Abstract
The salinization of grassland in arid and semi-arid areas is a serious environmental issue in China. Halophytes show extreme salt tolerance and are grown in saline-alkaline environments. Their rhizosphere microorganisms contribute significantly to plant stress tolerance. To study bacterial and fungal community structure changes in Chinese ryegrass (Leymus chinensis) rhizosphere soil under salt and alkali stress, pot experiments were conducted with different salt and alkali stress intensities. High-throughput sequencing was conducted, and the microbial diversity, community structure, and driving factors were analyzed in rhizosphere soil. The salinization of grassland in arid and semi-arid areas is a serious environmental issue in China. Halophytes show extreme salt tolerance and grow in saline-alkaline environments. A total of 549 species of bacteria from 28 phyla and 250 species from 11 phyla of fungi were detected in the rhizosphere soil of Leymus chinensis with different saline-alkali gradients. Alpha diversity analysis along saline-alkali gradients showed that bacterial community richness and diversity were the highest in the moderate saline-alkali group (pH = 8.28, EC = 160.4 μS·cm−1), while fungi had high richness and diversity in the control group (pH = 7.35, EC = 134.5 μS·cm−1). The bacteriophyta Proteobacteria, Acidobacteria, Plantomycetes, and the eumycota Ascomycota, Basidiomycota, and Glomeromycota were found with relative abundances of more than 10%. Saline-alkali gradients had significant effects on the abundance of the bacterial and fungal groups in the rhizosphere. The distribution of bacterial colony structure was not significant at the species level (P > 0.05). However, there were significant differences in the distribution of fungal structure and considerable differences in the composition of fungal species among the moderate saline-alkali group, severe saline-alkali group, and control group (P < 0.05). Correlation analysis showed that the bacterial phylum Gemmatimonadetes had a highly significant positive correlation with pH and EC (P < 0. 01). Saline-alkali stress significantly inhibited the abundance of the bacteria Latescibacteria, Cyanobacteria, and Bacteroides, and the fungi Zoopagomycota, Mortierllomycota, and Cryptomycota (P < 0. 05). Compared with fungi, bacterial community composition was most closely correlated with soil salinization. This report provided new insights into the responses of relationships between rhizosphere soil microorganisms and salt and alkali tolerance of plants.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abdel-Fattah GM, Abdul-Wasea AA (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat Triticum aestivum L plants grown in saline soil. Acta Physiol. Plant. 34(1):267–277
Assainar SK, Abbott LK, Mickan BS et al (2020) Polymer-coated rock mineral fertilizer has potential to substitute soluble fertilizer for increasing growth, nutrient uptake, and yield of wheat. Biol Fertil Soils 56(3):381–394
Bahram M, Hildebrand F, Forslund SK et al (2018) Structure and function of the global topsoil microbiome. Nature 560(7717):233–237
Bao SD (2020) Soil agrochemical analysis. China Agriculture Press, Beijing, China (In Chinese)
Baumann K, Dignac MF, Rumpel C et al (2013) Soil microbial diversity affects soil organic matter decomposition in a silty grass land soil. Biogeochemistry 114:201–212
Berendsen RL, Pieterse C, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486
Che R, Wang F, Wang W et al (2017) Increase in ammonia-oxidizing microbe abundance during degradation of alpine meadows may lead to greater soil nitrogen loss. Biogeochemistry 136(3):341–352
Chu DM, Ma J, Prince AL et al (2017) Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med 23(3):314–326
Cui JT, Li YN, Wang CY et al (2018) Characteristics of the rhizosphere bacterial community across different cultivation years in saline-alkaline paddy soils of Songnen Plain of China. Can J Microbiol 64:925–936
de Boer W, Folman LB, Summerbell RC et al (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol 29:795–811
DeBruyn JM, Nixon LT, Fawaz MN et al (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77:6295–6300
Ezawa T, Saito K (2018) How do arbuscular mycorrhizal fungi handle phosphate? new insight into fine-tuning of phosphate metabolism. New Phytol 220(4):1116–1121
Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol. 8(9):e1002687
Gai JP, Christie P, Feng G et al (2006) Twenty years of research on community composition and species distribution of arbuscular mycorrhizal fungi in China: a review. Mycorrhiza 16(4):229–239
Gamalero E, Bona E, Todeschini V et al (2020) Saline and arid soils: impact on bacteria, plants, and their interaction. Biology 9(6):116–142
Grice EA, Kong HH, Conlan S et al (2009) Topographical and temporal diversity of the human skin microbiome. Science 324(5931):1190–1192
Hafees FY & Malik KA (2000) Manual on biofertilizer technology. Pakistan: Nibge.
