Microscale distribution and function of soil microorganisms in the interface between rhizosphere and detritusphere
Highlights
► A novel experimental design to study the interface between rhizosphere and detritusphere. ► Soil, plant and residues differed in δ13C signatures and δ13C of PLFA was measured. ► Microbial community composition showed distinct gradients from roots and residues. ► Microbes in the interface incorporated more residue C than root C.
Introduction
In soils, the rhizosphere and the detritusphere are two hot spots of microbial activity due to the presence of easily available compounds from either roots or plant residues. Microbial density and enzyme activity are high close to the roots or residues and decrease with increasing distance, forming distinct gradients in millimetre scales. Moreover, microbial community structure changes with distance from roots or residues (e.g. Kandeler et al., 2001; Poll et al., 2006, 2008, 2010).
Roots modify the rhizosphere by taking up nutrients and releasing various substances such as sugars, organic acid anions and amino acids which are easily available nutrient sources for microorganisms. Hence, compared to the bulk soil, the rhizosphere of active roots is characterized by depletion of nutrients such as P and a high abundance and activity of microorganisms (Foster, 1986; Joner et al., 1995; Chen et al., 2002; Wang et al., 2005) as well as by high activity of enzymes released by roots and microorganisms (Tarafdar and Jungk, 1987; Joner et al., 1995; Badalucco et al., 1996). Abundance and activity of microorganisms and enzyme activity decrease with distance from the root surface creating distinct gradients within a few millimetres (Tarafdar and Jungk, 1987; Kandeler et al., 2001).
As the rhizosphere, the detritusphere is characterized by high concentrations of easily available compounds, particularly in the early stages of residue decomposition when water-soluble compounds are released (Bastian et al., 2009; Poll et al., 2010). After depletion of the water-soluble compounds, more complex compounds requiring specialized enzymes are decomposed more slowly (Theuerl and Buscot, 2010). Similarly to the rhizosphere there is a gradient of nutrient availability as well as of enzyme activity (Gaillard et al., 2003), microbial density and community composition with distance from the residues (Poll et al., 2006; Nicolardot et al., 2007; Bastian et al., 2009). Moreover, fungal community composition and abundance change over time as compounds within the residues are successively depleted (Poll et al., 2010). As a result of diffusion and mass flow as well as translocation via fungal hyphae and soil animals, residue C can be detected up to 4 mm from the residues with a greater distance in moist compared to dry soil (Gaillard et al., 2003; Poll et al., 2008). Depending on the C/N or C/P ratio of the residues, there may be net mineralization or net immobilisation in the microbial biomass in the residues, but also within the detritusphere several millimetres away from the residues (Moritsuka et al., 2004; Ha et al., 2007).
Thus, chemical, physical and biological properties of the rhizosphere and detritusphere have been studied extensively, but separately. However, in the field, roots usually grow in the vicinity of decomposing plant residues where rhizosphere and detritusphere may meet resulting an interface that is influenced by both rhizosphere and detritusphere properties. The conditions in the interface may change over time as release of C from decomposing residues and roots change. Thus the relative dominance of rhizosphere or detritusphere properties in the interface may also change. Microbial communities characteristic for rhizosphere and detritusphere may compete and create new communities that are specific for this interface. We designed a three-compartment pot system with living roots on one side and soil with residues on the other, each separated by a fine mesh from the 5 mm-wide middle compartment by a 50 μm mesh which was filled with soil only. In this system the three dimensions of the rhizosphere and detritusphere were reduced to two dimensions to allow accurate small-scale sampling at different distance from roots and residues. The slicing of the middle compartment into 1 mm layers provided information about extent and possible interactions of rhizosphere and detritusphere. In each layer, enzyme activity and microbial community composition by PLFA were measured.
The aims of this study were to (i) compare the changes induced by roots and residues and the extent of their zone of influence, (ii) assess if there is an overlap of their zones of influence when roots and residues are separated by 5 mm, and (iii) track the carbon flow from roots and residues into the microbial biomass by using soil, plants and residues with different 13C signatures and 13C-PLFA analyses.
Section snippets
Experimental set up
The experiment was conducted in a three-compartment pot system (diameter 100 mm, height 190 mm) with two equally-sized outer compartments, separated by a 50 μm polyamide mesh (SEFAR Nitex PA 6.6) from a 5 mm-wide middle compartment (Fig. 1). The outer compartments were filled with 664 g and the middle compartment with 99 g dry soil equivalent, sieved to 2 mm. The middle compartment consisted of three PVC frames with the outer two frames with the mesh and the middle frame defining the width of
Plant growth
Plant shoot and root dry matter increased 2.5 fold from 14 DAP to 23 DAP and did not differ significantly between the treatments (Table 1). The shoot N concentration at 23 DAP was 13–18 g kg−1 which is low to adequate (Marschner, 2012). On 14 DAP, maize had formed a few roots close to the mesh of the middle compartment; by the second harvest, 23 DAP, a dense root mat had formed in the lower half of the pot. A few fine roots had grown though the mesh or the gaps in the frame extending several mm
Discussion
The experiment showed microscale gradients and C fluxes in the detritusphere and rhizosphere. This experimental design allows direct comparison of rhizosphere and detritusphere effects and assessing whether their zones of influence overlap. In general, roots and residues had similar effects on the measured parameters. For some properties (fungal abundance, B/F ratio, N depletion), their gradients overlapped, whereas for most of the measured parameters, the two zones of influence remained
Conclusion
The results of this study show the existence of millimetre scale gradients in abundance of bacterial and fungal fatty acids, differential microbial community composition in the interface between rhizosphere and detritusphere as well as carbon flow from residues into soil microorganisms. Despite the small distance between roots and residues (5 mm), the two interfaces did not overlap from most parameters assessed. This suggests that unless roots and residues are separated by less than 2–3 mm,
Acknowledgements
We thank Sabine Rudolph and Heike Haslwimmer for expert technical assistance. We would also like to thank the two anonymous reviewers for their insightful and constructive comments which helped us to improve the manuscript considerably. This study was supported by a grant from the Australian-German Go8-DAAD funding scheme.
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