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Introduction of broadleaf species into monospecific Cunninghamia lanceolata plantations changed the soil Acidobacteria subgroups composition and nitrogen-cycling gene abundances

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Abstract

Aims

The introduction of broadleaf species into Cunninghamia lanceolata monoculture plantations could be a sustainable silvicultural practice for restoring soil fertility. We hypothesize that the addition of Phoebe bournei tree species will change soil physicochemical factors and microbial composition.

Methods

Soil physicochemical factors were determined. Bacterial composition and N-cycling functional genes were investigated by Illumina MiSeq sequencing and qPCR, respectively, and by using a co-occurrence network to explore the connections between the relative abundance of bacteria and soil physicochemical parameters.

Results

The introduction of P. bournei into C. lanceolata plantations increased available nutrients in the soil, decreased toxicity (Al3+ level), and slightly increased the soil bacterial diversity. The relative abundance of the total Acidobacteria community, as well as the most abundant subgroups (1, 2, and 3), were significantly higher in the monospecific stands. Different Acidobacteria subgroups behaved differently, i.e., Gp2 correlated negatively with soil nutrients and positively with the Al3+ level, while Gp17 showed the opposite behavior. Quantification of seven nitrogen cycling genes revealed that the nifH, nrfA, and nosZ abundances were higher in the mixed stands, while the nirK abundance was higher in the monospecific plantations. Co-occurrence network analyses showed a strong correlation between soil properties and the bacterial community.

Conclusion

P. bournei introduction into C. lanceolata plantations improved soil nutrients and affected the soil bacterial community. The higher nitrogen nifH and nrfA abundance in the mixed stands indicated a higher nitrogen fixation and dissimilatory nitrate reduction potential. Acidobacterial subgroups showed the opposite behavior to P. bournei introduction and could be used as indicators of soil nutrient changes.

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References

  • Ai C, Liang GQ, Sun JG, He P, Tang SH, YangSH ZW, Wang XB (2015) The alleviation of acid soil stress in rice by inorganic or organic ameliorants is associated with changes in soil enzyme activity and microbial community composition. Biol Fert Soils 51(4):465–477

    Article  CAS  Google Scholar 

  • Augusto L, Ranger J, Binkley D, Rothe A (2002) Impact of several common tree species of European temperate forests on soil fertility. Ann Forest Sci 59:233–253

    Article  Google Scholar 

  • Augusto L, Schrijver AD, Vesterdal L, Smolander A, Prescott C, Ranger J (2015) Influences of evergreen gymnosperm and deciduous angiosperm tree species on the functioning of temperate and boreal forests. Biol Rev 90:444–466

    Article  PubMed  Google Scholar 

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: An Open Source Software for Exploring and Manipulating Networks. Proceedings of the Third International Conference on Weblogs and Social Media, ICWSM 2009, San Jose, California, USA

  • Bonifacio E, Caimi A, Falsone G, Trofimov SY, Zanini E, Godbold DL (2008) Soil properties under Norway spruce differ in spruce dominated and mixed broadleaf forests of the Southern Taiga. Plant Soil 308:149–159

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cederlund H, Wessén E, Enwall K, Jones CM, Juhanson J, Pell M, Philippot L, Hallin S (2014) Soil carbon quality and nitrogen fertilization structure bacterial communities with predictable responses of major bacterial phyla. Appl Soil Ecol 84:62–68

    Article  Google Scholar 

  • Chang Y, Fenliang F, Alin S, Peiyuan C, Tingqiang Li (2015) Denitrification potential under different fertilization regimes is closely coupled with changes in the denitrifying community in a black soil. Appl Microbiol Biot 99:5719–5729

    Article  CAS  Google Scholar 

  • Chen AL, Lin SZ, Chen SP, Chen YZ (2006) Comparison on litterfall character of Phoebe bournei and Cunninghamia lanceolata plantation in the field of successive planting Cunninghamia lanceolata. J Fujian Coll Forest 26:289–293 (in Chinese with an English abstract)

    Google Scholar 

  • Chen C, Chen HYH, Chen X, Huang Z (2019) Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration. Nat Commun 10:1332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen CY, Zhang JW, Zhou CL, Zheng HY (1990) Researches on improving the quality of forest land and the productivity of artificial Cunninghamia lanceolata stands. Chin J Appl Ecol 1:97–106 (in Chinese with an English abstract)