Hashem A, Tabassum B, Abd_Allah EF, (2019) Bacillus subtilis: a plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi J Biol Sci 26(6):1291–1297
Hou YL, Zeng WZ, Hou ML et al (2021) Responses of the soil microbial community to salinity stress in maize fields. Biology 10:1114
Jennifer MD, Lauren TN, Mariam NF et al (2011) Global biogeography and quantitative seasonal dynamics of gemmatimonadetes in soil. Appl Environ Microbiol 77(17):6295–6300
Jin-Huan L, Anjum SA, Mei-Ru L et al (2015) Modulation of morpho-physiological traits of Leymus Chinensis (Trin) through exogenous application of brassinolide under salt stress. J Anim Plant Sci 25(4):1055–1062
Jones RT, Robeson MS, Lauber CL et al (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3(4):442–453
Johnson JS, Spakowicz DJ, Hong BY et al (2019) Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun 10(1):1–11
Kamble PN, Gaikwad VB, Kuchekar SR et al (2014) Microbial growth, biomass, community structure and nutrient limitation in high pH and salinity soils from Pravaranagar (India). Eur J Soil Biol 65:87–95
Khomich M, Davey L, Kauserud H et al (2017) Fungal communities in Scandinavian lakes along a longitudinal gradient. Fungal Ecol 27:36–46
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Lauber CL, Hamady M, Knight R et al (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120
Lim SJ, Shin MN, Son JK et al (2017) Evaluation of soil pore-water salinity using a Decagon GS3 sensor in saline-alkali reclaimed tidal lands. Comput Electron Agric 132:49–55
Li MY, Wang JL, Zhou Q et al (2021) Analysis on the rhizosphere fungal community structure of four halophytes in Southern Xinjiang. Acta Ecol Sin 41(21):1–12 ((In Chinese))
Li JD, Fang JY (2017) Study on the ecological function of Chinese grassland. Science Press, Beijing, China (In Chinese)
Liu JJ, Sui YY, Yu ZH et al (2015) Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Bio Biochem 83:29–39
Li XZ, Sun P, Zhang YN et al (2020) A novel pgpr strain kocuria rhizophila y1 enhances salt stress tolerance in maize by regulating phytohormone levels, nutrient acquisition, redox potential, ion homeostasis, photosynthetic capacity and stress-responsive genes expression. Environ. Exp. Bot. 174:104023
Li Y, Yang XD, Qin L et al (2018) The bacterial diversity and community structures in rhizosphere soil of two halophytes, Lycium ruthenicum and Kalidium capsicum. Acta Ecol Sin 38(9):3118–3131 ((In Chinese))
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet 17:10–12
Nacke H, Thürmer A, Wollherr A et al (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6(2):e17000
Nuccio EE, Anderson-Furgeson J, Estera KY et al (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97(5):1307–1318
Ondrasek G, Begić HB, Zovko M et al (2019) Biogeochemistry of soil organic matter in agroecosystems & environmental implications. Sci Total Environ 658:1559–1573
Ondrasek G, Rengel Z (2021) Environmental salinization processes: detection, implications & solutions. Sci. Total Environ. 754(39):142432
Ondrasek G, Rengel Z, Romic D et al (2012) Salinity decreases dissolved organic carbon in the rhizosphere and increases trace element phyto-accumulation. Eur J Soil Sci 63(5):685–693
Pankaj U, Singh DN, Mishra P et al (2020) Autochthonous halotolerant plant growth-promoting rhizobacteria promote bacoside a yield of Bacopa monnieri (L) Nash and phytoextraction of salt-affected soil. Pedosphere 30(5):671–683
Pasic L, Kovce B, Sket B et al (2010) Diversity of microbial communities colonizing the walls of a Karstic cave in Slovenia. FEMS Microbiol Ecol 71:50–60
Pii Y, Mimmo T, Tomasi N et al (2015) Microbial interactions in the rhizosphere beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. a review Biol Fertil Soil 51(4):403–415
