Soil bacterial community differences along a coastal restoration chronosequence

  • Dongfeng Yan
  • Andrew Bissett
  • Nicholas Gellie
  • Jacob G. Mills
  • Andrew J. LoweEmail author
  • Martin F. BreedEmail author


Restoration interventions such as revegetation are globally-important to combat biodiversity declines and land degradation. However, restoration projects are generally poorly monitored because current approaches to monitoring are limited in their ability to assess important components of biodiversity, such as belowground microbial diversity. Since soil bacterial communities mediate many belowground ecosystems processes and represent substantial biodiversity in their own right, bacteria are important components to monitor during ecosystem restoration. High-throughput amplicon sequencing (DNA metabarcoding) has been put forward as a potential cost-effective, scalable and easy-to-standardise partial solution to restoration’s monitoring problem. However, its application to restoration projects has to date been limited. Here, we used DNA metabarcoding of bacterial 16S rRNA gene from soil DNA to explore community differences across a 16-year restoration chronosequence. The bacterial composition in the oldest revegetation sites was comparable to the remnant sites. Proteobacteria and Acidobacteria were significantly higher in relative sequence abundance, while Actinobacteria was significantly lower, with time since revegetation. Classes Alphaproteobacteria and Acidobacteria were indicative of remnant and the oldest revegetation sites, while Deltaproteobacteria and Rubrobacteria were characteristic of younger revegetation sites. Changes in the soil physical and chemical characteristics associated with revegetation appear to shape bacterial community structure and composition. These findings provide evidence that revegetation can have positive effects on belowground microbial communities, and help demonstrate that the soil bacterial community can be restored towards its native state by revegetation, which may be useful in restoration monitoring.


Bacterial community Coastal restoration DNA metabarcoding Environmental microbiome Revegetation 



This work was supported by funding from the China Scholarship Council (201408410176 awarded to DY). We thank L. Blake, M. Durant, I. Fox, F. Hutchings, C. Jackson, M. Laws, J. McDonald for technical and field assistance. We are grateful for the contribution of the Biomes of Australian Soil Environments (BASE) consortium ( in the generation of data used in this publication. The BASE project is supported by funding from Bioplatforms Australia through the Australian Government National Collaborative Research Infrastructure Strategy.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

11258_2019_979_MOESM1_ESM.docx (123 kb)
Supplementary file1 (DOCX 123 kb)


  1. Allison VJ, Yermakov Z, Miller RM, Jastrow JD, Matamala R (2007) Using landscape and depth gradients to decouple the impact of correlated environmental variables on soil microbial community composition. Soil Biol Biochem 39:505–516CrossRefGoogle Scholar
  2. An S, Huang Y, Zheng F (2009) Evaluation of soil microbial indices along a revegetation chronosequence in grassland soils on the Loess Plateau, Northwest China. Appl Soil Ecol 41:286–292CrossRefGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Baldrian P (2019) The known and the unknown in soil microbial ecology. FEMS Microbiol Ecol 95:9CrossRefGoogle Scholar
  5. Balint M, Bahram M, Eren AM, Faust K, Fuhrman JA, Lindahl B, O'Hara RB, Opik M, Sogin ML, Unterseher M, Tedersoo L (2016) Millions of reads, thousands of taxa: microbial community structure and associations analyzed via marker genes. FEMS Microbiol Rev 40:686–700PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bandick AK, Dick RP (1999) Field management effects on soil enzyme activities. Soil Biol Biochem 31:1471–1479CrossRefGoogle Scholar