    Google Scholar 

  • Chen LC, Wang SL, Wang P, Kong CH (2014) Autoinhibition and soil allelochemical (cyclic dipeptide) levels in replanted Chinese fir (Cunninghamia lanceolata) plantations. Plant Soil 374:793–801

    Article  CAS  Google Scholar 

  • Chen S (2002) The water holding capacity and soil fertility in the mixed forest of Cunninghamia lanceolata and Altingia gracilides. Acta Ecol Sin 22:957–961 (in Chinese with an English abstract)

    Google Scholar 

  • Chen SP, Sun WH, Xiong YF, Jiang YT, Liu XD, Liao XY, Zhang DY, Jiang SZ, Li Y, Liu B (2020) The Phoebe genome sheds light on the evolution of magnoliids. Hortic Res 7:146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawud SM, Raulund-Rasmussen K, Domisch T, Finér L, Jaroszewicz B, Vesterdal L (2016) Is Tree Species Diversity or Species Identity the More Important Driver of Soil Carbon Stocks, C/N Ratio, and pH? Ecosystems 19:645–660

    Article  CAS  Google Scholar 

  • Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms – A review. Soil Biol Biochem 75:54–63

    Article  CAS  Google Scholar 

  • Gerlich M, Neumann S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30

    Article  Google Scholar 

  • Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Wang S, Zeng D (2006) Effects of single Chinese fir and mixed leaf litters on soil chemical, microbial properties and soil enzyme activities. Plant Soil 282:379–386

    Article  CAS  Google Scholar 

  • Iwashima N, Masunaga T, Fujimaki R, Toyota A, Tayasu I, Hiura T, Kaneko N (2012) Effect of vegetation switch on soil chemical properties. Soil Sci Plant Nutr 58:783–792

    Article  CAS  Google Scholar 

  • Jennifer M, Talbot DJ, Yelle, James, Nowick, Kathleen, K. (2011) Litter decay rates are determined by lignin chemistry. Biogeochemistry 108:279–295

    Google Scholar 

  • Jennings SB, Brown ND, Sheil D (1999) Assessing forest canopies and understorey illumination: canopy closure, canopy cover and other measures. Forestry 72(1):59–74

    Article  Google Scholar 

  • Jiang Y, Chen C, Xu Z, Liu Y (2012) Effects of single and mixed species forest ecosystems on diversity and function of soil microbial community in subtropical China. J Soil Sediment 12:228–240

    Article  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  CAS  PubMed  Google Scholar 

  • Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vázquez PG, Malik AA, Roy J, Scheu S (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707

  • Langille MGI, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei B, Liu B, Luo CD, Zhang J, Xue YJ, Liu L (2014) Catabatic effect from artificial mixed plantation of Cunninghamia lanceolata on soil aluminum toxicity. Acta Ecol Sin 34(11):2884–2891 (in Chinese with an English abstract)

    CAS  Google Scholar 

  • Li L, Duan Z, Xu M, Hu J, Wang S, Hu Z, Zhang Q, Wang S (2010) Effect of monospecific and mixed Cunninghamia lanceolata plantations on microbial community and two functional genes involved in nitrogen cycling. Plant Soil 327:413–428

    Article  CAS  Google Scholar 

  • Li Q, Zhao XL, Hu CR (2006) ISO10390:2005 Soil Quality-Determination of pH. Pollution Control Technology (in Chinese with an English abstract)

  • Lidman J, Jonsson M, Burrows RM, Bundschuh M, Sponseller RA (2017) Composition of riparian litter input regulates organic matter decomposition: Implications for headwater stream functioning in a managed forest landscape. Ecol Evol 7:1068–1077

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin BP, He ZM, Lin SZ, Hu HT, Qiu LJ, Liu ZM (2017) Needles macronutrient concentrations and retranslocation characteristics in Chinese fir plantations of different ages. J Forest Environ 37:34–39 (in Chinese with an English abstract)

    Google Scholar 

  • Lin KM, Zhang ZQ, Cao GQ, He ZM, Ma XQ (2006) Decomposition characteristics and its nutrient dynamics of leaf litter mixtures of both Chinese fir and Phoeba bournei. Acta Ecol Sin 26:2732–2738 (in Chinese with an English abstract)

