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Temporal Changes in the Ectomycorrhizal Community in Two Soil Horizons of a Temperate Oak Forest Pierre-Emmanuel Courty, Alain Franc, J-Claude Pierrat, Jean Garbaye

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Temporal Changes in the Ectomycorrhizal Community in Two Soil Horizons of a Temperate Oak Forest Pierre-Emmanuel Courty, Alain Franc, J-Claude Pierrat, Jean Garbaye Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest Pierre-Emmanuel Courty, Alain Franc, J-Claude Pierrat, Jean Garbaye To cite this version: Pierre-Emmanuel Courty, Alain Franc, J-Claude Pierrat, Jean Garbaye. Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Applied and Environmental Microbiology, American Society for Microbiology, 2008, 74 (18), pp.5792-5801. 10.1128/AEM.01592- 08. hal-01195010 HAL Id: hal-01195010 https://hal.archives-ouvertes.fr/hal-01195010 Submitted on 31 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Sept. 2008, p. 5792–5801 Vol. 74, No. 18 0099-2240/08/$08.00ϩ0 doi:10.1128/AEM.01592-08 Copyright © 2008, American Society for Microbiology. All Rights Reserved. Temporal Changes in the Ectomycorrhizal Community in Two Soil Horizons of a Temperate Oak Forestᰔ† Pierre-Emmanuel Courty,1* Alain Franc,2 Jean-Claude Pierrat,3 and Jean Garbaye1 UMR 1136 INRA-Nancy Universite´, Interactions Arbres/Micro-organisms, INRA-Nancy, 54280 Champenoux, France1; INRA Pierroton, UMR Biodiversite´, Ge`nes et Communaute´s, 33612 Cestas, France2; and UMR 1092 INRA-ENGREF Etudes des Ressources Foreˆt/Bois, ENGREF Nancy, 54000 Nancy, France3 Received 11 July 2008/Accepted 11 July 2008 The species structure of an ectomycorrhizal (ECM) community was assessed monthly for 15 months in the two horizons (A1 and A2) of an oak temperate forest in northeastern France. Ectomycorrhizal species were identified each month by internal transcribed spacer sequencing. Seventy-five fungal symbionts were identified. The community was dominated by Tomentellaceae, Russulaceae, Cortinariaceae, and Boletales. Four species are abundant in the study site: Lactarius quietus, Tomentella sublilacina, Cenococcum geophilum, and Russula sp1. The relative abundance of each species varied depending on the soil horizon and over time. Some species, such as L. quietus, were present in the A1 and A2 horizons. C. geophilum was located particularly in the A2 horizon, whereas T. sublilacina was more abundant in A1. Some species, such as Clavulina sp., were detected in winter, while T. sublilacina and L. quietus were present all year long. Our results support the hypothesis that a rapid turnover of species composition of the ECM community occurs over the course of a month. The spatial and temporal unequal distribution of ECM species could be explained by their ecological preferences, driven by such factors as root longevity, competition for resources, and resistance to environmental variability. The fine roots of social tree species in temperate and boreal specific competition, and community stability (38). A spatial forests are symbiotically associated with fungi (52), forming niche differentiation of ECM species and of ECM exploration composite organs called ectomycorrhizas (ECM). The ECM types (1) could be due to specific physicochemical properties of fungi play a crucial role in tree health by enhancing the nutri- soil horizons (47) and to differential resource utilization (35, ent acquisition, drought tolerance, and pathogen resistance of 39). However, despite acknowledgment of the functional im- their hosts. ECMs efficiently take up water and organic and portance of ECM fungi in host tree nutrition, very little is inorganic nutrients from the soil via the extramatricial myce- known about the distribution and abundance of ECM and lium and translocate these to colonized tree roots, receiving about the spatiotemporal structure of the ECM community in carbohydrates from the host in return (52). Most of the ecto- forest soil (13, 25, 29, 37, 58). mycorrhizal roots are located in the top 20 centimeters of the The present work addressed these issues for an oak forest in soil, an area which is enriched in organic matter and where northeastern France by monthly sampling of fine roots in two nutrients are concentrated (50). The ECM fungal community soil horizons for 15 months and characterization of the struc- is species rich at the forest stand level, where hundreds of ture and relative abundance of species of the ECM community different fungal symbionts can be identified by morphotyping in each sample. The objectives of the study were to describe and DNA-based molecular methods (13, 17, 36, 56). the ECM community structure in time and space to obtain Beside its species composition, the structure is an important information about the spatiotemporal