Anthropogenic N Deposition Slows Decay by Favoring Bacterial Metabolism: Insights from Metagenomic Analyses

Freedman, Zachary; Upchurch, Rima A.; Zak, Donald R.; Cline, Lauren C.

doi:10.3389/fmicb.2016.00259

Cited by 61 publications

(52 citation statements)

References 72 publications

(103 reference statements)

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“…, b) In our study system, experimental N deposition has had an overall positive effect on the abundance of bacterial genes mediating plant cell‐wall decay (Freedman et al. ). Furthermore, experimental N deposition has increased the abundance of bacterial laccase‐like multicopper oxidase (LMCO) genes (Freedman and Zak ), which may play similar roles to fungal laccases in lignin decay (Ridge et al.…”

Section: Discussionmentioning

confidence: 81%

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Entwistle

Zak

Argiroff

2018

Ecological Monographs

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Atmospheric nitrogen (N) deposition has increased dramatically since preindustrial times and continues to increase across many regions of the Earth. In temperate forests, this agent of global change has increased soil carbon (C) storage, but the mechanisms underlying this response are not understood. One long‐standing hypothesis proposed to explain the accumulation of soil C proposes that higher inorganic N availability may suppress both the activity and abundance of fungi that decay lignin and other polyphenols in soil. In field studies, elevated rates of N deposition have reduced the activity of enzymes mediating lignin decay, but a decline in the abundance of lignolytic fungi has not been definitively documented to date. Here, we tested the hypothesis that elevated rates of anthropogenic N deposition reduce the abundance of lignolytic fungi. We conducted a field experiment in which we compared fungal communities colonizing low‐lignin, high‐lignin, and wood substrates in a northern hardwood forest that is part of a long‐term N deposition experiment. We reasoned that if lignolytic fungi decline under experimental N deposition, this effect should be most evident among fungi colonizing high‐lignin and wood substrates. Using molecular approaches, we provide evidence that anthropogenic N deposition reduces the relative abundance of lignolytic fungi on both wood and a high‐lignin substrate. Furthermore, experimental N deposition increased total fungal abundance on a low‐lignin substrate, reduced fungal abundance on wood, and had no significant effect on fungal abundance on a high‐lignin substrate. We simultaneously examined these responses in the surrounding soil and forest floor, in which we did not observe significant reductions in the relative abundance of lignolytic fungi or in the size of the fungal community; however, we did detect a change in community composition in the forest floor that appears to be driven by a shift away from lignolytic fungi and towards cellulolytic fungi. Our results provide direct evidence that reductions in the abundance of lignolytic fungi are part of the mechanism by which anthropogenic N deposition increases soil C storage.

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Section: Discussionmentioning

confidence: 81%

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Entwistle

Zak

Argiroff

2018

Ecological Monographs

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“…Virtually all OSC subfamilies are unique to eukaryotes, with the exception of the sterol synthases, which have been identified and characterized in a handful of aerobic methanotrophs and myxobacteria. Recent analyses of environmental samples suggest that sterol production in bacteria is more widespread than previously thought 14 .…”

Section: Hopanoid Structure and Biosynthesismentioning

confidence: 98%

Hopanoid lipids: from membranes to plant–bacteria interactions

et al. 2018

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Lipid research represents a frontier for microbiology, as showcased by hopanoid lipids. Hopanoids, which resemble sterols and are found in the membranes of diverse bacteria, have left an extensive molecular fossil record. They were first discovered by petroleum geologists. Today, hopanoid-producing bacteria remain abundant in various ecosystems, such as the rhizosphere. Recently, great progress has been made in our understanding of hopanoid biosynthesis, facilitated in part by technical advances in lipid identification and quantification. A variety of genetically tractable, hopanoid-producing bacteria have been cultured, and tools to manipulate hopanoid biosynthesis and detect hopanoids are improving. However, we still have much to learn regarding how hopanoid production is regulated, how hopanoids act biophysically and biochemically, and how their production affects bacterial interactions with other organisms, such as plants. The study of hopanoids thus offers rich opportunities for discovery.

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“…It is plausible this relationship occurs because N addition directly impairs enzymatic activities of SAP (Deforest, Zak, Pregitzer, & Burton, 2004;Freedman, Romanowicz, Upchurch, & Zak, 2015;Freedman, Upchurch, Zak, & Cline, 2016) which may reduce their ability to both decompose litter and accrue biomass (Waldrop, Zak, Sinsabaugh, Gallo, & Lauber, 2004;Zak, Holmes, Burton, Pregitzer, & Talhelm, 2008). It is plausible this relationship occurs because N addition directly impairs enzymatic activities of SAP (Deforest, Zak, Pregitzer, & Burton, 2004;Freedman, Romanowicz, Upchurch, & Zak, 2015;Freedman, Upchurch, Zak, & Cline, 2016) which may reduce their ability to both decompose litter and accrue biomass (Waldrop, Zak, Sinsabaugh, Gallo, & Lauber, 2004;Zak, Holmes, Burton, Pregitzer, & Talhelm, 2008).…”

Section: Microbial Community Responsementioning

confidence: 99%

Anthropogenic nitrogen enrichment enhances soil carbon accumulation by impacting saprotrophs rather than ectomycorrhizal fungal activity

Maaroufi

Nordin

Palmqvist

et al. 2019

Global Change Biology

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There is evidence that anthropogenic nitrogen (N) deposition enhances carbon (C) sequestration in boreal forest soils. However, it is unclear how free‐living saprotrophs (bacteria and fungi, SAP) and ectomycorrhizal (EM) fungi responses to N addition impact soil C dynamics. Our aim was to investigate how SAP and EM communities are impacted by N enrichment and to estimate whether these changes influence decay of litter and humus. We conducted a long‐term experiment in northern Sweden, maintained since 2004, consisting of ambient, low N additions (0, 3, 6, and 12 kg N ha−1 year−1) simulating current N deposition rates in the boreal region, as well as a high N addition (50 kg N ha−1 year−1). Our data showed that long‐term N enrichment impeded mass loss of litter, but not of humus, and only in response to the highest N addition treatment. Furthermore, our data showed that EM fungi reduced the mass of N and P in both substrates during the incubation period compared to when only SAP organisms were present. Low N additions had no effect on microbial community structure, while the high N addition decreased fungal and bacterial biomasses and altered EM fungi and SAP community composition. Actinomycetes were the only bacterial SAP to show increased biomass in response to the highest N addition. These results provide a mechanistic understanding of how anthropogenic N enrichment can influence soil C accumulation rates and suggest that current N deposition rates in the boreal region (≤12 kg N ha−1 year−1) are likely to have a minor impact on the soil microbial community and the decomposition of humus and litter.

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Anthropogenic N Deposition Slows Decay by Favoring Bacterial Metabolism: Insights from Metagenomic Analyses

Cited by 61 publications

References 72 publications

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Hopanoid lipids: from membranes to plant–bacteria interactions

Anthropogenic nitrogen enrichment enhances soil carbon accumulation by impacting saprotrophs rather than ectomycorrhizal fungal activity

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