Research Paper
Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil

https://doi.org/10.1016/j.soilbio.2010.08.010Get rights and content

Abstract

Plants often impact the rate of native soil organic matter turnover through root interactions with soil organisms; however the role of root-microbial interactions in mediation of the “priming effect” is not well understood. We examined the effects of living plant roots and N fertilization on belowground C dynamics in a California annual grassland soil (Haploxeralf) during a two-year greenhouse study. The fate of 13C-labeled belowground C (roots and organic matter) was followed under planted (Avena barbata) and unplanted conditions, and with and without supplemental N (20 kg N ha−1 season−1) over two periods of plant growth, each followed by a dry, fallow period of 120 d. Turnover of belowground 13C SOM was followed using 13C-phospholipid fatty acid (PLFA) biomarkers. Living roots increased the turnover and loss of belowground 13C compared with unplanted soils. Planted soils had 20% less belowground 13C present than in unplanted soils after 2 cycles of planting and fallow. After 2 treatment cycles, unlabeled soil C was 4.8% higher in planted soils than unplanted. The addition of N to soils decreased the turnover of enriched belowground 13C during the first treatment season in both planted and unplanted soils, however no effect of N was observed thereafter. Our findings suggest that A. barbata may increase soil C levels over time because root and exudate C inputs are significant, but that increase will be moderated by an overall faster C mineralization rate of belowground C. N addition may slow soil C losses; however, the effect was minor and transient in this system. The labeled root-derived 13C was initially recovered in gram negative (highest enrichment), gram positive, and fungal biomarkers. With successive growing seasons, the labeled C in the gram negative and fungal markers declined, while gram positive markers continued to accumulate labeled belowground C. The rhizosphere of A. barbata shifted the microbial community composition, resulting in greater abundances of gram negative markers and lower abundances of gram positive, actinobacteria and cyclopropyl PLFA markers compared to unplanted soil. However, the longer-term utilization of labeled belowground C by gram positive bacteria was enhanced in the rhizosphere microbial community compared with unplanted soils. We suggest that the activities of gram positive bacteria may be major controllers of multi-year rhizosphere-related priming of SOM decomposition.

Introduction

Priming effects are short-term changes in the turnover rate of soil organic matter (SOM) induced by the addition of C and/or nutrients to soil. The modification of native soil C and N mineralization rates from C and N inputs to soils has been observed for decades (e.g., Löhnis, 1926, Bingeman et al., 1953, Wu et al., 1993), however the mechanisms that control the degree and direction of priming effects have not yet been established experimentally (Kuzyakov et al., 2000, Fontaine et al., 2003). Living plants, through their contribution of exudates to the soil rhizosphere, can act as SOM priming agents (e.g., Bottner et al., 1999, Cheng et al., 2003, Cheng and Kuzyakov, 2005). Living roots also alter the soil physical, hydrological, and chemical environment and associated biological processes important to nutrient cycling, plant productivity, and ecosystem C balance (Gregory, 2006). Given the multiple and interacting effects of roots on soil C and N cycling and soil water dynamics, it has been extremely challenging to identify and quantify the primary mechanisms responsible for living root impacts on SOM dynamics. Consequently, soil priming effects from living roots are not present in most ecosystem-scale models of SOM dynamics (Peltoniemi et al., 2007).

Root priming effects on SOM decomposition can be large enough to impact ecosystem-level net C exchange. Living roots can significantly alter soil C (and N) mineralization rates, both negatively (50% lower) and positively (380% higher) and can result in SOM losses that are as large as the amount of root C added to soil (Cheng and Kuzyakov, 2005). Processes in the rhizosphere are primarily controlled by the interactions among roots, fauna and the microbiological community (Hawkes et al., 2007). Dormaar, in his 1990 review on the topic (Dormaar, 1990), concluded that rhizosphere effects on water and N availability should control the degree and direction of SOM priming and that the diversity of the microflora present at all stages of interaction comprise a critical unknown in the process. Shifts in soil microbial community structure due to living roots have been measured, but because the background soil microbial community it is large and complex, changes can seem relatively small (Steer and Harris, 2000, DeAngelis et al., 2008). Faster microbial biomass turnover has been shown to enhance SOM priming from the rhizosphere of soybean and wheat; however, this relationship was sensitive to substrate utilization efficiency (Cheng, 2009). Others have focused on the activity of specific functional groups of microorganisms in response to rhizodeposition (Fontaine and Barot, 2005). As soil microbes are often energy limited in soils, organic compounds exuded by roots such as sugars and amino acids may act as co-metabolites enabling the production and activity of a wide assortment of oxidative and hydrolytic enzymes capable of breaking down macromolecular components of SOM (Fontaine and Barot, 2005). Alternatively rapidly-responding populations specializing in use of small molecular weight labile compounds may dominate the consumption of exudates and rhizodeposits and result in a less positive, neutral or negative priming of SOM. Experimental evidence however, has not yet produced a direct link between SOM priming and microbial community dynamics. The question remains as to importance of root-induced changes in the composition of associated soil microbial communities in priming decomposition of SOM.

