Soil respiration and extracellular enzyme production respond differently across seasons to elevated temperatures

Abstract

Background and aims

The activity of extracellular enzymes is one control on soil organic matter decomposition and serves as a driver of heterotrophic soil respiration. To understand how temperature sensitive enzyme reactions will influence the processing of soil carbon substrates at elevated temperatures, we deployed a passive warming experiment in a deciduous forest with highly invaded understory plant communities and high soil nitrogen concentrations.

Methods

We seasonally assessed six extracellular enzyme activities and measured soil respiration in the field and in laboratory incubations, to determine if soil carbon use and nutrient cycling responded to 3.5 years of warming.

Results

Field measurements indicate soil respiration was 24% lower and the production of the recalcitrant C-acquiring enzyme phenoloxidase was also lower in warmed plots during fall and winter. In the spring, phosphate (P) acquiring enzyme activity increased in response to warming. In lab incubations, soil respiration was not different between warmed and control soils.

Conclusions

Despite minimal changes to C stores after 3.5 years of warming, recalcitrant C-use and nutrient processing enzymes responded differentially to higher temperatures in fall, winter, and spring. This suggests that C- and nutrient cycle responses to warming can change throughout the seasons, perhaps mediated by plant phenological changes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    CAS  Article  Google Scholar 

  2. Allison SD et al (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:36–340

    Article  Google Scholar 

  3. Allison SD et al (2014) Substrate concentration constraints on microbial decomposition. Soil Biol Biochem 79:43–49

    CAS  Article  Google Scholar 

  4. Ashton I et al (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  5. Bahn M et al (2010) Soil respiration at mean annual temperature predicts annual total across vegetation types and biomes. Biogeosciences 7:2147–2157

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Baldrian P et al (2013) Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem 56:60–68

    CAS  Article  Google Scholar 

  7. Bardgett RD et al (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME 2:805–814

    CAS  Article  Google Scholar 

  8. Bölscher T et al (2017) Temperature sensitivity of substrate-use efficiency can result from altered microbial physiology without change to community composition. Soil Biol Biochem 109:59–69

    Article  Google Scholar 

  9. Bradford MA et al (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327

    Article  PubMed  Google Scholar 

  10. Bradford et al. (2010) Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob Chang Biol 16:1576–1588

    Article  Google Scholar 

  11. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427

    CAS  Article  Google Scholar 

  12. Burns RG et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    CAS  Article  Google Scholar 

  13. Chapman SK et al (2016) Impacts of soil nitrogen and carbon additions on Forest understory communities with a long nitrogen deposition history. Ecosystems 19:142–154

    CAS  Article  Google Scholar 

  14. Cleland EE et al (2007) Shifting plant phenology in response to global change. Ecol Evolut 22:357–365

    Article  Google Scholar 

  15. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173

    CAS  Article  PubMed  Google Scholar 

  16. DeAngelis KM et al (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:1–13

    Article  Google Scholar 

  17. Deforest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41:1180–1186

    CAS  Article  Google Scholar 

  18. Dorrepaal E et al (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:616–619

    CAS  Article  Google Scholar 

  19. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    CAS  Article  Google Scholar 

  20. Eliasson PE et al (2005) The response of heterotrophic CO2 flux to soil warming. Glob Chang Biol 11:167–181

    Article  Google Scholar 

  21. Estiarte M, Penuelas J (2015) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob Chang Biol 21:1005–1017

    Article  PubMed  Google Scholar 

  22. Fierer N et al (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326

    Article  Google Scholar 

  23. Frey SD et al (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398

    CAS  Article  Google Scholar 

  24. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362

    CAS  Article  PubMed  Google Scholar 

  25. German DP et al (2011) Soil Biology & Biochemistry Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    CAS  Article  Google Scholar 

  26. German DP et al (2012) The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Chang Biol 18:1468–1479

    Article  Google Scholar 

  27. Giasson MA et al (2013) Soil respiration in a northeastern US temperate forest: a 22-year synthesis. Ecosphere 4:1–28

    Article  Google Scholar 

  28. Gilliam FS et al (2006) Effects of atmospheric nitrogen deposition on the herbaceous layer of a central Appalachian hardwood Forest. J Torrey Bot Soc 133:240–254

