Soil microbes and plants – raising interest, mutual gains
Impacts of Soil Microbes on Plant Population Dynamics and Productivity – the 8th New Phytologist Symposium, Helsinki, Finland, 10–14 June 2002
Ecologists are realising more and more that what goes on in soil, whether activities of plant roots themselves or associated soil organisms, has a very important bearing on the success of different plant species and on plant competition and community structure. The conference organisers set themselves the formidable task of bringing together scientists working at scales from the gene through to the ecosystem. Here, a few of the diverse contributions that may have challenged participants to think outside their usual conceptual boundaries are highlighted.
Mutualistic symbioses and extreme complexity
Mutualistic symbioses (mycorrhizas and N2-fixers) provided a connecting theme through most sessions, reflecting the wide recognition of their likely importance in natural and managed ecosystems. The first major challenge was a timely one, directed at the ‘received wisdom’ about mutualistic symbioses, particularly arbuscular mycorrhizas (AM) (Fitter, University of York, UK). Current knowledge is grounded in reductive experiments, often on single plant species paired with single fungi, that commenced approx. 50 yr ago. Many of the questions that have been addressed, using increasingly sophisticated techniques, were outlined in the extremely influential book ‘Endomycorrhizas’ (Sanders et al., 1975). The outcome is a corpus of general knowledge about the interactions between the symbionts – their growth, cellular and molecular interactions and physiology, and more recently functional diversity and nonnutritional benefits to their symbiotic partners (e.g. drought tolerance, interactions with pathogens and effects on soil structure). Now that we do have some ‘general rules’, they can and must be tested. This maxim should apply more widely than just to AM symbioses.
Fitter's challenges were that AM fungi represent a more diverse taxon than would be expected from the existence of c. 150 described species and that there is more evidence of plant/fungus specificity than has been revealed so far, using those AM fungi that can be isolated as spores and nurtured easily in pot cultures. Thus, AM may not fit the accepted theory that mutualisms should have broad partner ranges and low α diversity (Law & Lewis, 1983; Douglas, 1998). Extreme genetic complexity is certainly implied in much recent research. To this must be added increasing evidence for diversity of function between different pairs of fungal and plant symbionts, revealed in pot experiments (Jakobsen et al., 2002) and in analyses of gene expression in different ectomycorrhizal partnerships (Martin, INRA, France). The implications of such diversity in ecological interactions are enormous, and will impact on the feedback between plants and members of the soil community (including nutrient cycling organisms, pathogens and AM fungi) which can regulate the diversity of the plant communities (Bever, University of Indiana, USA; Bardgett, University of Lancaster, UK; Zobel, Tartu University, Estonia).
Taking research out into the field
Garbaye (INRA, France) urged the imperative to adopt new approaches to determining the importance of the multifunctional roles of ectomycorrhizal fungi in mature boreal and temperate forests, not just in seedlings. The challenges in these and all other ecosystems are considerable and, as Jones (Okanagan University College, Canada) showed, field bioassays in forests indicate that clearcutting may not reduce colonisation/diversity of ectomycorrhizal fungi as is widely believed based on glasshouse studies. The findings are highly relevant to the ways forests are managed. These pleas for investigations in the field, over wide areas and long time scales, would surely be supported by David Read and others advocating the need for field relevance.
Nutrient turnover and acquisition
The effects of herbivory on plant communities have traditionally been studied by looking at the performance of the plants and changes in community composition, but Bardgett (Lancaster University, UK) showed convincingly that feedbacks through the soil are crucial, involving plant nutrition, plant productivity, food supply for the above-ground grazers and return of faeces and urine to the soil. He combined data from field scale experiments, root biology and N cycling to test hypotheses on the effects of grazing by large above-ground herbivores on plant productivity and species composition in both productive and unproductive sites. In Canada, lodgepole pine and western red cedar can grow in extremely nutrient poor environments in situations where the N budgets do not add up until, as Chanway (University of British Columbia, Canada) showed, the inputs from free-living diazotrophs are taken into account. Some of these N2 fixers appear to be associated with the tuberculate, AM roots of red cedar.
In a logical extension of this focus on nutrient turnover and acquisition, Tibbett (CSIRO, Australia) highlighted the part played by ectomycorrhizal fungi (again) in plant exploitation of nutrient patches, such as those provided by seeds. The response of plants to patches in terms of plasticity in root growth has been relatively well explored (Robinson, 1994) and those plants that are apparently unresponsive to localised sources themselves may depend on the activities of their mycorrhizal symbionts (see also Farley & Fitter, 1999). The outcome may well depend on which of the functionally diverse assemblage of fungi actually colonise the roots.