Ren H, Huang B, Fernández-García V et al (2020) Biochar and rhizobacteria amendments improve several soil properties and bacterial diversity. Microorganisms 8(4):502–519
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One. 6
Sun T, Miao J, Saleem M et al (2020) Bacterial compatibility and immobilization with biochar improved tebuconazole degradation, soil microbiome composition and functioning. J Hazard Mater 398:122941
Tian Y, Liu Y, Yue L et al (2022) Bacterial inoculant and sucrose amendments improve the growth of rheum palmatum L. by reprograming its metabolite composition and altering its soil microbial community. Int J Mol Sci 23(3):1694
Umesh PD, Narain SP, Mishra P et al (2020) Autochthonous halotolerant plant growth-promoting rhizobacteria promote bacoside a yield of bacopa monnieri (l.) nash and phytoextraction of salt-affected soil. Pedosphere 30(5):97–109
Wakelin SA, Macdonald LM, Rogers SL et al (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813
Wang DL, Wang L (2019) A new perspective on the concept of grassland management. Chin Sci Bull 64(11):1106–1113
Wang LX, Fang C, Wang K (2015) Physiological responses of LeymusChinensis to long-term salt, alkali and mixed salt-alkali stresses. J Plant Nutr 38(4):526–540
Wichern J, Wichern F, Joergensen RG (2006) Impact of salinity on soil microbial communities and the decomposition of maize in acidic soils. Geoderma 137:100–108
Wu PF, Li DX, Kong LF et al (2019) The diversity and biogeography of microeukaryotes in the euphotic zone of the northwestern Pacific Ocean. Sci Total Environ 698:134289
Yamamoto K, Shiwa Y, Ishige T et al (2018) Bacterial diversity associated with the rhizosphere and endosphere of two halophytes: Glaux maritima and Salicornia europaea. Front Microbiol 9:2878
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4
Zhang Y, Liu X, Cong J et al (2017) The microbially mediated soil organic carbon loss under degenerative succession in an alpine meadow. Mol Ecol 26(14):3676–3686
Zhang ZM, Ci DW, Zhang GC et al (2017) Diversity of microbial community structure in the spermosphere of saline-alkali soil in Shandong area. Acta Microbiol Sin 57(4):582–596
Zhao S, Liu JJ, Banerjee S et al (2020) Biogeographical distribution of bacterial communities in saline agricultural soil. Geoderma 361:114095
Zhao Y, Liu Z, Wu J (2020) Grassland ecosystem services: a systematic review of research advances and future directions. Landsc Ecol 35:1–22
Zhou J, Gu Y, Zou C et al (2007) Phylogenetic diversity of bacteria in an earth-cave in Guizhou province, southwest of China. J Microbiol 45:105–111
Zhu RF, Liu JL, Wang JL et al (2020) Study on bacterial community diversity and environmental factors in rhizosphere soil of Leymuschinensis. Acta Agrestia Sinica 28(3):652–660
Ziegler M, Engel M, Welzl G et al (2013) Development of a simple root model to study the effects of single exudates on the development of bacterial community structure. J Microbiol Methods 94(1):30–36
Funding
This work was supported by the Department of Science and Technology of Jilin Province [grant number 20200403004SF]; the Jilin Province Development and Reform Commission [grant number 2019C056-6]; the Education Department of Jilin Province [JJKH20210283KJ].
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Binshuo Liu: writing–original draft. Yunhang Hu: investigation. Ying Wang: data analysis. Honghai Xue: writing–review and editing. Zhonghe Li and Ming Li: conceptualization and methodology.
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Liu, B., Hu, Y., Wang, Y. et al. Effects of saline-alkali stress on bacterial and fungal community diversity in Leymus chinensis rhizosphere soil. Environ Sci Pollut Res 29, 70000–70013 (2022). https://doi.org/10.1007/s11356-022-20270-6
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DOI: https://doi.org/10.1007/s11356-022-20270-6