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Plant growth–promoting bacteria improve maize growth through reshaping the rhizobacterial community in low-nitrogen and low-phosphorus soil

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Abstract

The effects of 13 plant growth–promoting rhizobacteria (PGPR) from the maize rhizosphere and a model PGPR strain Azospirillum brasilense Az39 on maize growth were monitored in a 3-year field inoculation experiment (from 2018 to 2020) with low-nitrogen (N) (N input reduced by 50%) and low-phosphorus (P) (no P supply) soils in Northeast China. The effects of four efficient PGPR that stably promoted maize plant growth and affected on the composition and function of the rhizobacterial community were further investigated in 2019 and 2020. On average, Sinorhizobium sp. A15, Bacillus sp. A28, Sphingomonas sp. A55, and Enterobacter sp. P24 stably increased grain yield by 8.1–17.8% and 11.0–20.1% in low-N and low-P soil, respectively. Inoculation of these four strains increased the abundance and species richness of rhizobacteria, enriched special beneficial bacteria such as Chloroflexia_KD4-96 and Bacilli, and decreased bacterial functions related to soil-N loss. We conclude that some PGPR can N- and P-use efficiency and maize yield through reshaping the rhizobacterial community.

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Data availability

The obtained sequences were submitted to the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) with accession number SRP309888. Other data that supports the findings of this study are available in the supplementary material of this article.

References

  • Adesemoye A, Torbert H, Kloepper J (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929

    Article  CAS  PubMed  Google Scholar 

  • Ahmad F, Ahmad I, Khan M (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  CAS  PubMed  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473

    Article  PubMed  PubMed Central  Google Scholar 

  • Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13

    Article  CAS  Google Scholar 

  • Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microb Biot 28:1327–1350

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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 

  • Cassán F, Coniglio A, López G, Molina R, Nievas S, de Carlan CLN, Donadio F, Torres D, Rosas S, Pedrosa FO (2020) Everything you must know about Azospirillum and its impact on agriculture and beyond. Biol Fert Soils 56:461–479

    Article  Google Scholar 

  • Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130

    Article  CAS  Google Scholar 

  • Chang CH, Yang SS (2009) Thermo-tolerant phosphate-solubilizing microbes for multi-functional biofertilizer preparation. Bioresource Technol 100:1648–1658

    Article  CAS  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fert Soils 48:489–499

    Article  Google Scholar 

  • Chaudhary DR, Rathore AP, Sharma S (2020) Effect of halotolerant plant growth promoting rhizobacteria inoculation on soil microbial community structure and nutrients. Appl Soil Ecol 150:103461

    Article  Google Scholar 

  • Chen L, Hao Z, Li K, Sha Y, Wang E, Sui X, Mi G, Tian C, Chen W (2021a) Effects of growth-promoting rhizobacteria on maize growth and rhizosphere microbial community under conservation tillage in Northeast China. Microb Biotechnol 14:535–550

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Li KK, Shi WJ, Wang XL, Wang ET, Liu JF, Sui XH, Mi GH, Tian CF, Chen WX (2021b) Negative impacts of excessive nitrogen fertilization on the abundance and diversity of diazotrophs in black soil under maize monocropping. Geoderma 393:114999

    Article  CAS  Google Scholar 

  • Chen Q, Ding J, Zhu Y, He J, Hu H (2020) Soil bacterial taxonomic diversity is critical to maintaining the plant productivity. Environ Int 140:105766

    Article  PubMed  Google Scholar 

  • Contosta AR, Frey SD, Cooper AB (2015) Soil microbial communities vary as much over time as with chronic warming and nitrogen additions. Soil Biol Biochem 88:19–24

    Article  CAS  Google Scholar 

  • Díaz-Zorita M, Fernández-Canigia MV (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. Eur J Soil Biol 45:3–11

    Article  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Funct Plant Biol 28:871–879

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Meth 10:996–998

    Article  CAS  Google Scholar 

  • Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microb 67:5285–5293

    Article  CAS  Google Scholar 

  • El-Tarabily KA, ElBaghdady KZ, AlKhajeh AS, Ayyash MM, Aljneibi RS, El-Keblawy A, AbuQamar SF (2020) Polyamine-producing actinobacteria enhance biomass production and seed yield in Salicornia bigelovii. Biol Fertil Soils 56:499–519

    Article  CAS  Google Scholar 

  • Fasching C, Akotoye C, Bižić M, Fonvielle J, Ionescu D, Mathavarajah S, Zoccarato L, Walsh DA, Grossart HP, Xenopoulos MA (2020) Linking stream microbial community functional genes to dissolved organic matter and inorganic nutrients. Limnol Oceanogr 65:S71–S87

