Advertisement

Plant and Soil

, Volume 423, Issue 1–2, pp 327–338 | Cite as

Response of soil microbial community dynamics to Robinia pseudoacacia L. afforestation in the loess plateau: a chronosequence approach

  • Jinliang Liu
  • Zhonglan Yang
  • Peng Dang
  • Hailan Zhu
  • Yang Gao
  • Vu Ngoc Ha
  • Zhong ZhaoEmail author
Regular Article

Abstract

Aims

The objective was to analyze soil microbial community dynamics and their responses to changes in vegetation and soil properties after Robinia pseudoacacia afforestation along a chronosequence.

Methods

We investigated changes in vegetation communities, soil properties and soil microbial communities 5, 15, 25, and 35 years (Y) after R. pseudoacacia afforestation on cropland on the Loess Plateau. Soil microbial community compositions were analyzed using 16S rRNA and ITS high-throughput gene sequencing.

Results

The diversity and richness of understory vegetation community decreased with restoration stage, and available phosphorus and ammonium contents in soil were consistently low. The bacterial communities converted from Acidobacteria- to Proteobacteria-dominant communities within 25-Y but transitioned again to Acidobacteria-dominant communities at the 35-Y sites. Ascomycota and Zygomycota were the dominant fungal phyla at all sites. Compared to the cropland, fungal community composition changed at the 5-Y sites and the bacterial community composition changed at the 25-Y sites.

Conclusions

R. pseudoacacia afforestation significantly altered soil bacteria richness rather than its diversity. The planted R. pseudoacacia rapidly altered the soil fungal community composition and altered bacterial community composition at the 25-Y. The changes in soil bacterial communities were driven by the phyla of Actinobacteria, Gemmatimonadetes and Nitrospirae and lagged behind the changes in vegetation communities. Phosphorus was a principal factor in shaping microbial community composition.

Keywords

Afforestation Loess plateau Robinia pseudoacacia Soil microbial community 16S rRNA and ITS high-throughput gene sequencing 

Notes

Acknowledgments

This work was financially supported by the Research Special Topic under the auspices of the Forestry Science and Technology Support Plan, Researches and Demonstration of the Key Technology for Plantation Sustainable Management in the Loess Plateau (Grant No. 2012BAD22B0302).

Supplementary material

11104_2017_3516_MOESM1_ESM.xlsx (10 kb)
Supplementary S1 (XLSX 10 kb)
11104_2017_3516_MOESM2_ESM.xls (52 kb)
Supplementary S2 (XLS 52 kb)

