Skip to main content

Advertisement

Springer Nature Link
Log in

Arbuscular mycorrhizal fungal communities show low resistance and high resilience to wildfire disturbance

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Wildfires are important disturbances that help to shape the structure and function of forest ecosystems, and arbuscular mycorrhizal fungi (AMF) are key players in the post-fire recovery of soils and understory vegetation. We aimed to investigate the response of AMF communities to wildfire over different timescales.

Methods

Primer set AMV4.5NF/AMDGR was used to amplify soil 18S rRNA gene fragments for the 454 GS-FLX pyrosequencing platform to examine belowground AMF communities 1 and 11 years following low- and high-intensity wildfires in the Greater Khingan Mountains of China.

Results

The majority of AMF sequences detected were annotated as Glomeraceae, Claroideoglomeraceae, Diversisporaceae and Acaulosporaceae. Both AMF community composition and alpha-diversity were correlated with herbaceous and shrubby biomass, available phosphorus (AP) and NH4 +, which were in turn altered by wildfire. AMF community composition, alpha-diversity, and phylogenetic structure were significantly altered 1-year-post-fire. However, AMF communities were indistinguishable from unburned forest soils 11-year-post-fire.

Conclusions

Our results indicated that AMF communities are resilient to wildfire on decadal timescales. This resilience appears to depend on the post-fire regrowth of understory vegetation and the subsequent recovery of soil chemical properties.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Barcenas-Moreno G, Garcia-Orenes F, Mataix-Solera J, Mataix-Beneyto J, Baath E (2011) Soil microbial recolonisation after a fire in a Mediterranean forest. Biol Fertil Soils 47:261–272

    Article  Google Scholar 

  • Bergeron Y, Dubuc M (1989) Succession in the southern part of the Canadian boreal forest. Vegetation 79:51–63

    Article  Google Scholar 

  • Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632

    Article  PubMed  Google Scholar 

  • Bollen GJ (1969) The selective effect of heat treatment on the microflora of a greenhouse soil. Neth J Plant Pathol 75:157–163

    Article  Google Scholar 

  • Buchholz K, Motto H (1981) Abundances and vertical distributions of Mycorrhizae in plains and barrens forest soils from the New-Jersey pine barrens. Bull Torrey Bot Club 108:268–271

    Article  Google Scholar 

  • Cairney JW, Bastias BA (2007) Influences of fire on forest soil fungal communities. Can J For Res 37:207–215

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Chang Y, He HS, Bishop I, Hu YM, Bu RC, Xu CG, Li X (2007) Long-term forest landscape responses to fire exclusion in the Great Xing’an Mountains, China. Int J Wildland Fire 16:34–44

    Article  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Ruffy TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • Choromanska U, DeLuca TH (2001) Prescribed fire alters the impact of wildfire on soil biochemical properties in a ponderosa pine forest. Soil Sci Soc Am J 65:232–238

    Article  CAS  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Deka HK, Mishra RR (1983) The effect of slash burning on soil microflora. Plant Soil 73:167–175

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Didham RK, Norton DA (2006) When are alternative stable states more likely to occur? Oikos 113:357–362

    Article  Google Scholar 

  • Didham RK, Watts CH, Norton DA (2005) Are systems with strong underlying biotic regimes more likely to exhibit alternative stable states? Oikos 110:09–416

    Article  Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster that BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Egger KN (1986) The influence of the microflora on physical properties of soils. I. Effects associated with filamentous algae and fungi. Aust J Soil Res 2:111–112

    Google Scholar 

  • Fang L, Yang J (2014) Atmospheric effects on the performance and threshold extrapolation of multi-temporal Landsat derived dNBR for burn severity assessment. Int J Appl Earth Obs Geoinf 33:10–20

    Article  Google Scholar 

  • Fernández I, Cabaneiro A, Carballas T (1997) Organic matter changes immediately after a wildfire in an Atlantic forest soil and comparison with laboratory soil heating. Soil Biol Biochem 29:1–11

    Article  Google Scholar 

  • Ferrenberg S, O’Neill SP, Knelman JE, Todd B, Duddan S, Nemergut DR (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J 13:1–10

