Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere

MINIREVIEW Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere Gabriele Berg1 & Kornelia Smalla2 1 Graz University of Technology, Environmental Biotechnology, Graz, Austria; and 2Julius Kühn-Institut – Federal Research Centre for Cultivated Plants (JKI), Braunschweig, Germany Received 16 September 2008; revised 4 December 2008; accepted 14 December 2008. First published online 25 February 2009. DOI:10.1111/j.1574-6941.2009.00654.x Editor: Philippe Lemanceau Keywords microbial communities; environmental factors; plant–microorganism interaction. Abstract The rhizosphere is of central importance not only for plant nutrition, health and quality but also for microorganism-driven carbon sequestration, ecosystem functioning and nutrient cycling in terrestrial ecosystems. A multitude of biotic and abiotic factors are assumed to influence the structural and functional diversity of microbial communities in the rhizosphere. In this review, recent studies on the influence of the two factors, plant species and soil type, on rhizosphere-associated microbial communities are discussed. Root exudates and the response of microorganisms to the latter as well as to root morphology were shown to shape rhizosphere microbial communities. All studies revealed that soil is the main reservoir for rhizosphere microorganisms. Many secrets of microbial life in the rhizosphere were recently uncovered due to the enormous progress in molecular and microscopic tools. Physiological and molecular data on the factors that drive selection processes in the rhizosphere are presented here. Furthermore, implications for agriculture, nature conservation and biotechnology will also be discussed. Introduction The term ‘rhizosphere’ was coined by Hiltner in 1904 to describe the portion of soil where microorganism-mediated processes are under the influence of the root system. Functions of the rhizosphere are of central importance for plant nutrition, health and quality. The well-studied rhizosphere effect describes the phenomenon that, in comparison with bulk soil, the biomass and activity of microorganisms is enhanced as a result of exudation of compounds by the root (Sørensen, 1997; Raaijmakers et al., 2009). Because of the enormous importance of plant–microorganism interactions in the rhizosphere for carbon sequestration, ecosystem functioning and nutrient cycling in natural ecosystems as well as in agricultural and forest systems (Singh et al., 2004), it is crucial to understand the factors influencing the microbial communities in this habitat. The use of polyphasic approaches combining novel cultivation-independent and more traditional techniques to study microbial communities led to a significantly better understanding of community structure and function in the rhizosphere in the last decade. Several biotic and abiotic FEMS Microbiol Ecol 68 (2009) 1–13 factors influencing the structural and functional diversity of bacterial communities (Fig. 1), for example, climate and season, grazers and animals, pesticide treatments, soil type and structure and plant health and developmental stage, were investigated (Lemanceau et al., 1995; Siciliano et al., 2001; Graner et al., 2003; reviewed in Garbeva et al., 2004; Jousset et al., 2006; Rasche et al., 2006b). Different soil types are assumed to harbour specific microbial communities, as recently shown in a continental-scale study of soil bacterial communities (Fierer & Jackson, 2006). In contrast to what we know about the biodiversity of macroorganisms, the microbial biogeography is controlled primarily by edaphic variables, especially by pH (Fierer & Jackson, 2006). Furthermore, the bacterial community composition changed with age of soil that developed over c. 77 000 years of intermittent aeolian deposition, and the overall diversity, richness and evenness of the communities increased (Tarlera et al., 2008). Plants affect these indigenous microbial populations in soil; each plant species is thought to select specific microbial populations. Root exudates are a driving force in this process, but researchers are only beginning to understand the role of single compounds in mediating 2009 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved c Correspondence: Gabriele Berg, Graz University of Technology, Environmental Biotechnology, Petersgasse 12, A-8010 Graz, Austria. Tel.: 143 316 8738310; fax: 143 316 8738819; e-mail: 2 G. Berg & K. Smalla Plant–microorganism interactions Influencing environmental factors Biotic factors Root exudates Plant species* Microbial soil communities Plant developmental stage Plant health Animals and grazers Rhizosphere competence Human activities Chemotaxis Recognition Adherence Colonization and growth Abiotic factors Soil quality: type and structure* Geography Climate Treatments/Pesticides Positive interaction Biocontrol of pathogens Phytohormones Availability of micronutrients Enhancement of stress tolerance Negative interaction Pathogenesis Fig. 1. Influencing factors of rhizosphere microbial communities and model how microbial communities were selected from soil: by root exudates and their rhizosphere competence. Factors that are analysed in the review. belowground interactions (reviewed in Bais et al., 2006; Haichar et al., 2008). The composition of root exudates varies from plant to plant and affects the relative abundance of microorganisms in the vicinity of the root (Somers et al., 2004). Plants not only provide nutrients for microorganisms, but some plant species also contain unique antimicrobial metabolites in their exudates. Many of them are used as medical plants, for example camomile, thyme and eucalyptus. The existing huge diversity of plant species with an estimated range from 310 000 to 422 000 species (Pitman & Jörgensen, 2002) and corresponding secondary metabolites of plants (Buchanan et al., 2000) affects below-ground diversity. Interestingly, invasive plants can have major effects on microbial communities in soil (Van der Putten et al., 2007). There is no doubt that both factors, soil properties as well as plant species, influence the structure and function of microbial communities. However, the extent to which both factors contribute to microbial communities is not fully understood. There are several contrasting reports in the literature indicating plant or soil type as dominant factor (Grayston c 2009 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved et al., 1998; Girvan et al., 2003; Nunan et al., 2005). This review will present historical and more recent findings about plant specificity of rhizosphere communities and will analyse the background for this phenomenon on the basis of examples and physiological data. Furthermore, conclusions for agriculture, nature conservation and biotechnology will be discussed. (...truncated)