Biology and Fertility of Soils

, Volume 53, Issue 4, pp 457–468 | Cite as

Response of microbial diversity to C:N:P stoichiometry in fine root and microbial biomass following afforestation

  • Chengjie Ren
  • Ji Chen
  • Jian Deng
  • Fazhu Zhao
  • Xinhui Han
  • Gaihe Yang
  • Xiaogang Tong
  • Yongzhong Feng
  • Shelby Shelton
  • Guangxin Ren
Original Paper

Abstract

Soil samples were collected in June and October from areas with three land-use types, i.e., Robinia pseudoacacia L. (RP), Caragana korshinskii Kom. (CK), and abandoned land (AL), of which the former two were afforested areas, whereas the latter was not. These areas were converted from similar farmlands 40 years prior. Illumina sequencing of 16S rRNA gene and fungal ITS gene was used to analyze soil bacterial and fungal diversity. Additionally, plant communities, soil properties, fine root biomass, and C, N, and P levels in fine root and microbial biomass were estimated. Compared to AL, the C:N:P stoichiometry in fine root and microbial biomass in the afforested lands was synchronously changed, especially the N:P ratio. Soil microbial diversities were affected by afforestation and were more related to N:P ratio than C:P and C:N ratios. Moreover, Alpha-proteobacteria, Gamma-proteobacteria, and Bacteroidetes were significantly more abundant in afforested soils than in the AL soil, and the abundances of Actinobacteria, Chloroflexi, Cyanobacteria, and Nitrospirae ranked as AL > RP or CK. For fungal taxa, Ascomycota abundance responded positively to afforestation, whereas Basidiomycota abundance responded negatively. Changes of soil microbial taxa were significantly correlated with the N:P ratio in fine root and microbial biomass, which explained 54.1 and 55% of the total variation in bacterial and fungal taxa, respectively. Thus, our results provide evidence that compositions of soil microbial communities are linked to the N:P ratio in the plant-soil system.

Keywords

Afforestation C:N:P stoichiometry Illumina sequencing Soil microbial communities 

Notes

Acknowledgements

The authors especially thank Pinsheng Sun, Yadong Xu, and Tao Wang (Northwest A&F University) for their help with the fieldwork. This work was supported by the National Natural Science Foundation of China (No. 41301601, 41571501).

Supplementary material

374_2017_1197_MOESM1_ESM.docx (1018 kb)
ESM 1 (DOCX 1017 kb)