  7. Banning NC, Gleeson DB, Grigg AH, Grant CD, Andersen GL, Brodie EL, Murphy D (2011a) Soil microbial community successional patterns during forest ecosystem restoration. Appl Environ Microbiol 77:6158–6164PubMedPubMedCentralCrossRefGoogle Scholar
  8. Banning NC, Phillips IR, Jones DL, Murphy DV (2011b) Development of microbial diversity and functional potential in Bauxite Residue Sand under rhabilitation. Restor Ecol 19:78–87CrossRefGoogle Scholar
  9. Barnes MA, Turner CR (2015) The ecology of environmental DNA and implications for conservation genetics. Conserv Genet 17:1–17CrossRefGoogle Scholar
  10. Bissett A, Fitzgerald A, Meintjes T, Mele PM, Reith F, Dennis PG, Breed MF, Brown B, Brown MV, Brugger J, Byrne M, Caddy-Retalic S, Carmody B, Coates DJ, Correa C, Ferrari BC, Gupta VV, Hamonts K, Haslem A, Hugenholtz P, Karan M, Koval J, Lowe AJ, Macdonald S, McGrath L, Martin D, Morgan M, North KI, Paungfoo-Lonhienne C, Pendall E, Phillips L, Pirzl R, Powell JR, Ragan MA, Schmidt S, Seymour N, Snape I, Stephen JR, Stevens M, Tinning M, Williams K, Yeoh YK, Zammit CM, Young A (2016) Introducing BASE: the biomes of Australian soil environments soil microbial diversity database. Gigascience 5:1–11CrossRefGoogle Scholar
  11. Breed MF, Harrison PA, Blyth C, Byrne M, Gaget V, Gellie NJC, Groom SVC, Hodgson R, Mills JG, Prowse TAA, Steane DA, Mohr JJ (2019) The potential of genomics for restoring ecosystems and biodiversity. Nat Rev Genet 20(10):615–628PubMedCrossRefGoogle Scholar
  12. Bullock JM, Aronson J, Newton AC, Pywell RF, Rey-Benayas JM (2011) Restoration of ecosystem services and biodiversity: conflicts and opportunities. Trends Ecol Evol 26:541–549PubMedCrossRefGoogle Scholar
  13. Bulman SR, McDougal RL, Hill K, Lear G (2018) Opportunities and limitations for DNA metabarcoding in Australasian plant-pathogen biosecurity. Australas Plant Pathol 47:467–474CrossRefGoogle Scholar
  14. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733PubMedCrossRefGoogle Scholar
  15. Cavagnaro T, Cunningham S, Fitzpatrick S (2016) Pastures to woodlands: changes in soil microbial communities and carbon following reforestation. Appl Soil Ecol 107:24–32CrossRefGoogle Scholar
  16. Collen B, Nicholson E (2014) Taking the measure of change. Science 346:166–167PubMedCrossRefGoogle Scholar
  17. Corlett RT (2017) A bigger toolbox: biotechnology in biodiversity conservation. Trends Biotechnol 35:55–65PubMedCrossRefGoogle Scholar
  18. Cowart DA, Pinheiro M, Mouchel O, Maguer M, Grall J, Mine J, Arnaud-Haond S (2015) Metabarcoding is powerful yet still blind: a comparative analysis of morphological and molecular surveys of seagrass communities. PLoS ONE 10:e0117562PubMedPubMedCentralCrossRefGoogle Scholar
  19. De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684CrossRefGoogle Scholar
  20. De Palma A, Sanchez-Ortiz K, Martin PA, Chadwick A, Gilbert G, Bates AE, Börger L, Contu S, Hill SLL, Purvis A (2018) Challenges with inferring how land-use affects terrestrial biodiversity: study design, time, space and synthesis. In: Bohan DA, Dumbrell AJ, Woodward G, Jackson M (eds) Advances in ecological research. Academic Press, Cambridge, pp 163–199Google Scholar
  21. Delgado-Baquerizo M, Powell JR, Hamonts K, Reith F, Mele P, Brown MV, Dennis PG, Ferrari BC, Fitzgerald A, Young A, Singh BK, Bissett A (2017) Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale. New Phytol 215(3):1186–1196PubMedCrossRefGoogle Scholar
  22. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  24. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996PubMedCrossRefGoogle Scholar
  25. Egidi E, Wood JL, Celestina C, May TW, Mele P, Edwards J, Powell J, Bissett A, Franks AE (2019) Delving into the dark ecology: a continent-wide assessment of patterns of composition in soil fungal communities from Australian tussock grasslands. Fung Ecol 39:356–370CrossRefGoogle Scholar