    Google Scholar 

  • Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243

    Article  Google Scholar 

  • French NHF, Kasischke ES, Hall RJ, Murphy KA, Verbyla DL, Hoy EE, Allen JL (2008) Using Landsat data to assess fire and burn severity in the North American boreal forest region: an overview and summary of results. Int J Wildland Fire 17:443–462

    Article  Google Scholar 

  • Goldammer JG (1999) Fire-induced conversion of a lowland tropical rainforest to savanna in East Kalimantan, Indonesia. Science 284:1782–1783

    Article  Google Scholar 

  • Granstrom A, Schimmel J (1993) Heat-effects on seeds and rhizomes of a selection of boreal forest plants and potential reaction to fire. Oecologia 94:307–313

    Article  Google Scholar 

  • Guénon R, Vennetier M, Dupuy N, Roussos S, Pailler A, Gros R (2011) Trends in recovery of Mediterranean soil chemical properties and microbial activities after infrequent and frequent wildfires. Land Degrad Dev 24:115–128

    Article  Google Scholar 

  • Hamman ST, Burke IC, Stromberger ME (2007) Relationships between microbial community structure and soil environmental conditions in a recently burned system. Soil Biol Biochem 39:1703–1711

    Article  CAS  Google Scholar 

  • 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. For Ecol Manag 220:166–184

    Article  Google Scholar 

  • Horn S, Caruso T, Verbruggen E, Rilling MC, Hempel S (2014) Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME J 14:1–12

    Google Scholar 

  • Hoy EE, French NH, Turetsky MR, Trigg SN, Kasischke ES (2008) Evaluating the potential of Landsat TM/ETM+ imagery for assessing fire severity in Alaskan black spruce forests. Int J Wildland Fire 17:500–514

    Article  Google Scholar 

  • Isobe K, Otsuka S, Sudiana IM, Nurkanto A, Senoo K (2009) Community composition of soil bacteria nearly a decade after a fire in a tropical rainforest in East Kalimantan, Indonesia. J Gen Appl Microbiol 55:329–337

    Article  CAS  PubMed  Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Article  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Key C, Benson N (2005) Landscape assessment: ground measure of severity, the Composite Burn Index; and remote sensing of severity, the Normalized Burn Ratio. In: FIREMON: fire effects monitoring and inventory system. General Technical Report RMRS-GTR-164-CD: LA1-LA51. United States Department of Agriculture, Rocky Mountain Research Station, Ogden, Utah, USA

  • Leduc SD, Lilleskov EA, Horton TR, Rothstein DE (2013) Ectomycorrhizal fungal succession coincides with shifts in organic nitrogen availability and canopy closure in post-wildfire jack pine forests. Oecologia 172:257–269

    Article  PubMed  Google Scholar 

  • Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 8:1399–1410

    Article  Google Scholar 

  • Lekberg Y, Schnoor T, Kjøller R, Gibbons SM, Hansen LH, Al-Soud W, Sørensen SJ, RosendahL S (2011) 454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J Ecol 100:151–160

    Article  Google Scholar 

  • Lekberg Y, Gibbons SM, RosendahL S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu ZH, Yang J, Chang Y, Weisberg PJ, He HS (2012) Spatial patterns and drivers of fire occurrence and its future trend under climate change in a boreal forest of Northeast China. Glob Chang Biol 18:2041–2056

    Article  Google Scholar 

  • Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179

    CAS  PubMed  Google Scholar 

  • Luo YQ, Hui DF, Zhang DQ (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63

    Article  PubMed  Google Scholar 

  • Moora M, Öpik M, Sen R, Zobel M (2004) Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Funct Ecol 18:554–562

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437

    Article  CAS  PubMed  Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Article  CAS  PubMed  Google Scholar 

  • Ostlund L, Zackrisson O, Axelsson AL (1997) The history and transformation of a Scandinavian boreal forest landscape since the 19th century. Can J For Res 27:1198–1206

    Article  Google Scholar 

  • Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rees DC, Juday GP (2002) Plant species diversity on logged versusburned sites in central Alaska. For Ecol Manag 155:291–302

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  CAS  PubMed  Google Scholar 

  • Rosendahl S, Matzen HB (2008) Genetic structure of arbuscular mycorrhizal populations in fallow and cultivated soils. New Phytol 179:1154–1161

    Article  PubMed  Google Scholar 

  • Saia S, Benitez E, Garcia-Garrido JM, Settanni L, Amato G, Giambalvo D (2014) The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. J Agric Sci 152:370–378

