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Relationship between pepper (Capsicum annuum L.) root morphology, inter-root soil bacterial community structure and diversity under water–air intercropping conditions

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Abstract

Main conclusion

The combination of water and gas at an aeration rate of 15 mg/L and irrigation amount of 0.8 Ep significantly promoted the root morphology, inter-root soil bacterial community structure and diversity of pepper, enhanced the structure of molecular symbiotic network, and stimulated the potential ecosystem function.

Abstract

Poor aeration adversely affects the root morphology of pepper (Capsicum annuum L.) and bacterial community. It is critical to understand the effects of water–air interactions on root morphology and bacterial community structure and diversity. A randomized block experiment was conducted under the two aeration rates of dissolved oxygen mass concentrations, including A: 15 mg/L, O: 40 mg/L, and C: non-aeration as control treatment, and two irrigation rates of W1 and W2 (0.8 Ep and 1.0 Ep). The results showed that aerated irrigation had a significant effect on the root morphology of pepper. Compared with treatment CW1, treatment AW1 increased root dry weight, root length, root volume, and root surface area by 13.63%, 11.09%, 59.47%, and 61.67%, respectively (P < 0.05). Aerated irrigation significantly increased the relative abundance of Actinobacteria, Gemmatimonadetes, Alphaproteobacteria, Gemmatimonas, Sphingomonas, and KD4-96 aerobic beneficial bacteria. It decreased the relative abundance of Proteobacteria, Monomycetes, Bacteroidetes, Corynebacterium, Gammaproteobacteria, Anaerolineae, Subgroup_6, MND1, Haliangium, and Thiobacillus. The Pielou_e, Shannon and Simpson indexes of treatment AW1 were significantly higher than treatments OW1 and CW1. The results of the β-diversity of bacterial communities showed that the structure of soil bacterial communities differed significantly among treatments. Actinobacteria was a key phylum affecting root morphology, and AW1 treatment was highly correlated with Actinobacteria. Molecular ecological network analysis showed a relatively high number of bacterial network nodes and more complex relationships among species under the aeration of level 15 mg/L and 0.8 Ep, as well as the emergence of new phylum-level beneficial species: Dependentiae, BRC1, Cyanobacteria, Deinococcus-Thermus, Firmicutes, and Planctomycetes. Therefore, the aeration of 15 mg/L and 0.8 times crop-evaporation coefficient can increase root morphology, inter-root soil bacterial community diversity and bacterial network structure, and enhance potential ecosystem functions in the rhizosphere.

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Data availability

The data reported in this study are contained within the article.

Abbreviations

NMDS:

Non-metric dimensional scaling

RDA:

Redundancy analysis

References

  • Abbas T, Zhang Q, Jin H, Li Y, Liang Y, Di H, Zhao Y (2019) Anammox microbial community and activity changes in response to water and dissolved oxygen managements in a paddy-wheat soil of Southern China. Sci Total Environ 672:305–313

    Article  CAS  PubMed  Google Scholar 

  • Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE (2016) Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem 97:188–198

    Article  CAS  Google Scholar 

  • Bardgett RD, Van Der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511

    Article  CAS  PubMed  Google Scholar 

  • Bastida F, Crowther TW, Prieto I, Routh D, García C, Jehmlich N (2018) Climate shapes the protein abundance of dominant soil bacteria. Sci Total Environ 640:18–21

    Article  PubMed  Google Scholar 

  • Ben-Noah I, Friendman SP (2016) Oxygation of clayey soils by adding hydrogen peroxide to the irrigation solution: lysimetric experiments. Rhizosphere-Neth 2:1–11

    Google Scholar 

  • Bhattarai SP, Su N, Midmore DJ (2005) Oxygation unlocks yield potentials of crops in oxygen-limited soil environments. Adv Agron 88:313–377

    Article  CAS  Google Scholar 

  • Bhattarai SP, Pendergast L, Midmore DJ (2006) Root aeration improves yield and water use efficiency of tomato in heavy clay and saline soils. Sci Hortic 108(3):278–288

    Article  Google Scholar 

  • Bhattarai SP, Midmore DJ, Pendergast L (2008) Yield, water-use efficiencies and root distribution of soybean, chickpea and pumpkin under different subsurface drip irrigation depths and oxygation treatments in vertisols. Irrigation Sci 26(5):439–450

    Article  Google Scholar 

  • Biggs-Weber E, Aigle A, Prosser JI, Gubry-Rangin C (2020) Oxygen preference of deeply-rooted mesophilic thaumarchaeota in forest soil. Soil Biol Biochem 148:107848

