Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function

Cheeke, Tanya E.; Phillips, Richard P.; Brzostek, Edward R.; Rosling, Anna; Bever, James D.; Fransson, Petra

doi:10.1111/nph.14343

Cited by 186 publications

(160 citation statements)

References 67 publications

(98 reference statements)

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“…Alternatively, differences in microbial growth and turnover may reflect differences in the microbial community composition (Kallenbach et al., ). In agreement with previous studies on the active soil microbial community (Cheeke et al., ), we observed differences in the GluN:GalN ratio indicating differences in the microbial community composition across a gradient of ECM dominance.…”

Section: Discussionsupporting

confidence: 93%

Tree mycorrhizal type predicts within‐site variability in the storage and distribution of soil organic matter

Craig

Turner

Liang

et al. 2018

Global Change Biology

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Forest soils store large amounts of carbon (C) and nitrogen (N), yet how predicted shifts in forest composition will impact long-term C and N persistence remains poorly understood. A recent hypothesis predicts that soils under trees associated with arbuscular mycorrhizas (AM) store less C than soils dominated by trees associated with ectomycorrhizas (ECM), due to slower decomposition in ECM-dominated forests. However, an incipient hypothesis predicts that systems with rapid decomposition-e.g. most AM-dominated forests-enhance soil organic matter (SOM) stabilization by accelerating the production of microbial residues. To address these contrasting predictions, we quantified soil C and N to 1 m depth across gradients of ECM-dominance in three temperate forests. By focusing on sites where AM- and ECM-plants co-occur, our analysis controls for climatic factors that covary with mycorrhizal dominance across broad scales. We found that while ECM stands contain more SOM in topsoil, AM stands contain more SOM when subsoil to 1 m depth is included. Biomarkers and soil fractionations reveal that these patterns are driven by an accumulation of microbial residues in AM-dominated soils. Collectively, our results support emerging theory on SOM formation, demonstrate the importance of subsurface soils in mediating plant effects on soil C and N, and indicate that shifts in the mycorrhizal composition of temperate forests may alter the stabilization of SOM.

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Section: Discussionsupporting

confidence: 93%

Tree mycorrhizal type predicts within‐site variability in the storage and distribution of soil organic matter

Craig

Turner

Liang

et al. 2018

Global Change Biology

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182

140

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“…While changes in bacterial community may be influenced by overall fungal community composition, these shifts in bacterial community composition are tightly coupled to %AM colonization (a metric of belowground C allocation) suggesting that plant responses to N fertilization feedback on bacterial community structure and function (Figure c). While we cannot rule out that N‐induced declines in total fungal biomass led to reductions in liginolytic enzyme activity (DeForest et al., ; Frey et al., ; Treseder, ; Wallenstein et al., ), the dominance of AM trees in our plots, whose inorganic nutrient economy is largely driven by bacteria, suggests that free‐living fungi may not be an important driver of N deposition responses in AM‐dominated systems (Cheeke et al., ; Phillips, Brzostek, & Midgley, ).…”

Section: Discussionmentioning

confidence: 84%

Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long‐term N fertilization

Carrara

Walter

Hawkins

et al. 2018

Global Change Biology

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Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant-microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root-microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long-term (>25 years), whole-watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.

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“…Here we did not focus on P resorption because Rosling et al () have investigated P cycling at these same field sites and found little effect of mycorrhizal type on litter P and inorganic P cycling, suggesting that differences in P resorption between ECM and AM forests should be relatively small in our temperate forests. The three forest sites – Griffy Woods (GW; 39°11′ N, 86°30′ W), Morgan Monroe State Forest (MMSF; 39°19′ N, 86°25′ W) and Lilly‐Dickey Woods (LDW; 39°14′ N, 86°13′ W) – differ in species composition, soil type and land‐use history (Cheeke et al, ), yet all are within 30 km from one another and thus experience the same climate. At each site, 15 permanent research plots (15 m × 15 m) were established that vary in the relative abundance of ECM and AM trees, offering a unique opportunity to explore relationships between mycorrhizal dominance and resorption.…”

Section: Methodsmentioning

confidence: 99%

Foliar nutrient resorption differs between arbuscular mycorrhizal and ectomycorrhizal trees at local and global scales

Zhang

Lü

Hartmann

et al. 2018

Global Ecol Biogeogr

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Aim Trees associating with ectomycorrhizal (ECM) fungi typically occur in infertile soils and use nutrients more conservatively than arbuscular mycorrhizal (AM) trees. We hypothesized that ECM trees would have greater nutrient resorption (i.e., proportion of nutrients resorbed during leaf senescence) than AM trees. Location Global. Methods We synthesized nitrogen (N) and phosphorus (P) resorption data from 378 species from sub/tropical, temperate and boreal forests, including 43 studies where ECM and AM trees co‐occurred, and conducted a meta‐analysis. Additionally, we quantified N resorption in 45 plots varying in ECM‐AM tree abundances in the temperate deciduous forests of southern Indiana, USA. Results Overall, resorption patterns were driven primarily by mycorrhizal type, climate zone, and to a lesser degree, leaf habit. In the boreal forest, P resorption was 76% greater for ECM than AM trees (p < .05). In the sub/tropics, AM trees resorbed 30% more N than ECM trees. At the sites where AM and ECM trees co‐occurred, ECM trees resorbed more N in temperate forests (15% greater; p < .001) whereas AM trees tended to resorb more N in sub/tropical forests (by 29%; p = .08). Besides, deciduous ECM trees resorbed more N (10%) and P (15%) than deciduous AM trees, while evergreen ECM and AM trees did not differ. In the deciduous forests of Indiana, where ECM and AM trees co‐occurred, the relative abundance of ECM trees in a plot was positively correlated to plot‐scale N resorption (R2 = .25, p = .001), indicating greater nutrient conservatism with increasing ECM‐dominance. Main conclusions Our results indicate that mycorrhizal association – in addition to other factors – is correlated with the degree to which trees recycle nutrients, with the strongest effects occurring for N resorption by temperate deciduous trees.

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Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function

Cited by 186 publications

References 67 publications

Tree mycorrhizal type predicts within‐site variability in the storage and distribution of soil organic matter

Tree mycorrhizal type predicts within‐site variability in the storage and distribution of soil organic matter

Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long‐term N fertilization

Foliar nutrient resorption differs between arbuscular mycorrhizal and ectomycorrhizal trees at local and global scales

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