References

  1. Augusto L, Delerue F, Gallet-Budynek A, Achat DL (2013) Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Global Biogeochem Cy 27:804–815. doi: 10.1002/gbc.20069 CrossRefGoogle Scholar
  2. Barea JM, Azcón R, Azcón-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton Leeuw Int J G 81:343–351. doi: 10.1023/A:1020588701325 CrossRefGoogle Scholar
  3. Bastida F, Hernandez T, Albaladejo J, Garcia C (2013) Phylogenetic and functional changes in the microbial community of long-term restored soils under semiarid climate. Soil Biol Biochem 65:12–21. doi: 10.1016/j.soilbio.2013.04.022 CrossRefGoogle Scholar
  4. Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014) Rhizosphere stoichiometry: are C : N: P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytol 201:505–517. doi: 10.1111/nph.12531 CrossRefPubMedGoogle Scholar
  5. Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci U S A 105:10583–10588. doi: 10.1073/pnas.0709942105 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465. doi: 10.2134/agronj1962.00021962005400050028x CrossRefGoogle Scholar
  7. Braak CJFt, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, NY ASA. http://edepot.wur.nl/54192
  8. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi: 10.1016/0038-0717(85)90144-0 CrossRefGoogle Scholar
  9. Bui EN, Henderson BL (2013) C: N: P stoichiometry in Australian soils with respect to vegetation and environmental factors. Plant Soil 373:553–568. doi: 10.1007/s11104-013-1823-9 CrossRefGoogle Scholar
  10. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi: 10.1038/ismej.2012.8 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Clarke K, Gorley R, Somerfield P, Warwick R (2014) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, PlymouthGoogle Scholar
  12. Crowther TW, Maynard DS, Leff JW, Oldfield EE, McCulley RL, Fierer N, Bradford MA (2014) Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Glob Chang Biol 20:2983–2994. doi: 10.1111/gcb.12565 CrossRefPubMedGoogle Scholar
  13. Davidson EA, Howarth RW (2007) Environmental science—nutrients in synergy. Nature 449:1000–1001. doi: 10.1038/4491000a CrossRefPubMedGoogle Scholar
  14. De Vos B, Van Meirvenne M, Quataert P, Deckers J, Muys B (2005) Predictive quality of pedotransfer functions for estimating bulk density of forest soils. Soil Sci Soc Am J 69:500–510. doi: 10.2136/sssaj2005.0500 CrossRefGoogle Scholar
  15. DeLuca TH, Zackrisson O, Nilsson M-C, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920. doi: 10.1038/nature01051 CrossRefPubMedGoogle Scholar
  16. Deng Q, Cheng XX, Hui DF, Zhang Q, Li M, Zhang QF (2016) Soil microbial community and its interaction with soil carbon and nitrogen dynamics following afforestation in central China. Sci Total Environ 541:230–237. doi: 10.1016/j.scitotenv.2015.09.080 CrossRefPubMedGoogle Scholar
  17. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943. doi: 10.1046/j.1461-0248.2003.00518.x CrossRefGoogle Scholar
  18. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi: 10.1016/S0038-0717(03)00123-8 CrossRefGoogle Scholar
  19. Fontaine S, Henault C, Aamor A, Bdioui N, Bloor J, Maire V, Mary B, Revaillot S, Maron P (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96. doi: 10.1016/j.soilbio.2010.09.017 CrossRefGoogle Scholar
  20. Fu BJ, Chen LD, Ma KM, Zhou HF, Wang J (2000) The relationships between land use and soil conditions in the hilly area of the loess plateau in northern Shaanxi, China. Catena 39:69–78. doi: 10.1016/S0341-8162(99)00084-3 CrossRefGoogle Scholar
  21. Ganie MA, Mukhtar M, Dar MA, Ramzan S (2016) Soil microbiological activity and carbon dynamics in the current climate change scenarios: a review. Pedosphere 26:577–591. doi: 10.1016/S1002-0160(15)60068-6 CrossRefGoogle Scholar
  22. de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064. doi: 10.1111/j.1469-8137.2010.03427.x CrossRefPubMedGoogle Scholar
  23. Green JJ, Dawson LA, Proctor J, Duff EI, Elston DA (2005) Fine root dynamics in a tropical rain forest is influenced by rainfall. Plant Soil 276:23–32. doi: 10.1007/s11104-004-0331-3 CrossRefGoogle Scholar