    Article  CAS  Google Scholar 

  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME2. Nat Biotechnol 37:852–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botta GF, Tolón BA, Bienvenido F, Rivero D, Laureda DA, Ezquerra CA, Contessotto EE (2018) Sunflower (Helianthus annuus L.) harvest: Tractor and grain chaser traffic effects on soil compaction and crop yields. Land Degrad Dev 29:4252–4261

    Article  Google Scholar 

  • Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262

    Article  CAS  Google Scholar 

  • Burke DJ, Weintraub MN, Hewins CR, Kalisz S (2011) Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem 43:795–803

    Article  CAS  Google Scholar 

  • Callahan BJ, Mcmurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhu Y, Shao T, Long X, Gao X, Zhou Z (2019) Relationship between rhizosphere soil properties and disease severity in highbush blueberry (Vaccinium corymbosum). Appl Soil Ecol 137:187–194

    Article  Google Scholar 

  • Chen Z, Lin L, Li Y, Chen Y, Zhang H, Han H, Wu N, Nicola F, Li Y, Ren X (2021) Shifts in rhizosphere bacterial community structure, co-occurrence network, and function of miscanthus following cadmium exposure. Environ Sci 42(8):3997–4004 (in Chinese)

    Google Scholar 

  • Dai J, Tian P, Zhang Y, Su J (2019) Rhizobacteria community structure and diversity of six salt-tolerant plants in Yinbei salin soil. Acta Ecol Sin 39(08):2705–2714

    CAS  Google Scholar 

  • Deng Y, Jiang Y, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13(1):113. https://doi.org/10.1186/1471-2105-13-113

    Article  PubMed  PubMed Central  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072

    Article  CAS  Google Scholar 

  • Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903

    Article  CAS  Google Scholar 

  • Else MA, Coupland D, Dutton L, Jackson MB (2001) Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiol Plant 111:46–54

    Article  CAS  Google Scholar 

  • Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia-is survival a balancing act? Trends Plant Sci 9:449–456. https://doi.org/10.1016/j.tplants.2004.07.005

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Li M, Lu P (2019) Bacterial community in the rhizosphere soil of Betula platyphylla in the Daqing Mountain, Hohhot. Acta Ecol Sin 39(10):3586–3596

    CAS  Google Scholar 

  • Garcia-Gil J, Plaza CC, Soler-Rovira P, Polo A (2000) Long-term effects of municipal solid waste compost application on soil enzyme activities and microbial biomass. Soil Biol Biochem 32:1907–1913

    Article  CAS  Google Scholar 

  • Hong-Thao PT, Mai-Linh NV, Hong-Lien NT, Van Hieu N (2016) Biological characteristics and antimicrobial activity of endophytic Streptomyces sp. TQR12–4 isolated from elite Citrus nobilis cultivar Ham Yen of Vietnam. Int J Microbiol 2016:7207818

    Article  PubMed  PubMed Central  Google Scholar 

  • Horchani F, Aschi-smiti S, Brouquisse R (2010) Involvement of nitrate reduction in the tolerance of tomato (Solanum lycopersicum L.) plants to prolonged root hypoxia. Acta Physiol Plant 32(6):1113–1123

    Article  Google Scholar 

  • Hu X, Liu J, Wei D, Zhu P, Cui X, Zhou B, Chen X, Jin J, Liu X, Wang G (2018) Comparison on fungal molecular ecological networks of agricultural soils with different latitudes in the black soil region of Northeast China. Chin J Appl Ecol 29(11):3802–3810 (in Chinese)

    Google Scholar 

  • Huan D (2012) A review of diversity-stability relationship of soil microbial community: what do we not know? J Environ Sci 24(6):1027–1035

    Article  Google Scholar 

  • Huang J, Hu T, Yasir M, Gao Y, Chen C, Zhu R, Wang X, Yuan H, Yang J (2019) Root growth dynamics and yield responses of rice (Oryza sativa L.) under drought-flood abrupt alternating conditions. Environ Exp Bot 157(6):11–25

    Article  Google Scholar 

  • Imlay JA (2002) How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 46:111–153

    Article  CAS  PubMed  Google Scholar 

  • Khumoetsile M, Dani O (2000) Root zone solute dynamics under drip irrigation: a review. Plant Soil 222:163–190

    Article  Google Scholar 

  • Kladivko EJ (2001) Tillage systems and soil ecology. Soil till Res 61(1–2):61–76

    Article  Google Scholar 

  • Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, Gonzalez A, Kosciolek T, Mccall L, Mcdonald D, Melnik AV, Morton JT, Navas J, Quinn RA, Sanders JG, Swafford AD, Thompson LR, Tripathi A, Xu ZJ, Zaneveld JR, Zhu QY, Gregory CJ, Dorrestein PC (2018) Best practices for analysing microbiomes. Nat Rev Microbiol 16:410–422