The relationship between N-availability and rhizosphere-induced SOM priming has been observed in recent field studies (e.g., Bradford et al., 2008). A meta-analysis of N fertilization effects on litter and SOC decomposition by Knorr et al. (2005) concluded that N additions: i) stimulate the initial decomposition of fresh and/or high-quality litter in low N deposition regions; and ii) suppress decomposition of recalcitrant litter and SOM under moderate to high N depositional levels. In the rhizosphere, N availability may be limited by competition between plant roots and the soil biota. DeAngelis et al. (2008) recently reported increased N-cycling enzymatic activity (chitinase, proteases), bacterial cell densities, and dissolved N in the rhizosphere of Avena barbata compared with unplanted soil. This greater N-cycling activity in the rhizosphere was accompanied by bacterial-density-dependent behaviors that may have been fueled by rhizodeposits that enhanced growth and activity of selected microbial populations (DeAngelis et al., 2008). In addition to N, P availability may play an important role in controlling SOM priming (Bradford et al., 2008).

Root uptake of soil water may reduce water availability sufficiently to limit microbial activity and alter the characteristics of SOM priming (Dijkstra and Cheng, 2007). Alternatively, the more frequent wetting-drying cycles and more pronounced changes in moisture in the rhizosphere compared to root-free soil may accelerate C cycling (Lundquist et al., 1999) and also alter the microbial community structure (Steenwerth et al., 2005). Overall, the net effect of soil moisture on soil C cycling due to the rhizosphere may be neutral, as slower SOM decomposition in drier conditions may be offset by faster decomposition after re-wetting (Magid et al., 1999).

The utilization of 13C stable isotopes in conjunction with microbial community analysis using phospholipid fatty acid (PLFA) has been an effective tool for studying the degradation of simple 13C-labeled substrates by soil microbial communities (Boschker et al., 1998, Arao, 1999). More recently, the 13C-PLFA approach was used to describe the basis of the functional response of soil microbes to climate change (Waldrop and Firestone, 2006b). This approach has also been important in describing the flow of rhizodeposits into rhizosphere communities (Butler et al., 2003, Denef et al., 2007). While the combination of 13C stable isotopes and community analysis by PLFA provides an important approach to understanding the microbial community connection between root C and SOM priming, PLFA provides a “broad brush” analysis of complex microbial communities. Although the resulting picture lacks phylogenetic and population-level information, this PLFA approach does provide potentially important insight into root-microbial-SOM interactions. We examined the effects of living roots on enriched belowground 13C turnover in an annual grassland soil using the 13C-PLFA technique. We investigated the influence of added N on the effects of the planted versus unplanted soils and we minimized root effects on soil water status by monitoring and adjusting soil water content. We asked the following questions: (i) what are the effects of living roots on the composition of the soil microbial community and the community’s utilization of recent root debris and older SOM?; (ii) does the availability of N effect the magnitude, mechanism, or net impact of living roots in SOM priming?

Section snippets

Experimental design

A greenhouse study was conducted at the University of California, Berkeley from 2004 to 2006 to examine the effects of living roots and N fertilization on soil C cycling. Soil (0–15 cm depth) was excavated for the greenhouse study from the Schubert Watershed at the Sierra Foothills Research Center and Extension Center. The soil sampling site is located near Marysville, California (39°15′ N, 121°17′ W) at an elevation of 200 m. The vegetation is hardwood rangeland, with an overstory dominated by

Soil C dynamics

At the end of the pre-treatment fallow period (T2), all belowground C pools were enriched in 13C above unlabeled soil (Fig. 2). Extractable DOC, microbial biomass C and light fraction C were all significantly more enriched in 13C than the dense fraction C pool (Fig. 2). While unlabeled C was dominantly found in the dense fraction of the soil C pool (82%), a much smaller portion of the 13C-labeled organic C (48%) was associated with the dense fraction (data not shown). The high 13C enrichment of

Discussion

The rhizosphere activity of A. barbata in California’s oak grasslands may increase soil C levels over time as root C inputs are significant, but that increase will be moderated by an overall faster rate of native SOM mineralization. Our results and those of several others (Cheng and Kuzyakov, 2005) indicate that SOM priming from living roots is an important component of soil C cycling. Our findings suggest that while increases in N fertilization may slow soil C losses, these declines appear

Conclusions

Living roots increased the turnover and loss of belowground 13C compared with unplanted soils. Planted soils had 20% less belowground 13C present than in unplanted soils after 2 treatment cycles (growth period plus dry fallow period). The addition of N to soils decreased the turnover of enriched belowground 13C during the first treatment season in both planted and unplanted soils, however no effect of N was observed thereafter. Our findings suggest that A. barbata may increase soil C levels

Acknowledgements

This research was supported by Kearney Foundation of Soil Science as part of its 2001–2006 mission, “Soil Carbon and California Terrestrial Ecosystems”. We acknowledge the contributions to this research from undergraduate research assistants Julian Fortney and Betty Liu.

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