  24. Güsewell S, Gessner MO (2009) N: P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219. doi: 10.1111/j.1365-2435.2008.01478.x CrossRefGoogle Scholar
  25. Hannula S, Boschker H, de Boer W, Van Veen J (2012) 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytol 194:784–799. doi: 10.1111/j.1469-8137.2012.04089.x CrossRefPubMedGoogle Scholar
  26. Hu YL, Zeng DH, Ma XQ, Chang SX (2016) Root rather than leaf litter input drives soil carbon sequestration after afforestation on a marginal cropland. Forest Ecol Manag 362:38–45. doi: 10.1016/j.foreco.2015.11.048 CrossRefGoogle Scholar
  27. Jorquera MA, Inostroza NG, Lagos LM, Barra PJ, Marileo LG, Rilling JI, Campos DC, Crowley DE, Richardson AE, Mora ML (2014) Bacterial community structure and detection of putative plant growth-promoting rhizobacteria associated with plants grown in Chilean agro-ecosystems and undisturbed ecosystems. Biol Fert Soils 50:1141–1153. doi: 10.1007/s00374-014-0935-6 CrossRefGoogle Scholar
  28. Krashevska V, Klarner B, Widyastuti R, Maraun M, Scheu S (2015) Impact of tropical lowland rainforest conversion into rubber and oil palm plantations on soil microbial communities. Biol Fert Soils 51:697–705. doi: 10.1007/s00374-015-1021-4 CrossRefGoogle Scholar
  29. Lai ZR, Zhang YQ, Liu JB, Wu B, Qin SG, Fa KY (2016) Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China. Forest Ecol Manag 359:381–388. doi: 10.1016/j.foreco.2015.04.025 CrossRefGoogle Scholar
  30. Li A, Fahey TJ, Pawlowska TE, Fisk MC, Burtis J (2015a) Fine root decomposition, nutrient mobilization and fungal communities in a pine forest ecosystem. Soil Biol Biochem 83:76–83. doi: 10.1016/j.soilbio.2015.01.019 CrossRefGoogle Scholar
  31. Li J, Li ZA, Wang FM, Zou B, Chen Y, Zhao J, Mo QF, Li YW, Li XB, Xia HP (2015b) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fert Soils 51:207–215. doi: 10.1007/s00374-014-0964-1 CrossRefGoogle Scholar
  32. Lin CF, Yang YS, Guo JF, Chen GS, Xie JS (2011) Fine root decomposition of evergreen broadleaved and coniferous tree species in mid-subtropical China: dynamics of dry mass, nutrient and organic fractions. Plant Soil 338:311–327. doi: 10.1007/s11104-010-0547-3 CrossRefGoogle Scholar
  33. Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38. doi: 10.1016/j.soilbio.2011.08.017 CrossRefGoogle Scholar
  34. Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704. doi: 10.1111/j.1469-8137.2011.03967.x CrossRefPubMedGoogle Scholar
  35. Marriott CA, Hudson G, Hamilton D, Neilson R, Boag B, Handley LL, Wishart J, Scrimgeour CM, Robinson D (1997) Spatial variability of soil total C and N and their stable isotopes in an upland Scottish grassland. Plant Soil 196:151–162. doi: 10.1023/A:1004288610550 CrossRefGoogle Scholar
  36. McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C: N: P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85:2390–2401. doi: 10.1890/03-0351 CrossRefGoogle Scholar
  37. Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Natl Acad Sci U S A 105:19780–19785. doi: 10.1073/pnas.0805600105 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mooshammer M, Wanek W, Schnecker J, Wild B, Leitner S, Hofhansl F, Blochl A, Hammerle I, Frank AH, Fuchslueger L, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2012) Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter. Ecology 93:770–782. doi: 10.1890/11-0721.1 CrossRefPubMedGoogle Scholar
  39. Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22. doi: 10.3389/fmicb.2014.00022 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mouhamadou B, Puissant J, Personeni E, Desclos-Theveniau M, Kastl EM, Schloter M, Zinger L, Roy J, Geremia RA, Lavorel S (2013) Effects of two grass species on the composition of soil fungal communities. Biol Fert Soils 49:1131–1139. doi: 10.1007/s00374-013-0810-x CrossRefGoogle Scholar
  41. Mukherjee PK, Chandra J, Retuerto M, Sikaroodi M, Brown RE, Jurevic R, Salata RA, Lederman MM, Gillevet PM, Ghannoum MA (2014) Oral mycobiome analysis of HIV-infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog 10:e1003996. doi: 10.1371/journal.ppat.1003996 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nemergut DR, Townsend AR, Sattin SR, Freeman KR, Fierer N, Neff JC, Bowman WD, Schadt CW, Weintraub MN, Schmidt SK (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105. doi: 10.1111/j.1462-2920.2008.01735.x CrossRefPubMedGoogle Scholar
