with depth, and community composition wasdistinctly differentbetween shallow and deeper soil depths with higher numbers of unknown taxa in lower soil depths. Fungal communities differed between native and exotic plant communities. Microbial community networks were strongly shaped by biotic and abiotic factors concurrently and were the only microbial measurement affected by irrigation. In general, fungal communities were more connected in native plant communities than exotic, especially below 10 cm. Fungal networks were also more connected at lower soil depths albeit with fewer nodes. Bacterial communities demonstrated higher complexity, and greater connectedness and nodes, at lower soil depths for native plant communities. Exotic plant communities’ bacterial network connectedness altered at lower soil depths dependent on irrigation treatments. Microbial extracellular enzyme activity for carbon cycling enzymes significantly declined with soil depth, but enzymes associated with nitrogen and phosphorus cycling continued to have similar activities up to 1 m deep. Our results indicate that native and exotic grasslands have significantly different fungal communities in depths up to 1 m and that both fungal and bacterial networks are strongly shaped jointly by plant communities and abiotic factors. Soil depth is independently a major determinant of both fungal and bacterial community structures, functions, and co‐occurrence networks and demonstrates further the importance of including soil itself when investigating plant–microbe interactions.

     
    more » « less