Sustained increase in soil respiration after nine years of warming in an alpine meadow on the Tibetan Plateau

Highlights

• Soil respiration was still increased after 9 years of warming.

• Microbial biomass only decreased at the 0–10 cm.

• Both the bacterial and fungal composition had no change.

• Abundance of Actinobacteria decreased at 20–30 and 30–50 cm, which negatively correlated with R_s.

Abstract

Soil microbes are key determinants of soil carbon (C) dynamics. The response of the soil microbial community to climate warming modulates the feedback between ecosystem C cycling and future climate change. We conducted a long-term manipulative warming (1.6 °C increase of the soil temperature at 5 cm) experiment to examine the soil respiration, microbial biomass, and community composition at an alpine meadow site on the Qinghai-Tibetan Plateau. After nine years of warming, soil respiration (3.5 μmol m² s⁻¹ in control in the growing season) increased in the warmed plots. In the early growing season, the increase in heterotrophic respiration (R_h) accounted for more than 90% of the increase in soil respiration. The warming effect gradually decreased during the mid and late growing season (46%). Microbial biomass C and nitrogen declined significantly in the 0–10 cm to the 30–50 cm layer. Warming did not significantly affect microbial biomass C and N in any soil depth layer. Metabolic activity of microbes in terms of R_h per unit microbial biomass C significantly increased by 66% in warmed plots. The bacterial and fungal community composition did not significantly change in the warmed plots. The relative abundance of Actinobacteria decreased at 20–30 cm and 30–50 cm soil depths, but that of Cercozoa increased in all four soil layers. The relative Actinobacteria abundance was negatively correlated with R_h and metabolic activity in the 10–20 and 20–30 cm layers. Our results indicate a decrease in Actinobacteria abundance, increases in metabolic activity, and no substrate limitation sustained the positive warming effect on soil respiration throughout the last 9 years. This implies that climate warming could trigger a substantial loss of soil C to the atmosphere in the alpine meadow on the Qinghai-Tibet Plateau.

Introduction

Soil respiration (R_s), the efflux of carbon dioxide from the microbial decomposition of soil organic matter (heterotrophic respiration, R_h) and root respiration, is an important component of terrestrial carbon (C) fluxes (Luo and Zhou, 2006). The magnitude and direction of the response of R_s to climate change determines the terrestrial C balance and is key in developing future climate projections (Cox et al., 2000, Melillo et al., 2002, Friedlingstein et al., 2006, Koven et al., 2011). Regions with colder climates are considerably more responsive to climate warming than warmer regions (Carey et al., 2016) because the magnitude of warming is stronger and cold regions store a huge amount of C in the soil, especially in permafrost regions (Liu and Chen, 2000, Liu et al., 2012, Biskaborn et al., 2019).

Although most warming experiments stimulated R_s in various ecosystems (Rustad et al., 2001, Carey et al., 2016), differences in R_s responses to short-term and long-term warming remain largely controversial and inconsistent (Luo et al., 2001, Reth et al., 2009, Melillo et al., 2011, Melillo et al., 2017, Metcalfe, 2017). The gradual decline in increased R_s from warming has been observed in field experiments (Wan and Luo, 2003, Knorr et al., 2005, Pold et al., 2017) and in a lab incubation experiment (Li et al., 2019). The decreased positive warming effect on R_s could be attributed to 1) changes in decomposable substrate availability (Wan and Luo, 2003), 2) changes in substrate quality due to shifts in plant community dominance (Classen et al., 2015), and 3) changes in the microbial community, corresponding functional genes, and the resilience/acclimation of the microbial community (Griffiths and Philippot, 2013, Crowther and Bradford, 2013, Cheng et al., 2017). However, a sustained stimulation of R_s after ten years of warming has also as well been observed, likely due to a lack of soil water limitation and enhanced microbial growth and activity (Reth et al., 2009).

The soil microbial community is an important link in ecosystem C and nitrogen cycling, thus changes in microbial community composition and physiological processes can modify ecosystem C and nitrogen processes (Allison et al., 2010). The soil microbial community may exhibit strong resilience, in that in the long-term it may return to pre-warming state after a short-term change in community composition or function in response to climate warming (Classen et al., 2015). The resilience of the soil microbial community occurs because 1) many fast growing microorganisms quickly recover after a disturbance, 2) physiologically flexible microbes can acclimate to the new abiotic conditions over time and return to their original abundance even if the relative abundance of some taxa decreased initially, and 3) if physiological adaptation is not possible, the rapid evolution (through mutations or horizontal gene exchange) may allow microbial taxa to adapt to new environmental conditions and recover from disturbance (Allison and Martiny, 2008, Classen et al., 2015). However, other studies also reported no difference between short and long-term warming on the microbial community (Wang et al., 2014, Romero-Olivares et al., 2017), which implies that the microbial communities can be resistant to warming.

The soil of the Qinghai-Tibetan Plateau (QTP) contains 2.5% of the world’s soil C pool (Liu et al., 2012), and is predicted to emit substantial amounts of C to the atmosphere under future warming scenarios (Crowther et al., 2016). The soil microbial community structure here was found to change in the short-term warming (Xiong et al., 2014a, Xiong et al., 2014b), but how soil microbes adapt to long-term warming and how long-term warming influences soil C decomposition needs to be further investigated. A previous warming experiment in the QTP found no thermal acclimation of R_s and reduced soil moisture (Peng et al., 2014a, Peng et al., 2014b, Peng et al., 2015). Although a warming-induced decline in soil moisture was observed to limit soil microbial activity in a montane meadow (Saleska et al., 1999), the relatively higher soil organic matter and soil water availability during the thawing of permafrost led us to hypothesize that the increase of R_s and R_h in an alpine meadow on the QTP is sustained. The adaptation of microbes to extreme environments makes the soil microbial community more resistant to climate disturbance (Contosta et al., 2015). Thus, we also hypothesized that the soil microbial community of the alpine meadow soil is resistant to long-term warming. The objectives of our study were to determine 1) whether the positive effect of climate warming on R_s and R_h declines after 9 years of artificial warming, 2) whether the microbial community was altered due to nine years of warming, and 3) how the microbial community composition response relates to changes in R_s and R_h in an alpine meadow of the permafrost area in the QTP.