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Mar 30, 2010 - Fabiola Bastian & Pascal Thiébeau & Lionel Ranjard &. Pierre-Alain Maron ... Springer Science+Business Media, LLC 2010. Abstract The effect ...
Microb Ecol (2010) 60:291–303 DOI 10.1007/s00248-010-9648-z

ENVIRONMENTAL MICROBIOLOGY

In Situ Dynamics and Spatial Heterogeneity of Soil Bacterial Communities Under Different Crop Residue Management Noémie Pascault & Bernard Nicolardot & Fabiola Bastian & Pascal Thiébeau & Lionel Ranjard & Pierre-Alain Maron

Received: 25 September 2009 / Accepted: 20 February 2010 / Published online: 30 March 2010 # Springer Science+Business Media, LLC 2010

Abstract The effect of the location of wheat residues (soil surface vs. incorporated in soil) on their decomposition and on soil bacterial communities was investigated by the means of a field experiment. Bacterial-automated ribosomal intergenic spacer analysis of DNA extracts from residues, detritusphere (soil adjacent to residues), and bulk soil evidenced that residues constitute the zone of maximal changes in bacterial composition. However, the location of the residues influenced greatly their decomposition and the dynamics of the colonizing bacterial communities. Sequencing of 16S rRNA gene in DNA extracts from the residues at the early, middle, and late stages of degradation Electronic supplementary material The online version of this article (doi:10.1007/s00248-010-9648-z) contains supplementary material, which is available to authorized users. N. Pascault : F. Bastian : L. Ranjard : P.-A. Maron (*) UMR Microbiologie du Sol et de l’Environnement, INRA/Université de Bourgogne CMSE, BP 86510, 17 rue de Sully, 21065 Dijon Cedex, France e-mail: [email protected] B. Nicolardot INRA-Unité d’agronomie de Laon-Reims-Mons, 2 Esplanade Roland Garros, BP 224, 51686 Reims Cedex 2, France P. Thiébeau INRA, UMR-614 Fractionnement des Agro-Ressources et Environnement, 2 Esplanade Roland Garros, BP 224, 51686 Reims Cedex 2, France Present Address: B. Nicolardot AgroSup Dijon UMR 1210 INRA-AgroSup Dijon–Université de Bourgogne “Biologie et Gestion des Adventices”, 26 Bd Docteur Petitjean, BP 87999, 21079 Dijon Cedex, France

confirmed the difference of composition of the bacterial community according to the location. Bacteria belonging to the γ-subgroup of proteobacteria were stimulated when residues were incorporated whereas the α-subgroup was stimulated when residues were left at the soil surface. Moreover, Actinobacteria were more represented when residues were left at the soil surface. According to the ecological attributes of the populations identified, our results suggested that climatic fluctuations at the soil surface select populations harboring enhanced catabolic and/or survival capacities whereas residues characteristics likely constitute the main determinant of the composition of the bacterial community colonizing incorporated residues.

Introduction Soil organic matter (SOM) represents the largest pool of organic carbon in the biosphere and plays a central role in the regulation of many of the soil functions and consequently, for numerous ecosystem goods and services that humanity depends upon [15–51]. In agrosystems, considerable changes have occurred in SOM content as a result of cultivation, with a decrease in carbon stock generally observed in intensive cultivation or continuous cropping systems compared with prairies, grasslands, or forests [35]. Such a decrease can have dramatic consequences for the ability of soils to support sustainable crop growth. To maintain soil carbon stocks and consequently, agrosystem productivity and economic returns, organic amendments such as crop residues are commonly applied [8]. Accumulation of SOM is highly dependent on the activity of soil heterotrophic microorganisms responsible for the transformation of residues into complex and stabilized organic compounds. The biochemical nature