    Article  CAS  PubMed  Google Scholar 

  • Kong HK, Sang MK, An JH, Kim S, Jin YJ, Song J (2022) Changes in the composition and microbial community of the pepper rhizosphere in field with bacterial wilt disease. Plant Pathol J 38(6):692–699

    Article  PubMed  PubMed Central  Google Scholar 

  • Laforest-Lapointe I, Paquette A, Messier C, Kembel SW (2017) Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546(7656):145–147

    Article  CAS  PubMed  Google Scholar 

  • Lei H, Jin C, Hu S, Pan H, Li Y, Wang L (2019a) Effects of aerated subsurface drip irrigation on soil aeration under greenhouse purple eggplant cropping system. J Jiangsu Univer (nat Sci Edition) 40(3):325–331 (in Chinese)

    Google Scholar 

  • Lei H, Yang H, Liu H, Pan H, Liu X, Zang M (2019b) Characteristics and influencing factors of N2O emission from greenhouse tomato field soil under water-fertilizer-air coupling drip irrigation. Trans CASE 35(11):95–104 (in Chinese)

    Google Scholar 

  • Lei H, Xiao Z, Zhang Z, Jin C, Pan H, Sun K (2021) Effects of oxygen and nitrogen coupled irrigation on soil fertility and bacterial community under greenhouse pepper cropping. Tran CASE 37(1):158–166 (in Chinese)

    Google Scholar 

  • Li Z, Zhang R, Wang X, Wang J, Zhang C, Tian C (2011) Carbon dioxide fluxes and concentrations in a cotton field in northwestern China: effects of plastic mulching and drip irrigation. Pedosphere 21(2):178–185

    Article  CAS  Google Scholar 

  • Li B, Li Y, Wei J, Song X, Shi R, Hou Y, Liu Y (2020) Effects of different land use types on the molecular ecological network of soil bacteria. Environ Sci 41(3):1456–1465

    Google Scholar 

  • Li P, Liu M, Ma X, Wu M, Jiang C, Liu K, Liu J, Li Z (2020a) Responses of microbial communities to a gradient of pig manure amendment in red paddy soils. Sci Total Environt 705:135884

    Article  CAS  Google Scholar 

  • Li Y, Niu W, Zhang M, Wang J, Zhang Z (2020b) Artificial soil aeration increases soil bacterial diversity and tomato root performance under greenhouse conditions. Land Degrad Dev 31(12):1443–1461

    Article  Google Scholar 

  • Li W, Siddique MS, Graham N, Yu W (2022) Influence of temperature on biofilm formation mechanisms using a gravity-driven membrane (GDM) system: insights from microbial community structures and metabolomics. Environ Sci Technol 56(12):8908–8919

    Article  CAS  PubMed  Google Scholar 

  • Machado RM, Do RM, Oliveira G, Portas CA (2003) Tomato root distribution, yield and fruit quality under subsurface drip irrigation. Plant Soil 255:333–341

    Article  CAS  Google Scholar 

  • Muhammad I, Wang J, Sainju UM, Zhang S, Zhao F, Khan A (2021) Cover cropping enhances soil microbial biomass and affects microbial community structure: a meta-analysis. Geoderma 381:114696

    Article  CAS  Google Scholar 

  • Niu W, Jia Z, Zhang X, Shao H (2012) Effects of soil rhizosphere aeration on the root growth and water absorption of tomato. Clean-Soil Air Water 40(12):1364–1371

    Article  CAS  Google Scholar 

  • Pendergast L, Bhattarai SP, Midmore DJ (2013) Benefits of oxygation of subsurface drip-irrigation water for cotton in a Vertosol. Crop Pasture Sci 64:1171–1181

    Article  CAS  Google Scholar 

  • Santos LNSD, Matsura EE, Gonçalves IZ, Barbosa EAA, Nazário AA, Tuta NF, Elaiuy MCL, Feitosa DRC, Sousa ACMD (2016) Water storage in the soil profile under subsurface drip irrigation: evaluating two installation depths of emitters and two water qualities. Agr Water Manage 170:91–98

    Article  Google Scholar 

  • Šibanc N, Dumbrell AJ, Mandic-Mulec I, Maček I (2014) Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria. Soil Biol Biochem 68:348–356

    Article  Google Scholar 

  • Sun C, Wang D, Shen X, Liu J, Lan T, Wang W, Xie H, Zhang Y (2020) Effects of biochar, compost and straw input on root exudation of maize (Zea mays L.): from function to morphology. Agric Ecosyst Environ 297(3):106952

