Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure
Introduction
The decomposition of soil organic matter (SOM), approximated by soil heterotrophic respiration in most publications, is affected by numerous factors such as temperature, moisture, vegetation and soil type (Jenkinson et al., 1991, Raich and Schlesinger, 1992, Lloyd and Taylor, 1994, Kirschbaum, 1995, Shen et al., 2009, Schmidt et al., 2011). In the majority of studies, temperature is reported to enhance SOM decomposition rate quasi-exponentially, and therefore an exponential index of temperature sensitivity, termed Q10, is widely used to describe the thermal response of SOM decomposition. This Q10 reflects the synoptic response of SOM decomposition to temperature and is assumed constant previously (∼2.0; e.g., Jenkinson et al., 1991). Although the decomposition rate increases exponentially with increasing temperature in the short-term, warming does not necessarily increase SOM decomposition to a similar extent. Indeed, SOM decomposition has been frequently observed to acclimate in response to warming (Hartley et al., 2007, Allison et al., 2010, Bradford et al., 2010, Crowther and Bradford, 2013), yielding lower-than-expected decomposition rates under prolonged warmer conditions. Such thermal acclimation may thus render current predictions of future carbon cycling that do not take into account thermal acclimation uncertain.
Although thermal acclimation of SOM decomposition is often observed (Dieleman et al., 2012), the underlying mechanisms are still a matter of scientific debate (Luo, 2007, Hartley et al., 2008, Vicca et al., 2009, Bradford et al., 2010, Conant et al., 2011, Crowther and Bradford, 2013), and it remains particularly unclear how warming affects the Q10 of SOM decomposition (Bradford et al., 2008). On the one hand, substrate depletion due to faster microbial consumption under warmer conditions may reduce the temperature sensitivity of SOM decomposition at higher temperatures (Eliasson et al., 2005, Hartley et al., 2007, Hartley et al., 2008), especially over long timescales. On the other hand, it has also been suggested that the temperature sensitivity of SOM decomposition increases with increasing molecular complexity of substrates (Knorr et al., 2005, Davidson and Janssens, 2006, Hartley and Ineson, 2008, Craine et al., 2010, Conant et al., 2011). A rapid depletion of labile substrate and an increase of recalcitrant substrate during the initial stages of experimental warming (Hartley et al., 2007, Hartley et al., 2008, Ziegler et al., 2013), without any microbial adjustment, could therefore lead to increased temperature sensitivity of SOM decomposition by warming, as observed by Rinnan et al. (2009). These contrasting observations indicate that alterations in the temperature sensitivity of SOM decomposition with warming cannot be fully explained by substrate depletion.
Alternatively, reduced temperature sensitivity at higher temperatures may also result from shifts in the composition of soil microbial communities (Luo et al., 2001, Zhang et al., 2005, Hartley et al., 2007, Luo, 2007, Malcolm et al., 2008, Vicca et al., 2009, Conant et al., 2011, Crowther et al., 2012). Although several authors have reported that soil microorganisms do not experience detectable shifts in community composition after minor experimental warming (Biasi et al., 2008, Schindlbacher et al., 2011, Kuffner et al., 2012), shifts in soil microbial communities, in addition to the frequently observed reduction in microbial biomass induced by increasing temperature (Bradford et al., 2008, Frey et al., 2008, Rousk et al., 2012, Weedon et al., 2012), have also been documented. For instance, Zogg et al. (1997) showed that within 16 weeks, the soil microbial communities shifted significantly in composition at higher temperature. Using δ13CO2 and phospholipid fatty acids (PLFAs) analyses, Biasi et al. (2005) also found that the soil microbial community composition changed with rising temperature. Altered microbial communities may exhibit different temperature dependencies (Frey et al., 2008, Malcolm et al., 2008, Balser and Wixon, 2009), and consequently result in the observed thermal acclimation of SOM decomposition (Luo, 2007). Although it has been shown that soil microbial community composition can shift with temperature, there is still a lack of direct experimental evidence relating the thermal acclimation of SOM decomposition to shifts in soil microbial community structure and functioning (Conant et al., 2011).
