Journal of Soils and Sediments

, Volume 19, Issue 5, pp 2485–2495 | Cite as

Influence of rice cultivars on soil bacterial microbiome under elevated carbon dioxide

  • Jiangbing Xu
  • Jianwei Zhang
  • Chunwu Zhu
  • Jianguo Zhu
  • Xiangui Lin
  • Youzhi FengEmail author
Soils, Sec 5 • Soil and Landscape Ecology • Research Article



Elevated CO2 concentration (eCO2) may stimulate plant growth and influence the soil microbial community, but questions remain for whether microbial responses to elevated CO2 would vary by different CO2-responsive plants. We thus attempted to elaborate the changes of soil microbiome to different rice cultivars under the eCO2 condition.

Materials and methods

Two rice cultivars, i.e., the CO2-tolerant cultivar, Wuyunjing23 (WYJ23), and the CO2-sensitive one, Yandao 6 (YD6), were grown under eCO2 and ambient CO2 (aCO2) conditions. The contents of dissolved organic carbon (DOC) and nitrogen (DON) in soil were measured. Real-time qualitative PCR (qPCR) and high-throughput sequencing techniques were employed to characterize the bacterial community. Furthermore, co-occurrence network analysis was applied to reveal the ecological interactions among bacterial taxa.

Results and discussion

No significant differences were found among all treatments in terms of bacterial population, alpha-diversity indices, and bacterial community structure. However, the topological parameters of ecological networks highlighted the distinct co-occurrence patterns among treatments. YD6 under eCO2 led to more links, lower modularity, and greater centralization degree compared to that under aCO2. Opposite trends of those parameters were observed for WYJ23 under eCO2 compared to that under aCO2. Besides, more Proteobacteria and Acidobacteria served as keystone taxa in the CO2-sensitive cultivar treatments, compared to those in WYJ23, implying the different influences of rice cultivars on the microbial ecological network.


Different rice cultivars under eCO2 did not influence the alpha- and beta-diversity of the soil bacterial community, but changed the co-occurrence network of the community. More attention should be paid to the assembly mechanisms of the soil microbial microbiome when evaluating the impacts of productive crops on the soil-plant ecosystem under the eCO2 condition.


16S rRNA gene Co-occurrence network Free air carbon dioxide enrichment Rice cultivar 



This work was supported by the National Basic Research Program (973 Program) (grant number 2014CB954500), National Natural Science Foundation of China (grant numbers 41430859, 41671267, and 41501264), National Key R&D Program (grant number 2016YFD0200306), Youth Innovation Promotion Association, CAS (Member No. 2014271), and Research Program for Key Technologies of Sponge City Construction and Management in Guyuan City (Grant NO. SCHM-2018).

Supplementary material

11368_2018_2220_MOESM1_ESM.docx (16 kb)
ESM 1 (DOCX 15 kb)


