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

Francoeur, Steven N.; Neely, Robert K.; Underwood, Savannah L; Kuehn, Kevin A.

doi:10.1111/fwb.13442

Cited by 10 publications

(8 citation statements)

References 61 publications

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“…In addition to alleviating nutrient limitation, elevated levels of fungal biomass in the NP treatment may have been due in part to a positive association with algae. Although this aspect of producer–decomposer coupling has not been previously reported in northern peatlands, aquatic fungi are known to have close associations with algae in other freshwater ecosystems (Danger et al., 2013; Francoeur et al., 2020; Kuehn et al., 2014). For example, the fungal response to nutrients was much more subdued when algae were excluded by blocking sunlight in a lake biofilm (Wyatt et al., 2019).…”

Section: Discussionmentioning

confidence: 92%

“…For example, the fungal response to nutrients was much more subdued when algae were excluded by blocking sunlight in a lake biofilm (Wyatt et al., 2019). Similarly, fungal growth and production were lower on plant litter where algal photosynthesis was experimentally inhibited in a temperate wetland (Francoeur et al., 2020). The ability of fungi but not bacteria to respond to nutrient enrichment is interesting as it points to possible antagonistic interactions between these two competitors in the presence of algae.…”

Section: Discussionmentioning

confidence: 96%

“…In conditions where sufficient sunlight reaches submersed surfaces, algal members of the biofilm fix inorganic carbon into organic forms during photosynthesis. A portion of this photosynthetic product is released into the surrounding environment (Bertilsson & Jones, 2003) where it serves as a source of energy for heterotrophic microorganisms, including bacteria (Cole, 1982; Francoeur et al., 2020; Kuehn et al., 2014; Wyatt & Rober, 2020) and fungi (Halvorson et al., 2019; Kuehn et al., 2014; Wyatt et al., 2019). These decomposers, in turn, convert organic nutrients into inorganic forms, making them available for uptake by resource‐limited algae (Daufresne & Loreau, 2001; Kuehn et al., 2014; Mesquita et al., 2019).…”

Section: Introductionmentioning

confidence: 99%

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Carbon subsidies shift a northern peatland biofilm community towards heterotrophy in low but not high nutrient conditions

2020

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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 and 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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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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Carbon subsidies shift a northern peatland biofilm community towards heterotrophy in low but not high nutrient conditions

2020

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“…Halvorson, Barry, et al (2019) observed negative priming of leaf litter decomposition, whereby labile C from algae stimulated fungi to invest more energy in growth and reproduction rather than decomposition of recalcitrant carbon. Work by Francoeur, Neely, Underwood, and Kuehn (2020) supported the hypothesis that benthic algal photosynthesis strongly influences heterotrophic microbial activity on macrophyte leaf litter, especially that of fungi, throughout microbial community development, but how much algal photosynthesis stimulates heterotrophs may not depend on differences in litter nutrient content according to leaf litter stoichiometry. Halvorson, Francoeur, Francoeur, Findlay, and Kuehn (2019) conducted a meta-analysis across leaf litter decomposition experiments to investigate the influence and fate of dissolved N and P in algal-mediated priming.…”

Section: Algal Ecologymentioning

confidence: 91%

Substratum‐associated microbiota

Furey

Lee

Clemans

2020

Water Environment Research

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Highlights of new, interesting, and emerging research findings on substratum-associated microbiota covered from a survey of 2019 literature from primarily freshwaters provide insight into research trends of interest to the Water Environment Federation and others interested in benthic, aquatic environments. Coverage of topics on bottom-associated or attached algae and cyanobacteria, though not comprehensive, includes new methods, taxa new-to-science, nutrient dynamics, auto-and heterotrophic interactions, grazers, bioassessment, herbicides and other pollutants, metal contaminants, and nuisance, and bloom-forming and harmful algae. Coverage of bacteria, also not comprehensive, focuses on the ecology of benthic biofilms and microbial communities, along with the ecology of microbes like Caulobacter crescentus, Rhodobacter, and other freshwater microbial species. Bacterial topics covered also include metagenomics and metatranscriptomics, toxins and pollutants, bacterial pathogens and bacteriophages, and bacterial physiology. Readers may use this literature review to learn about or renew their interest in the recent advances and discoveries regarding substratum-associated microbiota. © 2020 Water Environment Federation • Practitioner points • This review of literature from 2019 on substratum-associated microbiota presents highlights of findings on algae, cyanobacteria, and bacteria from primarily freshwaters. • Coverage of algae and cyanobacteria includes findings on new methods, taxa new to science, nutrient dynamics, auto-and heterotrophic interactions, grazers, bioassessment, herbicides and other pollutants, metal contaminants, and nuisance, bloomforming and harmful algae. • Coverage of bacteria includes findings on ecology of benthic biofilms and microbial communities, the ecology of microbes, metagenomics and metatranscriptomics, toxins and pollutants, bacterial pathogens and bacteriophages, and bacterial physiology. • Highlights of new, noteworthy and emerging topics build on those from 2018 and will be of relevance to the Water Environment Federation and others interested in benthic, aquatic environments

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“…For example, in drylands with aridity >0.70, the enzymatic C:nutrient (N and P) ratios decline significantly as the aridity increases, and the enzymatic N:P ratios are generally higher than those with aridity <0.70 ( Feng et al, 2019 ). The elevated litter N:P increases P limitation in heterotrophic microbes associated with submerged plant litter, and thus leads to higher relative activity of P-acquiring enzymes and lower enzymatic N:P ratio ( Francoeur et al, 2020 ). Furthermore, the microbial nutrient limitation may have the potential to predict changes in ecosystem C storage, which are mainly studied in soil ecosystems ( Wang et al, 2020 ; Cui et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Extracellular enzyme stoichiometry reveals carbon and nitrogen limitations closely linked to bacterial communities in China’s largest saline lake

et al. 2022

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Saline lakes possess substantial carbon storage and play essential roles in global carbon cycling. Benthic microorganisms mine and decompose sediment organic matter via extracellular enzymes to acquire limiting nutrients and thus meet their element budgets, which ultimately causes variations in sediment carbon storage. However, current knowledge about microbial nutrient limitation and the associated organic carbon changes especially in saline lake remains elusive. Therefore, we took Qinghai Lake, the largest saline lake of China, as an example to identify the patterns and drivers of microbial metabolic limitations quantified by the vector analyses of extracellular enzyme stoichiometry. Benthic microorganisms were dominantly colimited by carbon (C) and nitrogen (N). Such microbial C limitation was aggravated upon the increases in water salinity and sediment total phosphorus, which suggests that sediment C loss would be elevated when the lake water is concentrated (increasing salinity) and phosphorus becomes enriched under climate change and nutrient pollution, respectively. Microbial N limitation was predominantly intensified by water total nitrogen and inhibited by C limitation. Among the microbial drivers of extracellular enzyme investments, bacterial community structure consistently exerted significant effects on the C, N, and P cycles and microbial C and N limitations, while fungi only altered the P cycle through species richness. These findings advance our knowledge of microbial metabolic limitation in saline lakes, which will provide insights towards a better understanding of global sediment C storage dynamics under climate warming and intensified human activity.

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

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 10 publications

References 61 publications

Carbon subsidies shift a northern peatland biofilm community towards heterotrophy in low but not high nutrient conditions

Carbon subsidies shift a northern peatland biofilm community towards heterotrophy in low but not high nutrient conditions

Substratum‐associated microbiota

Extracellular enzyme stoichiometry reveals carbon and nitrogen limitations closely linked to bacterial communities in China’s largest saline lake

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