Translocating subtropical forest soils to a warmer region alters microbial communities and increases the decomposition of mineral-associated organic carbon

https://doi.org/10.1016/j.soilbio.2020.107707Get rights and content

Highlights

  • Climate warming enhanced mineral-associated organic C decompaction.

  • Warming reduced bacterial biomass and shifted microbial community composition.

  • Warming increased the relative abundance of fungi and the ratio of fungi to bacteria.

  • Warming increased oxidase and mass-specific oxidase activities.

Abstract

It is not clear how soil organic carbon (SOC) and its related microbial processes respond to climate warming in subtropical forest, which limits our ability to predict the response and feedback of such forests to future warming. Here, we translocated a forest microcosm from a high-elevation site to a low-elevation site (600 m–30 m a.s.l.) in a subtropical forest, to study the responses of SOC fractions, microbial communities and enzyme activities to increases in soil temperature (ca. 1.69 °C). Results showed that translocation to a warmer region significantly decreased the total SOC content by an average of 21.1% after three years of soil warming. Warming non-significantly decreased the particulate organic C (POC) and microbial C (MBC) content by 15.7% and 15.2%, respectively, and increased the light fraction organic C (LFOC) and dissolved organic C (DOC) content by 15.5% and 2.3%, respectively. By contrast, warming significantly decreased the <53 μm fraction organic C (N-POC, −15.3%) and heavy fraction organic C (HFOC, −14.8%) content. Warming significantly decreased the relative abundance of total bacteria (−2.7%), G+ bacteria (−6.1%), G bacteria (−6.6%) and actinomycetes (−10.8%), but increased the relative abundance of fungi (+22%). The oxidase and mass-specific oxidase activities were significantly increased by 32–70% in the warming soils. The decline in the N-POC was highly correlated to the increases in the relative abundance of fungi, the ratio of fungal to bacterial biomass (F:B), oxidase and mass-specific oxidase activities. Our results suggest that climate warming may increase the potential for fungal decomposition of mineral-associated organic C by increasing oxidase activities, leading to greater C losses in the subtropical forest than previously estimated.

Introduction

Tropical and subtropical forests account for approximately 30% of all soil carbon (C) in terrestrial ecosystems (Jobbágy and Jackson, 2000; Crowther et al., 2019). Given the large amounts of soil C that are stored and cycled in forests of the tropic regions (Beer et al., 2010), relatively small changes in the soil organic C (SOC) pool in such forests may affect the global C balance (Zhou et al., 2013; Cavaleri et al., 2015). Many studies over the past two decades have indicated that warming generally enhances SOC decomposition, but these field warming experiments were mainly located at high latitudes or high elevations (Lu et al., 2013; Cheng et al., 2017; Melillo et al., 2017). At lower latitudes, subtropical forests which actively accumulate C in large enough quantities (Yu et al., 2014) may experience significant increases in surface temperatures in the coming decades (Zhou et al., 2011, Zhou et al., 2011). However, our knowledge of the sensitivity of the SOC in the subtropical forest response to climate warming is very limited (Cavaleri et al., 2015; Crowther et al., 2016; Li et al., 2018; Wang et al., 2019). Therefore, investigating how SOC in low-latitude forests respond to climate warming is crucial for our understanding of future global-scale climate change and biogeochemical cycling.

Soil organic matter is a continuum of progressively decomposing organic compounds (Lehmann and Kleber, 2015). The decomposition and turnover of SOC is jointly affected by the ability of decomposers to access SOC and the degree to which SOC are protected from decomposition by soil minerals and aggregates (Schmidt et al., 2011; Lehmann and Kleber, 2015). Fractionating SOC into particulate fractions (organic fragments) and mineral-associated fractions based on their bio-accessibility may provide new insight into the turnover of the SOC continuum under global changes (Cotrufo et al., 2015; Lehmann and Kleber, 2015; Gentsch et al., 2018). For example, the light fraction organic C (LFOC; < 1.7 g cm−3) and particulate size > 53 μm fraction organic C (POC) generally represent more readily accessible SOC fractions consisting mainly of decaying organic fragments and thus they theoretically turn over relatively fast (von Lützow et al., 2007; Wagai et al., 2013). By contrast, organic C in the heavy fraction (HFOC, > 1.7 g cm−3) and particulate size < 53 μm fraction (N-POC) are more microbially altered and rich in mineral-associated compounds (Gentsch et al., 2018; Karhu et al., 2019), thus theoretically have longer residence times than the particulate C (von Lützow et al., 2007).

