Microbial diversity and physicochemical properties in farmland soils amended by effective microorganisms and fulvic acid for cropping Asian ginseng


  • Yonghua XU Jilin Agricultural University, National and Local Joint Engineering Research Center for Ginseng Breeding and Application (CN)
  • Chenyang LIU Jilin Agricultural University, National and Local Joint Engineering Research Center for Ginseng Breeding and Application (CN)
  • Jingshan BAO Jilin Agricultural University, National and Local Joint Engineering Research Center for Ginseng Breeding and Application (CN)
  • He ZHU Jilin Agricultural University, College of Resources and Environment (CN)
  • Yuanhui CHEN Jilin Agricultural University, Key Laboratory of Straw Biology and Utilization (CN)
  • Yunqing LUO Jilin Agricultural University (CN)
  • Lianxue ZHANG Jilin Agricultural University, National and Local Joint Engineering Research Center for Ginseng Breeding and Application (CN)




Asian ginseng, effective microorganisms, farmland soil quality, fulvic acid, soil microbial activities


Demand for products made from the dry mass of Asian ginseng (Panax ginseng) is growing, but harvest is limited by fungal disease infection when ginseng is replanted in the same field. Rotated cropping with maize can cope with the replant limit, but it may take decades. We aimed to amend post-maize-cropping farmland soils for cultivating Asian ginseng, using effective microorganisms EMs and fulvic acid (FA) additives and detecting and comparing their effects on soil microbial diversity and physiochemical properties. Amendments promoted seedling survival and depressed disease-infection. Both EMs and FA increased the relative abundances of Pseudomonas, Flavobacterium, Duganella, and Massilia spp., but, decreased the relative abundances of Fusarium and Sistotrema. In addition, soil nutrient availability and properties that benefitted nutrient availabilities were promoted. In conclusion, amendments with EMs and FA improved the fertility of farmland soils, and the quality of Asian ginseng, and revealed the relationship between soil microbial diversity and physiochemical properties.


Abdel-Baky YR, Abouziena HF, Amin AA, Rashad El-Sh M, Abd El-Sttar AM (2019). Improve quality and productivity of some faba bean cultivars with foliar application of fulvic acid. Bulletin of the National Research Centre 43(1):2. https://doi.org/10.1186/s42269-018-0040-3

Aiello D, Restuccia C, Stefani E, Vitale A, Cirvilleri G (2019). Postharvest biocontrol ability of Pseudomonas synxantha against Monilinia fructicola and Monilinia fructigena on stone fruit. Postharvest Biology and Technology 149:83-89. https://doi.org/10.1016/j.postharvbio.2018.11.020

Aydin SK, Dalgic S, Karaman M, Kirlangic OF, Yildirim H (2017). Effects of fulvic acid on different cancer cell lines. Proceedings 1(10):1031. https://doi.org/10.3390/proceedings1101031

Bending GD, Putland C, Rayns F (2000). Changes in microbial community metabolism and labile organic matter fractions as early indicators of the impact of management on soil biological quality. Biology and Fertility of Soils 31(1):78-84. https://doi.org/10.1007/s003740050627

Beyaert RP (2006). Influence of nitrogen fertilization on the growth and yield of North American ginseng. Journal of Herbs, Spices and Medicinal Plants 11(4):65-80. https://doi.org/10.1300/J044v11n04_08

Borowiak K, Wolna-Maruwka A, Niewiadomska A, Budka A, Schroeter-Zakrzewska A, Stasik R (2021). The effects of various doses and types of effective microorganism applications on microbial and enzyme activity of medium and the photosynthetic activity of scarlet sage. Agronomy 11(3):603.

Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012). Manipulating the soil microbiome to increase soil health and plant fertility. Biology and Fertility of Soils 48(5):489-499. https://doi.org/10.1007/s00374-012-0691-4

Chen C, Bauske EM, Musson G, Rodriguezkabana R, Kloepper JW (1995). Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biological Control 5(1):83-91. https://doi.org/10.1006/bcon.1995.1009

Cheng F, Peng X, Zhao P, Yuan J, Zhong C, Cheng Y, Cui C, Zhang S (2013). Soil microbial biomass, basal respiration and enzyme activity of main forest types in the Qinling Mountains. PloS One 8(6):e67353. https://doi.org/10.1371/journal.pone.0067353

Cho S-J, Kim M-H, Lee Y-O (2016)/ Effect of pH on soil bacterial diversity. Journal of Ecology and Environment 40(1):10. https://doi.org/10.1186/s41610-016-0004-1

Cummings SP (2009). The application of plant growth promoting rhizobacteria (PGPR) in low input and organic cultivation of graminaceous crops; potential and problems. Environmental Biotechnology 5:43-50.

Cupples AM (2005). Principles and Applications of Soil Microbiology. Second Edition. Journal of Environmental Quality 34(2):731-732. https://doi.org/10.2134/jeq2005.0731dup

Dong L, Xu J, Li Y, Fang H, Niu W, Li X, Zhang Y, Ding W, Chen S (2018). Manipulation of microbial community in the rhizosphere alleviates the replanting issues in Panax ginseng. Soil Biology and Biochemistry 125:64-74. https://doi.org/10.1016/j.soilbio.2018.06.028

Dong L, Xu J, Zhang L, Cheng R, Wei G, Su H, Yang J, Qian J, Xu R, Chen S (2018). Rhizospheric microbial communities are driven by Panax ginseng at different growth stages and biocontrol bacteria alleviates replanting mortality. Acta Pharmaceutica Sinica B 8(2):272-282. https://doi.org/10.1016/j.apsb.2017.12.011

Dong LL, Xu J, Li Y, Fang HL, Niu WH, Li XW, Zhang YJ, Ding WL, Chen SL (2018). Manipulation of microbial community in the rhizosphere alleviates the replanting issues in Panax ginseng. Soil Biology and Biochemistry 125:64-74. https://doi.org/10.1016/j.soilbio.2018.06.028

Edgar RC (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10(10):996. https://doi.org/10.1038/nmeth.2604

Feng GD, Yang SZ, Li HP, Zhu HH (2016). Massilia putida sp nov., a dimethyl disulfide-producing bacterium isolated from wolfram mine tailing. International Journal of Systematic and Evolutionary Microbiology 66:50-55. https://doi.org/10.1099/ijsem.0.000670

Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003). Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Applied and Environmental Microbiology 69(3):1800-1809. https://doi.org/10.1128/aem.69.3.1800-1809.2003

Gong G-Q, Zhao Y-F, Zhang Y-j, Deng B, Liu W-X, Wang M, Yuan X, Xu L-W (2020). Establishment of a molecular structure model for classified products of coal-based fulvic acid. Fuel 267:117210. https://doi.org/10.1016/j.fuel.2020.117210

Green SJ, Prakash O, Jasrotia P, Overholt WA, Cardenas E, Hubbard D, … Kostka JE (2012). Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Applied and Environmental Microbiology 78(4):1039-1047. https://doi.org/10.1128/aem.06435-11

Guan YS (1986). Soil enzyme and its research methods. Beijing, China: Agricultural Press of China.

Guiñazú LB, Andrés JA, Del Papa MF, Pistorio M, Rosas SB (2010). Response of alfalfa (Medicago sativa L.) to single and mixed inoculation with phosphate-solubilizing bacteria and Sinorhizobium meliloti. Biology and Fertility of Soils 46(2):185-190. https://doi.org/10.1007/s00374-009-0408-5

Haack FS, Poehlein A, Kroger C, Voigt CA, Piepenbring M, Bode HB, Daniel R, Schafer W, Streit WR (2016). Molecular keys to the Janthinobacterium and Duganella spp. interaction with the plant pathogen Fusarium graminearum. Frontiers in Microbiology 7:1668. https://doi.org/10.3389/fmicb.2016.01668

Hadar Y, Papadopoulou KK (2012). Suppressive composts: microbial ecology links between abiotic environments and healthy plants. In: Van Alfen NK, Leach JE, Lindow S (Eds). Annual Review of Phytopathology, pp 133-153.