Pathogens and transposons
Examples of ecology in action at smaller scales were provided by several studies of pathogens. The search for biocontrol agents, and identification of the attributes that make a good one, is essentially physiological/molecular ecology. The significant pathogen Fusarium oxysporum appeared as the target organism several times: in molecular and biochemical analyses of the antagonistic strategies adopted by Pseudomonas (Lugtenberg, Leiden University, The Netherlands); and by closely related non-pathogenic fusaria (Alabouvette, INRA, Dijon, France). Negative effects of AM fungi on F. oxysporum appear (at the larger scale) to be the predominant ‘benefit’ of the symbiosis in maintaining wild populations of the grass Vulpia ciliata (Watkinson, University of East Anglia, UK). Elucidating the mechanisms by which AM fungi antagonise F. oxysporum in or near Vulpia roots will need similar approaches to those used by the plant pathologists.
The ‘life-cycle’ of retrotransposons in plant genomes, the way in which they are transcribed in response to stress, the sites in which they are inserted, and the cost of synthesis of the resulting repetitive DNA (Schulman, University of Helsinki, Finland) add up to ‘ecology of DNA’ operating at a molecular level. Studies are yielding fundamental information about genome evolution, as well as fingerprints that can themselves be used as aids in larger scale plant ecology. Again at the level of genes, Martin (INRA, Champenoux, France) described his explorations of the transcriptome of Pisolithus/Eucalyptus ectomycorrhizas with EST/cDNA arrays during formation of the mantle and Hartig net and establishment of new symbiotic functions. Surprisingly, perhaps, no symbiosis-specific genes in either plant or fungus have been cloned and many genes are unaffected. Of the 15–20% that show a significant change in expression, most are involved in general activation of protein synthesis and energy metabolism; there are also increased levels of cell surface proteins probably involved in formation of the symbiotic interface. So far so good. But perhaps the most important message was that application of the same techniques to less well defined mycorrhizal interactions (Populus/Laccaria and Douglas Fir/Laccaria) gives different stories. This is yet another illustration of the need to test generalisations and be aware of the potential dangers of extrapolating directly from simple and easy-to-work-with ‘model systems’ to more complex ecological situations.
New techniques are being applied in molecular ecology too, leading to the identification of members of the Archea, not only in soil and water (Jurgens, University of Helsinki, Finland), but among the bacterial populations and biofilms in mycorrhizospheres (Bending, Horticulture Research International, UK; Bomberg, University of Helsinki, Finland; Sen, University of Helsinki, Finland). The next step is to find out what these organisms are doing in soil and in the hyphosphere.
The usefulness and safety of genetic modification of both plants and microorganisms provided stimulating and controversial presentations. On the one hand, van Montagu (Ghent University, Belgium) expressed the view that genetic transformation of crops was the (only) way forward to cope with the future food needs of the world and that there were no ecological risks in following this path. This view was supported from the practical standpoint of breeding rice for different ecological situations (Datta, IRRI, Phillipines). However, the issue is not as clear cut as these proponents would wish, particularly for soil microorganisms, as shown by van Elsas (PRI, The Netherlands). Studies of the Escherichia coli genome show that it has evolved by acquiring remnants of genes and plasmids by horizontal gene transfer (HGT) over approx. 1 million years (a rather short time in evolutionary history) and most bacterial genomes are similar. A model system to investigate HGT revealed that the process appears to be ‘a community event’ involving groups of bacteria in regions of high activity, such as the rhizosphere. This finding suggests that there may be risks in releasing genetically modified microorganisms, although Hirsch (IACR-Rothamsted, UK) found no evidence for HGT between rhizobial strains persisting in soil for 5 yr. Is this time-scale long enough? What time-scale should be considered? The jury is still out on the benefits and risks of genetic modification to improve plant (crop) growth and performance and it will be crucial to take evidence-based approaches to evaluating requests for release of transgenic organisms and to assess their ecological risks (Amijee, Pioneer Overseas Corporation, Belgium).
Was anything missing from the symposium or, rather, what might be included in future meetings? Many presentations described heterogeneous distribution of organisms and the importance for them of heterogeneous supplies of nutrients in the rhizosphere and ‘patches’, but there was little or no discussion of the habitats in which soil organisms or roots live – varied sizes, continuity and tortuosity of the soil pore system or the physicochemical characteristics controlling water availability, atmosphere, pH, and so on. This information on the spatial and physicochemical environment is crucial to understanding the mechanisms underlying the feedbacks between plant productivity and soil biological activity in different ecosystems and soils. In future, biologists and soil physicists and chemists will need to get together at small meetings where they can discuss and exploit their somewhat different conceptual views of the soil environment to further increase our understanding.