Exponential growth of “snow molds” at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q 10 values (original) (raw)
Abstract
Numerous studies have demonstrated exceptionally high temperature sensitivity of the beneath-snow respiratory flux in cold-winter ecosystems. The most common, but still untested, explanation for this high sensitivity is a physical one based on the observation that water availability in soils increases exponentially as soils warm from −3 to 0°C. Here, we present evidence for a biological hypothesis to explain exponential kinetics and high Q 10 values as beneath-snow soils warm from −3 to 0°C during the early spring in a high-elevation subalpine forest. First, we show that some of the dominant organisms of the beneath-snow microbial community, “snow molds”, exhibit robust exponential growth at temperatures from −3 to −0.3°C. Second, Q 10 values based on growth rates across the temperature range of −2 to −0.3°C for these snow molds vary from 22 to 330. Third, we derive an analytical equation that combines the relative contributions of microbial growth and microbial metabolism to the temperature sensitivity of respiration. Finally, we use this equation to show that with only moderate snow mold growth (several generations), the combined sensitivities of growth and metabolism to small changes in beneath-snow soil temperature, create a double exponential in the Q 10 function that may explain the extremely high (~1 × 106) Q 10 values observed in past studies. Our biological explanation for high Q 10 levels is supported by several independent studies that have demonstrated build up of microbial biomass under the snow as temperatures warm from −2 to 0°C.
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References
- Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biol Biochem 10:215–221. doi:10.1016/0038-0717(78)90099-8
Article Google Scholar - Bergero R, Ghirlanda M, Varese GC, Intili D, Luppi AM (1999) Psychro-oligotrophic fungi from Arctic soils of Franz Joseph Land. Polar Biol 21:361–368. doi:10.1007/s003000050374
Article Google Scholar - Brooks PD, Schmidt SK, Williams MW (1997) Winter production of CO2 and N2O from alpine tundra: environmental controls and relationship to inter-system C and N fluxes. Oecologia 110:403–413
Google Scholar - Brooks PD, Williams MW, Schmidt SK (1998) Inorganic N and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry 43:1–15. doi:10.1023/A:1005947511910
Article Google Scholar - Brooks PD, McKnight D, Elder K (2005) Carbon limitation of soil respiration under winter snowpacks: potential feedbacks between growing season and winter carbon fluxes. Glob Change Biol 11:231–238. doi:10.1111/j.1365-2486.2004.00877.x
Article Google Scholar - Brunner W, Focht DD (1984) Deterministic three-half-order kinetic model for microbial degradation of carbon substrates in soil. Appl Environ Microbiol 47:167–172
Google Scholar - Campbell JL, Mitchell MJ, Groffman PM, Christenson LM, Hardy JP (2005) Winter in northeastern North America: a critical period for ecological processes. Front Ecol Environ 3:314–322
Article Google Scholar - Colores GM, Schmidt SK, Fisk MC (1996) Estimating the biomass of microbial functional groups using rates of growth-related soil respiration. Soil Biol Biochem 28:1569–1577. doi:10.1016/S0038-0717(96)00253-2
Article Google Scholar - Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. doi:10.1038/nature04514
Article Google Scholar - Grogan P, Jonasson S (2006) Ecosystem CO2 production during winter in a Swedish subarctic region: the relative importance of climate and vegetation type. Glob Change Biol 12:1479–1495. doi:10.1111/j.1365-2486.2006.01184.x
Article Google Scholar - Hartig R (1888) Herpotrichia nigra n. sp. Allgem Forst Jagdzeit 64:15–17
Google Scholar - Hess TF, Schmidt SK (1995) Improved procedure for obtaining statistically valid parameter estimates from soil respiration data. Soil Biol Biochem 27:1–7. doi:10.1016/0038-0717(94)00166-X
Article Google Scholar - Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton, NJ
Google Scholar - Hsiang T, Matsumoto N, Millett SM (1999) Biology and management of Typhula snow molds of turfgrass. Plant Dis 83:788–798. doi:10.1094/PDIS.1999.83.9.788
Article Google Scholar - Kerry E (1990) Effects of temperature on growth rates of fungi from sub-Antarctic Macquarie Island and Casey, Antarctica. Polar Biol 10:293–299
Google Scholar - Larsen KS, Grogan P, Jonasson S, Michelsen A (2007) Respiration and microbial dynamics in two subarctic ecosystems during winter and spring thaw: effects of increased snow depth. Arct Antarct Alp Res 39:268–276. doi:10.1657/1523-0430(2007)39[268:RAMDIT]2.0.CO;2
Article Google Scholar - Ley RE, Williams MW, Schmidt SK (2004) Microbial population dynamics in an extreme environment: Controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry 68:313–335. doi:10.1023/B:BIOG.0000031032.58611.d0
Article Google Scholar - Lipson DA, Schmidt SK (2002) Kinetics of microbial processes and population growth in soil. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York, pp 1748–1757
Google Scholar - Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631
Article Google Scholar - Lipson DA, Schmidt SK, Monson RK (2000) Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32:441–448. doi:10.1016/S0038-0717(99)00068-1