  1. Austin EE, Castro HF, Sides KE, Schadt CW, Classen AT (2009) Assessment of 10 years of CO2 fumigation on soil microbial communities and function in a sweetgum plantation. Soil Biol Biochem 41(3):514–520CrossRefGoogle Scholar
  2. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57(1):233–266CrossRefGoogle Scholar
  3. Barberan A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6(2):343–351CrossRefGoogle Scholar
  4. Barrat A, Barthélemy M, Pastor-Satorras R, Vespignani A (2004) The architecture of complex weighted networks. P Natl Acad Sci USA 101(11):3747–3752CrossRefGoogle Scholar
  5. Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219CrossRefGoogle Scholar
  6. Bhattacharyya P, Roy KS, Neogi S, Manna MC, Adhya TK, Rao KS, Nayak AK (2013) Influence of elevated carbon dioxide and temperature on belowground carbon allocation and enzyme activities in tropical flooded soil planted with rice. Environ Monit Assess 185(10):8659–8671CrossRefGoogle Scholar
  7. 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. P Natl Acad Sci USA 105(30):10583–10588CrossRefGoogle Scholar
  8. Calfapietra C, Ainsworth EA, Beier C, De Angelis P, Ellsworth DS, Godbold DL, Hendrey GR, Hickler T, Hoosbeek MR, Karnosky DF, King J, Korner C, Leakey ADB, Lewin KF, Liberloo M, Long SP, Lukac M, Matyssek R, Miglietta F, Nagy J, Norby RJ, Oren R, Percy KE, Rogers A, Mugnozza GS, Stitt M, Taylor G, Ceulemans R, Grp E-FF (2010) Challenges in elevated CO2 experiments on forests. Trends Plant Sci 15(1):5–10CrossRefGoogle Scholar
  9. Calvo OC, Franzaring J, Schmid I, Muller M, Brohon N, Fangmeier A (2017) Atmospheric CO2 enrichment and drought stress modify root exudation of barley. Glob Chang Biol 23(3):1292–1304CrossRefGoogle Scholar
  10. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336CrossRefGoogle Scholar
  11. Cheng L, Booker FL, Tu C, Burkey KO, Zhou LS, Shew HD, Rufty TW, Hu SJ (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337(6098):1084–1087CrossRefGoogle Scholar
  12. Chung HG, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol 13(5):980–989CrossRefGoogle Scholar
  13. Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13(1):113CrossRefGoogle Scholar
  14. Drigo B, Kowalchuk GA, van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44(5):667–679CrossRefGoogle Scholar
  15. Drigo B, Nielsen UN, Jeffries TC, Curlevski NJA, Singh BK, Duursma RA, Anderson IC (2017) Interactive effects of seasonal drought and elevated atmospheric carbon dioxide concentration on prokaryotic rhizosphere communities. Environ Microbiol 19(8):3175–3185CrossRefGoogle Scholar
  16. Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. P Natl Acad Sci USA 107(24):10938–10942CrossRefGoogle Scholar
  17. Ebersberger D, Werrnbter N, Niklaus PA, Kandeler E (2004) Effects of long term CO2 enrichment on microbial community structure in calcareous grassland. Plant Soil 264(1–2):313–323CrossRefGoogle Scholar
  18. Edgar RC (2017) SEARCH_16S: a new algorithm for identifying 16S ribosomal RNA genes in contigs and chromosomes. bioRxiv:124131Google Scholar
  19. Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7:44641Google Scholar
  20. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10(8):538–550CrossRefGoogle Scholar
  21. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364CrossRefGoogle Scholar
  22. Gu YF, Wang YY, Lu SE, Xiang QJ, Yu XM, Zhao K, Zou LK, Chen Q, Tu SH, Zhang XP (2017) Long-term fertilization structures bacterial and archaeal communities along soil depth gradient in a paddy soil. Front Microbiol 8:1516CrossRefGoogle Scholar
  23. Guimerà R, Nunes Amaral LA (2005) Functional cartography of complex metabolic networks. Nature 433:895–900CrossRefGoogle Scholar
  24. He SB, Guo LX, Niu MY, Miao FH, Jiao S, Hu TM, Long MX (2017) Ecological diversity and co-occurrence patterns of bacterial community through soil profile in response to long-term switchgrass cultivation. Sci Rep 7:3608Google Scholar
