Role and perspective of Azotobacter in crops production

Reginawanti Hindersah, Nadia Nuraniya Kamaluddin, Suman Samanta, Saon Banerjee, Sarita Sarkar

Abstract

Low nitrogen content in soil is usually overcome by chemical fertilization. After long application period, high-dose and intensive use of N fertilizers can cause ammonia volatilization and nitrates accumulation in soil. In sustainable agriculture, the use of bacterial inoculant integrated with nutrient management system has a role in soil health and productivity. Azotobacter-based biofertilizer is suggested as a chemical nitrogen fertilizer substitute or addition in crop production to improve available nutrients in the soil, provide some metabolites during plant growth, and minimize fertilizer doses. The objective of this literature reviewed paper is to discuss the role of Azotobacter in agriculture; and the prospective of Azotobacter to increase yield and substitute the chemical fertilizer in food crops production. The results revealed that mechanisms by Azotobacter in plant growth enhancement are as biofertilizer, biostimulant, and bioprotectant. Nitrogen fixation by Azotobacter is the mechanism to provide available nitrogen for uptake by roots. Azotobacter stimulates plant growth through phytohormones synthesis; indole acetic acid, cytokinins, and gibberellins are detected in the liquid culture of Azotobacter. An indirect effect of Azotobacter is exopolysaccharide production and plant protection. Inoculation of Azotobacter in the field integrated with organic matter and reduced chemical fertilizer are reported to improve plant growth and yield.

Keywords

Biofertilizer; Crops yield; Chemical fertilizer; Climate change; Plant growth promoting mechanism

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References

Abdel-Hamid, M. S., Elbaz, A. F., Ragab, A. A., Hamza, H. A., & El Halafawy, K. A. (2010). Identification and characterization of Azotobacter chroococcum isolated from some Egyptian soils. Journal of Agricultural Chemistry and Biotechnology, 1(2), 93–104.

Abdel-Hamid S, M., Hamza, H., Elbaz, A., Ragab, A., & Halafawy, K. (2012). Factors affecting cyst formation of Azotobacter chroococcum for its application as a biofertilizer.

Akinrinlola, R. J., Yuen, G. Y., Drijber, R. A., & Adesemoye, A. O. (2018). Evaluation of Bacillus Strains for Plant Growth Promotion and Predictability of Efficacy by In Vitro Physiological Traits. International Journal of Microbiology, 2018, 5686874. https://doi.org/10.1155/2018/5686874

Arjun, D. J., Roshan, B. O., & Sushma, M. (2015). Role of Azotobacter in soil fertility and sustainability–a review. Advances in Plants & Agriculture Research. https://doi.org/10.15406/apar.2015.02.00069

Bag, P., Panda, P., Paramanik, B., Mahato, B., & Choudhury, A. (2017). Atmospheric nitrogen fixing capacity of Azotobacter isolate from Cooch Behar and Jalpaiguri Districts soil of West Bengal. International Journal of Current Microbiology and Applied Sciences, 6, 1775–1788. https://doi.org/10.20546/ijcmas.2017.603.204

Bageshwar, U., Srivastava, M., Pardha-Saradhi, P., Paul, S., Sellamuthu, G., Jaat, R., … Das, H. (2017). An environment friendly engineered Azotobacter can replace substantial amount of urea fertilizer and yet sustain same wheat yield. Applied and environmental microbiology, 83. https://doi.org/10.1128/AEM.00590-17

Banerjee, A., Supakar, S., & Banerjee, R. (2014). Melanin from the nitrogen-fixing bacterium Azotobacter chroococcum: a spectroscopic characterization. PLoS One, 9(1), e84574.

Banik, A., Dash, G. K., Swain, P., Kumar, U., Mukhopadhyay, S. K., & Dangar, T. K. (2019). Application of rice (Oryza sativa L.) root endophytic diazotrophic Azotobacter sp. strain Avi2 (MCC 3432) can increase rice yield under green house and field condition. Microbiological Research, 219, 56–65. https://doi.org/https://doi.org/10.1016/j.micres.2018.11.004

Baral, B., & Adhikari, P. (2014). Effect of Azotobacter on Growth and Yield of Maize. SAARC Journal of Agriculture, 11(2 SE-Articles). https://doi.org/10.3329/sja.v11i2.18409

Baral, B. R., & Adhikari, P. (2013). Effect of Azotobacter on growth and yield of maize. SAARC Journal of Agriculture, 11(2), 141–147.

Bhattacharjee, R., & Dey, U. (2014). Biofertilizer, away towards organic agriculture: A review. African Journal of Microbiology Research, 8(24), 2332–2343.

Calvo, P., Nelson, L., & Kloepper, J. W. (2014). Agricultural uses of plant biostimulants. Plant and Soil, 383(1–2), 3–41.

Chauhan, S., Wadhwa, K., Vasudeva, M., & Narula, N. (2012). Potential of Azotobacter spp. as biocontrol agents against Rhizoctonia solani and Fusarium oxysporum in cotton (Gossypium hirsutum), guar (Cyamopsis tetragonoloba), and tomato (Lycopersicum esculentum). Archives of Agronomy and Soil Science, 58(12), 1365–1385.

Danapriatna, N. N. (2016). Penjaringan Azotobacter Sp Dan Azospirillum Sp Dari Ekosistem Lahan Sawah Sebagai Sumber Isolat Pupuk Hayati Penambat Nitrogen. Jurnal Agrotek Indonesia (Indonesian Journal of Agrotech), 1(2).

Devi, S., Choudhary, M., Jat, P. K., Singh, S. P., & Rolaniya, M. K. (2017). Influenced of organic and biofertilizers on yield and quality of cabbage (Brassica oleracea var. capitata). International Journal of Chemical Studies, 5(4), 818–820.

Din, M., Nelofer, R., Salman, M., Abdullah, Khan, F. H., Khan, A., … Khan, M. (2019). Production of nitrogen fixing Azotobacter (SR-4) and phosphorus solubilizing Aspergillus niger and their evaluation on Lagenaria siceraria and Abelmoschus esculentus. Biotechnology Reports (Amsterdam, Netherlands), 22, e00323–e00323. https://doi.org/10.1016/j.btre.2019.e00323

Emtiazi, G., Ethemadifar, Z., & Habibi, M. H. (2004). Paper-Production of extra-cellular polymer in Azotobacter and biosorption of metal by exopolymer. African Journal of Biotechnology, 3(6), 330–333.

Espín, G. (2016, Agustus). Genes Involved in the Formation of Desiccation- Resistant Cysts in Azotobacter Vinelandii. Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria. https://doi.org/doi:10.1002/9781119004813.ch67

Fan, X. H., Li, Y. C., & Alva, A. K. (2011). Effects of Temperature and Soil Type on Ammonia Volatilization from Slow-Release Nitrogen Fertilizers. Communications in Soil Science and Plant Analysis, 42(10), 1111–1122. https://doi.org/10.1080/00103624.2011.566957

García, A., Castillo, T., Ramos, D., Ahumada-Manuel, C. L., Núñez, C., Galindo, E., … Peña, C. (2020). Molecular weight and viscosifying power of alginates produced by mutant strains of Azotobacter vinelandii under microaerophilic conditions. Biotechnology Reports, 26, e00436. https://doi.org/https://doi.org/10.1016/j.btre.2020.e00436

Gauri, S. S., Mandal, S. M., & Pati, B. R. (2012). Impact of Azotobacter exopolysaccharides on sustainable agriculture. Applied Microbiology and Biotechnology, 95(2), 331–338.

Geng, Y., Cao, G., Wang, L., & Wang, S. (2019). Effects of equal chemical fertilizer substitutions with organic manure on yield, dry matter, and nitrogen uptake of spring maize and soil nitrogen distribution. PloS one, 14(7), e0219512.

Glick, B. R. (2012). Plant Growth-Promoting Bacteria: Mechanisms and Applications. Scientifica, 2012, 963401. https://doi.org/10.6064/2012/963401

Gospodaryov, D., & Lushchak, V. (2011). Some properties of melanin produced by Azotobacter chroococcum and its possible application in biotechnology. Biotechnologia Acta, 4(2).

Harahap, N., Dwi, A. S., & Gofar, N. (2018). The potential of exopolysaccharide-producing bacteria from rhizosphere of rubber plants for improving soil aggregate. Journal of Degraded and Mining Lands Management, 5(3), 1275.

Haroun, A. A., & Abdel-Hamid, M. S. (2015). Evaluation and characterization of polyhydroxybutrate produced by Azotobacter chroococcum. Biotechnol. An Indian J, 11(9), 347–354.

Helaly, A. A., Hassan, S. M., Craker, L. E., & Mady, E. (2020). Effects of growth-promoting bacteria on growth, yield, and nutritional value of collard plants. Annals of Agricultural Sciences, 65(1), 77–82. https://doi.org/https://doi.org/10.1016/j.aoas.2020.01.001

Hindersah, R., Priyanka, P., Rumahlewang, W., & Kalay, A. M. (2016). Selection and Bioassay of Azotobacter sp. Isolates to Improve Growth of Chili (Capsicum annum L.) on Entisols in Ambon. Microbiology Indonesia, 10(4), 2.

Hindersah, R, & Kamaluddin, N. N. (2014). Pengaruh Timbal terhadap Kepadatan Sel dan kadar Eksopolisakarida Kultur Cair Azotobacter. Bionatura, 16(1).

Hindersah, Reginawanti. (2015). Growth and Exopolysachharide composition of nitrogen fixing bacteria Azotobacter spp. in the presence of cadmium. In Prosiding Seminar Nasional Masyarakat Biodiversitas Indonesia (Vol. 1, hal. 1644–1648).

Hindersah, Reginawanti, Kalay, M., Talahaturuson, A., & Lakburlawal, Y. (2018). NITROGEN FIXING BACTERIA AZOTOBACTER AS BIOFERTILIZER AND BIOCONTROL IN LONG BEAN. Agric, 30(1), 25–32.

Istifadaha, N., Ningtyasb, D. N. Y., Suryatmana, P., & Fitriatin, B. N. (2017). The abilities of endophytic and biofertilizing bacteria and their combinations to suppress bacterial wilt disease (Ralstonia solanacearum) of chili. KnE Life Sciences, 296–304.

Jadhav, H. P., & Sayyed, R. Z. (2016). Hydrolytic enzymes of rhizospheric microbes in crop protection. MOJ Cell Sci Rep, 3(5), 135–136.

Jadon, P., Selladurai, R., Yadav, S. S., Coumar, M. V., Dotaniya, M. L., Singh, A. K., … Kundu, S. (2018). Volatilization and leaching losses of nitrogen from different coated urea fertilizers. Journal of soil science and plant nutrition, 18(4), 1036–1047.

Jiang, F., Chen, L., Belimov, A. A., Shaposhnikov, A. I., Gong, F., Meng, X., … Dodd, I. C. (2012). Multiple impacts of the plant growth-promoting rhizobacterium Variovorax paradoxus 5C-2 on nutrient and ABA relations of Pisum sativum. Journal of Experimental Botany, 63(18), 6421–6430. https://doi.org/10.1093/jxb/ers301

Jiménez, D. J., Montaña, J. S., & Martínez, M. M. (2011). Characterization of free nitrogen fixing bacteria of the genus Azotobacter in organic vegetable-grown Colombian soils. Brazilian Journal of Microbiology, 42(3), 846–858.

Kalay, A. M., Hindersah, R., Talahaturuson, A., & Latupapua, A. I. (2017). Dual inoculation of Azotobacter chroococcum and Trichoderma harzianum to control leaf blight (Rhizoctonia solani) and increase yield of choy sum. International J. of Scientific & Engineering, 8, 1288–1292.

Kennedy, C., Rudnick, P., MacDonald, M. L., & Melton, T. (2015, September). Azotobacter. Bergey’s Manual of Systematics of Archaea and Bacteria. https://doi.org/doi:10.1002/9781118960608.gbm01207

Khanafari, A., & Sepahei, A. A. (2007). Alginate biopolymer production by Azotobacter chroococcum from whey degradation. International Journal of Environmental Science & Technology, 4(4), 427–432. https://doi.org/10.1007/BF03325977

Kumar, A., Kumar, K., Kumar, P., Maurya, R., Prasad, S., & Singh, S. K. (2014). Production of indole acetic acid by Azotobacter strains associated with mungbean. Plant Archives, 14(1), 41–42.

Kumar, P., Thakur, S., Dhingra, G. K., Singh, A., Pal, M. K., Harshvardhan, K., … Maheshwari, D. K. (2018). Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatalysis and agricultural biotechnology, 15, 264–269.

Kurrey, D. K., Sharma, R., Lahre, M. K., & Kurrey, R. L. (2018). Effect of Azotobacter on physio-chemical characteristics of soil in onion field. The Pharma Innovation Journal, 7(2), 108–113.

Liu, D., Chen, L., Zhu, X., Wang, Y., Xuan, Y., Liu, X., … Duan, Y. (2018). Klebsiella pneumoniae SnebYK Mediates Resistance Against Heterodera glycines and Promotes Soybean Growth . Frontiers in Microbiology .

Loperfido, B., & Sadoff, H. L. (1973). Germination of <em>Azotobacter vinelandii</em> Cysts: Sequence of Macromolecular Synthesis and Nitrogen Fixation. Journal of Bacteriology, 113(2), 841 LP – 846.

Mahato, S., & Kafle, A. (2018). Comparative study of Azotobacter with or without other fertilizers on growth and yield of wheat in Western hills of Nepal. Annals of Agrarian Science, 16(3), 250–256. https://doi.org/https://doi.org/10.1016/j.aasci.2018.04.004

Massah, J., & Azadegan, B. (2016). Effect of chemical fertilizers on soil compaction and degradation. AMA, Agricultural Mechanization in Asia, Africa and Latin America.

Maurya, B. R., Kumar, A., Raghuwanshi, R., & Singh, V. (2012). Diversity of Azotobacter and Azospirillum in rhizosphere of different crop rotations in eastern Uttar Pradesh of India. Research Journal of Microbiology, 7(2), 123.

Mazid, M., & Khan, T. A. (2015). Future of Bio-fertilizers in Indian agriculture: An Overview. International Journal of Agricultural and Food Research; Vol 3, No 3 (2014).

Mazinani, Z., Aminafshar, M., Asgharzadeh, A., & Chamani, M. (2012). Different Methods for Isolation and Preliminary Identification of Azotobacter. International Journal of Agricultural Science and Research.

Mazinani, Z., & Asgharzadeh, A. (2014). Genetic diversity of Azotobacter strains isolated from soils by amplified ribosomal DNA restriction analysis. