Skip to main content

Advertisement

Log in

Temporal Changes Rather than Long-Term Repeated Burning Predominately Control the Shift in the Abundance of Soil Denitrifying Community in an Australian Sclerophyll Forest

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

To understand the temporal dynamics of soil bacterial denitrifying community in response to long-term prescribed burning and its resilience and recovery following a fire, a wet sclerophyll forest study site under two treatments (2 yearly burning (2YB) and no burning (NB)) and with 40-year-old burning history was used. Similar temporal patterns in the abundance of total (16S rRNA) and denitrifying (narG, nirK, nirS, nosZ) bacteria between two burning treatments revealed strong temporal influences. The magnitude of burning impacts on the abundance of 16S rRNA and denitrification genes was smaller compared with the impact of sampling time, but significant burning and temporal impacts were recorded for all (P < 0.001)—except for the nirS gene. Impacts of prescribed fire on the abundance of soil denitrifying community could be observed immediately after fire, and this impact diminished over a 24-month period prior to the next prescribed burning event. In conclusion, temporal changes govern the fluctuations of the abundance of soil denitrifying genes over the sampling period and the denitrifying community can recover after fire, suggesting that this community is resilient to the effects of prescribed burning. A combination of biotic and abiotic factors may account for the different temporal dynamics of denitrification gene abundance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Neary DG, Klopatek CC, DeBano LF, Ffolliott PF (1999) Fire effects on belowground sustainability: a review and synthesis. Forest Ecol Manag 122:51–71

    Article  Google Scholar 

  2. Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10

    Article  PubMed  Google Scholar 

  3. Westling AL, Hidalgo HG, Cayan DR, Swetnam TW (2006) Warming and earlier spring increases western U.S. forest wildfire activity. Science 31:940–943

    Article  Google Scholar 

  4. Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. Forest Ecol Mange 220:160–184

    Google Scholar 

  5. DeLuca TH, Sala A (2006) Frequent fire alters nitrogen transformation in ponderosa pine stands of the inland northwest. Ecology 87:2511–2522

    Article  PubMed  Google Scholar 

  6. Wang QK, Zhang MC, Wang SL (2012) A meta-analysis on the response of microbial biomass, dissolved organic matter, respiration, and N mineralization in mineral soil to fire in forest ecosystems. Forest Ecol Manag 271:91–97

    Article  Google Scholar 

  7. Wade D, Lunsford JD (1989) A guide for prescribed fire in Southern forests. USDA Forest Service Technical Publication R8-TP 11, Atlanta, GA

  8. Pietikäinen J, Fritze H (1995) Clear-cutting and prescribed burning in coniferous forest: comparison of effects on soil fungal and total biomass, respiration activity and nitrification. Soil Biol Biochem 27:101–109

    Article  Google Scholar 

  9. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641

    Article  PubMed  Google Scholar 

  10. Rinnan R, Michelsen A, Baath E, Jonasson S (2007) Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob Change Biol 13:28–39

    Article  Google Scholar 

  11. Xiang XJ, Shi Y, Yang J, Kong JJ, Lin XG, Zhang HY, Zeng J, Chu HY (2014) Rapid recovery of soil bacterial communities after wildfire in a Chinese boreal forest. Sci Rep 4:3829. doi:10.1038/srep03829

    PubMed  PubMed Central  Google Scholar 

  12. DeBano LF (2000) The role of fire and soil heating on water repellence in wildland environments: a review. J Hydrol 231:195–206

    Article  Google Scholar 

  13. Hamman ST, Burke IC, Knapp EE (2008) Soil nutrients and microbial activity after early and late season prescribed burns in a Sierra Nevada mixed conifer forest. Forest Ecol Mange 256:367–374

    Article  Google Scholar 

  14. Knicker H (2007) How does fire affect the nature and stability of soil organic nitrogen and carbon? A review. Biogeochemistry 85:91–118

    Article  CAS  Google Scholar 

  15. Grogen P, Bruns TD, ChapinIII FS (2000) Fire effects on ecosystem cycling in a Californian bishop pine forest. Oecologia 122:537–544