Herrera LM, Brana V, Fraguas LF, Castro-Sowinski S (2019). Characterization of the cellulase-secretome produced by the Antarctic bacterium Flavobacterium sp. AUG42. Microbiological Research 223:13-21. https://doi.org/10.1016/j.micres.2019.03.009

Higa T, Wididana GN (1991). The concept and theories of effective microorganisms. In: Parr JF, Hornic SB, Whitman CE (Eds). Proceedings of the First International Conference on Kyusei Nature Farming. US Department of Agriculture, pp 118-124.

Iglesias MB, Lopez ML, Echeverria G, Vinas I, Zudaire L, Abadias M (2018). Evaluation of biocontrol capacity of Pseudomonas graminis CPA-7 against foodborne pathogens on fresh-cut pear and its effect on fruit volatile compounds. Food Microbiology 76:226-236. https://doi.org/10.1016/j.fm.2018.04.007

Inceoglu O, Hoogwout EF, Hill P, van Elsas JD (2010). Effect of DNA Extraction Method On The Apparent Microbial Diversity Of Soil. Applied and Environmental Microbiology 76(10):3378-3382. https://doi.org/10.1128/aem.02715-09

Jackson LE, Bowles TM, Hodson AK, Lazcano C (2012). Soil microbial-root and microbial-rhizosphere processes to increase nitrogen availability and retention in agroecosystems. Current Opinion in Environmental Sustainability 4(5):517-522. https://doi.org/10.1016/j.cosust.2012.08.003

Jiao X-L, Zhang X-S, Lu X-H, Qin R, Bi Y-M, Gao W-W (2019). Effects of maize rotation on the physicochemical properties and microbial communities of American ginseng cultivated soil. Scientific Reports 9(1):8615. https://doi.org/10.1038/s41598-019-44530-7

Kang H, Hwang YG, Lee TG, Jin CR, Cho CH, Jeong HY, Kim DO (2016). Use of gold nanoparticle fertilizer enhances the ginsenoside contents and anti-inflammatory effects of red ginseng. Journal of Microbiology and Biotechnology 26(10):1668-1674. https://doi.org/10.4014/jmb.1604.04034

Kim Y-K, Hong S-J, Jee H-J, Shim C-K, Park J-H, Han E-J, An N-H, Yoo J-H (2011). Population dynamics of effective microorganisms in microbial pesticides and environmental-friendly organic materials according to storing period and temperature. The Korean Journal of Pesticide Science 15(1):55-60.

Kotroczó Z, Veres Z, Fekete I, Krakomperger Z, Tóth JA, Lajtha K, Tóthmérész B (2014). Soil enzyme activity in response to long-term organic matter manipulation. Soil Biology and Biochemistry 70:237-243. https://doi.org/10.1016/j.soilbio.2013.12.028

Kuzyakov Y, Xu XL (2013). Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist 198(3):656-669. https://doi.org/10.1111/nph.12235

Landesman WJ, Nelson DM, Fitzpatrick MC (2014). Soil properties and tree species drive beta-diversity of soil bacterial communities. Soil Biology and Biochemistry 76:201-209. https://doi.org/10.1016/j.soilbio.2014.05.025

Lauber CL, Hamady M, Knight R, Fierer N (2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology 75(15):5111-5120. https://doi.org/10.1128/aem.00335-09

Li Z, Liu Z, Zhang M, Chen Q, Zheng L, Li YC, Sun L (2021). The combined application of controlled-release urea and fulvic acid improved the soil nutrient supply and maize yield. Archives of Agronomy and Soil Science 67(5):633-646. 10.1080/03650340.2020.1742326

Li ZB, Zheng DJ, Tian YQ, Che XQ, Zhou RJ, Fu JF (2015). Effects of pesticide-fertilizer on soil microbial population and physicochemical properties in Panax ginseng continuous cropping soil. Journal of Jilin Agricultural University 37(1):73-76 (in Chinese with English abstract).

