Susceptibility of new soil organic carbon to mineralization during dry-wet cycling in soils from contrasting ends of a precipitation gradient
Introduction
The persistence of soil organic carbon (SOC) depends on the physicochemical and biological factors that affect the probability and rate of mineralization (Schmidt et al., 2011; Dynarski et al., 2020; Lehmann et al., 2020). Interrelated ecosystem properties, such as climate and geochemistry, co-govern SOC susceptibility to microbial mineralization, enabling some soils to maintain higher concentrations of SOC than others (Schmidt et al., 2011; Rasmussen et al., 2018; Hall et al., 2020; Abramoff et al., 2021; Heckman et al., 2022). Precipitation patterns regulate the bell-shaped relationship between soil moisture and decomposition rates that drive soil carbon cycling (Schuur and Matson, 2001; Derner and Schuman, 2007; Meier and Leuschner, 2010; Berthrong et al., 2012; Chang et al., 2014). While high levels of precipitation may cause SOC to accumulate, due to oxygen-limitation, higher levels of precipitation also accelerate leaching and cause the loss of mineral phases that could otherwise stabilize soil organic matter (Torn et al., 1997; Thompson et al., 2011; Kleber et al., 2015; Kramer and Chadwick, 2018; Possinger et al., 2020). Feedbacks between precipitation, soil geochemistry, and microbial activity complicate the dynamics of SOC cycling, creating spatiotemporal variation in SOC persistence that is difficult to predict.
Natural precipitation gradients provide opportunities to contrast the relative influences of climate-driven soil properties on SOC persistence. Previous research at the Kohala Mountain transect, Hawai'i, demonstrated that iron and SOC concentrations co-governed the long-term persistence of SOC (Grant et al., 2022). At Kohala Mountain, subsoil OM tended to co-localize with Fe-oxides on soil particles where rainfall was low (40% of the OM in the observed areas) and far less (5% of OM) where rainfall had leached iron from soils (Inagaki et al., 2020). The age of bulk SOC was also much younger in iron-depleted soils relative to non-leached soils at equivalent depth, suggesting a link between iron minerology and the rate of SOC turnover. Yet, soils from higher rainfall regions had accumulated substantially more SOC, ostensibly due to more frequent water saturation and reduced rates of decomposition (Grant et al., 2022). It remains unclear how these contrasting soil properties influence the cycling of new OM inputs. Here, we used soils sourced from the Kohala transect to probe the relative importance mineralogy, SOC content, and microbial activity play in determining the susceptibility of new organic carbon inputs to mineralization.
Several biological, chemical, and thermal measures of the potential susceptibility of SOC to mineralization are used to estimate its turnover rate (Paul et al., 2006; Plante et al., 2011; Gregorich et al., 2015). Soil respiration provides the most direct measure of SOC susceptibility, but conventional respiration measurements do not capture important dynamics affecting OM turnover in soil (Six et al., 2004; Bernal et al., 2016). Soil drying and rewetting stimulates respiration, eliciting a phenomenon known as the ‘Birch Effect.’ Although we lack a complete mechanistic understanding of the Birch effect, major drivers include soil processes, such as SOC remobilization, organo-mineral bond dissolution, aggregate dispersion, induced mortality and biomass turnover, and the reintroduction of occluded OM and microbes (Unger et al., 2010; Evans et al., 2016; Fraser et al., 2016). Here, we used dry-wet cycling, and the resulting Birch effect, to assess SOC susceptibility to mineralization in a manner aligned with environmental exposures in mesic systems.
The efficiency by which organic carbon is converted, or sequentially cycled, into microbial biomass is an important aspect of soil OM formation that modulates the persistence of SOC (Miltner et al., 2012; Cotrufo et al., 2013; Liang et al., 2017; Woolf and Lehmann, 2019). Substrate use efficiency (SUE) can be estimated for individual carbon sources and is measured in biomass produced per unit substrate consumed (Cbiomass/Cbiomass + Crespired). SUE is correlated with soil moisture and organic matter quality (Manzoni et al., 2012, 2018; Öquist et al., 2017; Butcher et al., 2020), which differ across precipitation gradients (Saiz et al., 2012; Campo and Merino, 2016). Importantly, SUE can be used to approximate the efficiency of individual populations, whole communities, or as an integrated measure of the overarching influences of ecosystem properties (SUEE) that affect carbon cycling over longer timescales, beyond the lifespan of an individual organism (Geyer et al., 2016). Here, we use SUEE as a measure of the efficiency of microbial metabolism under environmental conditions that reflect ecosystem properties, such as soil mineralogy and resource availability.