    Article  Google Scholar 

  16. Prieto-Fernández Á, Carballas M, Carballas T (2004) Inorganic and organic N pools in soils burned or heated: immediate alterations and evolution after forest wildfires. Geoderma 121:291–306

    Article  Google Scholar 

  17. Ravishankara AR, Daniel JS, Portmann WR (2009) Nitrous oxide (N2O): the dominate ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  CAS  PubMed  Google Scholar 

  18. Schulze ES, Wirth C, Heimann M (2000) Managing forests after Kyoto. Science 289:2058–2059

    Article  CAS  PubMed  Google Scholar 

  19. Chapuis-Lardy L, Wrage N, Metay A, Chotte JL, Bernoux M (2007) Soils, a sink for N2O? A review. Glob Change Biol 13:1–17

    Article  Google Scholar 

  20. Dalal RC, Allen DE (2008) Greenhouse gas fluxes from natural ecosystems. Aust J Bot 56:369–407

    Article  CAS  Google Scholar 

  21. Hu HW, Chen DL, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749

    Article  PubMed  Google Scholar 

  22. Canfield DC, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330:192–196

    Article  CAS  PubMed  Google Scholar 

  23. Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microb 64:3769–3775

    CAS  Google Scholar 

  24. Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Phillippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Meth 59:327–335

    Article  CAS  Google Scholar 

  25. Levy-Booth D, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25

    Article  CAS  Google Scholar 

  26. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    Article  PubMed  Google Scholar 

  27. Wang H, Yang SH, Yang JP, Ya-min LV, Zhao X, Pang JL (2014) Temporal changes in soil bacterial and archaeal communities with different fertilizers in tea orchards. J Zhejiang Univ-SCI B 15:953–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2013) Seasonal variation in functional properties of microbial communities in beech forest soil. Soil Biol Biochem 60:95–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lauber CL, Ramirez KS, Aanderud Z, Lennon J, Fierer N (2013) Temporal variability in soil microbial communities across land-use types. ISME J 7:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Thomas C, Gleixner G (2013) Seasonal differences in tree species’ influence on soil microbial communities. Soil Biol Biochem 66:239–248

    Article  Google Scholar 

  31. Bååth E, Frostegard A, Pennanen T, Fritze H (1995) Microbial community structure and pH response in relation to soil organic-matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol Biochem 27:229–240

    Article  Google Scholar 

  32. Mamilov AS, Dilly OM (2002) Soil microbial eco-physiology as affected by short-term variations in environmental conditions. Soil Biol Biochem 34:1283–1290

    Article  CAS  Google Scholar 

  33. Bergner B, Johnstone J, Treseder KK (2004) Experimental warming and burn severity alter soil CO2 flux and soil functional groups in a recently burned boreal forest. Glob Change Biol 10:1996–2004

    Article  Google Scholar 

  34. Pietikäinen J, Fritze H (1993) Microbial biomass and activity in the humus layer following burning: short term effects of two different fires. Can J Forest Res 23:1275–1285

    Article  Google Scholar 

  35. Campbell CD, Cameron CM, Bastias BA, Chen CR, Cairney JWG (2008) Long term repeated burning in a wet sclerophyll forest reduces fungal and bacterial biomass and responses to carbon substrates. Soil Biol Biochem 40:2246–2252

    Article  CAS  Google Scholar 

  36. Isbell RF (1996) The Australian soil classification. CSIRO Publishing, Collingwood

    Google Scholar 

  37. Guinto DF, Xu ZH, House APN, Saffigna PG (2001) Soil chemical properties and forest floor nutrients under repeated prescribed-burning in eucalypt forests of south-east Queensland, Australia. New Zeal J For Sci 13:170–187

    Google Scholar 

  38. Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33:943–951

    Article  CAS  Google Scholar 

  39. Kauri T (1982) Seasonal fluctuations in numbers of aerobic bacteria and their spores in four horizons of beech forest soil. Soil Biol Biochem 14:185–190

    Article  Google Scholar 

  40. Rogers BF, TateIII RL (2001) Temporal analysis of the soil microbial community along a toposequence in pineland soils. Soil Biol Biochem 33:1398–1401

    Article  Google Scholar 

  41. Jhonmaie AM, Nakagoshi N, Isagi Y (2006) Soil microbial biomass, abundance, and diversity in a Japanese red pine forest: first year after fire. J For Res 11:165–173

    Article  Google Scholar 

  42. Bastias BA, Huang ZQ, Blumfield T, Xu ZH, Cairney JWG (2006) Influence of repeated prescribed burning on the soil fungal community in an eastern Australian wet sclerophyll forest. Soil Biol Biochem 38:3492–3501

    Article  CAS  Google Scholar 

  43. Rapp M (1990) N status and mineralization in natural and disturbed Mediterranean forests and coppices. Plant Soil 128:21–30

    Article  CAS  Google Scholar 

  44. Kaye JP, Hart SC (1998) Ecological restoration alters N transformation in a ponderosa pine-bunchgrass ecosystem. Ecol Appl 8:1052–1060

    Google Scholar 

  45. Davidson EA, Hart SC, Firestone MK (1992) Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73:1148–1156

    Article  Google Scholar 

  46. Stark JM, Hart SC (1997) High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385:61–64

    Article  CAS  Google Scholar 

  47. Giovannini G, Lucchesi S, Giachetti M (1990) Effects of heating on some chemical parameters related to soil fertility and plant growth. Soil Sci 149:344–350

    Article  CAS  Google Scholar 

  48. Dumontet S, Dinel H, Scopa A, Mazzatura A, Saracino A (1996) Post-fire soil microbial biomass and nutrient content of a pine forest soil from a dunal Mediterranean environment. Soil Biol Biochem 28:1467–1475

    Article  CAS  Google Scholar 

  49. Saleh-Lakha S, Shannon KE, Henderson SL, Goyer C, Trevors JT, Zebarth BJ, Buton DL (2009) Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Appl Environ Microb 75:3903–3911

    Article  CAS  Google Scholar 

  50. Klemedtsson L, Svensson BH, Rosswall T (1988) Relationships between soil moisture content and nitrous oxide production during nitrification and denitrification. Biol Fert Soils 6:106–111

    Google Scholar 

  51. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  CAS  Google Scholar 

  52. Yarwood SA, Myrold DD, Hӧgberg MN (2009) Termination of belowground C addition by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiol Ecol 70:151–162

    Article  CAS  PubMed  Google Scholar 

  53. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    Article  CAS  PubMed  Google Scholar 

  54. Marhan S, Phillippot L, Bru D, Rudolph S, Franzaring J, Hӧgy P, Fangmeier A, Kandeler E (2011) Abundance and activity of nitrate reducers in an arable soil are more affected by temporal variation and soil depth than by elevated atmosphere [CO2]. FEMS Microbiol Ecol 76:209–219

    Article  CAS  PubMed  Google Scholar 

  55. Wolsing M, Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48:261–271

    Article  CAS  PubMed  Google Scholar 

  56. Song K, Kang H, Zhang L, Mitscg WJ (2012) Seasonal and spatial variations of denitrification and denitrifying bacterial community structure in created riverine wetlands. Ecol Eng 38:130–134

    Article  Google Scholar 

  57. Phillippot L, Čuhel J, Saby NPA, Cheneby D, Chronakova A, Bru D, Arrouay D, Martin-Laurent F, Šimek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526

    Article  Google Scholar 

  58. Phillippot L, Hallin S, Borjesson G, Baggs EM (2009) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Marijke Heenan, Haibo Dong, and Enqing Hou for their assistance in the field sampling. This research was supported under Australian Research Council’s Future Fellowship (project number FT0990547).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xian Liu.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 63 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Chen, C.R., Hughes, J.M. et al. Temporal Changes Rather than Long-Term Repeated Burning Predominately Control the Shift in the Abundance of Soil Denitrifying Community in an Australian Sclerophyll Forest. Microb Ecol 73, 177–187 (2017). https://doi.org/10.1007/s00248-016-0894-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0894-6

Keywords

Navigation