  43. Peichl M, Leava NA, Kiely G (2012) Above- and belowground ecosystem biomass, carbon and nitrogen allocation in recently afforested grassland and adjacent intensively managed grassland. Plant Soil 350:281–296. doi: 10.1007/s11104-011-0905-9 CrossRefGoogle Scholar
  44. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. doi: 10.1111/j.1461-0248.2010.01570.x CrossRefPubMedGoogle Scholar
  45. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fert Soils 51:403–415. doi: 10.1007/s00374-015-0996-1 CrossRefGoogle Scholar
  46. Ren CJ, Zhao FZ, Kang D, Yang GH, Han XH, Tong XG, Feng YZ, Ren GX (2016a) Linkages of C:N:P stoichiometry and bacterial community in soil following afforestation of former farmland. Forest Ecol Manag 376:59–66. doi: 10.1016/j.foreco.2016.06.004 CrossRefGoogle Scholar
  47. Ren CJ, Kang D, Wu JP, Zhao FZ, Yang GH, Han XH, Feng YZ, Ren GX (2016b) Temporal variation in soil enzyme activities after afforestation in the Loess Plateau, China. Geoderma 282:103–111. doi: 10.1016/j.geoderma.2016.07.018 CrossRefGoogle Scholar
  48. Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80:735–746. doi: 10.1111/j.1574-6941.2012.01343.x CrossRefPubMedGoogle Scholar
  49. Taş N, Prestat E, McFarland JW, Wickland KP, Knight R, Berhe AA, Jansson JK (2014) Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest. ISME J 8:1904–1919. doi: 10.1038/ismej.2014.36 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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. doi: 10.1111/j.1461-0248.2007.01139.x CrossRefPubMedGoogle Scholar
  51. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. doi: 10.1016/0038-0717(87)90052-6 CrossRefGoogle Scholar
  52. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15. doi: 10.1890/08-0127.1 CrossRefPubMedGoogle Scholar
  53. Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270. doi: 10.1073/pnas.1320054111 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Weber CF, Vilgalys R, Kuske CR (2013) Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:78. doi: 10.3389/Fmicb.2013.00078 CrossRefPubMedPubMedCentralGoogle Scholar
  55. el Zahar HF, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. doi: 10.1038/ismej.2008.80 CrossRefGoogle Scholar
  56. Zhang C, Xue S, Liu GB, Song ZL (2011) A comparison of soil qualities of different revegetation types in the Loess Plateau, China. Plant Soil 347:163–178. doi: 10.1007/s11104-011-0836-5 CrossRefGoogle Scholar
  57. Zhang C, Liu GB, Xue S, Wang G (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. doi: 10.1016/j.soilbio.2016.02.013 CrossRefGoogle Scholar
  58. Zhao FZ, Kang D, Han XH, Yang GH, Feng YZ, Ren GX (2015) Soil stoichiometry and carbon storage in long-term afforestation soil affected by understory vegetation diversity. Ecol Eng 74:415–422. doi: 10.1016/j.ecoleng.2014.11.010 CrossRefGoogle Scholar
  59. Zheng FL (2006) Effect of vegetation changes on soil erosion on the Loess Plateau. Pedosphere 16:420–427. doi: 10.1016/S1002-0160(15)60068-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Chengjie Ren
    • 1
    • 2
  • Ji Chen
    • 3
  • Jian Deng
    • 1
    • 2
  • Fazhu Zhao
    • 4
  • Xinhui Han
    • 1
    • 2
  • Gaihe Yang
    • 1
    • 2
  • Xiaogang Tong
    • 5
  • Yongzhong Feng
    • 1
    • 2
  • Shelby Shelton
    • 6
  • Guangxin Ren
    • 1
    • 2
  1. 1.College of AgronomyNorthwest A&F UniversityYanglingChina
  2. 2.The Research Center of Recycle Agricultural Engineering and Technology of Shaanxi ProvinceYanglingChina
  3. 3.Center for Ecological and Environmental Sciences, Key Laboratory for Space Bioscience & BiotechnologyNorthwestern Polytechnical UniversityXi’anChina
  4. 4.College of Urban and Environmental ScienceNorthwest UniversityXi’anChina
  5. 5.College of Natural Resources and EnvironmentNorthwest A&F UniversityYanglingChina
  6. 6.Milken Institute of Public HealthThe George Washington UniversityWashingtonUSA

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