  26. Epstein S (2013) The phenomenon of microbial uncultivability. Curr Opin Microbiol 16:636–642PubMedCrossRefGoogle Scholar
  27. Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, De Barba M, Gielly L, Lopes CM, Boyer F, Pompanon F, Rayé G, Taberlet P (2015) Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol Ecol Resour 15:543–556PubMedCrossRefGoogle Scholar
  28. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefGoogle Scholar
  29. Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173CrossRefGoogle Scholar
  30. Gellie NJC, Mills JG, Breed MF, Lowe AJ (2017) Revegetation rewilds the soil bacterial microbiome of an old field. Mol Ecol 26:2895–2904PubMedCrossRefPubMedCentralGoogle Scholar
  31. Gomez-Escribano JP, Alt S, Bibb MJ (2016) Next generation sequencing of Actinobacteria for the discovery of novel natural products. Mar Drugs 14:78PubMedCentralCrossRefGoogle Scholar
  32. Guo XP, Chen HYH, Meng MJ, Biswas SR, Ye LX, Zhang JC (2016) Effects of land use change on the composition of soil microbial communities in a managed subtropical forest. For Ecol Manag 373:93–99CrossRefGoogle Scholar
  33. Guo Y, Chen X, Wu Y, Zhang L, Cheng J, Wei G, Lin Y (2018) Natural revegetation of a semiarid habitat alters taxonomic and functional diversity of soil microbial communities. Sci Tot Environ 635:598–606CrossRefGoogle Scholar
  34. Hamonts K, Bissett A, Macdonald BCT, Barton PS, Manning AD, Young A (2017) Effects of ecological restoration on soil microbial diversity in a temperate grassy woodland. Appl Soil Ecol 117–118:117–128CrossRefGoogle Scholar
  35. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497PubMedPubMedCentralCrossRefGoogle Scholar
  36. Harris JA (2003) Measurements of the soil microbial community for estimating the success of restoration. Eur J Soil Sci 54:801–808CrossRefGoogle Scholar
  37. Harris J (2009) Soil microbial communities and restoration ecology: facilitators or followers? Science 325:573–574PubMedCrossRefPubMedCentralGoogle Scholar
  38. Herrera PS, Lebeis SL, Bailey JK (2016) Giving back to the community: microbial mechanisms of plant-soil interactions. Funct Ecol 30:1043–1052CrossRefGoogle Scholar
  39. Hua J, Feng Y, Jiang Q, Bao X, Yin Y (2017) Shift of bacterial community structure along different coastal reclamation histories in Jiangsu, Eastern China. Sci Rep 7:10096PubMedPubMedCentralCrossRefGoogle Scholar
  40. Huang X, Liu L, Wen T, Zhu R, Zhang J, Cai Z (2015) Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f.sp cubense infected soil during and after reductive soil disinfestation. Microbiol Res 181:33–42PubMedCrossRefGoogle Scholar
  41. Jesus EC, Marsh TL, Tiedje JM, de Moreira FMS (2009) Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J 3:1004–1011CrossRefGoogle Scholar
  42. Ji Y, Ashton L, Pedley SM, Edwards DP, Tang Y, Nakamura A, Kitching R, Dolman PM, Woodcock P, Edwards FA, Larsen TH, Hsu WW, Benedick S, Hamer KC, Wilcove DS, Bruce C, Wang X, Levi T, Lott M, Emerson BC, Yu DW (2013) Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecol Lett 16:1245–1257PubMedCrossRefGoogle Scholar
  43. Jost L (2006) Entropy and diversity. Oikos 113:363–375CrossRefGoogle Scholar
  44. Koch H, Luecker S, Albertsen M, Kitzinger K, Herbold C, Spieck E, Nielsen PH, Wagner M, Daims H (2015) Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc Natl Acad Sci USA 112:11371–11376PubMedCrossRefGoogle Scholar
  45. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199CrossRefGoogle Scholar
  46. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 125–175Google Scholar
  47. Li J, Tong X, Awasthi MK, Wu F, Ha S, Ma J, Sun X, He C (2018) Dynamics of soil microbial biomass and enzyme activities along a chronosequence of desertified land revegetation. Ecol Eng 111:22–30CrossRefGoogle Scholar
