In this review, we explore how microbes that live belowground indirectly and directly influence the productivity, diversity and composition of plant communities. We identify research gaps and propose new avenues of research. First, we discuss the impact of microbes on plant productivity and plant diversity. Second, we investigate the significance of microbial diversity. Third, we discuss the characteristics of bacterial and fungal dominated soil ecosystems and how the relative abundance of bacteria and fungi affect ecosystem functioning. We end with conclusions and identify future research priorities. Our ultimate aim is to highlight the significance of soil microbes for the productivity and diversity of plant communities, and the strong interdependence of plant and soil microbial communities.
The relationship between microbial diversity, plant diversity and plant productivity
There is currently much interest in the relationship between soil microbial diversity and ecosystem functioning. Key questions are whether diverse microbial communities are better adapted to perform specific functions in ecosystems compared with species poor microbial communities. This question is also important in view of reduced microbial diversity in many anthropogenically disturbed soil ecosystems (Torsvik et al. 1996; Gans et al. 2005). So far, only a few studies have examined effects of microbial diversity on plant diversity and productivity. Several studies have manipulated the diversity of mycorrhizal fungal symbionts and determined how this affected plant productivity and diversity. Some of these studies observed that plant productivity, plant diversity and nutrient acquisition increased with increasing fungal diversity (Van der Heijden et al. 1998; Jonsson et al. 2001; Maherali & Klironomos 2007), while other studies found no effects (e.g. Van der Heijden et al. 2006b). For instance, Van der Heijden et al. (1998) observed that grassland microcosms with the greatest mycorrhizal fungal diversity had 105% higher plant diversity, and 42% higher plant productivity, respectively, compared with microcosms where only one fungus was inoculated. In recent work, Maherali & Klironomos (2007) provided a mechanistic explanation for the observation that AM fungal diversity can promote plant productivity. They observed that there is functional complementarity between different AM fungal families: one mycorrhizal fungal family (the Glomeraceae) provided protection against fungal pathogens, while another family (the Gigasporaceae) enhanced plant P uptake. Subsequently plant productivity was enhanced when members of both fungal families were simultaneously present. However, in contrast to the this, Vogelsang et al. (2006) showed that biomass in microcosms inoculated with a mixture of six AM fungi was comparable with the biomass in the treatment with the best single mycorrhizal fungus, pointing to the importance of species identity rather than diversity per se. Thus, there are alternative explanations and supportive studies to explain effects of mycorrhizal diversity, and additional experiments are required to solve this issue.
It is still unclear whether bacterial diversity promotes plant diversity or ecosystem functioning. Several legumes form host specific associations with N-fixing rhizobia bacteria (Sprent 2001; Van der Heijden et al. 2006a). This suggests that the presence of a diverse rhizobial community is required to enhance legume diversity. Moreover, endophytic and root-associated bacteria might stimulate plant diversity if different bacteria promote growth of different host plants.
A number of studies have examined how microbial communities that vary in composition and diversity influence the decomposition of plant material, and hence the liberation of nutrients for plant growth. Some of these studies found that microbial diversity enhanced decomposition while others found no effect, negative effects, or observed that specific microbial species, and not diversity per se, determined decomposition (reviewed by Hattenschwiler et al. 2005). For instance, a study by Bonkowski & Roy (2005) showed that microbial diversity (measured as functional diversity) enhanced decomposition and nitrogen leaching from grassland microcosms. Moreover, diversity effects appear to be strongest at the species poor end of diversity gradients when only few microbes are present (e.g. Setala & McLean 2004; Wertz et al. 2006). It also appears that there is considerable functional redundancy among decomposing microbes (Hattenschwiler et al. 2005) and many microbes have similar effects on decomposition. However, some studies only mention initial differences in microbial composition and it is likely that microbial treatments have changed during the experiment, making it difficult to make firm conclusions.
There are a number of mechanisms by which microbial diversity might enhance decomposition, and hence the provision of nutrients for plant productivity. Some biochemical reactions require specific conditions, are incompatible, or are performed by specialised microbes with unique physiological properties (e.g. lignin degradation by specialised fungi –De Boer et al. 2005). Hence, division of metabolic labour, or compartmentalization, might be necessary to perform specific reactions during decomposition. For instance, a recent study by Lindahl et al. (2007) showed that litter decomposition by fungi is spatially separated and performed by two distinct groups of fungi that inhabit different parts of the soil horizon. Saprotrophic fungi are confined to the surface layer decomposing freshly fallen litter and they are mainly responsible for the mineralization of carbon. Mycorrhizal fungi, in contrast, dominate the underlying soil horizons and are specialized on more decomposed litter and humus, most likely mobilizing nitrogen and delivering it to their host plants. Moreover, the chemical composition of litter from different plant species is variable and different microbes might be needed to decompose the various litter types. Furthermore, fungal hyphae can act as vectors for bacterial transport, enabling bacteria to colonize new substrate faster (Kohlmeier et al. 2005). This so-called ‘fungal highway’ could facilitate decomposition by bacteria, especially under dry conditions when bacteria could use hyphal biofilms for dispersal and colonization of new substrate (Perotto & Bonfante 1997). Hence, these observations point to the importance of microbial diversity for decomposition, but more studies are needed to better understand the mechanisms involved.