  25. He Z, Piceno Y, Deng Y, Xu M, Lu Z, DeSantis T, Andersen G, Hobbie SE, Reich PB, Zhou J (2012) The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide. ISME J 6(2):259–272CrossRefGoogle Scholar
  26. IPCC (2014) Climate change 2013—the physical science basis: Working Group I contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  27. Jiang Y, Li S, Li R, Zhang J, Liu Y, Lv L, Zhu H, Wu W, Li W (2017) Plant cultivars imprint the rhizosphere bacterial community composition and association networks. Soil Biol Biochem 109:145–155CrossRefGoogle Scholar
  28. Johnson DV, Jain SM, Al-Khayri JM (2016) Advances in plant breeding strategies: agronomic, abiotic and biotic, vol 2. Springer, BerlinGoogle Scholar
  29. Kim HY, Lieffering M, Kobayashi K, Okada M, Mitchell MW, Gumpertz M (2003) Effects of free-air CO2 enrichment and nitrogen supply on the yield of temperate paddy rice crops. Field Crop Res 83(3):261–270CrossRefGoogle Scholar
  30. Lee SH, Kang H (2016) Elevated CO2 causes a change in microbial communities of rhizosphere and bulk soil of salt marsh system. Appl Soil Ecol 108:307–314CrossRefGoogle Scholar
  31. Liang Y, Zhao H, Deng Y, Zhou J, Li G, Sun B (2016) Long-term oil contamination alters the molecular ecological networks of soil microbial functional genes. Front Microbiol 7:60Google Scholar
  32. Ling N, Zhu C, Xue C, Chen H, Duan YH, Peng C, Guo SW, Shen QR (2016) Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol Biochem 99:137–149CrossRefGoogle Scholar
  33. Liu Y, Li M, Zheng JW, Li LQ, Zhang XH, Zheng JF, Pan GX, Yu XY, Wang JF (2014) Short-term responses of microbial community and functioning to experimental CO2 enrichment and warming in a Chinese paddy field. Soil Biol Biochem 77:58–68CrossRefGoogle Scholar
  34. Liu Y, Zhang H, Xiong MG, Li F, Li LQ, Wang GL, Pan GX (2017) Abundance and composition response of wheat field soil bacterial and fungal communities to elevated CO2 and increased air temperature. Biol Fertil Soils 53(1):3–8CrossRefGoogle Scholar
  35. Long SP, Ainsworth EA, Leakey ADB, Nösberger J, Ort DR (2006) Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312(5782):1918–1921CrossRefGoogle Scholar
  36. Norby RJ, Zak DR (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. In: Futuyma DJ, Shaffer HB, Simberloff D (eds) Annual review of ecology, evolution, and systematics, vol 42. Annual review of ecology evolution and systematics. Pp 181-203Google Scholar
  37. Oberholster T, Vikram S, Cowan D, Valverde A (2018) Key microbial taxa in the rhizosphere of sorghum and sunflower grown in crop rotation. Sci Total Environ 624:530–539CrossRefGoogle Scholar
  38. Okada M, Lieffering M, Nakamura H, Yoshimoto M, Kim HY, Kobayashi K (2001) Free-air CO2 enrichment (FACE) using pure CO2 injection: system description. New Phytol 150(2):251–260CrossRefGoogle Scholar
  39. Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Simpson G, Solymos P, Henry M, Stevens H, Wagner H (2013) Vegan: community ecology packageGoogle Scholar
  40. Okubo T, Liu DY, Tsurumaru H, Ikeda S, Asakawa S, Tokida T, Tago K, Hayatsu M, Aoki N, Ishimaru K, Ujiie K, Usui Y, Nakamura H, Sakai H, Hayashi K, Hasegawa T, Minamisawa K (2015) Elevated atmospheric CO2 levels affect community structure of rice root-associated bacteria. Front Microbiol 6:136CrossRefGoogle Scholar
  41. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. P Natl Acad Sci USA 104(50):19891–19896CrossRefGoogle Scholar
  42. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46(8):609–620CrossRefGoogle Scholar
  43. Qin H, Niu L, Wu Q, Chen J, Li Y, Liang C, Xu Q, Fuhrmann JJ, Shen Y (2017) Bamboo forest expansion increases soil organic carbon through its effect on soil arbuscular mycorrhizal fungal community and abundance. Plant Soil 420(1–2):407–421CrossRefGoogle Scholar
  44. Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  45. Sapp M, Harrison M, Hany U, Charlton A, Thwaites R (2015) Comparing the effect of digestate and chemical fertiliser on soil bacteria. Appl Soil Ecol 86:1–9CrossRefGoogle Scholar