Global temperatures are rising and this trend is likely to continue with the continuing increase of greenhouse gas concentrations in the atmosphere (IPCC, 2007). Increasing temperature could result in a positive feedback on the SOM decomposition, and therefore tend to upset the dynamic equilibrium of the terrestrial carbon cycling (Luo and Weng, 2011). However, thermal acclimation of SOM decomposition may reduce this positive feedback effect and thus yield lower carbon emission from soils than what has been predicted previously (Allison et al., 2010).
In this study, we conducted a laboratory incubation experiment to test the role of microbial community structure and functioning in the thermal acclimation of SOM decomposition. The experiment contained two periods: a 72-day pre-incubation period during which soil samples were incubated at temperatures of 5, 15, and 25 °C, and an 11-day incubation period during which half of the samples from each pre-incubation temperature were incubated at 5 °C and the other half at 25 °C. By comparing the temperature sensitivity of SOM decomposition corresponding to the three pre-incubation temperatures, we aimed to test the hypothesis that the temperature sensitivity would be lower for soils that had experienced high pre-incubation temperatures than for soils that had experienced low pre-incubation temperatures (i.e., thermal acclimation would occur as observed in many previous studies). By analyzing soil microbial community PLFAs, microbial biomass carbon, dissolved organic carbon, and enzyme activities related to SOM decomposition at the end of both periods, we also aimed to analyze the relative contributions of these factors to the thermal acclimation of SOM decomposition.
Section snippets
Artificial soil mixture
We composed an artificial soil for incubation by mixing clay (15%), sand (60%), and organic matter (25%) to ensure the homogeneity of the samples incubated. Artificial soils can be used in laboratory incubations to eliminate the confounding effects of factors other than the factor of interest (Guenet et al., 2011), although it differs from natural soils in its aggregate structure and resultant sorption-adsorption dynamics of substrates. By using the artificial soil, we also aimed to minimize
Changes in DOC, MBC and SOM decomposition rates
No significant differences were found in TOC, TN or the C/N ratio among the pre-incubation temperatures at the end of the 72-day pre-incubation (P > 0.05). In general, very small differences in DOC concentrations were observed in our experiment (Figs. 1a and b and 2b). At the end of the incubation during which four samples of each pre-incubation temperature were exposed to 5 °C and four others to 25 °C, the DOC concentration was significantly higher in samples incubated at 25 °C than those
Temperature-induced acclimation of SOM decomposition
Thermal acclimation of SOM decomposition can be categorized into three types (Bradford et al., 2008). Type I adaptation refers to lower decomposition rates (R) as a function of decreased Q10 by warming, type II adaptation to lower R at all measurement temperatures (changes in Q10 are not necessary), and type III adaptation to lower R only at intermediate temperatures owing to the modified optimum temperature for R (Bradford et al., 2008). The observed thermal acclimation of SOM decomposition (
Conclusion
The thermal acclimation of SOM decomposition occurred with a decrease in the temperature sensitivity of SOM decomposition within weeks. Soil microbial communities can also adapt to altered temperatures very rapidly, with those pre-incubated at high temperatures being less responsive to the temperature shifts in the subsequent incubation period. Although other microbial properties such as MBC and enzyme activities were also altered by the temperature changes, the down-regulation of temperature
Acknowledgments
We thank Nadine Calluy, Marc Wellens and Anne Cools for their helps on lab analyses, Arie Weeren and Dr. Guojun Lin for helping with statistical analyses. Two anonymous reviewers made constructive comments on the earlier versions of the manuscript. The National Natural Science Foundation of China (NSFC-31290222, 31130011) and the Natural Science Foundation of Guangdong province (S2012020011084) are acknowledged to fund HW's visiting study in the University of Antwerp. BG is a visiting
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