    Article  Google Scholar 

  • Slik JWF, Verburg RW, Kessler PJA (2002) Effects of fire and selective logging on the tree species composition of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodivers Conserv 11:85–98

    Article  Google Scholar 

  • Smithwick EA, Kashian DM, Ryan MG, Turner MG (2009) Long-term ecosystem nitrogen storage and soil nitrogen availability in post-fire lodgepole pine ecosystems. Ecosystems 12:792–806

    Article  CAS  Google Scholar 

  • Song YY, Zeng RS, Xu JF, Li J, Shen X (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5, e13324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stendell ER, Horton TR, Bruns TD (1999) Early effects of prescribed fire on the structure of the ectomycorrhizal fungus community in a Sierra Nevada ponderosa pine forest. Mycol Res 103:1353–1359

    Article  Google Scholar 

  • Sykorova Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14

    Article  CAS  PubMed  Google Scholar 

  • van der Heijden MG (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:651

    Article  Google Scholar 

  • van der Heijden MG, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091

    Article  Google Scholar 

  • Vernes K, Johnson CN, Castellano MA (2004) Fire-related changes in biomass of hypogeous sporocarps at foraging points used by a tropical mycophagous marsupial. Mycol Res 108:1438–1446

    Article  PubMed  Google Scholar 

  • Visser S (1995) Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytol 129:389–401

    Article  Google Scholar 

  • Wang CK, Gower ST, Wang YH, Zhao HX, Yan P, Bond-Lamberty BP (2001) The influence of fire on carbon distribution and net primary production of boreal Larix gmelinii forests in north-eastern China. Glob Chang Biol 7:719–730

    Article  Google Scholar 

  • Wang QK, Zhong 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. For Ecol Manag 271:91–97

    Article  Google Scholar 

  • Wardle DA, Zackrisson O, Nilsson MC (1998) The charcoal effect in Boreal forests: mechanisms and ecological consequences. Oecologia 115:419–426

    Article  Google Scholar 

  • Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155

    Article  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    Article  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Zuur AF, Leno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgments

We thank Wenhua Cai, Zhihua Liu, Weili Liu and Lei Fang for assistance in sampling. This work was supported by the Strategic Priority Research Program (Grant #XDB15010101) of Chinese Academy of Sciences, National Program on Key Basic Research Project (973 Program, Grant #2014CB954002), and National Natural Science Foundation of China (41371254, 41071121). S.M.G. was supported by an EPA STAR Graduate Fellowship and by the National Institutes of Health Training Grant 5T-32EB-00941. The authors declare no conflicts of interest.

Author information

Author notes

    Authors and Affiliations

    1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, East Beijing Road 71, Nanjing, 210008, China

      Xingjia Xiang, Ruibo Sun & Haiyan Chu

    2. Graduate Program in Biophysical Sciences, University of Chicago, Chicago, IL, USA

      Sean M. Gibbons

    3. State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Wenhua Road 72, Shenyang, 110164, China

      Jian Yang & Jianjian Kong

    4. University of Chinese Academy of Sciences, Beijing, 100049, China

      Xingjia Xiang & Ruibo Sun

    Authors
    1. Xingjia Xiang
      View author publications

      You can also search for this author inPubMed Google Scholar

    2. Sean M. Gibbons
      View author publications

      You can also search for this author inPubMed Google Scholar

    3. Jian Yang
      View author publications

      You can also search for this author inPubMed Google Scholar

    4. Jianjian Kong
      View author publications

      You can also search for this author inPubMed Google Scholar

    5. Ruibo Sun
      View author publications

      You can also search for this author inPubMed Google Scholar

    6. Haiyan Chu
      View author publications

      You can also search for this author inPubMed Google Scholar

    Corresponding author

    Correspondence to Haiyan Chu.

    Additional information

    Responsible Editor: Hans Lambers.

    Xingjia Xiang and Sean M. Gibbons contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    ESM 1

    (DOCX 41572 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Xiang, X., Gibbons, S.M., Yang, J. et al. Arbuscular mycorrhizal fungal communities show low resistance and high resilience to wildfire disturbance. Plant Soil 397, 347–356 (2015). https://doi.org/10.1007/s11104-015-2633-z

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11104-015-2633-z

    Keywords