However, evidence from the past two decades has indicated that the temperature sensitivity of particulate and mineral-associated organic C are highly inconsistent (Henry et al., 2005; Plante et al., 2010; Cheng et al., 2011; Benbi et al., 2014; Karhu et al., 2019; Zhang et al., 2019). For example, Song et al. (2012) found that 5-years warming decreased soil LFOC by 12% and did not affect HFOC content in a temperate steppe. While, Zhang et al. (2019) reported that the LFOC, HFOC and total SOC content were not changed after 5-years of infrared radiant warming. Benbi et al. (2014) suggested that the temperature sensitivity of particulate C was obviously higher than that of the mineral-associated organic C. In contrast, some other studies found that the temperature sensitivity of particulate C was similar or slightly higher than that of mineral-associated organic C (Schnecker et al., 2016; Karhu et al., 2019). Therefore, it is necessary to further study how global warming may affect the particulate and mineral-associated organic C fractions, especially in the tropical and subtropical regions where much less information is currently available. (Cavaleri et al., 2015; Crowther et al., 2016; Li et al., 2018).

Soil microorganisms are key components of belowground ecosystems and play important roles in C cycling (Allison et al., 2010; Crowther et al., 2019). Previous studies showed that warming greatly affects the composition of microbial communities (Pold et al., 2015; Xu et al., 2015; Fang et al., 2016; Li et al., 2018) and such changes are highly associated with alterations in microbial functions (Wang et al., 2012; Liu et al., 2017, Liu et al., 2017; Xiao et al., 2018). For example, the increase in fungal biomass relative to bacterial biomass in warmed soils (Li et al., 2018) leads to the microbes using more C as a resource for growth (Ziegler et al., 2013), which stimulates the decomposition of slower-turnover organic compounds (Carney et al., 2007; Cheng et al., 2017).

Enzymes that are secreted by microorganisms also play critical roles in SOC degradation (Nannipieri et al., 2012). Due to various extracellular enzymes are secreted by different microbial groups, changes in microbial community composition may affect the degradation of different C fractions (Sinsabaugh, 2010). For instance, most fungi mainly secrete oxidase that degrade phenolic compounds that are indicative of organic compounds with slower turnover times (Sinsabaugh, 2010; Wang et al., 2012; Tian and Shi, 2014). Investigating the temperature sensitivity of soil microbial communities and enzyme activities may provide a mechanistic link to alterations in soil C fractions in response to global warming (Wang et al., 2012; Ziegler et al., 2013; Cheng et al., 2017).

Currently, species are migrating to higher elevations and higher latitudes under the background of global warming (Chen et al., 2011). Conversely, translocating a microcosm ecosystem to lower altitudes or lower latitudes exposes the microcosm to a warmer climate (Luan et al., 2014; Fang et al., 2016; Nottingham et al., 2019). Unlike the infrared or cable heating manipulations, translocation experiment result in the air and soil being warmed under natural conditions. In May of 2012, we started a microcosm forest ecosystem translocation experiment from a high-elevation site to a low-elevation site in a typical, mature subtropical forest in the Dinghushan Biosphere Reserve (DBR) in South China. Our previous results indicated that translocating a subtropical model forest to a warmer region increases litter decomposition and soil respiration (Li et al., 2016; Liu et al., 2017, Liu et al., 2017). This present study aimed to explore how particulate and mineral-associated organic C respond to warming and its related microbial processes. We hypothesized that (1) the LFOC and POC will be preferentially decomposed in warming soils since they are more readily accessible to microbes, and thus the total SOC content would be decreased, (2) changes in organic C fractions would be correlated with the changes in the composition and function of soil microbial communities.

Section snippets

Study site

The study was conducted in the DBR (23°09′N–23°11′N, 112°30′E−112°33′E), which is a United Nations Educational, Scientific and Cultural Organization/Man and the Biosphere site in central Guangdong Province, South China. The reserve covers 1155 ha with a typical tropical monsoon climate and is located in a subtropical/tropical moist forest biota (Holdridge, 1967). The mean annual temperature is approximately 21.4 °C and the relative humidity averages 80% throughout the year. The mean annual

Soil temperature and moisture

Repeated ANOVAs showed that the downward translocation treatment led to a significant increase in soil temperature (Fig. 1). The average monthly soil temperature at 5 cm depth in the warmed soils was 1.69 °C higher (P < 0.001) than in the ambient soils (from June 2013 to June 2015). This difference in soil temperature was most evident in the dry season, with +1.97 °C observed in dry season (P < 0.001) and +1.44 °C in the wet season (P < 0.01). Soil moisture was not significantly affected by

Discussion

Through a comprehensive analysis of the effects of climate warming on soil C stocks using data collected from 49 field experiments, Crowther et al. (2016) showed that global warming may considerably increase C losses from soils, particularly in soil C-rich high-latitude ecosystems. Here, our results suggested that warming may also lead to considerable SOC losses in lower altitude forests.

