van der Heijden, Marcel

Wagg, Cameron

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COMMENTARYSoil microbial diversity and agro-ecosystem functioningMarcel G. A. van der Heijden & Cameron WaggReceived: 12 October 2012 /Accepted: 22 November 2012 /Published online: 8 December 2012# Springer Science+Business Media Dordrecht 2012Keywords Plant-soil feedback .Microbialdiversity . Mycorrhiza . Agro-ecosystems . Speciesrichness . Microbe . Ecosystem functioningSoil microbes represent the unseen majority of life onEarth and are essential for the functioning of terrestrialecosystems as they catalyze unique and indispensabletransformations in the biogeochemical cycles of thebiosphere (Whitman et al. 1998; van der Heijden et al.2008). The significance of soil microbial diversity forthe functioning of agricultural and natural ecosystems isstill poorly understood and soil microbial communitiescan be considered as a black box (Kennedy and Smith1995; Cortois and de Deyn 2012). Unraveling what soilmicrobes are doing in this black box has been identifiedas one of the major research areas in science.An increasing number of studies demonstrate thatagricultural practices, such as tree based intercropping(Lacombe et al. 2009; Bainard et al. 2012a, b), organicfarming (Mäder et al. 2002; Bengtsson et al. 2005;Birkhofer et al. 2008; Verbruggen et al. 2010), reducedsoil tillage (van Capelle et al. 2012), crop rotation(Altieri 1999; Cavagnaro and Martin 2011) and landuse extensification (Postma-Blaauw et al. 2010; de Vrieset al. 2012) have a positive impact on the abundance andrichness of specific groups of soil organisms (e.g. arbus-cular mycorrhizal fungi, earthworms) and on soil micro-bial diversity. Thus, by adapting farm managementpractices it is possible to favor recruitment of specificgroups of soil organisms and enhance microbial diver-sity. As such, these findings make it possible to providepolicy makers with recommendations on enhancing soilbiodiversity in agricultural ecosystems. There are anumber of mechanisms by which microbial diversitycan support agro-ecosystem functioning and particularecosystem functions such as plant productivity and de-composition. For instance, microbes can form “consor-tia” that enhance plant productivity (e.g. when differentmicrobes provide different limiting resources toplants) or decomposition (e.g. when plant materialis decomposed by specialized microbes with uniquephysiological properties that succeed each other). Asa consequence, microbial diversity can promote eco-system functioning. However, in other cases, thepresence of key stone species (e.g. specific patho-gens, nitrogen fixers) rather than diversity “per se”may determine agro-ecosystem functioning. Untilnow, it is still poorly understood, whether increasedsoil (microbial) diversity is beneficial for the func-tioning and sustainability of agricultural systems.Plant Soil (2013) 363:1–5DOI 10.1007/s11104-012-1545-4Responsible Editor: Hans Lambers.M. G. A. van der Heijden (*) : C. WaggEcological Farming Systems, Agroscope Reckenholz-Tänikon, Research Station ART,Reckenholzstrasse 191,8046 Zürich, Switzerlande-mail: marcel.vanderheijden@art.admin.chM. G. A. van der HeijdenInstitute of Evolutionary Biology and EnvironmentalStudies, University of Zürich,Winterthurestrasse 190,8057 Zürich, SwitzerlandM. G. A. van der HeijdenPlant-Microbe Interactions, Institute of EnvironmentalBiology, Faculty of Science, Utrecht University,3508 TC Utrecht, The NetherlandsIn this issue (doi:10.1007/s11104-012-1321-5) anextensive study by Bainard and colleagues showedthat things are certainly not simple. They used soilfrom conventional agricultural fields and from tree-based intercropping systems as inoculum in a glass-house bioassay and assessed the influence of soilbiotic communities conditioned by these two differentpractices on three agricultural crops. In earlier work itwas shown that soils from tree based intercroppingsystems had higher microbial diversity compared toconventionally managed soils (Lacombe et al. 2009;Bainard et al. 2012b). Hence, it was hypothesized thatplants would benefit when inoculated with soils derivedfrom tree based intercropping systems. In contrast totheir hypothesis, there were no differences in effectsbetween farming systems inocula. Moreover, two ofthe three crops (barley and canola) grew best in soil withsterilized inoculum. Thus, the results from this study donot indicate that plants benefit from increased microbialdiversity (but see below). Instead, soil pathogensappeared to be a stronger driver of plant productivitythan diversity for two of the investigated crop species inthis study.Bottlenecks and advancesThe great difficulty in assessing the impact of soilmicrobes on plant productivity and ecosystem pro-cesses arises since microbial diversity and abundancecannot be easily manipulated without simultaneouslychanging other factors or organisms (Read 2002).Hence, it is a common approach to perform green-house experiments under controlled conditions in ster-ilized soil and add soil inoculum (Bainard et al. 2012a;Verbruggen et al. 2012; Maherali and Klironomos2007; Wagg et al. 2011). By adding soil inoculumfrom fields with different microbial diversity it issubsequently possible to mimic differences in micro-bial communities under controlled conditions and testtheir impact on plants and ecosystems. When doingthis, it is important to verify that differences in soilmicrobial diversity are responsible for observedeffects. Consequently, it is required to demonstrate atthe beginning and at the end of the experiment that soilmicrobial diversity differs among treatments. Theexperiments by Bainard et al. (2012a) were very large(750 pots) and hence such information was not pre-sented (e.g. it is extremely laborious and financiallydemanding to determine microbial community com-position of 750 pots). Thus, with the results presentedit was not possible to draw firm conclusions. Furtherwork is needed to test whether enhanced microbialdiversity in tree-based intercropping systems