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 sha** microbial community composition.
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References
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
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
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
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
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
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
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
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
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
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
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
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
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
Finotti R, Freitas SR, Cerqueira R, Vieira MV (2003) A method to determine the minimum number of litter traps in litterfall studies. Biotropica 35:419–421
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
Grossman R, Reinsch T (2002) 2.1 bulk density and linear extensibility methods of soil analysis: part 4 physical methods. 4:201–228
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
Islam KR, Weil RR (2000) Land use effects on soil quality in a tropical forest ecosystem of Bangladesh. Agric Ecosyst Environ 79(1):9–16
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
** 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
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 292:9–16
Keeney D, Nelson D, Page A (1982) Methods of soil analysis. Part. 2. Chemical and microbiological properties. Eds CA black et al:711-733
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
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
Liu G, Deng T (1991) Mathematical model of the relationship between nitrogen-fixation by black locust and soil conditions. Soil Biol Biochem 23:1–7
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
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
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
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
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
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
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
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
OriginLab O (2016) Data analysis and graphing software. OriginLab Corp., Northampton
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
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 19:121–131
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
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
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
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
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 78
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
Steege HT (2004) Measuring biological diversity. Environ Ecol Stat 1(2):95–103
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
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
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
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
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
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
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components vol 34. Princeton University Press, New Jersey
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
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
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
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).
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Liu, J., Yang, Z., Dang, P. et al. Response of soil microbial community dynamics to Robinia pseudoacacia L. afforestation in the loess plateau: a chronosequence approach. Plant Soil 423, 327–338 (2018). https://doi.org/10.1007/s11104-017-3516-2
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DOI: https://doi.org/10.1007/s11104-017-3516-2