References

  1. Baldrian P (2006) Fungal laccases - occurrence and properties. FEMS Microbiol Rev 30:215–242.  https://doi.org/10.1111/j.1574-4976.2005.00010.x CrossRefPubMedGoogle Scholar
  2. Benesperi R, Giuliani C, Zanetti S, Gennai M, Lippi MM, Guidi T, Nascimbene J, Foggi B.. (2012) Forest plant diversity is threatened by Robinia Pseudoacacia (black-locust) invasion biodiversity and conservation. Biodiversity and Conservation 21:3555–3568 doi: https://doi.org/10.1007/s10531-012-0380-5
  3. Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol 79:2519–2526.  https://doi.org/10.1128/Aem.03870-12 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bolat I, Kara O, Sensoy H, Yüksel K (2016) Influences of black locust (Robinia Pseudoacacia L.) afforestation on soil microbial biomass and activity. iForest - Biogeosciences and Forestry 9:171–177.  https://doi.org/10.3832/ifor1410-007 CrossRefGoogle Scholar
  5. Buzhdygan OY, Rudenko SS, Kazanci C, Patten BC (2016) Effect of invasive black locust (Robinia Pseudoacacia L.) on nitrogen cycle in floodplain ecosystem. Ecol Model 319:170–177.  https://doi.org/10.1016/j.ecolmodel.2015.07.025 CrossRefGoogle Scholar
  6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chodak M, Klimek B, Niklinska M (2016) Composition and activity of soil microbial communities in different types of temperate forests. Biol Fert Soils 52:1093–1104.  https://doi.org/10.1007/s00374-016-1144-2 CrossRefGoogle Scholar
  8. Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological Flora of the British isles:Robinia Pseudoacacia. J Ecol 101:1623–1640.  https://doi.org/10.1111/1365-2745.12162 CrossRefGoogle Scholar
  9. De Marco A, Arena C, Giordano M, Virzo De Santo A (2013) Impact of the invasive tree black locust on soil properties of Mediterranean stone pine-holm oak forests. Plant Soil 372:473–486.  https://doi.org/10.1007/s11104-013-1753-6 CrossRefGoogle Scholar
  10. Dzwonko Z, Loster S (1997) Effects of dominant trees and anthropogenic disturbances on species richness and floristic composition of secondary communities in southern Poland. J Appl Ecol 34:861–870.  https://doi.org/10.2307/2405277 CrossRefGoogle Scholar
  11. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  12. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364.  https://doi.org/10.1890/05-1839 CrossRefPubMedGoogle Scholar
  14. Finotti R, Freitas SR, Cerqueira R, Vieira MV (2003) A method to determine the minimum number of litter traps in litterfall studies. Biotropica 35:419–421CrossRefGoogle Scholar
  15. Frouz J, Pizl V, Cienciala E, Kalcik J (2009) Carbon storage in post-mining forest soil, the role of tree biomass and soil bioturbation. Biogeochemistry 94:111–121.  https://doi.org/10.1007/s10533-009-9313-0 CrossRefGoogle Scholar
  16. Grossman R, Reinsch T (2002) 2.1 bulk density and linear extensibility methods of soil analysis: part 4 physical methods. 4:201–228Google Scholar
  17. Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc Natl Acad Sci USA 105:17842–17847.  https://doi.org/10.1073/pnas.0808254105 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Islam KR, Weil RR (2000) Land use effects on soil quality in a tropical forest ecosystem of Bangladesh. Agric Ecosyst Environ 79(1):9–16CrossRefGoogle Scholar
  19. Jiao JY, Zhang ZG, Bai WJ, Jia YF, Wang N (2012) Assessing the ecological success of restoration by afforestation on the Chinese loess plateau. Restor Ecol 20:240–249.  https://doi.org/10.1111/j.1526-100X.2010.00756.x CrossRefGoogle Scholar
  20. Jin Z, Li XR, Wang YQ, Wang Y, Wang KB, Cui BL (2016) Comparing watershed black locust afforestation and natural revegetation impacts on soil nitrogen on the Loess Plateau of China Sci Rep-Uk 6.  https://doi.org/10.1038/srep25048
  21. Józefowska A, Pietrzykowski M, Woś B, Cajthaml T, Frouz J (2017) The effects of tree species and substrate on carbon sequestration and chemical and biological properties in reforested post-mining soils. Geoderma 292:9–16CrossRefGoogle Scholar
  22. Keeney D, Nelson D, Page A (1982) Methods of soil analysis. Part. 2. Chemical and microbiological properties. Eds CA black et al:711-733Google Scholar
  23. Kou M, Garcia-Fayos P, Hu S, Jiao JY (2016) The effect of Robinia Pseudoacacia afforestation on soil and vegetation properties in the loess plateau (China): a chronosequence approach. For Ecol Manag 375:146–158.  https://doi.org/10.1016/j.foreco.2016.05.025 CrossRefGoogle Scholar
  24. Lewis DE, White JR, Wafula D, Athar R, Dickerson T, Williams HN, Chauhan A (2010) Soil functional diversity analysis of a bauxite-mined restoration Chronosequence. Microb Ecol 59:710–723.  https://doi.org/10.1007/s00248-009-9621-x CrossRefPubMedGoogle Scholar
  25. Liu G, Deng T (1991) Mathematical model of the relationship between nitrogen-fixation by black locust and soil conditions. Soil Biol Biochem 23:1–7CrossRefGoogle Scholar
  26. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC.. (2012) Defining the core Arabidopsis Thaliana root microbiome. Nature 488:86−+.  https://doi.org/10.1038/nature11237
  27. Malcolm GM, Bush DS, Rice SK (2008) Soil nitrogen conditions approach preinvasion levels following restoration of nitrogen-fixing black locust (Robinia Pseudoacacia) stands in a pine-oak ecosystem. Restor Ecol 16:70–78.  https://doi.org/10.1111/j.1526-100X.2007.00263.x CrossRefGoogle Scholar
  28. Mao PL, HX M, Cao BH, Qin YJ, Shao HB, Wang SM, Tai XG (2016) Dynamic characteristics of soil properties in a Robinia Pseudoacacia vegetation and coastal eco-restoration. Ecol Eng 92:132–137.  https://doi.org/10.1016/j.ecoleng.2016.03.037 CrossRefGoogle Scholar
