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Fungal communities mediate but do not control leaf litter chemical transformation in a temperate oak forest

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Abstract

Background and Aims

In temperate forests, fungi are the main actors in leaf litter decomposition. Still, we have minimal knowledge of their influence on changes in leaf litter chemistry. Thus, we aimed to determine the main drivers behind leaf litter chemical transformation during decomposition.

Methods

We monitored the development of fungal communities, extracellular enzyme activities, and litter chemical properties during a long-term (768 days) transplantation experiment of two chemically-contrasted intraspecific oak leaf litters.

Results

Initial differences in substrate chemistry between native and transplanted Quercus petraea litters incubated at the same forest site largely persisted throughout the decomposition process, indicating that initial substrate quality constrained litter chemical transformation. The two litter types also maintained distinct fungal communities despite similar enzyme profiles. This suggests that fungi act more as constrained mediators rather than controllers of chemical changes during litter decay. Further, the litter elemental (i.e., nutrient composition) and organic (i.e., lignin and carbohydrate composition) chemistries tended respectively to diverge and converge over time between the native and transplanted litter types.

Conclusion

The results highlight that leaf litter chemical transformation is a dynamic process mediated—but not oriented— by fungal communities. The factors influencing changes in leaf litter's organic and elemental chemical properties may be decoupled, with potentially contrasting consequences on forest carbon stocks and soil fertility.

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Data availability

Raw.fastq files for each sample were deposited in the NCBI Short Read Archive as accession PRJNA928603. Other data generated during this experiment are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank the two anonymous reviewers for their constructive feedback that greatly helped improving the manuscript. FM held a PhD fellowship awarded by the Grand Est and the Laboratory of excellence ARBRE. This project (LeafLitterOME) was supported by funds obtained from the French National Research Agency (ANR) as part of the ‘Investissements d’Avenir’ program (ANR-11-LABX-0002-01, Lab of Excellence ARBRE). The Breuil site belongs to the French national research infrastructure ANAEE-France (ANR-11-INBS-0001). The MOS network site Champenoux belongs to the French national infrastructure IN-SYLVA.

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Correspondence to François Maillard.

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We state that there is no conflict of interest.

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Responsible Editor: Alfonso Escudero.

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Supplementary Information

Below is the link to the electronic supplementary material.

11104_2023_6040_Fig8_ESM.png

Figure S1. Leaf litter monosaccharide contents depending on incubation time and leaf litter type (native and transplanted) (means ± SE). Potential effects of incubation time, leaf litter type, and their interaction are tested using two-way analysis of variance (ANOVA) (*P < 0.05; **P < 0.01; ***P < 0.001) (PNG 1963 kb)

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11104_2023_6040_Fig9_ESM.png

Figure S2. Leaf litter nutrient content depending on incubation time and leaf litter type (native and transplanted) (means ± SE). Potential effects of incubation time, leaf litter type, and their interaction are tested using two-way analysis of variance (ANOVA) (*P < 0.05; **P < 0.01; ***P < 0.001) (PNG 1969 kb)

High resolution image (TIF 57194 kb)

11104_2023_6040_Fig10_ESM.png

Figure S3. OTU richness and ergosterol content depending on incubation time and leaf litter type (native and transplanted) (means ± SE). Potential effects of incubation time, leaf litter type, and their interaction are tested using two-way analysis of variance (ANOVA) (*P < 0.05; **P < 0.01; ***P < 0.001) (PNG 515 kb)

High resolution image (TIF 14529 kb)

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Figure S4. Mantel correlations between the leaf litter organic chemistry (glucose, galactose, mannose, xylose, arabinose, glucuronic acid, galacturonic acid, rhamnose, fucose, and lignin), elemental chemistry (N, P, K, Ca, Al, Fe, Mn, Mg, S, Si, Na), extracellular enzyme activities (β-glucosidase, cellobiohydrolase, xylosidase, glucuronidase, acid phosphatase, and N-acetylglucosaminidase), and fungal communities (OTU composition) depending on litter type (native and transplanted) (PNG 254 kb)

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Maillard, F., Leduc, V., Viotti, C. et al. Fungal communities mediate but do not control leaf litter chemical transformation in a temperate oak forest. Plant Soil 489, 573–591 (2023). https://doi.org/10.1007/s11104-023-06040-4

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  • DOI: https://doi.org/10.1007/s11104-023-06040-4

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