    Article  CAS  Google Scholar 

  • Takeshi F, Julia BS (2004) Plant responses to hypoxia—is survival a balancing act. Trends Plant Sci 9(9):449–456

    Article  Google Scholar 

  • Wagg C, Bender SF, Widmer F, Van Der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci India B 111(14):5266–5270

    CAS  Google Scholar 

  • Wan S, Yan Z, Kang Y, Yuan B, Jiao Y, Song J (2019) Using soil matric potential underneath the drip emitter to regulate soil moisture distribution and improve greenhouse tomato production. J Irrig Drain 38(5):1–11 (in Chinese)

    Google Scholar 

  • Wang Z, Chen X, Lü D, Li W, Wang T, Wei C (2020) Effects of water and fertilizer coupling on the yield and quality of processing tomato under aerated drip irrigation. Trans CASE 36(19):66–75 (in Chinese)

    Google Scholar 

  • Xu K, Stewart PS, Xia F, Huang CT, McFeters GA (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microb 64:4035–4039

    Article  CAS  Google Scholar 

  • Xu C, Wang D, Chen S, Chen L, Zhang X (2013) Effects of aeration on root physiology and nitrogen metabolism in rice. Rice Sci 20(2):148–153

    Article  Google Scholar 

  • Yang J, Duan Y, Zhang R, Liu C, Wang Y, Li M, Ding Y, Awasthi MK, Li Y (2020) Connecting soil dissolved organic matter to soil bacterial community structure in a long-term grass-mulching apple orchard. Ind Crop Prod 149(4):112344

    Article  CAS  Google Scholar 

  • Zhang Z, Zhang Z, Li T, Qin Z, Sun D, Song J (2021) 15N tracer analysis of nitrogen uptake and utilization by rice roots under water and biochar management. Tran Chin Soc Agr Mach 52(6):295–304 (in Chinese)

    Google Scholar 

  • Zhao X, Li T, Sun Z (2010) Effects of substrate-aeration cultivation pattern on tomato growth. Chin J App Ecol 21(1):74–78 (in Chinese)

    CAS  Google Scholar 

  • Zhou Y, Zhou B, Xu F (2019) Appropriate dissolved oxygen concentration and application stage of micro-nano bubble water oxygation in greenhouse crop plantation. Agr Water Manag 223(C):105713

    Article  Google Scholar 

  • Zhou Y, Bastida F, Zhou B, Sun Y, Gu T, Li S, Li Y (2020) Soil fertility and crop production are fostered by micro-nano bubble irrigation with associated changes in soil bacterial community. Soil Biol Biochem 141:107663

    Article  CAS  Google Scholar 

  • Zhou Y, Bastida F, Liu Y, He J, Chen W, Wang X, Xiao Y, Song P, Li Y (2022) Impacts and mechanisms of nanobubbles level in drip irrigation system on soil fertility, water use efficiency and crop production: the perspective of soil microbial community. J Clean Prod 333:130050

    Article  CAS  Google Scholar 

  • Zhu Y, Cai H, Song L, Chen H (2017) Impacts of oxygation on plant growth, yield and fruit quality of tomato. Tran Chin Soc Agr Mach 48(8):199–211 (in Chinese)

    Google Scholar 

  • Zhu L, Wang X, Chen F, Li C, Wu L (2019) Effects of the successive planting of Eucalyptus urophylla on soil bacterial and fungal community structure, diversity, microbial biomass, and enzyme activity. Land Degrad Dev 30:636–646

    Article  Google Scholar 

  • Zhu J, Niu W, Zhang Z, Siddique KH, Sun D, Yang R (2022) Distinct roles for soil bacterial and fungal communities associated with the availability of carbon and phosphorus under aerated drip irrigation. Agr Water Manag 274:107925

    Article  Google Scholar 

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Acknowledgements

We want to extend recognition of the support provided financial support by the National Natural Science Foundation of China (No.52079052), the Science and Technology Research Plan in Henan province (212102110032), and the Major Science and Technology Innovation Project in Shandong, Key Research & Development Plan (2019JZZY010710), China.

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Correspondence to Hongwei Pan.

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None. All authors have approved the manuscript. I declare on behalf of all authors that the work described is original research that has not been published previously and is not under consideration for publication elsewhere, in whole or in part.

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Lei, H., Jin, C., Xiao, Z. et al. Relationship between pepper (Capsicum annuum L.) root morphology, inter-root soil bacterial community structure and diversity under water–air intercropping conditions. Planta 257, 98 (2023). https://doi.org/10.1007/s00425-023-04134-y

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