can pro-vide additional ecological services to these systems.A number of recent developments provide oppor-tunities for understanding how soil microbial commu-nities influence the productivity and sustainability ofcropping systems. First, costs for the molecular char-acterization of microbial communities (e.g. by highthroughput sequencing) has declined considerably inrecent years, making it now possible to characterizemicrobial communities for a larger number of sam-ples. Second, fluxes of carbon and nutrients that aremediated by microbes can be measured with (stable)isotopes and related technology (such as stable isotopeprobing, see Vandenkoornhuyse et al. 2007; Kiers etal. 2011). With these techniques it is possible to showwhich microbes are active, thus providing mechanisticinsights into the role of specific soil microbial com-munities in driving ecosystem functioning. Third, it isdifficult to manipulate microbial diversity becausemany microbes readily disperse via air and water. Asa consequence, microbes can easily contaminate potsand cause unwanted changes in experimental treat-ments. Hence, differences in the effects of microbialdiversity at the start of the experiment may eventuallydisappear, especially if experiments are performedover longer periods of time. Recently, we developedan experimental system in which it is possible tomanipulate microbial diversity in experimental eco-systems without contamination from the outside(Fig. 1). Such tools provide new avenues for testingwhether soil microbial diversity influence ecosystemfunctioning and whether soils with high microbialdiversity are important for sustaining agriculturalproduction.Applicability of soil biodiversity researchin Agro-EcosystemsThe experiments by Bainard et al. also show thatgrowth responses of crops in response to soil inocula-tion are variable. Barley and canola performed best insterilized soil and these crops also did not benefit fromthe presence of arbuscular mycorrhizal (AM) fungi,soil fungi that facilitate plant growth by providing2 Plant Soil (2013) 363:1–5plant inaccessible nutrients. This is perhaps to beexpected since canola does not form AM fungal asso-ciations and a number of studies showed that barleydoes not necessarily benefit from AM fungi (e.g.Grace et al. 2009). Thus, it appears that the impactof plant antagonists of these crops on productivitywas larger than those of beneficial soil organisms. Incontrast, soybean grew equally well in sterilized andnon-sterilized soil and in a second experiment, Bai-nard et al. demonstrate soybean performed better inFig. 1 Schematic draw (a) and photograph (b) of an experi-mental microcosm in which plants can be grown under con-trolled conditions without microbial contamination from theoutside. In order to prevent microbial contamination, fillingand planting of the microcosms needs to be performed in alaminar flow hood and all material needs to be sterilized orautoclaved before use. Moreover, during the growth period,incoming pressured air is filtered through a hydrophobic filter(0.22 μm), while water/nutrient solution is filtered through ahydrophilic filter (0.22 μm) to prevent contamination from theoutside. Replicated microcosms can be inoculated with soilinoculum from different agricultural fields or microcosms canbe inoculated with different (numbers of) microbes. Litter bagsor hyphal compartments with labelled material (13C and or 15N)can be added to the microcosms in order to test whether decom-position and/or nutrient uptake varies between microcosms withdifferent microbial diversity treatments. 13CO2 can be added tothe microcosms (instead of pressured air) to trace the fate ofassimilated C (to facilitate stable isotope probing). MicrocosmDesign: Marcel van der Heijden & Susanne de BruinPlant Soil (2013) 363:1–5 3pots inoculated with AM fungi, which is typical ofmost legumes. Thus, the effects of soil organisms oncrops is driven by the species identity and plant func-tional group of the crop, making it difficult to makegeneral recommendations about the benefits of soilmicrobial diversity in agro-ecosystems. Moreover,microbes not only influence plant productivity, but awide range of ecosystem functions are affected by soilmicrobes that indirectly affect plant productivity, notonly within a growing season but also over time (nu-trient losses, nutrient cycling, soil structure stabiliza-tion etc. – see van der Heijden et al. 2008). Suchindirect effects should not be overlooked when assess-ing the importance of soil microbial diversity.In conclusion, there are now a wide range of studiesdescribing how soil organisms and soil microbes respondto different agricultural practices. However, current un-derstanding as to whether such changes in soil(microbial) diversity are beneficial for the functioningof agro-ecosystems is only in its infancy. Only a fewstudies, often theoretical or performed under highly con-trolled conditions with a particular group of micro-organisms indicate that enhanced microbial diversitycan indeed be beneficial by providing a number of eco-system services (Brussaard et al. 2007; van der Heijden etal. 2008; Berendsen et al. 2012). The work by Bainard etal. provide new insights into the role of soil microbes inagro-ecosystem demonstrating negative soil feedback tobe a strong mechanism. At the same time these authorsalso illustrate there remain many important questions tobe addressed about the role of soil biodiversity in agro-ecosystems and its applicability.ReferencesAltieri MA (1999) The ecological role of biodiversity in agro-ecosystems. Agric Ecosyst Environ 74:19–31Bainard LD, Koch AM, Gordon AM, Klironomos JN (2012a)Growth response of crops to soil microbial communitiesfrom conventional monocropping and tree-based intercrop-ping systems. 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Soil microbial diversity and agro-ecosystem functioning

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Soil microbial diversity and agro-ecosystem functioning

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