Microbial diversity can also promote plant diversity and productivity when microbes associate with different plant species or when different microbes provide different resources. For instance, AM fungi and rhizobia can act synergistically and stimulate plant productivity by supplying different limiting nutrients to the plant (e.g. N by rhizobia and P by AM fungi). Many legumes benefit from this principle as they form tri-partite symbiotic associations with AM fungi and rhizobia thus, profiting from the distinct characteristics of both symbionts (Pacovsky et al. 1986). AM fungi have even been found to colonize root nodules (plant organs designed for N-fixation by rhizobia) of several legumes pointing to direct plant–AM fungi–rhizobia interactions (Scheublin et al. 2004).
Recent work has shown that microbial diversity in soil ecosystems is reduced because of land-use intensification and increased nutrient availability (e.g. Helgason et al. 1998; Fig. 2), nitrogen deposition (e.g. Lilleskov et al. 2002), and chemical contamination (Gans et al. 2005). The impact of this reduced diversity on plant diversity and productivity is unclear. We hypothesize that significance of microbes is highest at low nutrient availability (Fig. 2) and we expect that nutrient poor ecosystems are more vulnerable to reductions in microbial diversity and losses of specific microbial species or functional groups. These expectations are based on several observations. First, plant productivity in nutrient poor ecosystems is often enhanced by a range of microbial symbionts that acquire various limiting nutrients (see Impact of soil microbes on plant productivity for references). Several of these symbionts have a restricted host range (e.g. several rhizobia and some mycorrhizal fungi) and a reduction in microbial diversity could reduce growth of plant species that depend on specific microbial symbionts. For instance, Jonsson et al. (2001) observed that effects of fungal diversity were strongest at low nutrient availability, perhaps because different mycorrhizal fungi obtained limiting nutrients from different sources in the soil. In contrast, plants are often less dependent on mycorrhizal fungi and N-fixing bacteria when nutrient availability is high (e.g. Smith & Read 1997; Sprent 2001). Second, nutrient poor ecosystems are especially vulnerable to nutrient loss (e.g. because of microbial denitrification or leaching) because plant productivity is limited by nutrients in these ecosystems (Chapin 1980). Thus, small nutrient losses will immediately lead to a reduction of plant productivity in nutrient poor ecosystems. Third, chemical diversity in nutrient poor ecosystems is often high because such ecosystems are usually species rich, containing many different plant species that produce a wide range of secondary metabolites and recalcitrant defence compounds, including lignin and tannins (Lambers & Poorter 1992). It is likely that a wide range of physiological diverse microbes contributes to the break down of plant litter in nutrient poor ecosystems. Hence, these observations indicate that microbes and microbial diversity are likely to have the biggest impact on ecosystem performance in nutrient poor ecosystems. Following this, we hypothesize that the relationship between microbial diversity and ecosystem functioning is different for nutrient poor and nutrient rich ecosystems. We expect that microbial communities from nutrient rich ecosystems are functionally more redundant compared with microbial communities from nutrient poor ecosystems where microbes need specific adaptations to obtain resources [e.g. during decomposition or when forming (host specific) symbiotic associations with plants].
Figure 2. Hypothetical relationship between nutrient availability and the microbial contribution to plant productivity. Microbes are hypothesized to be most important for the productivity of nutrient poor ecosystems. It is also hypothesized that microbial diversity (–––) is negatively correlated with nutrient availability.
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Effects of increasing microbial diversity on plant productivity probably also depend on the number of functional groups that are present. Adding increasing numbers of species from a particular functional group (within functional group diversity) will probably add some degree of functional diversity and have slight effects on ecosystem functioning. However, adding different functional groups (between functional group diversity) or specific keystone species will probably have a bigger impact on plant productivity and particular ecosystem processes (Hooper et al. 2002). For instance, AM fungi, N-fixing bacteria and fungal decomposers all have different functions in ecosystems, and the absence of one group may have a big impact on plant productivity. The level of functional diversity may also be related to the phylogenetic relatedness among soil microbes. Microbial communities with diverse lineages may have a bigger impact on ecosystem processes because they are functionally more diverse, as was recently shown for AM fungi by Maherali & Klironomos (2007). Interestingly, despite the high level of bacterial species diversity found in soil, they have a lower phylogenetic diversity than other environments (Lozupone & Knight 2007), perhaps suggesting that soils contain a large number of microbial species with similar functions. Future work should address this issue, also focusing on the diversity of functional genes that affect particular ecosystem processes (see Conclusions and perspectives).