Liu X, Yang ZM, Gao LL, Xiang WY, Zhang B, Xie ZL, You JF (2014). Comparison of the characteristics of artificial ginseng bed soil in relation to the incidence of ginseng red skin disease. Experimental Agriculture 50(1):59-71. https://doi.org/10.1017/s0014479713000367

Malan C (2015). Review: humic and fulvic acids. A practical approach. In: Sustainable Soil Management Symposium. Cape Town, South Africa, Agrilibrium Publisher.

Marosz AJD (2009). Effect of fulvic and humic organic acids and calcium on growth and chlorophyll content of tree species grown under salt stress. Dendrobiology 62:47-53.

Nagel K, Schneemann I, Kajahn I, Labes A, Wiese J, Imhoff JF (2012). Beneficial effects of 2,4-diacetylphloroglucinol-producing pseudomonads on the marine alga Saccharina latissima. Aquatic Microbial Ecology 67(3):239-249. https://doi.org/10.3354/ame01595

Park K (2011). Composting of food waste and mixed poultry manure inoculated with effective microorganisms. Engineering in Agriculture, Environment and Food 4(4):106-111. https://doi.org/10.11165/eaef.4.106

Pratscher J, Dumont MG, Conrad R (2011). Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proceedings of the National Academy of Sciences 108(10):4170-4175. https://doi.org/10.1073/pnas.1010981108

Prescott CE, Vesterdal L (2021). Decomposition and transformations along the continuum from litter to soil organic matter in forest soils. Forest Ecology and Management 498:119522. https://doi.org/10.1016/j.foreco.2021.119522

Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research 35(21):7188-7196. https://doi.org/10.1093/nar/gkm864

Saleh DK, Abdollahi H, Noaparast M, Nosratabad AF, Tuovinen OH (2019). Dissolution of Al from metakaolin with carboxylic acids produced by Aspergillus niger, Penicillium bilaji, Pseudomonas putida, and Pseudomonas koreensis. Hydrometallurgy 186:235-243. https://doi.org/10.1016/j.hydromet.2019.03.014

Shin HR, Kim JY, Yun TK, Morgan G, Vainio H (2000). The cancer-preventive potential of Panax ginseng: a review of human and experimental evidence. Cancer Causes and Control 11(6):565-576. https://doi.org/10.1023/A:1008980200583

Smith JL, Paul EA (1990). The significance of soil microbial biomass estimations. In: Blollag JM, Stotzky G (Eds). Soil Biochemistry. 1st Edition. Taylor and Francis, Boca Raton, FL, USA, Routledge.

Soldati F (1999). Panax ginseng: Standardization and Biological Activity. In: Biologically Active Natural Products. CRC Press.

Soltani AA, Khavazi K, Rahmani HA, Omidvari M, Dahaji PA, Mirhoseyni H (2010). Plant growth promoting characteristics in some Flavobacterium spp. isolated from soils of Iran. The Journal of Agricultural Science 2:106-115.

Sun H, Wang QX, Zhang YY, Yang Z, Xu CL (2015). Integrated evaluation of soil fertility of Panax ginseng under different cultivation modes. Journal of Jilin Agricultural University 37(3):323-331 (in Chinese with English abstract).