    Article  CAS  Google Scholar 

  • Gadhave KR, Devlin PF, Ebertz A, Ross A, Gange AC (2018) Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness, and community composition in a context-specific manner. Microb Ecol 76:741–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu S, Hu Q, Cheng Y, Bai L, Liu Z, Xiao W, Gong Z, Wu Y, Feng K, Deng Y (2019) Application of organic fertilizer improves microbial community diversity and alters microbial network structure in tea (Camellia sinensis) plantation soils. Soil Till Res 195:104356

    Article  Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding K, Vitousek PM, Zhang F (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    Article  CAS  PubMed  Google Scholar 

  • Habib S, Kausar H, Saud H, Ismail M, Othman R (2016) Molecular characterization of stress tolerant plant growth promoting rhizobacteria (PGPR) for growth enhancement of rice. Int J Agric Biol 18:184–191

    Article  CAS  Google Scholar 

  • Hadley W (2016) Ggplot2: Elegrant graphics for data analysis. Springer. https://www.springer.com/us/book/9780387981413

  • Haskett TL, Tkacz A, Poole PS (2021) Engineering rhizobacteria for sustainable agriculture. ISME J 15:949–964

    Article  PubMed  Google Scholar 

  • Hu D, Li S, Li Y, Peng J, Wei X, Ma J, Zhang C, Jia N, Wang E, Wang Z (2020) Streptomyces sp. strain TOR3209: a rhizosphere bacterium promoting growth of tomato by affecting the rhizosphere microbial community. Sci Rep 10:20132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke X, Feng S, Wang J, Lu W, Zhang W, Chen M, Lin M (2019) Effect of inoculation with nitrogen-fixing bacterium Pseudomonas stutzeri A1501 on maize plant growth and the microbiome indigenous to the rhizosphere. Syst Appl Microbiol 42:248–260

    Article  CAS  PubMed  Google Scholar 

  • Kielak AM, Cipriano MA, Kuramae EE (2016) Acidobacteria strains from subdivision 1 act as plant growth-promoting bacteria. Arch Microbiol 198:987–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886

    Article  CAS  Google Scholar 

  • Krishnan R, Menon RR, Tanaka N, Busse HJ, Krishnamurthi S, Rameshkumar N (2016) Arthrobacter pokkalii sp nov, a novel plant associated actinobacterium with plant beneficial properties, isolated from saline tolerant pokkali rice, Kerala, India. PloS one 11:e0150322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krzmarzick MJ, Crary BB, Harding JJ, Oyerinde OO, Leri AC, Myneni SC, Novak PJ (2012) Natural niche for organohalide-respiring Chloroflexi. Appl Environ Microb 78:393–401

    Article  CAS  Google Scholar 

  • Kuypers MM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263

    Article  CAS  PubMed  Google Scholar 

  • Lee S-H, Ka J-O, Cho J-C (2008) Members of the phylum Acidobacteria are dominant and metabolically active in rhizosphere soil. Fems Microbiol Lett 285(2):263–269

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang M, Chen S (2021) Application of N2-fixing Paenibacillus triticisoli BJ-18 changes the compositions and functions of the bacterial, diazotrophic, and fungal microbiomes in the rhizosphere and root/shoot endosphere of wheat under field conditions. Biol Fert Soils 57:347–362

    Article  CAS  Google Scholar 

  • Liu XJ, Zhang FS (2011) Nitrogen fertilizer induced greenhouse gas emissions in China. Curr Opin Env Sust 3:407–413

    Article  CAS  Google Scholar 

  • Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277

    Article  CAS  PubMed  Google Scholar 

  • Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, Garcia-Gomez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitan J, Gutierrez JR, Huber-Sannwald E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang DL, Woods NN, Yuan X, Zaady E, Singh BK (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Natl Acad Sci USA 112:15684–15689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Viveros O, Jorquera M, Crowley D, Gajardo G, Mora M (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nut 10:293–319

    Google Scholar 

  • McKinley KR, Wetzel RG (1979) Photolithotrophy, photoheterotrophy, and chemoheterotrophy: patterns of resource utilization on an annual and a diurnal basis within a pelagic microbial community. Microb Ecol 5:1–15

    Article  CAS  PubMed  Google Scholar 

  • Nannipieri P, Penton CR, Purahong W, Scloter M, Van Elsas JD (2019) Recommendations for soil microbiome analyses. Biol Fertil Soils 55:765–766

    Article  Google Scholar 

  • NBSC (2019) National Bureau of Statistics of China. http://data.stats.gov.cn/

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H, (2013) Package ‘vegan.’ Community Ecology Package, Version 2:1–295

    Google Scholar 

  • Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart D, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1110

    Article  PubMed  PubMed Central  Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. P Natl Acad Sci USA 110:6548–6553

    Article  CAS  Google Scholar 

  • Perin G, Yunus IS, Valton M, Alobwede E, Jones PR (2019) Sunlight-driven recycling to increase nutrient use-efficiency in agriculture. Algal Res 41:101554