    CAS  Google Scholar 

  • Liu B, Luo C, Li X, Gray L, Zhang F, Liu M, Ju J, Lei B (2014) Research on the Threshold of Aluminum Toxicity and the Alleviation Effects of Exogenous Calcium, Phosphorus, and Nitrogen on the Growth of Chinese Fir Seedlings under Aluminum Stress. Commun Soil Sci Plant Anal 45:126–139

    Article  CAS  Google Scholar 

  • Liu C, Dong Y, Hou L, Deng N, Jiao R (2017) Acidobacteria community responses to nitrogen dose and form in chinese fir plantations in Southern China. Curr Microbiol 74:396–403

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2010) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo Y, Zhang X (2007) The assessment of soil degradation in successive rotations of Chinese fir plantation and the soil amelioration of mixed plantation of Chinese fir and broad-leaved. Acta Ecol Sin 27:715–724 (in Chinese with an English abstract)

    Google Scholar 

  • Ma ZH, Huang BL, Xu SS, Chen Y, Cao GQ (2016) Ion Flux in Roots of Chinese Fir (Cunninghamia lanceolata (Lamb.) Hook) under Aluminum Stress. PLoS ONE 11(6):e0156832

  • Martina P, Philipp S, Tobias R, Sara H (2018) Relative abundance of denitrifying and DNRA bacteria and their activity determine nitrogen retention or loss in agricultural soil. Soil Biol Biochem 123:97–104

    Article  CAS  Google Scholar 

  • Meng H, Li K, Nie M, Wan JR, Quan ZX, Fang CM, Chen JK, Gu JD, Li B (2013) Responses of bacterial and fungal communities to an elevation gradient in a subtropical montane forest of China. Appl Microbiol Biot 97:2219–2230

    Article  CAS  Google Scholar 

  • Naether A, Foesel BU, Naegele V, Wust PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navarrete AA, Kuramae EE, de Hollander M, Pijl AS, van Veen JA, Tsai SM (2013) Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. FEMS Microbiol Ecol 83:607–621

    Article  CAS  PubMed  Google Scholar 

  • Navarrete AA, Venturini AM, Meyer KM, Klein AM, Tiedje JM, Bohannan BJ, Nüsslein K, Tsai SM, Rodrigues JL (2015) Differential response of Acidobacteria subgroups to forest-to-pasture conversion and their biogeographic patterns in the western Brazilian Amazon. Front Microbiol 6:1443

    Article  PubMed  PubMed Central  Google Scholar 

  • Nussbaumer Y, Cole MA, Offler CE, Patrick JW (2015) Identifying and ameliorating nutrient limitations to reconstructing a forest ecosystem on mined land. Restor Ecol 24:202–211

    Article  Google Scholar 

  • Parrotta JA (1999) Productivity, nutrient cycling, and succession in single-and mixed-species plantations of Casuarina equisetifolia, Eucalyptus robusta, and Leucaena leucocephala in Puerto Rico. Forest Ecol Manag 124:45–77

    Article  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008

    Article  CAS  PubMed  Google Scholar 

  • Polemio M, Rhoades JD (1977) Determining Cation Exchange Capacity: A New Procedure for Calcareous and Gypsiferous Soils1. Soil Sci Soc Am J 41:524–528

    Article  CAS  Google Scholar 

  • Reich PB, Oleksyn J, Modrzynski F, Mrozinski P, Hobbie SE, Eissenstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818

    Article  Google Scholar 

  • Schloter M, Nannipieri P, SøRensen SJ, Van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10

    Article  CAS  Google Scholar 

  • Schmidt M, Veldkamp E, Corre MD (2015) Tree species diversity effects on productivity, soil nutrient availability and nutrient response efficiency in a temperate deciduous forest. Forest Ecol Manag 338:114–123

    Article  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, miropolsky L, S Garrett W, Huttenhower C, (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  PubMed  PubMed Central  Google Scholar 

  • Skyllberg U, Raulund-Rasmussen K, Borggaard OK (2001) pH buffering in acidic soils developed under Picea abies and Quercus robur—effects of soil organic matter, adsorbed cations and soil solution ionic strength. Biogeochemistry 56:51–74

    Article  CAS  Google Scholar 

  • Sofo A, Palese AM, Casacchia T, Xiloyannis C (2014) Sustainable soil management in olive orchards: Effects on telluric microorganisms. In: Parvaiz S, Rasool S (eds) Emerging Technologies and Management of Crop Stress Tolerance. Academic Press, San Diego, CA, pp 471–484

    Chapter  Google Scholar 

  • Ter Braak CJF, Šmilauer P (2002) CANOCO 4.5 Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination. Microcomputer Power, Ithaca, USA.

  • Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert JA, Jansson JK, Caporaso JG, Fuhrman JA (2016) Improved Bacterial 16S rRNA Gene (V4 and V4–5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. Msystems 1:e00009-00015

    Article  PubMed  Google Scholar 

  • Wang S, Liao L, Ma Y (1997) Nutrient return and productivity of mixed Cunninghamia lanceolata and Michelia macclurei plantations. Chin J Appl Ecol 8:347–352 (in Chinese with an English abstract)

    Google Scholar 

  • Wang Q, Wang S, Fan B, Yu X (2007) Litter production, leaf litter decomposition and nutrient return in Cunninghamia lanceolata plantations in south China: effect of planting conifers with broadleaved species. Plant Soil 297:201–211

    Article  CAS  Google Scholar 

  • Wang XY, Xing YJ, Yang LL, Shen YY, Li CF, Xu BB (2018) Seasonal dynamics of growth and leaf nutrients of young Phoebe bournei plantation. Hunan Forestry Ence & Technology 45:21–26 (in Chinese with an English abstract)

    Google Scholar 

  • Wang Y, Uchida Y, Shimomura Y, Akiyama H, Hayatsu M (2017) Responses of denitrifying bacterial communities to short-term waterlogging of soils. Sci Rep 7:803

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu ZZ (2005) Study on growth effect of the mixed forest of Cunninghamia lanceolata and Phoebe bournei. J Fujian Coll For 25:142–146 (in Chinese with an English abstract)

    Google Scholar 

  • Wu Z, Li J, Zheng J, Liu J, Liu S, Lin W, Wu C (2017) Soil microbial community structure and catabolic activity are significantly degenerated in successive rotations of Chinese fir plantations. Sci Rep 7:6691

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xia Z, Edith B, Qingkui W, Decai G, Jidong Z, Ping J, Jiabing W (2016) Biogeographic Distribution Patterns of Bacteria in Typical Chinese Forest Soils. Front Microbiol 7:1106

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu X, Wang X, Hu Y, Wang P, Sun Y (2020) Short-term effects of thinning on the development and communities of understory vegetation of Chinese fir plantations in Southeastern China. Peer J 8:e8536

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang YS, Liu CJ, Kutsch W, Chen GS, Yu XT (2004) Impact of continuous Chinese fir monoculture on soil. Pedosphere 14:117–124

    Google Scholar 

  • Yang YD, Hu YG, Wang ZM, Zeng ZH (2018) Variations of the nirS-, nirK-, and nosZ-denitrifying bacterial communities in a northern Chinese soil as affected by different long-term irrigation regimes. Environ Sci Pollut R 25:14057–14067

    Article  CAS  Google Scholar 

  • Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol Biochem 41:2044–2051

    Article  CAS  Google Scholar 

  • Zhang T, Wang X, Zhang B, Zhao Q (1999) Soil degradation in relation to land use and its countermeasures in the red and yellow soil region of southern China. Integrated watershed management in the global ecosystem. CRC Press, pp 51–64

  • Zhou ZF, Zheng YM, Shen JP, Zhang LM, He JZ (2011) Response of denitrification genes nirS, nirK, and nosZ to irrigation water quality in a Chinese agricultural soil. Environ Sci Pollut R 18:1644–1652

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Key Research and Development Program of China (2016YFD060030404) and Zhejiang Science and Technology Major Program on Agricultural New Variety Breeding (2016C02056-2).

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Authors and Affiliations

  1. State Key Laboratory of Subtropical Silviculture, School of Forestry & Bio-Technology, Zhejiang A&F University, Lin’an, 311300, Zhejiang, P.R. China

    Yuting Zhang, Kai Ding, Kim Yrjälä, Haiyan Liu, Zaikang Tong & Junhong Zhang

  2. Department of Forest Sciences, University of Helsinki, Helsinki, Finland

    Kai Ding

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  1. Yuting Zhang
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  2. Kai Ding
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  3. Kim Yrjälä
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Zhang, Y., Ding, K., Yrjälä, K. et al. Introduction of broadleaf species into monospecific Cunninghamia lanceolata plantations changed the soil Acidobacteria subgroups composition and nitrogen-cycling gene abundances. Plant Soil 467, 29–46 (2021). https://doi.org/10.1007/s11104-021-05014-8

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