Plant traits, stoichiometry and microbes as drivers of decomposition in the rhizosphere in a temperate grassland

Yolima Carrillo Colin Bell Akihiro Koyama Alberto Canarini Claudia M. Boot Matthew Wallenstein Elise Pendall

First published:10 March 2017 https://doi.org/10.1111/1365-2745.12772 Citations: 15

Summary

  1. It is becoming increasingly clear that plant roots can impact the decomposition of existing soil C in the rhizosphere. Studies under controlled conditions suggest this impact may be plant species dependent, but whether this is the case in natural conditions or what factors underlie this variation is mostly unknown.
  2. With a novel field‐based isotopic approach combining 13C‐enriched glucose and 5‐bromo‐2‐deoxyuridine additions, we compared in situ C decomposition of added labile C and native soil C (priming) among eight semi‐arid grassland species’ rhizospheres to investigate the factors driving inter‐species variation. We examined the influence of several rhizosphere factors related to soil chemistry, microbial activity, microbial community, microbial stoichiometry, plant chemistry and root morphology.
  3. Plant species generated distinct microbial and chemical rhizosphere environments, which translated into differences in the direction, magnitude and temporal dynamics of the soil C priming. Soil C decomposition was positively related to soil C/P and soil N/P (via its influence on the bacterial community), which in turn were positively related to plant N/P. Plant C/N was also a significant factor via its negative influence on soil N/P. In contrast, the main direct predictors of labile C decomposition were microbial biomass, microbial C/N and the C‐degrading enzymes, which in turn were linked to root morphology and C chemistry.
  4. Synthesis. Within this community, plant species’ rhizospheres can vary in their susceptibility to C loss in response to changes in C availability. Soil stoichiometry, driven by plant chemical traits, appeared to be the strongest driver of priming. Our study suggests that shifts in plant communities involving increases in N relative to P have the greatest potential to lead to C loss. We provide evidence of root morphology and C chemistry as drivers of labile C processing in soil, a novel empirical contribution to our understanding of the role of plant traits below‐ground. The contrasting regulation of different pools of soil C suggests observations of the regulation of simple C compounds should not be extrapolated to the whole C pool. Our findings provide support for rhizosphere‐driven mechanisms by which shifts in plant community composition could have implications on the ecosystem‐level C balance.

Introduction

Recent developments in multiple disciplines are re‐shaping our understanding of soil organic matter (SOM) stability not as a result of molecular properties of decomposition substrates, but as an ecosystem property, arising from the interaction of available carbon (C) with the biotic and abiotic environment in soil (Schmidt et al. 2011). One such development is the growing understanding that plant root activity and the environment it generates in its surroundings – the rhizosphere – can alter the decomposition of extant SOM, a phenomenon called the rhizosphere priming (RP) effect (Cheng & Kuzyakov 2005). Studies under controlled conditions suggest that C priming in the rhizosphere may be plant species dependent (e.g. Pausch et al. 2013; Cheng et al. 2014). Climate change can alter plant community composition via changes in relative abundance of species and community reordering through immigration and loss (Hickling et al. 2006; Zhu, Woodall & Clark 2012; Zelikova et al. 2014). Thus, understanding what drives the species dependency of priming in the rhizosphere is important to improve predictions of soil C dynamics in response to climate changes influencing plant community composition.


Most studies attribute RP to changes in C availability in soil via rhizodeposition and its effects on microbial activity (e.g. Allard et al. 2006; Dijkstra, Cheng & Johnson 2006; Cheng 2009; Bengtson, Barker & Grayston 2012; Hartley et al. 2012; Cheng et al. 2014). This interpretation stems from consistent observations of responses of plant‐free soil to the addition of C substrates under laboratory conditions (compiled in Zhang, Wang & Wang 2013). But, if C availability alone explained RP, we would not expect the wide variation in the magnitude, direction and plant species dependency of RP that has been observed (Cheng et al. 2014). Moreover, various other factors and environmental changes (e.g. elevated atmospheric CO2, warming, altered precipitation regimes, extreme weather events or biological disturbances) can generate changes in C availability which could elicit plant species‐specific priming responses. Nutrient availability, particularly of nitrogen (N), has also been suggested as a key driver of RP (Dijkstra et al. 2013; Cheng et al. 2014). The notion that it may not be just N availability but N‐phosphorus (P) stoichiometry that regulates RP has recently been put forward and offers a framework to reconcile the diversity of RP effects (Dijkstra et al. 2013). Under this framework, whether C inputs result in priming would depend on whether microbes are N or P limited. Positive priming may occur under N limitation (likely low N:P in soil) as microbes mine for organic N releasing C, while under P limitation (likely high N:P in soil) C addition may not cause priming because microbial mining for P, mostly in inorganic form, would not be expected to release soil C. However, most priming experiments assessing stoichiometric effects have been conducted in plant‐free soils (e.g. Hartley et al. 2010; Fontaine et al. 2011; Nottingham et al. 2012; Sullivan & Hart 2013; Kirkby et al. 2014) with a few using living plants under controlled conditions (e.g. Bengtson, Barker & Grayston 2012; Carrillo et al. 2014a,b). These experiments are useful for identifying and quantifying environmental and biotic controls over RP, but they do not necessarily translate to natural ecosystems.