In our study, three years of experimental warming significantly decreased topsoil SOC content by an average

Conclusions

In summary, short-term soil warming significantly reduced mineral-associated organic C by an average of 15%, contributing to the significant decline in total SOC content. Warming did not significantly affect the particulate C content. Warming significantly affected soil microbial communities in three aspects: decreasing microbial biomass (except for fungi), shifting community composition and changing functional activity of the communities. Warming decreased the relative abundance of total

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.

Acknowledgments

This study was funded by the National Natural Science Foundation of China (Grant Nos. 41977287, 41991285, and 31670487), the Science and Technology Programs of Guangzhou City (201903010021), Science and Technology Innovation Project of Guangdong Province Forestry (Grant No. 2019KJCX023), and the Guangdong Hundred, Thousand, and Ten Thousand Talents Program.

References (73)

  • M. von Lützow et al.

    SOM fractionation methods: relevance to functional pools and to stabilization mechanisms

    Soil Biology and Biochemistry

    (2007)
  • H. Wang et al.

    Contrasting responses of heterotrophic and root-dependent respiration to soil warming in a subtropical plantation

    Agricultural and Forest Meteorology

    (2017)
  • H. Wang et al.

    Experimental warming reduced topsoil carbon content and increased soil bacterial diversity in a subtropical planted forest

    Soil Biology and Biochemistry

    (2019)
  • W. Xiao et al.

    A meta-analysis of soil extracellular enzyme activities in response to global change

    Soil Biology and Biochemistry

    (2018)
  • G. Xu et al.

    Labile, recalcitrant, microbial carbon and nitrogen and the microbial community composition at two Abies faxoniana forest elevations under elevated temperatures

    Soil Biology and Biochemistry

    (2015)
  • S.E. Ziegler et al.

    Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils

    Soil Biology and Biochemistry

    (2013)
  • S.D. Allison et al.

    Soil-carbon response to warming depended on microbial physiology

    Nature Geoscience

    (2010)
  • C. Beer et al.

    Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate

    Science

    (2010)
  • D.A. Bossio et al.

    Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns

    Microbial Ecology

    (1998)
  • C.A. Cambardella et al.

    Particulate soil organic matter changes across a grassland cultivation sequence

    Soil Science Society of America Journal

    (1992)
  • K.M. Carney et al.

    Altered soil microbial community at elevated CO2 leads to loss of soil carbon

    Proceedings of the National Academy of Sciences

    (2007)
  • M.A. Cavaleri et al.

    Urgent need for warming experiments in tropical forests

    Global Change Biology

    (2015)
  • I.C. Chen et al.

    Rapid range shifts of species associated with high levels of climate warming

    Science

    (2011)
  • L. Cheng et al.

    Warming enhances old organic carbon decomposition through altering functional microbial communities

    The ISME Journal

    (2017)
  • X. Cheng et al.

    Soil organic matter dynamics in a North America tallgrass prairie after 9 yr of experimental warming

    Biogeosciences

    (2011)
  • R.T. Conant et al.

    Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance

    Ecology

    (2008)
  • M.F. Cotrufo et al.

    Soil organic matter formation from biochemical and physical pathways of litter mass loss

    Nature Geoscience

    (2015)
  • T.W. Crowther et al.

    Quantifying global soil carbon losses in response to warming

    Nature

    (2016)
  • T.W. Crowther et al.

    The global soil community and its influence on biogeochemistry

    Science

    (2019)
  • X. Fang et al.

    Increased litter input increases litter decomposition and soil respiration but has minor effects on soil organic carbon in subtropical forests

    Plant and Soil

    (2015)
  • X. Fang et al.

    Warming effects on biomass and composition of microbial communities and enzyme activities within soil aggregates in subtropical forest

    Biology and Fertility of Soils

    (2016)
  • A. Frostegård et al.

    The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil

    Biology and Fertility of Soils

    (1996)
  • N. Gentsch et al.

    Temperature response of permafrost soil carbon is attenuated by mineral protection

    Global Change Biology

    (2018)
  • J.D. Hemingway et al.

    Mineral protection regulates long-term global preservation of natural organic carbon

    Nature

    (2019)
  • H.A.L. Henry et al.

    Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland

    Global Change Biol.

    (2005)
  • L.R. Holdridge

    Life Zone Ecology

    (1967)
  • Cited by (0)

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