Article Google Scholar - Lipson DA, Monson RK, Schmidt SK, Weintraub MN (2008) The trade-off between growth rate and yield in microbial communities and the consequences for soil respiration in a high elevation coniferous forest. Biogeochemistry (in press, this issue)
- Mast MA, Wickland KP, Striegl RT, Clow DW (1998) Winter fluxes of CO2 and CH4 from subalpine soils in Rocky Mountain National Park, Colorado. Global Biogeochem Cycles 12:607–620. doi:10.1029/98GB02313
Article Google Scholar - Mikan CJ, Schimel JP, Doyle AP (2002) Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol Biochem 34:1785–1795. doi:10.1016/S0038-0717(02)00168-2
Article Google Scholar - Monson RK, Lipson DA, Burns SP, Turnipseed AA, Delany AC, Williams MW et al (2006a) Winter forest soil respiration controlled by climate and microbial community composition. Nature 439:711–714. doi:10.1038/nature04555
Article Google Scholar - Monson RK, Burns SP, Williams MW, Delany AC, Weintraub MN, Lipson DA (2006b) The contribution of beneath-snow respiration to total ecosystem respiration in a high-elevation, subalpine forest. Global Biogeochem Cycles 20. doi:10.1029/2005GB002684
- Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111. doi:10.1111/j.1574-6941.1999.tb00639.x
Article Google Scholar - Pugh GJF, Allsop D (1982) Microfungi on Signy Island, South Orkney Islands. Br Antarct Surv Bull 57:55–67
Google Scholar - Romanovsky VE, Osterkamp TE (2000) Effects of unfrozen water on heat and mass transport processes in the active layer of permafrost. Permafrost Periglac Proc 11:219–239. doi:10.1002/1099-1530(200007/09)11:3<219::AID-PPP352>3.0.CO;2-7
Article Google Scholar - Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361. doi:10.1126/science.1086940
Article Google Scholar - Schlegel HG (1992) General microbiology, 7th edn. Cambridge University Press, Cambridge
Google Scholar - Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and alleochemical availability in temperate soils. Plant Soil 259:1–7. doi:10.1023/B:PLSO.0000020933.32473.7e
Article Google Scholar - Schmidt SK, Alexander M, Shuler ML (1985) Predicting threshold concentrations of organic substrates for bacterial growth. J Theor Biol 114:1–8. doi:10.1016/S0022-5193(85)80250-2
Article Google Scholar - Schmidt SK, West AE, Brooks PD, Jaeger CH, Fisk MC, Holland E (2001) Soil-atmosphere gas exchange. In: Bowman W, Seastedt T (eds) The structure and function of an alpine ecosystem. Oxford University Press, Oxford, pp 254–265
Google Scholar - Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN et al (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88:1379–1385. doi:10.1890/06-0164
Article Google Scholar - Schmidt SK, Wilson KL, Gebauer MM, Meyer AF, King AJ (2008a) Phylogeny and ecophysiology of opportunistic “snow molds” from a sub-alpine forest ecosystem. Microb Ecol . doi:10.1007/s00248-008-9387-6
Google Scholar - Schmidt SK, Wilson KL, Meyer AF, Porter TM, Schadt CW, Moncalvo JM (2008b) The missing fungi—new insights from culture-independent molecular studies of soil. In: Zengler K (ed) Accessing uncultivated microorganisms: from the environment to organisms and genomes and back. American Society for Microbiology, Washington, pp 55–66
Google Scholar - Scow KM, Simkins S, Alexander M (1986) Kinetics of mineralization of organic compounds at low concentrations in soil. Appl Environ Microbiol 51:1028–1035
Google Scholar - Simkins S, Alexander M (1984) Models for mineralization kinetics with the variables of substrate concentration and population density. Appl Environ Microbiol 47:1299–1306
Google Scholar - Simms HR (1967) On the ecology of Herpotrichia nigra. Mycologia 59:902–909. doi:10.2307/3757200
Article Google Scholar - Sommerfeld RA, Massman WJ, Musselman RC, Mosier AR (1996) Diffusional flux of CO2 through snow: spatial and temporal variability among alpine-subalpine sites. Global Biogeochem Cycles 10:473–482. doi:10.1029/96GB01610
Article Google Scholar - Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a sub-alpine forest ecosystem. Oecologia 154:327–338. doi:10.1007/s00442-007-0804-1
Article Google Scholar - Wynn-Williams DD (1985) Comparative microbiology of moss-peat decomposition on the Scotia Arc and Antarctic Peninsula. In: Siefried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer-Verlag, Berlin, pp 204–210
Google Scholar
Acknowledgments
We thank M.M. Gebauer and A.F. Meyer for laboratory assistance and M.W. Williams and N. Trahan for helpful discussions. This work was supported by a grant from the Microbial Observatories Program of the National Science Foundation (MCB-0455606) and a grant from the Western Section of the National Institute for Climate Change Research (NICCR-MPC35TX-A2) administered by Northern Arizona University and funded by the US Department of Energy (BER Program).
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Authors and Affiliations
- Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA
S. K. Schmidt, K. L. Wilson & R. K. Monson - Department of Biology, San Diego State University, San Diego, CA, 92182-4614, USA
D. A. Lipson
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Schmidt, S.K., Wilson, K.L., Monson, R.K. et al. Exponential growth of “snow molds” at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q 10 values.Biogeochemistry 95, 13–21 (2009). https://doi.org/10.1007/s10533-008-9247-y
- Received: 13 May 2008
- Accepted: 04 September 2008
- Published: 26 September 2008
- Issue Date: August 2009
- DOI: https://doi.org/10.1007/s10533-008-9247-y