The question of whether microbial diversity is important to ecosystem functioning is interlinked with questions about the distribution of microbes and whether microbial diversity varies between ecosystems. Earlier work suggested that most microbes have a cosmopolitan distribution (Finlay & Clarke 1999). However, recent studies have shown that many microbes have restricted biogeographic distributions (e.g. Peay et al. 2007) suggesting that variations in the composition of microbial communities can impact ecosystem functioning. Also, little is known about factors that regulate microbial diversity at different temporal and spatial scales (Green & Bohannan 2006) and its interdependency with plant diversity (Zak et al. 2003); this is an area that needs much more attention, especially if microbial ecologists want to predict how microbial communities influence ecosystem functioning.
Bacterial and fungal dominated soil ecosystems
So far, we have focussed on the significance of microbial diversity and the importance of specific groups of soil microbes for ecosystem functioning. However, one biological property of soil that receives a large amount of attention is the relative abundance of bacteria and fungi in ecosystems, and associated changes in the faunal component of the soil food web. Bacteria and fungi often have very distinct functions, and ecosystems are often characterized by having fungal-dominated or bacteria dominated microbial communities and food webs, or combinations of both (Wardle et al. 2004b). Ecosystems with bacterial dominated microbial communities are characterized by high levels of disturbance, have a high nutrient availability, a neutral or mildly acidic pH, and often have reduced soil organic matter content, because of elevated biological activity (Table 2). In contrast, fungal dominated microbial communities occur in less disturbed, late successional sites, often with acid soils that are of high organic matter content and low resource quality (Table 2). Moreover, these types of soil communities are interchangeable: bacteria-dominated communities can change to fungal dominated communities, for example during primary succession (Bardgett et al. 2005) and following land abandonment (Zeller et al. 2001), whereas fungal dominated communities can shift to bacteria-dominated communities as a result of nutrient enrichment and intensive farming (e.g. De Vries et al. 2006).
Table 2. Suggested characteristics of fungal and bacterial dominated soil food webs
|Fungal dominated food web||Bacterial dominated food web|
|Closed nutrient cycles (internal cycling)||Open nutrient cycling (nutrient addition and loss)|
|Slow cycling of nutrients||Fast cycling of nutrients|
|Low nutrient availability||High nutrient availability|
|Slow growing plant species||Fast growing plant species|
|Low net primary productivity||High net primary productivity|
|Low leaf litter quality||High leaf litter quality|
|Low resource quality||High resource quality|
|Developed soils||Undeveloped soils|
|Rich in organic matter||Poor in organic matter|
|Late succession||Early succession|
Little is know about the functional significance for plant community dynamics of shifts between fungal and bacteria-dominated microbial communities and food webs. One general idea is that bacteria-dominated food webs enhance rates of nutrient mineralization and the availability of nutrients to plants, whereas fungal-dominated food webs promote ‘slow’ and highly conservative cycling of nutrients (Wardle et al. 2004b). This idea is supported by a number of studies that show shifts from fungal towards bacteria-dominated microbial communities to be associated with enhanced rates of nutrient cycling, and vice versa. For example, Bardgett et al. (2006) showed that the presence of the hemiparasite Rhinanthus minor in grassland lead to increased plant diversity and a shift in the composition of the microbial community towards increasing dominance of bacteria, which was associated with a significant increase in rates of nitrogen cycling in soil. Conversely, Wardle et al. (2004a) studied a series of long-term chronosequences (i.e. for 6000 to over 4 million years) where a decline in standing plant biomass over time occurred. This decline was associated with increasing substrate P limitation for microbes, which was paralleled with a shift in the composition of microbial communities towards fungal dominance. Together, these changes resulted in reduced rates of litter decomposition and mineralization of nutrients, setting a negative feedback in motion, which further intensified nutrient limitation leading to ecosystem decline.
Such feedback mechanisms between plants and soil communities also operate at the individual plant level. One suggestion is that specific plant species might select for bacteria or fungal dominated food webs which creates a feedback on the dominance and persistence of the same species within the plant community (Wardle 2002). For instance, fast-growing species produce large amounts of high-quality (i.e. N-rich) litter and root exudates, which promote ‘fast cycling’ bacteria-dominated food webs, leading to enhanced decomposition and nutrient cycling which further enforce the dominance of fast growing species within the community. In contrast, slow-growers produce low-quality, phenolic-rich litter which favours fungal-dominated food webs that are typically associated with low rates of nutrient cycling, hence further favouring the dominance of slow-growing species that are adapted to low nutrient availability. This framework suggests a form of mutualism between plants and their associated microbial community that is related to soil fertility. While these ideas have been discussed extensively in the literature they have not yet been tested experimentally and the mechanisms involved are unknown; this represents a major challenge for the future.