Accelerated microbial turnover but constant growth e ciency with warming in soil

Rising temperatures are expected to reduce global soil carbon 1 (C) stocks, driving a positive feedback to climate change1–3. 2 However, the mechanisms underlying this prediction are not 3 well understood, including how temperature a ects microbial 4 enzyme kinetics, growth e ciency (MGE), and turnover4,5. 5 Here, in a laboratory study, we show that microbial turnover 6 accelerates with warming and, along with enzyme kinetics, 7 determines the response of microbial respiration to tempera8 ture change. In contrast, MGE, which is generally thought to 9 decline with warming6–8, showed no temperature sensitivity. 10 Using a microbial-enzyme model, we show that temperature11 sensitive microbial turnover promotes soil C accumulation 12 with warming, in contrast to reduced soil C predicted by 13 traditional biogeochemical models. Furthermore, the e ect 14 of increased microbial turnover di ers from the e ects of 15 reduced MGE, causing larger increases in soil C stocks. Our 16 results demonstrate that the response of soil C to warming 17 is a ected by changes in microbial turnover. This control 18 should be included in the next generation of models to improve 19 prediction of soil C feedbacks to warming. 20 Many global C cycling models predict reductions in soil 21 C with climate warming2. More recent models that include 22 microbial controls over decomposition suggest a wider range of 23 potential responses5. These models reproduce present soil C stocks 24 more accurately than models that do not incorporate microbial 25 dynamics9, but their ability to predict soil C responses to climate 26 change is hampered by uncertainty in the temperature sensitivity of 27 microbial processes4. There is an active debate in recent literature 28 about which microbial mechanisms should be represented in soil C 29 cycling models7,10–13. 30 Warming increases kinetic energy, accelerating enzyme31 requiring reactions1 and stimulating C consumption by soil 32 microbes. Microbial C consumption and respiration, the largest 33 flux of C out of soil, is significantly affected by both the size 34 and functioning of the soil microbial community3,6. Warming may 35 change the soil microbial biomass carbon (MBC) concentration and 36 activities through two potentially concurrent mechanisms. First, 37 warming can decrease MGE, which is the proportion of substrate 38 C that is used for microbial growth relative to the total amount 39 of substrate C consumed7,14. Higher temperatures are generally 40 expected to reduce MGE, as warming limits microbial growth 41 by increasing the energy cost of maintaining existing biomass8. 42 However, responses of MGE in soil microbial communities are 43 equivocal, with studies reporting decreased MGE with temperature 44 increase15,16, no change14, or a variable response based on substrate 45 type17. It is unclear to what extent this variability is caused by the 46 methods and procedures used for measuring MGE in soil8. Second, 47 warming can affect microbial turnover rates18. Microbial turnover 48 is determined by microbial cell production and cell death, which 49 are processes that may be affected by temperature. Dead cells 50 may either adhere to soil particles and join the pool of soil organic 51 carbon (SOC) or bemetabolized by livingmicrobes19. Consequently 52 accelerated turnover can increase respiration per unit of MBC even 53 when MGE remains the same20. However, most studies of MGE 54 responses to warming do not account for the respiration and cell 55 death that result from turnover15–17. 56 We determined the temperature sensitivity ofMGE and turnover 57 to examine the mechanisms controlling the response of soil C 58 cycling processes to warming. We measured MGE and microbial 59 turnover in mineral soil and organic soil from the Marcell 60 Experimental Forest, Minnesota, after a one-week incubation at 5, 61 10, 15, or 20 C. We used metabolic tracer probing to determine 62 MGE (ref. 14). Q.1 In this method, MGE is calculated from the 63 fate of individual C-atoms in glucose and pyruvate. Unlike other 64 methods15–17, the metabolic tracer probing method determines 65 an MGE measurement almost entirely unaffected by microbial 66 turnover because it can be done very quickly (1 h or less at room 67 temperature) and calculates MGE based on metabolic modelling. 68 We combinedMGEmeasurements withmeasurements of microbial 69 respiration and MBC to calculate microbial turnover rates. 70 We found that MGE was not sensitive to temperature (Fig. 1). 71 Mean MGE was 0.72 (±0.01 s.e.m., n= 22) in mineral soil and 72 0.71 (±0.01 s.e.m., n= 21) in organic soil. Across all temperature 73 treatments and replicates, MGE ranged between 0.67 and 0.75. 74 These values for MGE are high relative to the average values 75 observed in soils and other ecosystems7,8,21. It is also higher than 76 0.6, an average maximum MGE value for pure culture studies8,22 77 (for further discussion on theoretical thermodynamic constraints 78 of MGE, see Supplementary Note). This high value suggests that 79 the active microbial community functions at high biochemical 80 efficiency and microorganisms with relatively high maintenance 81 costs contribute little to the total activity. High efficiency values may 82 also indicate additional energy sources (for example, from oxalate 83 or formate23), or direct incorporation of large amounts of cellular 84 compounds, such as amino acids14. However, what little information 85 is available suggests that these effects will be only slightly affected 86 by temperatures17. 87 Microbial growth efficiency is generally expected to decline 88 as a result of increased microbial maintenance costs at higher 89 temperatures6,7,24. This effect of temperature onmaintenance energy 90