  48. Liao H, Zheng C, Li J, Long J (2018) Dynamics of soil microbial recovery from cropland to orchard along a 20-year chronosequence in a degraded karst ecosystem. Sci Tot Environ 639:1051–1059CrossRefGoogle Scholar
  49. Liddicoat C, Weinstein P, Bissett A, Gellie NJ, Mills JG, Waycott M, Breed MF (2019) Can bacterial indicators of a grassy woodland restoration inform ecosystem assessment and microbiota-mediated human health? Environ Int 129:105–117PubMedCrossRefGoogle Scholar
  50. Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjoller R, Koljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user's guide. New Phytol 199:288–299PubMedPubMedCentralCrossRefGoogle Scholar
  51. Liu J, Li S, Ouyang Z, Tam C, Chen X (2008) Ecological and socioeconomic effects of China's policies for ecosystem services. Proc Natl Acad Sci USA 105:9477–9482PubMedCrossRefGoogle Scholar
  52. Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809PubMedCrossRefGoogle Scholar
  53. Luecker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damste JSS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107:13479–13484CrossRefGoogle Scholar
  54. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963PubMedPubMedCentralCrossRefGoogle Scholar
  55. Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755PubMedCrossRefGoogle Scholar
  56. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217PubMedPubMedCentralCrossRefGoogle Scholar
  57. Mihajlovski A, Gabarre A, Seyer D, Bousta F, Di Martino P (2017) Bacterial diversity on rock surface of the ruined part of a French historic monument: the Chaalis abbey. Int Biodeterior Biodegrad 120:161–169CrossRefGoogle Scholar
  58. Moon JB, Wardrop DH, Bruns MAV, Miller RM, Naithani KJ (2016) Land-use and land-cover effects on soil microbial community abundance and composition in headwater riparian wetlands. Soil Biol Biochem 97:215–233CrossRefGoogle Scholar
  59. Moreno M, de-Bashan LE, Hernandez J-P, Lopez BR, Bashan Y (2017) Success of long-term restoration of degraded arid land using native trees planted 11 years earlier. Plant Soil 421:83–92CrossRefGoogle Scholar
  60. Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122PubMedCrossRefGoogle Scholar
  61. Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., McGlinn D., Minchin P.R., O’Hara R.B., Simpson G.L., Solymos P., Stevens M.H.S., Szoecs E. and Wagner H. 2018. Vegan: community ecology package. R package version 2.5-1Google Scholar
  62. Qi S, Zheng H, Lin Q, Li G, Xi Z, Zhao X (2011) Effects of livestock grazing intensity on soil biota in a semiarid steppe of Inner Mongolia. Plant Soil 340:117–126CrossRefGoogle Scholar
  63. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  64. Reyers B, Biggs R, Cumming GS, Elmqvist T, Hejnowicz AP, Polasky S (2013) Getting the measure of ecosystem services: a social-ecological approach. Front Ecol Environ 11:268–273CrossRefGoogle Scholar
  65. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A (2014) Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2:e545PubMedPubMedCentralCrossRefGoogle Scholar
  66. Rime T, Hartmann M, Brunner I, Widmer F, Zeyer J, Frey B (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol Ecol 24:1091–1108PubMedCrossRefGoogle Scholar
  67. Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS Jr, Tsai SM, Feigl B, Tiedje JM, Bohannan BJ, Nuesslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci USA 110:988–993PubMedCrossRefGoogle Scholar
  68. Ros M, Hernandez MT, García C (2003) Soil microbial activity after restoration of a semiarid soil by organic amendments. Soil Biol Biochem 35:463–469CrossRefGoogle Scholar
  69. Ross D, Speir T, Tate K, Cairns A, Meyrick KF, Pansier EA (1982) Restoration of pasture after topsoil removal: effects on soil carbon and nitrogen mineralization, microbial biomass and enzyme activities. Soil Biol Biochem 14:575–581CrossRefGoogle Scholar
