Advertisement

Response of rhizosphere microbial communities to plant succession along a grassland chronosequence in a semiarid area

  • Zilin Song
  • Guobin Liu
  • Chao Zhang
Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • 14 Downloads

Abstract

Purpose

Changes in microbial communities during natural succession in semiarid areas have been widely studied but their association with plant and soil properties remains elusive. In the present study, we investigated plant characteristics, rhizosphere soil variables, and microbial communities along a chronosequence of grasslands forming on abandoned farmland on the Chinese Loess Plateau.

Materials and methods

Rhizosphere samples were collected from the early-stage dominant plant Artemisia capillaris from farmland abandoned for 5, 10, and 15 years and from the late-stage dominant plant Artemisia sacrorum from farmland abandoned for 10, 15, 20, and 30 years. Microbial community composition, including bacteria and fungi, was determined by high-throughput sequencing. Microbial succession rates represented by temporary turnover were assessed using the slope (w value) of linear regressions, based on log-transformed microbial community similarity over time.

Results and discussion

Cover and aboveground biomass of A. capillaris tended to decrease, whereas those of A. sacrorum increased during the succession. Although the rhizosphere bacteria of A. capillaris transitioned from Proteobacteria-dominant to Actinobacteria-dominant, the bacteria of A. sacrorum exhibited the opposite trend. Bacterial and fungal community diversity tended to increase logarithmically with increasing plant aboveground biomass, indicating that an increase in plant biomass could lead to enhanced rhizosphere microbial diversity, but the rate of enhancement decreased gradually. A lower temporary turnover rate of bacterial and fungal communities in the rhizosphere than that in the bulk soil indicated a higher successional rate of the rhizosphere microbial community. Levels of soil nutrients, such as organic carbon, nitrate nitrogen, and ammonium nitrogen, were closely associated with the abundance and diversity of bacterial and fungal communities, indicating their critical role in shaping the rhizosphere microbial community.

Conclusions

Our results indicate a close association between plant succession and rhizosphere microbial succession in a semiarid area. Plants affect the microbial communities possibly by changing the nutrient input into the rhizosphere.

Keywords

Grassland Microbial community Rhizosphere Succession 

Notes

Funding information

National Natural Sciences Foundation of China (41701556, 41771554), National Key Research and Development Program of China (2016YFC0501707), and Chinese University Scientific Fund (2452017111).

Supplementary material

11368_2019_2241_MOESM1_ESM.doc (1.7 mb)
ESM 1 (DOC 1768 kb)