  46. Shange RS, Ankumah RO, Ibekwe AM, Zabawa R, Dowd SE (2012) Distinct soil bacterial communities revealed under a diversely managed agroecosystem. PLoS one 7(7):e40338. CrossRefGoogle Scholar
  47. Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, Martiny JBH (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10(9):2200–2210CrossRefGoogle Scholar
  48. Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19(8):926–936CrossRefGoogle Scholar
  49. Shimono H, Okada M, Yamakawa Y, Nakamura H, Kobayashi K, Hasegawa T (2009) Genotypic variation in rice yield enhancement by elevated CO2 relates to growth before heading, and not to maturity group. J Exp Bot 60(2):523–532CrossRefGoogle Scholar
  50. Simonin M, Nunan N, Bloor JMG, Pouteau V, Niboyet A (2017) Short-term responses and resistance of soil microbial community structure to elevated CO2 and N addition in grassland mesocosms. FEMS Microbiol Lett 364(9):1–6CrossRefGoogle Scholar
  51. Sun L, Xun W, Huang T, Zhang G, Gao J, Ran W, Li D, Shen Q, Zhang R (2016) Alteration of the soil bacterial community during parent material maturation driven by different fertilization treatments. Soil Biol Biochem 96:207–215CrossRefGoogle Scholar
  52. Wang Y, Li H, Li J, Li X (2017) The diversity and co-occurrence patterns of diazotrophs in the steppes of Inner Mongolia. Catena 157:130–138CrossRefGoogle Scholar
  53. Wood SA, Gilbert JA, Leff JW, Fierer N, D'Angelo H, Bateman C, Gedallovich SM, Gillikin CM, Gradoville MR, Mansor P, Massmann A, Yang N, Turner BL, Brearley FQ, McGuire KL (2017) Consequences of tropical forest conversion to oil palm on soil bacterial community and network structure. Soil Biol Biochem 112:258–268CrossRefGoogle Scholar
  54. Xia WW, Jia ZJ, Bowatte S, Newton PCD (2017) Impact of elevated atmospheric CO2 on soil bacteria community in a grazed pasture after 12-year enrichment. Geoderma 285:19–26CrossRefGoogle Scholar
  55. Yang G, Peng M, Tian XL, Dong SL (2017) Molecular ecological network analysis reveals the effects of probiotics and florfenicol on intestinal microbiota homeostasis: an example of sea cucumber. Sci Rep 7:4778Google Scholar
  56. Yang LX, Huang JY, Yang HJ, Zhu JG, Liu HJ, Dong GC, Liu G, Han Y, Wang YL (2006) The impact of free-air CO2 enrichment (FACE) and N supply on yield formation of rice crops with large panicle. Field Crop Res 98(2–3):141–150CrossRefGoogle Scholar
  57. Yu Y, Zhang J, Petropoulos E, Baluja MQ, Zhu C, Zhu J, Lin X, Feng Y (2018) Divergent responses of the diazotrophic microbiome to elevated CO2 in two rice cultivars. Front Microbiol 9:1139CrossRefGoogle Scholar
  58. Zhou JZ, Deng Y, Luo F, He ZL, Yang YF (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2(4):e00122–11Google Scholar
  59. Zhu C, Xu X, Wang D, Zhu J, Liu G (2015) An indica rice genotype showed a similar yield enhancement to that of hybrid rice under free air carbon dioxide enrichment. Sci Rep 5:12719CrossRefGoogle Scholar
  60. Zhu C, Xu X, Wang D, Zhu J, Liu G, Seneweera S (2016) Elevated atmospheric [CO2] stimulates sugar accumulation and cellulose degradation rates of rice straw. GCB Bioenergy 8(3):579–587CrossRefGoogle Scholar
  61. Zhu CW, Zeng Q, Ziska LH, Zhu JG, Xie ZB, Liu G (2008) Effect of nitrogen supply on carbon dioxide-induced changes in competition between rice and barnyardgrass (Echinochloa crus-galli). Weed Sci 56(1):66–71CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Jiangbing Xu
    • 1
    • 2
  • Jianwei Zhang
    • 2
  • Chunwu Zhu
    • 2
  • Jianguo Zhu
    • 2
  • Xiangui Lin
    • 2
  • Youzhi Feng
    • 2
    Email author
  1. 1.International Center for Ecology, Meteorology and Environment (IceMe), School of Applied MeteorologyNanjing University of Information Science and TechnologyNanjingChina
  2. 2.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingChina

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