    Article  Google Scholar 

  29. Grandy AS et al (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711

    CAS  Article  Google Scholar 

  30. Hartley et al. (2007) Effects of 3 years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob Chang Biol 13:1761–1770

    Article  Google Scholar 

  31. Jian S et al (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol Biochem 101:32–43

    CAS  Article  Google Scholar 

  32. Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

    Article  Google Scholar 

  33. Kallenbach CM et al (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Karhu K et al (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513:81–84

    CAS  Article  PubMed  Google Scholar 

  35. Kirschbaum MUF (2006) Temporary carbon sequestration cannot prevent climate change. Mitig Adapt Strat GL 11:1151–1164

    Article  Google Scholar 

  36. Knorr W et al (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433:298–301

    CAS  Article  PubMed  Google Scholar 

  37. Luo Y et al (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625

    CAS  Article  PubMed  Google Scholar 

  38. Melillo JM et al (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–2176

    CAS  Article  PubMed  Google Scholar 

  39. Melillo JM et al (2017) Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358:101–105

    CAS  Article  PubMed  Google Scholar 

  40. Menzel A (2002) Phenology: its importance to the global change community. Clim Chang 54:379–385

    Article  Google Scholar 

  41. Moyes AB, Bowling DR (2016) Plant community composition and phenological stage drive soil carbon cycling along a tree-meadow ecotone. Plant Soil 401:231–242

    CAS  Article  Google Scholar 

  42. Oechel WC et al (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978–981

    CAS  Article  PubMed  Google Scholar 

  43. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    CAS  Article  Google Scholar 

  44. Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99

    CAS  Article  Google Scholar 

  45. Reyer CPO et al (2013) A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability. Glob Chang Biol 19:75–89

    Article  PubMed  Google Scholar 

  46. Richardson AD et al (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173

    Article  Google Scholar 

  47. Rochette P, Gregorich EG, Desjardins RL (1992) Comparison of static and dynamic closed chambers for measurement of soil respiration under field conditions. Can J Soil Sci 72:605–609

    Article  Google Scholar 

  48. Saiya-cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer Saccharum forest soil. Soil Biol Biochem 34:1309–1315

    CAS  Article  Google Scholar 

  49. Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Chang Biol 1:77–91

    Article  Google Scholar 

  50. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    CAS  Article  Google Scholar 

  51. Sinsabaugh RL et al (1991) An enzymic approach to the analysis of microbial activity during plant litter decomposition. Agric Ecosyst Environ 34:43–54

    CAS  Article  Google Scholar 

  52. Sinsabaugh RL et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  PubMed  Google Scholar 

  53. Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933

    CAS  Article  Google Scholar 

  54. Wallenstein et al. (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol 15:1631–1639

    Article  Google Scholar 

  55. Wallenstein M et al (2011) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil enzymology, soil biology. Springer, Berlin, Heidelberg, pp 245–258

    Google Scholar 

  56. Weedon JT et al (2014) No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub- arctic peat bog. Biogeochemistry 117:55–66

    CAS  Article  Google Scholar 

  57. Wu L et al (2017) Alpine soil carbon is vulnerable to rapid microbial decomposition under climate cooling. ISME (9):2102–2111

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Heather A. Kittredge.

Additional information

Responsible Editor: Harry Olde Venterink.

Electronic supplementary material

ESM 1

(DOCX 51.5 kb)

ESM 2

(DOCX 63.8 kb)

ESM 3

(DOCX 34.5 kb)

ESM 4

(DOCX 50.1 kb)

ESM 5

(DOCX 25.2 kb)

ESM 6

(DOCX 16.2 kb)

ESM 7

(DOCX 13.2 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kittredge, H.A., Cannone, T., Funk, J. et al. Soil respiration and extracellular enzyme production respond differently across seasons to elevated temperatures. Plant Soil 425, 351–361 (2018). https://doi.org/10.1007/s11104-018-3591-z

Download citation

Keywords

  • Carbon cycle
  • Extracellular enzyme activity
  • Seasonal shifts
  • Soil respiration
  • Warming