Accelerated microbial turnover but constant growth efficiency with warming in soil

Rising temperatures are expected to reduce global soil carbon (C) stocks, driving a positive feedback to climate change1–3. However, themechanisms underlying this prediction are not well understood, including how temperature a ects microbial enzyme kinetics, growth e ciency (MGE), and turnover4,5. Here, in a laboratory study, we show thatmicrobial turnover accelerates with warming and, along with enzyme kinetics, determines the response of microbial respiration to temperature change. In contrast, MGE, which is generally thought to decline with warming6–8, showed no temperature sensitivity. A microbial-enzyme model suggests that such temperature sensitive microbial turnover would promote soil C accumulation with warming, in contrast to reduced soil C predicted by traditional biogeochemical models. Furthermore, the e ect of increased microbial turnover di ers from the e ects of reduced MGE, causing larger increases in soil C stocks. Our results demonstrate that the response of soil C to warming is a ected by changes inmicrobial turnover. This control should be included in the next generation of models to improve prediction of soil C feedbacks to warming. Many global C cycling models predict reductions in soil C with climate warming2. More recent models that include microbial controls over decomposition suggest a wider range of potential responses5. These models reproduce present soil C stocks more accurately than models that do not incorporate microbial dynamics9, but their ability to predict soil C responses to climate change is hampered by uncertainty in the temperature sensitivity of microbial processes4. There is an active debate in recent literature about which microbial mechanisms should be represented in soil C cycling models7,10–13. Warming increases kinetic energy, accelerating enzymerequiring reactions1 and stimulating C consumption by soil microbes. Microbial C consumption and respiration, the largest flux of C out of soil, is significantly affected by both the size and functioning of the soil microbial community3,6. Warming may change the soil microbial biomass carbon (MBC) concentration and activities through two potentially concurrent mechanisms. First, warming can decrease MGE, which is the proportion of substrate C that is used for microbial growth relative to the total amount of substrate C consumed7,14. Higher temperatures are generally expected to reduce MGE, as warming limits microbial growth by increasing the energy cost of maintaining existing biomass8. However, responses of MGE in soil microbial communities are equivocal, with studies reporting decreased MGE with temperature increase15,16, no change14, or a variable response based on substrate type17. It is unclear to what extent this variability is caused by the methods and procedures used for measuring MGE in soil8. Second, warming can affect microbial turnover rates18. Microbial turnover is determined by microbial cell production and cell death, which are processes that may be affected by temperature. Dead cells may either adhere to soil particles and join the pool of soil organic carbon (SOC) or bemetabolized by livingmicrobes19. Consequently accelerated turnover can increase respiration per unit of MBC even when MGE remains the same20. However, most studies of MGE responses to warming do not account for respiration and cell death that result from turnover15–17. We determined the temperature sensitivity ofMGE and turnover to examine the mechanisms controlling the response of soil C cycling processes to warming. We measured MGE and microbial turnover in mineral soil and organic soil from the Marcell Experimental Forest, Minnesota, after a one-week incubation at 5, 10, 15, or 20 C. We used metabolic tracer probing to determine MGE (ref. 14). In this method, MGE is calculated from the fate of individual C-atoms in glucose and pyruvate using a metabolic model. Unlike other methods15–17, the metabolic tracer probing method determines MGE measurement over a very short period of time (1 h or less at room temperature), making it less sensitive to microbial turnover. We combined MGE measurements with measurements of microbial respiration and MBC to calculate microbial turnover rates. We found that MGE was not sensitive to temperature (Fig. 1). Mean MGE was 0.72 (±0.01 s.e.m., n= 22) in mineral soil and 0.71 (±0.01 s.e.m., n= 21) in organic soil. Across all temperature treatments and replicates, MGE ranged between 0.67 and 0.75. These values for MGE are high relative to the average values observed in soils and other ecosystems7,8,21. It is also higher than 0.6, an average maximum MGE value for pure culture studies8,22 (for further discussion on theoretical thermodynamic constraints of MGE, see Supplementary Note). This high value suggests that the active microbial community functions at high biochemical efficiency and microorganisms with relatively high maintenance costs contribute little to the total activity. High efficiency values may also indicate additional energy sources (for example, from oxalate or formate23), or direct incorporation of large amounts of cellular compounds, such as amino acids14. However, what little information is available suggests that these effects will only be slightly affected by temperature17. Microbial growth efficiency is generally expected to decline as a result of increased microbial maintenance costs at higher temperatures6,7,24. This effect of temperature onmaintenance energy