  29. Montecchia MS, Tosi M, Soria MA, Vogrig JA, Sydorenko O, Correa OS (2015) Pyrosequencing reveals changes in soil bacterial communities after conversion of yungas forests to agriculture. PLoS One 10(3):e0119426.  https://doi.org/10.1371/journal.pone.0119426 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata Y, Fujiyama A, Tsuda M, Kurokawa K (2014) Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res 21:217–227.  https://doi.org/10.1093/dnares/dst052 CrossRefPubMedGoogle Scholar
  31. Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S (2012) Environmental factors affect Acidobacterial communities below the subgroup level in grassland and Forest soils. Appl Environ Microbiol 78:7398–7406.  https://doi.org/10.1128/Aem.01325-12 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Niu HB, Liu WX, Wan FH, Liu B (2007) An invasive aster (Ageratina Adenophora) invades and dominates forest understories in China: altered soil microbial communities facilitate the invader and inhibit natives. Plant Soil 294:73–85.  https://doi.org/10.1007/s11104-007-9230-8 CrossRefGoogle Scholar
  33. Nunez-Mir GC, Iannone BV, Curtis K, Fei SL (2015) Evaluating the evolution of forest restoration research in a changing world: a "big literature" review. New For 46:669–682.  https://doi.org/10.1007/s11056-015-9503-7 CrossRefGoogle Scholar
  34. OriginLab O (2016) Data analysis and graphing software. OriginLab Corp., NorthamptonGoogle Scholar
  35. Papaioannou A, Chatzistathis T, Papaioannou E, Papadopoulos G (2016) Robinia pseudοacacia as a valuable invasive species for the restoration of degraded croplands. Catena 137:310–317.  https://doi.org/10.1016/j.catena.2015.09.019 CrossRefGoogle Scholar
  36. Peloquin RL, Hiebert RD (1999) The effects of black locust (Robinia Pseudoacacia L.) on species diversity and composition of black oak savanna/woodland communities. Nat Area J 19:121–131Google Scholar
  37. Ren C, Sun P, Kang D, Zhao F, Feng Y, Ren G, Han X, Yang G (2016) Responsiveness of soil nitrogen fractions and bacterial communities to afforestation in the loess hilly region (LHR) of China. Sci Rep-Uk 6.  https://doi.org/10.1038/srep28469
  38. Richardson DM, Rejmanek M (2011) Trees and shrubs as invasive alien species - a global review. Divers Distrib 17:788–809.  https://doi.org/10.1111/j.1472-4642.2011.00782.x CrossRefGoogle Scholar
  39. Sabate S, Gracia CA, Sanchez A (2002) Likely effects of climate change on growth of Quercus Ilex, Pinus Halepensis, Pinus Pinaster, Pinus Sylvestris and Fagus Sylvatica forests in the Mediterranean region. Forest Ecol Manag 162:23–37.  https://doi.org/10.1016/S0378-1127(02)00048-8 CrossRefGoogle Scholar
  40. Santos F, Nadelhoffer K, Bird JA (2016) Rapid fine root C and N mineralization in a northern temperate forest soil. Biogeochemistry 128:187–200.  https://doi.org/10.1007/s10533-016-0202-z CrossRefGoogle Scholar
  41. Schomaker ME, Zarnoch SJ, Bechtold WA, Latelle DJ, Burkman WG, Cox SM (2007) Crown-condition classification: a guide to data collection and analysis. Gen Tech Rep SRS-102. Asheville, US Department of Agriculture, Forest Service, Southern Research Station, p 78Google Scholar
  42. Sitzia T, Campagnaro T, Dainese M, Cierjacks A (2012) Plant species diversity in alien black locust stands: a paired comparison with native stands across a north-Mediterranean range expansion. For Ecol Manag 285:85–91.  https://doi.org/10.1016/j.foreco.2012.08.016 CrossRefGoogle Scholar
  43. Steege HT (2004) Measuring biological diversity. Environ Ecol Stat 1(2):95–103Google Scholar
  44. Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245.  https://doi.org/10.1016/S1369-5274(02)00324-7 CrossRefPubMedGoogle Scholar
  45. Trentanovi G, von der Lippe M, Sitzia T, Ziechmann U, Kowarik I, Cierjacks A (2013) Biotic homogenization at the community scale: disentangling the roles of urbanization and plant invasion. Divers Distrib 19:738–748.  https://doi.org/10.1111/ddi.12028 CrossRefGoogle Scholar
  46. Tripathi BM, Song W, Slik JWF, Sukri RS, Jaafar S, Dong K, Adams JM (2016) Distinctive tropical Forest variants have unique soil microbial communities, but not always low microbial diversity. Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.00376
  47. 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 11:296–310.  https://doi.org/10.1111/j.1461-0248.2007.01139.x CrossRefPubMedGoogle Scholar
  48. Vitkova M, Kolbek J (2010) Vegetation classification and synecology of bohemian Robinia pseudacacia stands in a central European context. Phytocoenologia 40:205–241.  https://doi.org/10.1127/0340-269x/2010/0040-0425 CrossRefGoogle Scholar
  49. Vitkova M, Tonika J, Mullerova J (2015) Black locust--successful invader of a wide range of soil conditions. Sci Total Environ 505:315–328.  https://doi.org/10.1016/j.scitotenv.2014.09.104 CrossRefPubMedGoogle Scholar
  50. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components vol 34. Princeton University Press, New JerseyGoogle Scholar
  51. Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Penuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr 85:133–155.  https://doi.org/10.1890/14-0777.1 CrossRefGoogle Scholar
  52. Zhang C, Liu GB, Xue S, Wang GL (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the loess plateau. Soil Biol Biochem 97:40–49.  https://doi.org/10.1016/j.soilbio.2016.02.013 CrossRefGoogle Scholar
  53. Zhao FZ, Zhang L, Ren CJ, Sun J, Han XH, Yang GH, Wang J (2016) Effect of microbial carbon, nitrogen, and phosphorus stoichiometry on soil carbon fractions under a black locust Forest within the central loess plateau of China. Soil Sci Soc Am J 80:1520–1530.  https://doi.org/10.2136/sssaj2016.06.0175 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.College of ForestryNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.Key Comprehensive Laboratory of ForestryYanglingPeople’s Republic of China
  3. 3.Key Laboratory of Silviculture on the Loess Plateau State Forestry AdministrationYanglingPeople’s Republic of China

Personalised recommendations