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363

    Article  Google Scholar 

  • Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Torres-Gutierrez R, El-Howeity M, Michiels J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161

    Article  CAS  Google Scholar 

  • Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  PubMed  Google Scholar 

  • Rondina ABL, dos Santos Sanzovo AW, Guimarães GS, Wendling JR, Nogueira MA, Hungria M (2020) Changes in root morphological traits in soybean co-inoculated with Bradyrhizobium spp. and Azospirillum brasilense or treated with A. brasilense exudates. Biol Fertil Soils 56:537–549

    Article  CAS  Google Scholar 

  • Savci S (2012) An agricultural pollutant: chemical fertilizer. Int J Environ Sci Dev 3:73

    Article  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:1–18

    Article  Google Scholar 

  • Sessitsch A, Pfaffenbichler N, Mitter B (2019) Microbiome applications from lab to field: facing complexity. Trends Plant Sci 24:194–198

    Article  CAS  PubMed  Google Scholar 

  • Soil Survey Staff (2014) Keys to Soil Taxonomy, 12th edn. USDA-Natural Resources Conservation Service, Washington DC

    Google Scholar 

  • Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, Arora DK (2011) Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol Fert Soils 47:907–916

    Article  CAS  Google Scholar 

  • van der Heijden MGA, de Bruin S, Luckerhoff L, van Logtestijn RSP, Schlaeppi K (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399

    Article  PubMed  CAS  Google Scholar 

  • Vasconcellos RL, Romagnoli EM, Taketani RG, Santos SN, Zucchi TD, Melo IS (2021) Impact of inoculation with Pseudomonas aestus CMAA 1215 (T) on the non-target resident bacterial community in a saline rhizosphere soil. Curr Microbiol 78:218–228

    Article  CAS  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Waldrop M, Firestone M (2006) Response of microbial community composition and function to soil climate change. Microb Ecol 52:716–724

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Li Q, Xu S, Zhao W, Lei Y, Song C, Huang Z (2018) Traits-based integration of multi-species inoculants facilitates shifts of indigenous soil bacterial community. Front Microbiol 9:1692

    Article  PubMed  PubMed Central  Google Scholar 

  • Weidner S, Koller R, Latz E, Kowalchuk G, Bonkowski M, Scheu S, Jousset A (2015) Bacterial diversity amplifies nutrient-based plant–soil feedbacks. Funct Ecol 29:1341–1349

    Article  Google Scholar 

  • Xiong W, Guo S, Jousset A, Zhao Q, Wu H, Li R, Kowalchuk GA, Shen Q (2017) Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem 114:238–247

    Article  CAS  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Gao X, Shen Z, Zhu C, Jiao Z, Li R, Shen Q (2019) Pre-colonization of PGPR triggers rhizosphere microbiota succession associated with crop yield enhancement. Plant Soil 439:553–567

    Article  CAS  Google Scholar 

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Acknowledgements

We sincerely thank Dr. Fabricio Cassán (Universidad Nacional de Río Cuarto, Córdoba, Argentina) for providing the Azospirillum brasilense Az39. Special thanks to Ye Sha, Zhanhong Hao, Yuna Wang, Rong Shi, and Wenjun Shi for assistance with field management. We thank Jennifer Smith, PhD, from Liwen Bianji (Edanz) (www.liwenbianji.cn) for editing the English text of a draft of this manuscript.

Funding

This work was financially supported by the National Natural Science Foundation of China (project U19A2035) and the National Key Research & Development Program of China (project 2017YFD0201801).

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Authors and Affiliations

  1. State Key Laboratory of Agrobiotechnology, Key Laboratory of Soil Microbiology, Ministry of Agriculture, College of Biological Sciences, China Agricultural University, Beijing, 100193, China

    La Chen, Keke Li, Jiaoying Shang, Yue Wu, Ting Chen, Yuqian Wanyan, Changfu Tian, Wenfeng Chen, Wenxin Chen & Xinhua Sui

  2. Escuela Nacional de Ciencias Biologicas, Instituto Politecnico Nacional, 11340, Mexico DF , Mexico

    Entao Wang

  3. Key Laboratory of Plant-Soil Interactions, Ministry of Education, College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

    Guohua Mi

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Contributions

GHM and XHS designed the study. LC and KKL performed the experiments. LC, JYS, YW, TC, and YQWY isolated the bacteria from the maize rhizosphere. LC analyzed the data and prepared the figures and tables. LC, ETW, XHS, and GHM wrote the manuscript. CFT, WFC, and WXC provided resources. All authors read and approved the paper.

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Correspondence to Guohua Mi or Xinhua Sui.

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Chen, L., Li, K., Shang, J. et al. Plant growth–promoting bacteria improve maize growth through reshaping the rhizobacterial community in low-nitrogen and low-phosphorus soil. Biol Fertil Soils 57, 1075–1088 (2021). https://doi.org/10.1007/s00374-021-01598-6

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