partitioning of the ECM characteristic of the ECM community. Differences in ECM species. community structure on different scales are well documented: on the ecosystem scale (postdisturbance or postplanting suc- cessions) and along forest dynamics (4, 28, 56, 65), on the MATERIALS AND METHODS seasonal scale (6, 8, 20, 33, 54), and along spatial dimensions Site and forest stand. The experimental site is a 100-year-old oak forest with (vertical scale [13, 14, 24, 49] and horizontal scale [36, 58]). In a continuous canopy and a hornbeam understory (Quercus petraea (Mattuschka) Liebl., Quercus robur Ehrh., and Carpinus betulus L.) in northeastern France a microsite or on a forest strand scale, species are distributed Ј Ј (48°75 N, 6°35 E; altitude, 250 m). The luvic cambisol (pH [H2O] 4.6) has a Ϫ1 neither uniformly nor randomly but rather are aggregated in loamy texture in the A1 (0 to 5 cm; P, 0.3 g kg according to the method patches or distributed along gradients (9, 12, 19, 24, 44). The described in reference 15; total C, 26.7 g kgϪ1; total N, 1.9 g kgϪ1; C/N, 14.6) and Ϫ1 Ϫ1 depth range for the A2 horizon (P, 0.39 g kg ; total C, 26.3 g kg ; total N, spatial heterogeneity of communities is important in terms of Ϫ1 succession, adaptation, maintenance of species diversity, inter- 1.94 g kg ; C/N, 13.4). The forest floor is flat, with scarce vegetation (oak seedlings, Convallaria majalis L., and Deschampsia cespitosa L.). Soil tempera- ture (°C) and water potential (in MPa) were measured three times a month with 20 psychrometric probes (Wescor PST-55-15-SF) (10 cm deep in the A2 horizon) * Corresponding author. Mailing address: UMR 1136 INRA-Nancy and a millivoltmeter (Wescor HR-33T; Logan, UT). Universite´, Interactions Arbres/Micro-organisms, INRA-Nancy, 54280 Root sampling and identification of ECM species. In the experimental site, the Champenoux, France. Phone: 33 3 83 39 40 41. Fax: 33 3 83 39 40 69. sampling area (24 by 24 m) was fenced against digging by wild boars. In this area, E-mail: [email protected]. six blocks (5 by 3 m) were materialized. We determined the size of the blocks by † Supplemental material for this article may be found at http://aem considering the number of samples needed from each block throughout the .asm.org/. duration of the study (15) and by taking into account that two samples should be ᰔ Published ahead of print on 25 July 2008. at least 1 m apart. Each block was placed at least 1.5 m from oak trees to prevent 5792 VOL. 74, 2008 TEMPORAL CHANGES IN ECTOMYCORRHIZAL COMMUNITY 5793 the bias due to stem flow. From July 2004 to September 2005, one soil core (10 all species are represented by a similar number of individuals and minimum cm in diameter and 25 cm deep) was randomly sampled monthly in each of the equitability that one species only is dominant and all others are sparsely repre- six blocks. The number and size of soil samples were chosen in accordance with sented. The equitability index (JЈ) is the component of species diversity that previous studies (13, 51, 55, 62). Soil samples were immediately transported to measures the relative abundance of species and was calculated as follows: JЈϭ the nearby laboratory and processed on the same day. The soil cores were sliced HЈ/log(S), where S is the number of species and HЈ the Shannon-Weiner index. into two samples: the top (0 to 5 cm), corresponding to the A1 horizon, enriched The Shannon-Weiner index is a measure of the information content that ac- in organic matter and containing densely packed fine roots, and the 5-to-25-cm counts for evenness and richness. It was used as an index of biodiversity in a ЈϭϪ⌺ layer, corresponding to the top of the A2 horizon. Roots were soaked in tap water sample: H [Pilog(Pi)], where Pi is the probability that one apex belongs to ϭ for 15 min before being gently washed. Fine roots were observed in water with ECM species i and can be derived from the equation Pi Ni/N, where Ni is the a stereomicroscope (magnification, ϫ40). First, ECM morphotypes (ectomycor- number of apexes in ECM species i and N the total number of apexes (45, 57). rhizae sharing common morphological features) were characterized according to the method of Agerer (3). ECM morphotypes were also superficially classified at the genus level (e.g., Russula, Lactarius, Cortinarius, Boletus, and Tomentella RESULTS spp.) or as “unidentified morphotype.” The mean temperature and mean water potential measured Each month and for each encountered morphotype, a few tips (three to five) Ϫ were kept at Ϫ20°C in Eppendorf tubes. Subsequently, the fungal symbiont of during the 15-month sampling period were 11.2°C and 0.79 the frozen root tips was identified by sequencing the internal transcribed spacer MPa, respectively (data not shown).
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