  70. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedPubMedCentralCrossRefGoogle Scholar
  71. Sigler WV, Zeyer J (2002) Microbial diversity and activity along the forefields of two receding glaciers. Microb Ecol 43:397–407PubMedCrossRefPubMedCentralGoogle Scholar
  72. Singh JS, Gupta VK (2018) Soil microbial biomass: a key soil driver in management of ecosystem functioning. Sci Tot Environ 634:497–500CrossRefGoogle Scholar
  73. Steenwerth KL, Jackson LE, Calderón FJ, Stromberg MR, Scow KM (2002) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 34:1599–1611CrossRefGoogle Scholar
  74. Strimmer K (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24:1461–1462PubMedCrossRefPubMedCentralGoogle Scholar
  75. Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050PubMedCrossRefPubMedCentralGoogle Scholar
  76. Temmerman S, Meire P, Bouma TJ, Herman PMJ, Ysebaert T, De Vriend HJ (2013) Ecosystem-based coastal defence in the face of global change. Nature 504:79–83PubMedCrossRefPubMedCentralGoogle Scholar
  77. Thomsen PF, Willerslev E (2015) Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18CrossRefGoogle Scholar
  78. Trivedi P, Delgado-Baquerizo M, Anderson IC, Singh BK (2016) Response of soil properties and microbial communities to agriculture: implications for primary productivity and soil health indicators. Front Plant Sci 7:990PubMedPubMedCentralGoogle Scholar
  79. Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF, Bellemain E, Besnard A, Coissac E, Boyer F (2016) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol 25:929–942PubMedPubMedCentralCrossRefGoogle Scholar
  80. Vandamme P, Opelt K, Knoechel N, Berg C, Schoenmann S, De Brandt E, Eberl L, Falsen E, Berg G (2007) Burkholderia bryophila sp nov and Burkholderia megapolitana sp nov., moss-associated species with antifungal and plant-growth-promoting properties. Int J Syst Evol Microbiol 57:2228–2235PubMedCrossRefGoogle Scholar
  81. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267PubMedPubMedCentralCrossRefGoogle Scholar
  82. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedPubMedCentralCrossRefGoogle Scholar
  83. Wheeler B, Torchiano M (2016) lmPerm: permutation tests for linear models. R package version 2.1.0Google Scholar
  84. Xue L, Ren H, Li S, Leng X, Yao X (2017) Soil bacterial community structure and co-occurrence pattern during vegetation restoration in Karst rocky desertification area. Front Microbiol 8:2377PubMedPubMedCentralCrossRefGoogle Scholar
  85. Yan D, Mills JG, Gellie NJC, Bissett A, Lowe AJ, Breed MF (2018) High-throughput eDNA monitoring of fungi to track functional recovery in ecological restoration. Biol Conserv 217:113–120CrossRefGoogle Scholar
  86. Yao M, Rui J, Li J, Wang J, Cao W, Li X (2018) Soil bacterial community shifts driven by restoration time and steppe types in the degraded steppe of Inner Mongolia. CATENA 165:228–236CrossRefGoogle Scholar
  87. You S, Kim M, Lee J, Chon J (2018) Coastal landscape planning for improving the value of ecosystem services in coastal areas: using system dynamics model. Environ Pollut 242:2040–2050PubMedCrossRefGoogle Scholar
  88. Zechmeister-Boltenstern S, Michel K, Pfeffer M (2011) Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen deposition. Plant Soil 343:37–50CrossRefGoogle Scholar
  89. Zheng J, Chen J, Pan G, Wang G, Liu X, Zhang X, Li L, Bian R, Cheng K, Zheng J (2017) A long-term hybrid poplar plantation on cropland reduces soil organic carbon mineralization and shifts microbial community abundance and composition. Appl Soil Ecol 111:94–104CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of ForestryHenan Agricultural UniversityZhengzhouChina
  2. 2.School of Biological Sciences and the Environment InstituteUniversity of AdelaideAdelaideAustralia
  3. 3.CSIROHobartAustralia

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