Mineral-Associated Soil Carbon is Resistant to Drought but Sensitive to Legumes and Microbial Biomass in an Australian Grassland
Drought is predicted to increase in many areas of the world with consequences for soil carbon (C) dynamics. Plant litter, root exudates and microbial biomass can be used as C substrates to form organo-mineral complexes. Drought effects on plants and microbes could potentially compromise these relative stable soil C pools, by reducing plant C inputs and/or microbial activity. We conducted a 2-year drought experiment using rainout shelters in a semi-natural grassland. We measured aboveground biomass and C and nitrogen (N) in particulate organic matter (Pom), the organo-mineral fraction (Omin), and microbial biomass within the first 15 cm of soil. Aboveground plant biomass was reduced by 50% under drought in both years, but only the dominant C4 grasses were significantly affected. Soil C pools were not affected by drought, but were significantly higher in the relatively wet second year compared to the first year. Omin-C was positively related to microbial C during the first year, and positively related to clay and silt content in the second year. Increases in Omin-C in the second year were explained by increases in legume biomass and its effect on Pom-N and microbial biomass N (MBN) through structural equation modeling. In conclusion, soil C pools were unaffected by the drought treatment. Drought resistant legumes enhanced formation of organo-mineral complexes through increasing Pom-N and MBN. Our findings also indicate the importance of microbes for the formation of Omin-C as long as soil minerals have not reached their maximum capacity to bind with C (that is, saturation).
Grassland ecosystems represent between 30 and 40% of the global land surface area, storing organic C in amounts comparable to forest ecosystems (White and others 2000). Environmental stresses can cause loss of C from terrestrial ecosystems, thereby increasing the atmospheric CO2 concentration and global warming potential. Foremost, water stress (that is, drought) can turn grassland ecosystems into C sources (Zhang and others 2010, 2011; Hoover and Rogers 2016), specifically by reducing net primary production (NPP; that is, C input to soil). Soil organic matter (SOM) decomposition (that is, C outputs from soil) is often maintained (Hoover and Rogers 2016), although, the response of SOM decomposition to drought will depend on drought intensity and timing of rewetting periods (Bloor and Bardgett 2012). Because SOM is made of C pools with different inherent levels of turnover and stability (Six and others 2002), understanding the C dynamics of different pools in response to environmental stress is critical to assess impacts of grassland ecosystems on CO2 release to the atmosphere. Therefore, understanding drought effects on C pools is particularly important for predicting climate change feedbacks in grassland ecosystems and possible legacy effects of post-drought periods.
Particulate organic matter (composed of plant litter and organic amendments in agricultural systems) is considered to have faster turnover times compared to organic matter bound to the soil mineral fraction (organo-mineral fraction) and that is considered more resistant to microbial mineralization (Cotrufo and others 2013; Feng and others 2014; Ahrens and others 2015). This mineral-associated pool of C is primarily determined by soil mineralogy as well as by plant and microbial inputs (Kögel-Knabner and others 2008; Cotrufo and others 2013). Organo-mineral C (Omin-C) is formed upon binding of organic matter (OM) to clay and silt (Mikutta and Kaiser 2011). Recently, it was suggested that the main source of C binding to the mineral fraction comes from plant-derived labile compounds (Cotrufo and others 2015). These labile compounds (either leachates from particulate organic matter decomposition or root exudates) can directly bind to the mineral fraction or can be incorporated into microbial biomass before it is bound to the mineral fraction (Castellano and others 2015). Indeed, microbial biomass was identified as a primary constituent of the organic matter in organo-mineral complexes (Solomon and others 2012; Kögel-Knabner 2017). The microbial pathway is supported by our previous experiment where we showed that plant-derived C in microbial biomass had a positive relationship with plant-derived C in the organo-mineral complexes (Canarini and Dijkstra 2015). Moreover, it has been shown that the efficiency at which microbes utilize plant compounds is positively correlated to the amount of soil C formed (Bradford and others 2013).
In a recent framework, Cotrufo and others (2013) suggested that plant inputs of low C/N ratio are preferentially utilized by microbes and ultimately incorporated into organo-mineral complexes (the Microbial Efficiency-Matrix Stabilization (MEMS) framework).Variation in the C/N ratio of plant community inputs associated with different plant functional groups (Aerts and Chapin III 1999; Kerkhoff and others 2006; Hobbie 2015; Canarini and others 2016a) could therefore result in differences in both the microbial activity (Enríquez and others 1993) and soil C storage (De Deyn and others 2008). Indeed, the presence of specific plant functional traits, such as biological N-fixation (that is, legumes), is recognized as an important driver of C accumulation in grasslands (Fornara and Tilman 2008; De Deyn and others 2009, 2011) and cropland soils (Kallenbach and others 2015; Frasier and others 2016). At the same time, plants have the ability to cause desorption of organic material bound to minerals through release of organic acids (Keiluweit and others 2015). All this highlights the control of plants and the plant community over soil C pools.
Drought effects on plants, microbes and their interactions could have indirect negative outcomes for organo-mineral complexes. However, information about drought effects on plant–microbe control over organo-mineral C is limited. Water availability can greatly impact NPP and shape the plant community composition (Yang and others 2011; Hoover and others 2015), depending on the stress intensity. For example, dominant species are often more sensitive to drought than subordinate species in grassland communities and decrease in biomass during water stress (Mariotte and others 2013). Because the plant community is an important player controlling soil processes (Díaz and Cabido 2001; Fornara and Tilman 2008; De Deyn and others 2009), drought-induced changes in plant community composition and structure could have significant impacts on C storage. Drought can also reduce the flux of C from root exudates (Kuzyakov and Gavrichkova 2010), which greatly contributes to microbial activity in soil (Shahzad and others 2015). At the same time, water stress limits the diffusion of substrates and slows down biological processes, directly reducing soil microbial activity (Schimel and others 2007), although rewetting periods following drought can enhance decomposition, thereby offsetting the reduction in decomposition during the drought period (Borken and Matzner 2009).
The aim of this study was to investigate drought effects on two soil C pools of different inherent turnover and stability (particulate organic C, or Pom-C, and Omin-C) and whether the C content of these pools was related to the abundance of specific plant functional groups, microbial biomass and soil nutrients. A drought manipulation (that is, reduced precipitation) experiment was undertaken in an Australian grassland using rainout shelters and compared to an ambient precipitation control. Previously, we found that one year of drought manipulation had no effect on Omin-C, but that this pool was positively related to fungi in the top 5 cm of the soil and to gram-negative bacteria deeper in the soil profile (5–15 cm; Canarini and others 2016b). Here, we assess drought effects on Omin-C through changes in plant community structure and microbial biomass spanning 2 years of water manipulation. We hypothesized that:
drought would reduce plant biomass and C inputs, thereby decreasing particulate organic C (Pom-C), microbial biomass C and to a lesser extent Omin-C;
microbial biomass C would relate positively to Omin-C because microbial biomass is the primary substrate for the formation of this pool;
drought effects on Omin-C formation would be mediated by plant functional group responses to drought.