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(depending on plant species) and organic amendment practices greatly influence the C mineralization versus sequestration ratio and therefore the repercussion on global climatic and atmospheric changes [22, 52, 57]. In this context, the challenge is to improve management of organic inputs in order to maximize the benefits while minimizing negative agronomic and environmental effects. To this end, progress in the knowledge of the factors affecting decomposition must be achieved and a better understanding of the interaction between microorganisms, organic matter, and agricultural practices would constitute a decisive step forward for this problematic [7]. Many attempts have been made to elucidate the influence of different factors on microbial processes involved in the carbon cycle [23, 24, 34, 37, 39, 43, 46]. These studies were all based on measurements of global quantitative parameters such as microbial biomass, respiration rate, enzymatic activities, or C and N turnover, thus considering microbial communities as a functional “black box”. These works provided estimations of organic carbon turnover in soil based on evaluations of the mineralization/immobilization ratio which was demonstrated to vary depending on soil type, biochemical characteristics of the residues, agricultural practices, climate, etc. [5]. However, prediction of the residence time of the residues is still not satisfactory, mainly because of a lack of knowledge concerning the parameters controlling degradation and in particular, the functional involvement of microbial actors [25]. In this context, to improve our ability to predict and manage the fate of organic matter in soil, microbial communities must no longer be considered as a “functional black box” and a major challenge for microbial ecology is to identify of the microbial populations involved in SOM degradation and to understand the influence of carbon sources and agricultural practices on the diversity of soil microbial communities. Recently, Bernard et al. [7] performed a microcosm experiment using the molecular DNA/ RNA-SIP approach to elucidate the dynamics and the diversity of bacterial populations actively assimilating C derived from 13C-labeled wheat residues incorporated in soil. They showed that residue incorporation induced a rapid succession of bacterial populations, with the stimulation of specific labeled bacterial populations belonging to the β- and γ-subgroups of Proteobacteria [7]. They linked the dynamics of diversity they observed with the degradation of both residues and soil organic matters on the basis of hypothesis of Fontaine et al. [19] dealing with the microbial involvement for priming-effect in soil. Similarly, Nicolardot et al. [40] performed a microcosm experiment to evaluate the influence of location (soil surface vs. incorporated into soil) and quality of plant residues (young rye vs. wheat straw) on both residue decomposition and genetic structure of soil microbial communities. The results obtained showed

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that depending on both the quality and the location of the residues, different genetic structures of microbial communities were stimulated, with a gradient observed from residue to bulk soil particularly for young rye. These results suggest that the quality of organic inputs and the way they are added to soil may represent a suitable way to manage the microbial component in soil and consequently the soil processes they are responsible for. However, all these studies were conducted in soil microcosm laboratory incubations and extrapolating to the field decomposition data derived from laboratory experiments must be undertaken with caution [10, 44] since variations in soil characteristics, climatic events, as well as seasonal variations occurring in natura can greatly influence residue degradation and microbial community dynamics. In the present work, our purpose was to evaluate under field conditions the influence of the location of wheat residues on residue degradation and the dynamics of bacterial communities colonizing the residue. To this end, we performed a field experiment in which mature wheat residues were added to soil either as mulch or incorporated into the soil by tillage. The dynamics of residue degradation and of soil bacterial communities were then assessed each month, from August 2005 to March 2006, in three soil zones, i.e., the residue, the detritusphere (soil adjacent to the residues), and the bulk soil. Evolutions in soil inorganic N content, as well as the quantitative and qualitative evolution of residues in each treatment were monitored. Furthermore, the bacterial community structure was assessed using the DNA fingerprinting technique for bacterial-automated ribosomal intergenic spacer analysis (B-ARISA) to characterize the succession of bacterial populations during the residue decomposition. Based on the dynamics of residue degradation and community structure, three sampling dates were selected for both amended treatments (residues left at the soil surface vs. incorporated) to build up 16S rRNA gene clone libraries from DNA extracts from residues and characterize the evolution of the composition of the bacterial community between an early (September 9, 2005), middle (November 8, 2005), and late (March 20, 2006) stage of decomposition.

Materials and Methods Site Description and Sampling A field experiment was set up on the Estrées-Mons INRA experimental station located at Mons (49.53°N, 3.01°E). Three samples were collected from the 0–20 soil layer and sent to the Arras Laboratory of Soil Analysis (INRA) for determination of soil properties following standardized meth-

Interaction Between Crop Residues and Soil Bacterial Diversity

ods (http://www.lille.inra.fr/las/methodes_d_analyse/sols). The main characteristics of the soil were as follows: clay (