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

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
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Abstract

Purpose

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.

Conclusions

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.

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References

  • 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):514–520

    Article  CAS  Google Scholar 

  • 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):233–266

    Article  CAS  Google Scholar 

  • 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):343–351

    Article  CAS  Google Scholar 

  • Barrat A, Barthélemy M, Pastor-Satorras R, Vespignani A (2004) The architecture of complex weighted networks. P Natl Acad Sci USA 101(11):3747–3752

    Article  CAS  Google Scholar 

  • Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219

    Article  Google Scholar 

  • 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):8659–8671

    Article  CAS  Google Scholar 

  • 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):10583–10588

    Article  Google Scholar 

  • 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):5–10

    Article  CAS  Google Scholar 

  • 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):1292–1304

    Article  Google Scholar 

  • 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):335–336

    Article  CAS  Google Scholar 

  • 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):1084–1087

    Article  CAS  Google Scholar 

  • 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):980–989

    Article  Google Scholar 

  • Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13(1):113

    Article  Google Scholar 

  • 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):667–679

    Article  Google Scholar 

  • 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):3175–3185

    Article  CAS  Google Scholar 

  • 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):10938–10942

    Article  Google Scholar 

  • 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):313–323

    Article  CAS  Google Scholar 

  • Edgar RC (2017) SEARCH_16S: a new algorithm for identifying 16S ribosomal RNA genes in contigs and chromosomes. bioRxiv:124131

  • 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 7:44641

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10(8):538–550

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364

    Article  Google Scholar 

  • 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 8:1516

    Article  Google Scholar 

  • Guimerà R, Nunes Amaral LA (2005) Functional cartography of complex metabolic networks. Nature 433:895–900

    Article  CAS  Google Scholar 

  • 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 7:3608

  • 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):259–272

    Article  CAS  Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • 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 109:145–155

    Article  CAS  Google Scholar 

  • Johnson DV, Jain SM, Al-Khayri JM (2016) Advances in plant breeding strategies: agronomic, abiotic and biotic, vol 2. Springer, Berlin

    Google Scholar 

  • 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):261–270

    Article  Google Scholar 

  • 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 108:307–314

    Article  Google Scholar 

  • 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 7:60

    Google Scholar 

  • 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 99:137–149

    Article  CAS  Google Scholar 

  • 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 77:58–68

    Article  CAS  Google Scholar 

  • 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):3–8

    Article  CAS  Google Scholar 

  • 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):1918–1921

    Article  CAS  Google Scholar 

  • 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 181-203

  • 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 624:530–539

    Article  CAS  Google Scholar 

  • 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):251–260

    Article  Google Scholar 

  • 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 package

    Google Scholar 

  • 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 6:136

    Article  Google Scholar 

  • Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. P Natl Acad Sci USA 104(50):19891–19896

    Article  Google Scholar 

  • 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):609–620

    Article  Google Scholar 

  • 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):407–421

    Article  CAS  Google Scholar 

  • Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • 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 86:1–9

    Article  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0040338

    Article  CAS  Google Scholar 

  • 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):2200–2210

    Article  Google Scholar 

  • 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):926–936

    Article  Google Scholar 

  • 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):523–532

    Article  CAS  Google Scholar 

  • 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):1–6

    Article  CAS  Google Scholar 

  • 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 96:207–215

    Article  CAS  Google Scholar 

  • Wang Y, Li H, Li J, Li X (2017) The diversity and co-occurrence patterns of diazotrophs in the steppes of Inner Mongolia. Catena 157:130–138

    Article  Google Scholar 

  • 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 112:258–268

    Article  CAS  Google Scholar 

  • 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 285:19–26

    Article  CAS  Google Scholar 

  • 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 7:4778

  • 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):141–150

    Article  Google Scholar 

  • 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 9:1139

    Article  Google Scholar 

  • 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):e00122–11

  • 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 5:12719

    Article  CAS  Google Scholar 

  • 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):579–587

    Article  CAS  Google Scholar 

  • 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):66–71

    Article  CAS  Google Scholar 

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Acknowledgements

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).

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  1. Jiangbing Xu and Jianwei Zhang contributed equally to this work.

Authors and Affiliations

  1. International Center for Ecology, Meteorology and Environment (IceMe), School of Applied Meteorology, Nanjing University of Information Science and Technology, Nanjing, 210044, China

    Jiangbing Xu

  2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Jiangbing Xu, Jianwei Zhang, Chunwu Zhu, Jianguo Zhu, Xiangui Lin & Youzhi Feng

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  1. Jiangbing Xu
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  2. Jianwei Zhang
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  3. Chunwu Zhu
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Correspondence to Youzhi Feng.

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Xu, J., Zhang, J., Zhu, C. et al. Influence of rice cultivars on soil bacterial microbiome under elevated carbon dioxide. J Soils Sediments 19, 2485–2495 (2019). https://doi.org/10.1007/s11368-018-2220-z

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