Tommonaro G, Abbamondi GR, Nicolaus B, Poli A, D’Angelo C, Iodice C, De Prisco R (2021). Productivity and nutritional trait improvements of different tomatoes cultivated with effective microorganisms’ technology. Agriculture 11(2):112. https://doi.org/10.3390/agriculture11020112

Tong A-Z, Liu W, Liu Q, Xia G-Q, Zhu J-Y (2021). Diversity and composition of the Panax ginseng rhizosphere microbiome in various cultivation modesand ages. BMC Microbiology 21(1):18. https://doi.org/10.1186/s12866-020-02081-2

Triplett Jr. GB, Van Doren Jr. DM (1969). Nitrogen, phosphorus, and potassium fertilization of non-tilled maize. Agronomy Journal 61(4):637-639. https://doi.org/10.2134/agronj1969.00021962006100040047x

UPARSE software (2021). UPARSE OTU clustering. http://drive5.com/uparse/

Visser S, Parkinson D (1992). Soil biological criteria as indicators of soil quality: Soil microorganisms. American Journal of Alternative Agriculture 7(1-2):33-37. https://doi.org/10.1017/S0889189300004434

Wang C, Liu D, Bai E (2018). Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biology and Biochemistry 120:126-133. https://doi.org/10.1016/j.soilbio.2018.02.003

Wang QG, Garrity M, Tiedje JM, Cole JR (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73:5261-5267.

Wang R, Dong LL, Xu J, Chen JW, Li XW, Chen SL (2016). Progress in improvement of continuous monoculture cropping problem in Panax ginseng by controlling soil-borne disease management. China Journal of Chinese Materia Medica 41(21):3890-3896 (in Chinese with English abstract).

Wei H, Xu C, Ma L, Duan J, Jiang L, Ren J (2014). Effect of late-season fertilization on nutrient reserves and carbohydrate accumulation in bareroot Larix olgensis seedlings. Journal of Plant Nutrition 37(2):279-293. https://doi.org/10.1080/01904167.2013.859697

Wei HX, Guo P, Zheng HF, He XY, Wang PJ, Ren ZB, Zhai C (2017). Micro-scale heterogeneity in urban forest soils affects fine root foraging by ornamental seedlings of Buddhist pine and Northeast yew. Urban Forestry and Urban Greening 28:63-72. https://doi.org/10.1016/j.ufug.2017.10.006

Xiao C, Yang L, Zhang L, Liu C, Han M (2016). Effects of cultivation ages and modes on microbial diversity in the rhizosphere soil of Panax ginseng. Journal of Ginseng Research 40(1):28-37. https://doi.org/10.1016/j.jgr.2015.04.004

Xing CH, Cai MZ, Yu HB (2007). Application of EM effective microorganism technology in environmental protection. Journal of Microbiology 5:93-97. http://doi.org/10.3969/j.issn.1005-7021.2007.05.021

Zhao J, Li Y, Wang B, Huang X, Yang L, Lan T, Zhang J, Cai Z (2017). Comparative soil microbial communities and activities in adjacent Sanqi ginseng monoculture and maize-Sanqi ginseng systems. Applied Soil Ecology 120:89-96. https://doi.org/10.1016/j.apsoil.2017.08.002

Zheng BX, Bi QF, Hao XL, Zhou GW, Yang XR (2017). Massilia phosphatilytica sp. nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil. International Journal of Systematic and Evolutionary Microbiology 67(8):2514-2519. https://doi.org/10.1099/ijsem.0.001916

Zhu KY, Liu HC, Wei HX, Zhou JH, Zou QC, Ma GY, Zhang JQ (2016). Prediction of nutrient leaching from culture of containerized Buddhist Pine and Japanese Maple seedlings exposed to extended photoperiod. International Journal of Agriculture and Biology 18(2):425-434. https://doi.org/10.17957/ijab/15.0108



How to Cite

XU, Y., LIU, C., BAO, J., ZHU, H., CHEN, Y., LUO, Y., & ZHANG, L. (2022). Microbial diversity and physicochemical properties in farmland soils amended by effective microorganisms and fulvic acid for cropping Asian ginseng. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(1), 12563. https://doi.org/10.15835/nbha50112563



Research Articles
DOI: 10.15835/nbha50112563