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Biology and Fertility of Soils

, Volume 54, Issue 8, pp 985–997 | Cite as

Soil microbial response following wildfires in thermic oak-pine forests

  • Michael S. Huffman
  • Michael D. Madritch
Original Paper
  • 175 Downloads

Abstract

The ecosystem response to wildfire is often linked to fire severity, with potentially large consequences for belowground biogeochemistry and microbial processes. While the impacts of wildfire on belowground processes are generally well documented, it remains unclear how fire affects the fine-scale composition of microbial communities. Here, we investigate the composition of soil bacterial and fungal communities in burned and unburned forests in an attempt to better understand how these diverse communities respond to wildfire. We explored the belowground responses to three wildfires in Linville Gorge, NC, USA. Wildfires generally increased soil carbon content while simultaneously reducing soil respiration. We employed amplicon sequencing to describe soil microbial communities and found that fires decreased both bacterial and fungal diversity. In addition, wildfires resulted in significant shifts in both bacterial and fungal community composition. Bacterial phylum-level distributions in response to fire were mixed without clear patterns, with members of Acidobacteria being representative of both burned and unburned sites. Fungal communities showed consistent increases in Ascomycota dominance and concurrent decreases in Basidiomycota and Zygomycota dominance in response to burning. Indicator species analysis confirmed shift to Ascomycota in burned sites. These shifts in microbial communities may reflect differences in the quality and quantity of soil organic matter following wildfires.

Keywords

Wildfire Soil microbial community Amplicon sequencing 

Notes

Acknowledgements

This work was supported by the Cratis D. Williams Graduate School, the Appalachian State University Biology Department, and the Grandfather Ranger district of the U.S.D.A Forest Service.

References

  1. Abatzoglou JT, Williams PA (2016) Impact of anthropogenic climate change on wildfire across western US forests. PNAS 113:11770–11775CrossRefGoogle Scholar
  2. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  4. Asemaninejad A, Thorn RG, Lindo Z (2016) Experimental climate change modifies degradative succession in boreal peatland fungal communities. Microb Ecol 73:521–531CrossRefGoogle Scholar
  5. Axelrood PE, Chow ML, Radomski CC, McDermott JM, Davies J (2002) Molecular characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48:655–674CrossRefGoogle Scholar
  6. Baldrian P, Valášková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–552CrossRefGoogle Scholar
  7. Banning NC, Murphy DV (2008) Effect of heat-induced disturbance on microbial biomass and activity in forest soil and the relationship between disturbance effects and microbial community structure. Appl Soil Ecol 40:109–119CrossRefGoogle Scholar
  8. Bers K, Sniegowski K, Albers P, Breugelmans P, Hendrickx L, De Mot R, Springael D (2011) A molecular toolbox to estimate the number and diversity of Variovorax in the environment: application in soils treated with the phenylurea herbicide linuron. FEMS Microbiol Ecol 76:14–25CrossRefGoogle Scholar
  9. Boerner REJ, Brinkman JA, Smith A (2005) Seasonal variations in enzyme activity and organic carbon in soil of a burned and unburned hardwood forest. Soil Biol Biochem 37:1419–1426CrossRefGoogle Scholar
  10. Bond-Lamberty B, Wang C, Gower ST (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Glob Chang Biol 10(10):1756–1766CrossRefGoogle Scholar
  11. Buchmann N (2000) Biotic and abiotic factors controlling soil respiration rates in Picea abies stands. Soil Biol Biochem 32:1625–1635CrossRefGoogle Scholar
  12. Buckley DH, Huangyutitham V, Nelson TA, Rumberger A, Thies JE (2006) Diversity of planctomycetes in soil in relation to soil history and environmental heterogeneity. App Environ Microbiol 72:4522–4531CrossRefGoogle Scholar
  13. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  14. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108:4516–4522CrossRefGoogle Scholar
  15. Carini R, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N. (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nature Microbiology  https://doi.org/10.1038/nmicrobiol.2016.242
  16. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  17. Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10CrossRefGoogle Scholar
  18. Choromanska U, DeLuca TH (2001) Prescribed fire alters the impact of wildfire on biochemical properties in a ponderosa pine forest. SSSAJ 65:232–238CrossRefGoogle Scholar
  19. Choromanska U, DeLuca TH (2002) Microbial activity and nitrogen mineralization in forest mineral soils following heating: evaluation of post-fire effects. Soil Biol Biochem 34:263–271CrossRefGoogle Scholar
  20. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007).Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229-240.CrossRefGoogle Scholar
  21. Cisneros-Dozal LM, Trumbore S, Hanson P (2006) Partitioning sources of soil-respired CO2 and their seasonal variation using a unique radiocarbon tracer. Glob Chang Biol 12:194–204CrossRefGoogle Scholar
  22. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145CrossRefGoogle Scholar
  23. DeBano LF, Neary DG, Ffolliott PF (1998) Fire’s effects on ecosystems. New York: Wiley; 1998Google Scholar
  24. Deng S, Popova IE, Dick L, Dick R (2013) Bench scale and microplate format assay of soil enzyme activities using spectroscopic and fluorometric approaches. Appl Soil Ecol 64:84–90CrossRefGoogle Scholar
  25. Dixon RK, Brown S, Houghton RA, Solomon AM, Trexler MC, Wisniewski J (1994) Carbon pools and flux of global forest ecosystems. Science 263:185–190CrossRefGoogle Scholar
  26. Dooley SR, Treseder KK (2012) The effect of fire on microbial biomass: a meta-analysis of field studies. Biogeochemistry 109:49–61CrossRefGoogle Scholar
  27. Dove N, Hart S (2017) Fire reduces fungal species richness and in situ mycorrhizal colonization: a meta-analysis. Fire Ecol 13:37–65CrossRefGoogle Scholar
  28. Dufrêne M, Legedre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  29. Dumas S, Neufeld HS, Melany CF (2007) Fire in a thermic oak-pine forest in Linville Gorge Wilderness Area, North Carolina: importance of the shrub layer to ecosystem response. Castanea 72:92–104CrossRefGoogle Scholar
  30. Dunn PH, Barro SC, Poth M (1985) Soil moisture affects survival of microorganisms in heated chaparral soil. Soil Biol Biochem 17:143–148CrossRefGoogle Scholar
  31. Fernández-González AJ, Martínez-Hidalgo P, Cobo-Díaz JF, Villadas PJ, Martínez-Molina E, Toro N, Tringe SG, Fernández-López M (2017) The rhizosphere microbiome of burned holm-oak: potential role of the genus Arthrobacter in the recovery of burned soils. Sci Rep 7:6008CrossRefGoogle Scholar
  32. Ginzburg O, Steinberger Y (2012) Effects of forest wildfire on soil microbial community activity and chemical components on a temporal-seasonal scale. Plant Soil 360:243–257CrossRefGoogle Scholar
  33. González-Pérez JA, Gonzalez-Vila GA, Gonzalo A, Knicker H (2004) The effect of fire on soil organic matter—a review. Environ Int 30:855–870CrossRefGoogle Scholar
  34. Hamman ST, Burke IC, Stromberger ME (2007) Relationships between microbial community structure and soil environmental conditions in a recently burned system. Soil Biol Biochem 39:1703–1711CrossRefGoogle Scholar
  35. Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146CrossRefGoogle Scholar
  36. Hart SC, DeLuca TH, Newman SG, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manag 220:166–184CrossRefGoogle Scholar
  37. Hernandez T, Garcia C, Reinhardt I (1997) Short-term effect of wildfire on the chemical, biochemical and microbiological wildfire effects on boreal soil Fungi 45 properties of Mediterranean pine forest soils. Biol Fertil Soils 25:109–116CrossRefGoogle Scholar
  38. Holden SR, Treseder KK (2013) A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol 4:163CrossRefGoogle Scholar
  39. Holden SR, Rogers BM, Treseder KK, Randerson JT (2016) Fire severity influences the response of soil microbes to a boreal forest fire. Environ Res Lett 11:035004CrossRefGoogle Scholar
  40. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728CrossRefGoogle Scholar
  41. Knight D (2006) Soil survey of Burke County, North Carolina. United States Department of Agriculture, Natural Resources Conservation ServiceGoogle Scholar
  42. Knoepp JD, Vose JM, Swank WT (2004) Long-term soil responses to site preparation burning in the southern Appalachians. For Sci 50:540–550Google Scholar
  43. Knoepp JD, DeBano LF, Neary DG (2005) Soil chemistry. In: Neary DG, Ryan KC, DeBano LF (eds) Wildland fire in ecosystem; effect of fire on soils and water. General Technical Report RMRS-GTR 42-4, U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Ogden, UT, pp 53–71Google Scholar
  44. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120CrossRefGoogle Scholar
  45. Lentile LB, Holden ZA, Smith AMS, Falkowski MJ, Hudak AT, Morgan P, Lewis SA, Gessler PE, Benson NC (2006) Remote sensing techniques to assess active fire characteristics and post-fire effects. Int J Wildland Fire 15:319–345CrossRefGoogle Scholar
  46. Lingens F, Blecher R, Blecher H, Blobel F, Eberspächer J, Fröhner C et al (1985) Phenylobacterium immobile gen. Nov., sp. Nov., a gram-negative bacterium that degrades the herbicide chloridazon. Int J Syst Bacteriol 35:26–39CrossRefGoogle Scholar
  47. Lumley RTC, Gignac D, Currah RS (2001) Microfungus communities of white spruce and trembling aspen logs at different stages of decay in disturbed and undisturbed sites in the boreal mixedwood region of Alberta. Can J Bot 79(1):76–92Google Scholar
  48. Madritch MD, Donaldson JR, Lindroth RL (2007) Canopy herbivory can mediate the influence of plant genotype on soil processes through frass deposition. Soil Biol Biochem 39:1192–1201CrossRefGoogle Scholar
  49. Martin M (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17.  https://doi.org/10.14806/ej.17.1.200 CrossRefGoogle Scholar
  50. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of micro-biome census data. PLoS One 8(4):e61217CrossRefGoogle Scholar
  51. Menkis A, Urbina H, James TY, Rosling A (2014) Archaeorhizomyces borealis sp. nov. and a sequence- based classification of related soil fungal species. Fungal Biol 118:943–955CrossRefGoogle Scholar
  52. Mikita-Barbato RA, Kelly JJ, Tate RL (2015) Wildfire effects on the properties and microbial community structure of organic horizon soils in the New Jersey Pinelands. Soil Biol Biochem 86:67–76CrossRefGoogle Scholar
  53. Mulvaney R (1996) Nitrogen - inorganic forms. In: Bartels J (ed) Methods of soil analysis part 3 chemical methods. Soil Sci Soc Am, Madison, WI, pp 1123–1184Google Scholar
  54. Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schoning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000CrossRefGoogle Scholar
  55. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19CrossRefGoogle Scholar
  56. Neary DG, Klopatek CC, DeBano LF, Elliott PF (1999) Fire effects on belowground sustainability: a review and synthesis. For Ecol Manag 122:51–71CrossRefGoogle Scholar
  57. Neff JC, Harden JW, Gleixner G (2005) Fire effects on soil organic matter content, composition, and nutrients in boreal interior Alaska. Can J For Res 35:2178–2187CrossRefGoogle Scholar
  58. Newell CL, Peet RK (1998) Vegetation of Linville Gorge Wilderness, North Carolina. Castanea 63:275–322Google Scholar
  59. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: community ecology package version 2.4–4. https://cran.r-project.org/web/packages/vegan/index. html
  60. Oliver AK, Callaham MA, Jr, Jumpponen A (2015) Soil fungal communities respond compositionally to recurring frequent prescribed burning in a managed southeastern US forest system. For Ecol Manag 345:1–9CrossRefGoogle Scholar
  61. Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974CrossRefGoogle Scholar
  62. Osono T, Takeda H (2006) Fungal decomposition of Abies needle and Betula leaf litter. Mycologia 98:172–179CrossRefGoogle Scholar
  63. Pandey A, Chaudhry S, Sharma A, Choudhary VS, Malviya MK, Chamoli S, Rinu K, Trivedi P, Palni LMS (2011) Recovery of Bacillus and Pseudomonas spp. from the ‘Fired Plots’ under shifting cultivation in Northeast India. Curr Microbiol 62:273–280CrossRefGoogle Scholar
  64. Perrakis D, Zell D (2008).Remote assessment of burn severity: a pilot study in landscape monitoring. Parks Canada Agency: Western and Northern Service Centre and National Fire CentreGoogle Scholar
  65. Pourreza M, Hosseini SM, Sinegani AAS, Matinizadeh M, Dick W (2014) Soil microbial activity in response to fire severity in Zagros oak (Quercus brantii Lindl.) forests, Iran, after one year. Geoderma 213:95–102CrossRefGoogle Scholar
  66. Prieto-Fernandez A, Acea MJ, Carballas T (1998) Soil microbial and extractable C and N after wildfire. Biol Fertil Soils 27:132–142CrossRefGoogle Scholar
  67. Prosser JI (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81:507–519CrossRefGoogle Scholar
  68. Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99CrossRefGoogle Scholar
  69. Reilly MJ, Wimberly MC, Newell CL (2006) Wildfire effects on beta-diversity and species turnover in a forested landscape. J Veg Sci 17:447–454Google Scholar
  70. Restaino JC, Peterson DL (2013) Wildfire and fuel treatment effects on forest carbon dynamics in the western United States. For Ecol Manage 303:46–60CrossRefGoogle Scholar
  71. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584CrossRefGoogle Scholar
  72. Rosling A, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl B, Menkis A, James T (2011) Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 33:876–879CrossRefGoogle Scholar
  73. Saiya-Cork K, 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 34:1309–1315CrossRefGoogle Scholar
  74. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B,Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537–7541.CrossRefGoogle Scholar
  75. Schloss PD, Gevers D, Westcott SL (2011) Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies. PLoS ONE 6(12):e27310CrossRefGoogle Scholar
  76. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762CrossRefGoogle Scholar
  77. Smith DP, Pea KG (2014) Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PloS One 9(2):e90234CrossRefGoogle Scholar
  78. Swanson ME, Franklin JF, Beschta RL, Crisafulli CM, DellaSala DA, Hutto RL, Lindenmayer DB, Swanson FJ (2011) The forgotten stage of forest succession: early-successional ecosystems on forest sites. Front Ecol Environ 9:117–125CrossRefGoogle Scholar
  79. Van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefGoogle Scholar
  80. Vestergaard G, Schulze S, Scholer A, Schloter A (2017) Making big data smart – how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484CrossRefGoogle Scholar
  81. Wang Q, Zhong M, Wang S (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. For Ecol Manage 271:91–97CrossRefGoogle Scholar
  82. Weber CF, Lockhart J, Charaska E, Aho K, Lohse KA (2014) Bacterial composition of soils in ponderosa pine and mixed conifer forests exposed to different wildfire burn severity. Soil Biol Biochem 69:242–250CrossRefGoogle Scholar
  83. Williams RJ, Hallgren SW, Wilson GWT (2012) Frequency of prescribed burning in an upland oak forest determines soil and litter properties and alters the soil microbial community. For Ecol Manag 265:241-247CrossRefGoogle Scholar
  84. Wimberly MC, Reilly MJ (2007) Assessment of fire severity and species diversity in the southern Appalachians using Landsat TM and ETMþ imagery. Remote Sens Environ 108:189–197CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyAppalachian State UniversityBooneUSA

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