Understanding the factors governing SOC persistence is a fundamental challenge for soil science. In this study, we investigated the susceptibility of new SO13C to mineralization following a months-long incubation and exposure to dry-wet cycling. We compared two soils (Andosols) that developed under contrasting precipitation regimes on Hawai'i. Soil from the lower rainfall region (‘lowrain’) had lower existing SOC and higher total iron and ferrihydrite concentrations than soil from the higher rainfall region (‘highrain’). Soils were incubated with either 13C-labeled glucose (soluble) or cellulose (insoluble) to probe the effect of substrate bioavailability on microbial metabolism. Our objective was to evaluate several factors that influence SOC susceptibility including: (i) mineralogy, with a focus on iron minerals, (ii) SOC content, and (iii) microbial SUEE. We hypothesized that iron concentrations would negatively correlate with SOC susceptibility via organo-mineral interactions (Huang and Hall, 2017; Rasmussen et al., 2018; Inagaki et al., 2020). We also hypothesized that the insoluble carbohydrate (cellulose) would be cycled at a lower SUEE than glucose, as in Öquist et al. (2017), because of the additional energy costs of enzymes required in polymer degradation (Manzoni et al., 2012). We employed high-resolution techniques (NanoSIMS) to characterize fine-scale patterns underlying differences in mineral- and organo-associated SOC. These methods allowed us to track the fate of substrate-derived carbon and to investigate the relative importance of mineral versus microbial properties affecting the susceptibility of SOC to mineralization.
Section snippets
Soil collection and characterization
Representative soil samples were collected from two sites on opposite ends (‘lowrain’ and ‘highrain’) of a precipitation gradient located within the Pu'u Eke forest reserve (20.0783 N, 155.7289 W) on the Kohala volcano (Island of Hawai'i, USA). Soils within each site possess similar properties and have been studied extensively to probe relationships among soil properties and carbon cycling (Chadwick et al., 2003; Grant et al., 2019, Grant et al., 2022; Inagaki et al., 2020). Mean annual
Soil mineralogy and iron composition
According to XRD, both the highrain and lowrain soils were a mixture of quartz (the dominant crystalline mineral phase), hematite, maghemite, ulvospinel, ilmenite, anorthite and amorphous or poorly crystalline minerals of varying composition (Fig. S2). Lowrain soil had a higher proportion of poorly crystalline minerals and broad spectral features concurring with XRD spectra of pure ferrihydrite (Kukkadapu et al., 2003), with interference from amorphous aluminosilicate minerals typical of
Discussion
Soils with differing edaphic properties (iron mineralogy and total SOC) were selected to evaluate the susceptibility of newly formed SO13C to microbial activity in a soil microcosm experiment. Sourced from contrasting ends of a natural precipitation gradient, these soils capture differences in pedological development, but were not intended to assess variation at the ecosystem scale or by depth. Soluble (13C-glucose) and insoluble (13C-cellulose) substrate was added to each soil and
Conclusions
We characterized the relationships between SOC susceptibility to mineralization during dry-wet cycling and climate-driven changes in soil physicochemical and biological properties using two soils from contrasting ends of a precipitation gradient. SO13C derived from the microbial processing of 13C-substrates was more stable in soil from the low rainfall region, where substrates were more likely to be converted into microbial biomass and associated with mineral surfaces (Fig. 5). We attribute
Author contributions
RCW contributed to the overall study design, specifically the susceptibility assay, and performed data analysis, research, and writing. LL contributed to the overall study design, measured SUE, performed data analysis, and made major contributions to writing. TMW contributed to the overall study design, coordinated experiments, performed data analysis, and made major contributions to research and writing. SAS performed NanoSIMS imaging and data analysis and contributed to writing. TMI performed
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the U.S. Department of Energy (DOE) Office of Biological & Environmental Research Genomic Science Program under award number DE-SC0016364. We acknowledge the support of Ingrid Kögel-Knabner and the Technical University Munich – Institute for Advanced Study, funded by the German Excellence Initiative (and the EU Seventh Framework Programme under grant agreement n° 291763). We thank the German Research Foundation (DFG) for the financial support for the NanoSIMS
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