Very little is known about the regulation or repercussions of variable RP in natural conditions (Gardenas et al. 2011; Cheng et al. 2014). Given that plants vary widely in the quality and quantity of rhizodeposition (Czarnota, Rimando & Weston 2003; Warembourg, Roumet & Lafont 2003; Jones, Nguyen & Finlay 2009) as well as in their biomass stoichiometry and nutrient demands (Hobbie 1992; Bell et al. 2014), it is not surprising that RP has been found to be species dependent at least under controlled conditions (Dijkstra & Cheng 2007; Bengtson, Barker & Grayston 2012; Pausch et al. 2013; Carrillo et al. 2016). In the complex plant–soil interface environment, it is likely that various factors simultaneously contribute to this species dependency. Plant traits associated with resource economy strategies have been linked to differences in soil C cycling (De Deyn, Cornelissen & Bardgett 2008; Klumpp & Soussana 2009; Orwin et al. 2010). Among plant traits, root traits (architectural, morphological, physiological), while more rarely considered than above‐ground traits, may regulate RP due to their intricate relationship with soil C and soil microbes (Bardgett, Mommer & De Vries 2014; Finzi et al. 2015), but this has not been explored empirically. Close correspondence between plant species and microbial community structure and activity in the rhizosphere (e.g. Hawkes et al. 2005; Kardol et al. 2010; Kuske et al. 2002) could also contribute to differing C dynamics. Microbial communities with different substrates use preferences that could affect responses to changes in C availability (Goldfarb et al. 2011) affecting the rates of decomposition (Creamer et al. 2015). Which of these potential drivers are most important under natural conditions remains an open question.


Stoichiometric relationships in the rhizosphere may be a critical driver of C and nutrient cycling in soil, as hypothesized by Bell et al. (2014) in their study of C:N:P ratios in plant, soil and enzymes. In the rhizosphere, stoichiometric relationships will vary across plant species due to the intimate linkages between rhizosphere components (plant–soil–microbe) and the wide inter‐species variation in plant stoichiometry and nutrient demand (Sistla & Schimel 2012). Stoichiometric variability in the rhizosphere may in turn influence soil and ecosystem C cycling. For example, invasions by particular plant species with distinctive nutrient ratios and demands have cascaded into soil C changes (e.g. Allison & Vitousek 2004; Strickland et al. 2010). Likewise, the importance of the C:N stoichiometry of simulated plant exudates on C function was demonstrated in a field experiment (Drake et al. 2013). They observed that C added alone constrained exoenzyme production limiting decomposition, but C:N of 10:1 induced C release. In a growth chamber study, Bengtson, Barker & Grayston (2012) concluded that in order for priming to occur, N‐limited plants and C‐limited microbes needed to occur together and thus priming was driven by the C and N stoichiometry of resources and demand. These studies are beginning to point at the functional role of the stoichiometry of the rhizosphere. However, a direct evaluation of the relationship between plant–soil–microbe stoichiometry and rhizosphere C cycling across plant species has not been explored in natural systems.


The particular combination of plant traits, distinct microbial communities and activity and stoichiometry in a species’ rhizosphere is likely to render a unique environment that would differ from other species in its susceptibility to SOM‐C decomposition when faced with a shift in available C. We compared in situ C decomposition of added labile C and native soil C (priming) among several semi‐arid grassland species’ rhizospheres to investigate the factors driving inter‐species variation. We examined the influence of several rhizosphere variables related to soil chemistry, microbial activity, microbial community and microbial stoichiometry, and evaluated the role of plant chemistry, plant root architecture and morphology in driving these soil and microbial variables. We hypothesized that (i) the rhizospheres of the plant species differ in their susceptibility to decomposition after C addition and this response would be proportional to the response of the microbial communities; (ii) among all soil and microbial factors, soil stoichiometry would be the best predictor of decomposition, particularly in the case of SOM because its greater diversity of compounds would impose more nutrient limitations; specifically, we hypothesize that the rhizospheres with low relative abundance of N and high relative abundance of P would show positive priming; and (iii) among plant traits, plant stoichiometry would be the main driver of decomposition by changing soil stoichiometry, particularly, plant N/P would be positively related to N/P in soil and priming of SOM would increase with lower plant N/P.