References

  1. Becquer A, Trap J, Irshad U, Ali MA, Claude P (2014) From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association. Front Plant Sci 5:548CrossRefGoogle Scholar
  2. Bell CW, Asao S, Calderon F, Wolk B, Wallenstein MD (2015) Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth. Soil Biol Biochem 85:170–182CrossRefGoogle Scholar
  3. Blaalid R, Carlsen T, Kumar S, Halvorsen R, Ugland KI, Fontana G, Kauserud H (2012) Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21:1897–1908CrossRefGoogle Scholar
  4. Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbial properties. Agronomy Society of America Agronomy Monograph 9, Madison, pp 595–624Google Scholar
  5. Chagas FO, Pessotti RC, Caraballo-Rodriguez AM, Pupo MT (2018) Chemical signaling involved in plant-microbe interactions. Chem Soc Rev 47:1652–1704CrossRefGoogle Scholar
  6. Cline LC, Zak DR (2015) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecolgy 96(12):3374–3385CrossRefGoogle Scholar
  7. Davey M, Blaalid R, Vik U, Carlsen T, Kauserud H, Eidesen PB (2015) Primary succession of Bistorta vivipara (L.) Delabre (Polygonaceae) root-associated fungi mirrors plant succession in two glacial chronosequences. Environ Microbiol 17(8):2777–2790CrossRefGoogle Scholar
  8. Deng L, Shangguan ZP, Sweeney S (2014) “Grain for Green” driven land use change and carbon sequestration on the Loess Plateau, China. Sci Rep 4:7039CrossRefGoogle Scholar
  9. Development Core Team R (2013) R version 3.0.1: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  10. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefGoogle Scholar
  11. Fierer N, Nemergut DR, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642CrossRefGoogle Scholar
  12. Filep T, Draskovits E, Szabo J, Koos S, Laszlo P, Szalai Z (2015) The dissolved organic matter as a potential soil quality indicator in arable soils of Hungary. Environ Assess 187(7):479CrossRefGoogle Scholar
  13. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10CrossRefGoogle Scholar
  14. Franke-Whittle IH, Manici LM, Insam H, Stres B (2015) Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil 395:317–333CrossRefGoogle Scholar
  15. Freedman ZB, Upchurch RA, Zak DR, Cline LC (2016) Anthropogenic N deposition slows decay by favoring bacterial metabolism: insights from metagenomic analyses. Frontier Microbiol 7:259Google Scholar
  16. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Frontier Microbiol 2:94Google Scholar
  17. Harantová L, Mudrák O, Kohout P, Elhottová D, Frouz J, Baldrian P (2017) Development of microbial community during primary succession in areas degraded by mining activities. Land Degrad Dev 28:2574–2584Google Scholar
  18. He F, Yang BS, Wang H, Yan QL, Cao YN, He XH (2016) Changes in composition and diversity of fungal communities along Quercus mongolica forests developments in Northeast China. Appl Soil Ecol 100:162–171CrossRefGoogle Scholar
  19. Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa-area relationship for bacteria. Nature 432:750–753CrossRefGoogle Scholar
  20. Jach-Smith LC, Jackson RD (2018) N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses. Soil Biol Biochem 116:148–157CrossRefGoogle Scholar
  21. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  22. Kardol P, De Deyn GB, Laliberte E, Mariotte P, Hawkes CV (2013) Biotic plant-soil feedbacks across temporal scales. J Ecol 101(2):309–315CrossRefGoogle Scholar
  23. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  24. Knelman JE, Grahama EB, Trahand NA, Schmidt SK, Nemerguta DR (2015) Fire severity shapes plant colonization effects on bacterial community structure, microbial biomass, and soil enzyme activity in secondary succession of a burned forest. Soil Biol Biochem 90:161–168CrossRefGoogle Scholar
  25. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992CrossRefGoogle Scholar
  26. Kuramae EE, Gamper HA, Yergeau E, Piceno YM, Brodie EL, DeSantis TZ, Andersen GL, Van veen JA, Kowalchuk GA (2010) Microbial secondary succession in a chronosequence of chalk grasslands. ISME J 4:711–715CrossRefGoogle Scholar
  27. Lagos LM, Navarrete OU, Maruyama F, Crowley DE, Cid FP, Mora ML, Jorquera MA (2014) Bacterial community structures in rhizosphere microsites of ryegrass (Lolium perenne var. Nui) as revealed by pyrosequencing. Biol Fertil Soils 50:1253–1266CrossRefGoogle Scholar
  28. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115CrossRefGoogle Scholar
  29. Lankau EW, Lankau RA (2014) Plant species capacity to drive soil fungal communities contributes to differential impacts of plant–soil legacies. Ecology 95(11):3221–3228CrossRefGoogle Scholar
  30. Liang Y, Jiang Y, Wang F, Wen C, Deng Y, Xue K, Qin Y, Yang Y, Wu L, Zhou J, Sun B (2015) Long-term soil transplant simulating climate change with latitude significantly alters microbial temporal turnover. ISME J 9(12):2561–2572CrossRefGoogle Scholar
  31. Lima AB, Cannavan FS, Navarrete AA, Teixeira WG, Kuramae EE, Tsai SM (2015) Amazonian dark earth and plant species from the Amazon region contribute to shape rhizosphere bacterial communities. Microbial Ecol 69:855–866CrossRefGoogle Scholar
  32. Lozano YM, Hortal S, Armas C, Pugnaire FI (2014) Interactions among soil, plants, and microorganisms drive secondary succession in a dry environment. Soil Biol Biochem 78:298–306CrossRefGoogle Scholar
  33. Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445CrossRefGoogle Scholar
  34. McHugh TA, Morrissey EM, Mueller RC, Gallegos-Graves LV, Kuske CR, Reed SC (2017) Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland. Environ Microbiol 19(4):1600–1611CrossRefGoogle Scholar
  35. Millard P, Singh BK (2010) Does grassland vegetation drive soil microbial diversity? Nutr Cycl Agroecosyst 88(2):147–158CrossRefGoogle Scholar
  36. Mukherjee S, Heinonen M, Dequvire M, Sipilä T, Pulkkinen P, Yrjälä K (2013) Secondary succession of bacterial communities and co-occurrence of phylotypes in oil-polluted Populus rhizosphere. Soil Biol Biochem 58:188–197CrossRefGoogle Scholar
  37. Munoz-Rojas M, Erickson T, Martini D, Dixon KW, Merritt DJ (2016) Soil physicochemical and microbiological indicators of short, medium nd long term post-fire recovery in semi-arid ecosystems. Ecol Indic 63:14–22CrossRefGoogle Scholar
  38. Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbial properties. Agronomy Society of America, Agronomy Monograph 9, Madison, pp 539–552Google Scholar
  39. Olsen SR, Sommers LE (1982) Phosphorous. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbial properties. Agronomy Society of America, Agronomy Monograph 9, Madison, Wisconsin, pp 403–430Google Scholar
  40. Paredes HS, Lebeis SL (2016) Giving back to the community: microbial mechanisms of plant–soil interactions. Funct Ecol 30:1043–1052CrossRefGoogle Scholar
  41. Peay KG, Kennedy PG, Bruns TD (2011) Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial. Fungal Ecol 4:233–240CrossRefGoogle Scholar
  42. Poosakkannu A, Nissinen R, Mannisto M, Kytoviita MM (2017) Microbial community composition but not diversity changes along succession in arctic sand dunes. Environ Microbiol 19:698–709CrossRefGoogle Scholar
  43. Siciliano SD, Palmer AS, Winsley T, Lamb E, Bissett A, Brown MV, van Dorst J, Ji M, Ferrari BC, Grogan P, Chu HY, Snape I (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20CrossRefGoogle Scholar
  44. Spohn M, Treichel NS, Cormann M, Schloter M, Fischer D (2015) Distribution of phosphatase activity and various bacterial phyla in the rhizosphere of Hordeum vulgare L. depending on P availability. Soil Biol Biochem 89:44–51CrossRefGoogle Scholar
  45. Tscherko D, Ute H, Marie-Claude M, Ellen K (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36:1685–1698CrossRefGoogle Scholar
  46. Walker LR, Walker J, Hobbs RJ (2007) Linking restoration and ecological succession. Springer, Amsterdam, pp 5–21CrossRefGoogle Scholar
  47. Wang GL, Liu GB, Xu MX (2009) Above and belowground dynamics of plant community succession following abandonment of farmland on the Loess Plateau, China. Plant Soil 316:227–239CrossRefGoogle Scholar
  48. Welc ME, Frossard E, Egli S, Else K, Bünema JJ (2014) Rhizosphere fungal assemblages and soil enzymatic activities in a 110-years alpine chronosequence. Soil Biol Biochem 74:21–30CrossRefGoogle Scholar
  49. Xiong J, Peng F, Sun H, Xue X, Chu H (2014) Divergent responses of soil fungi functional groups to short-term warming. Microb Ecol 68:708–715CrossRefGoogle Scholar
  50. Zeng QC, An SS, Liu Y (2017) Soil bacterial community response to vegetation succession after fencing in the grassland of China. Sci Total Environ 609:2–10CrossRefGoogle Scholar
  51. Zhang C, Liu GB, Xue S, Wang GL (2015) Changes in rhizospheric microbial community structure and function during the natural recovery of abandoned cropland on the Loess Plateau China. Ecol Eng 75:161–171CrossRefGoogle 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 Boil Biochem 97:40–49CrossRefGoogle Scholar
  53. Zhang C, Liu GB, Song ZL, Qu D, Fang LC, Deng L (2017) Natural succession on abandoned cropland effectively decreases the soil erodibility and improves the fungal diversity. Ecol Appl 27(7):2142–2154CrossRefGoogle Scholar
  54. Zhang KR, Cheng XL, Shu X, Liu Y, Zhang QF (2018) Linking soil bacterial and fungal communities to vegetation succession following agricultural abandonment. Plant Soil 431:19–36CrossRefGoogle Scholar
  55. Zhou WJ, Sha LQ, Schaefer DA, Zhang YP, Song QH, Tan ZH, Deng Y, Deng XB, Guan HL (2015) Direct effects of litter decomposition on soil dissolved organic carbon and nitrogen in a tropical rainforest. Soil Biol Biochem 81:255–258CrossRefGoogle Scholar
  56. Zhou J, Jiang X, Zhou BK, Zhao BS, Ma MC, Guan DW, Li J, Chen SF, Cao FM, Shen DL, Qin J (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.College of Natural Resources and EnvironmentNorthwest A&F UniversityYanglingPeople’s Republic of China
  3. 3.Institute of Soil and Water ConservationChinese Academy of Sciences and Ministry of Water ResourcesYanglingPeople’s Republic of China

Personalised recommendations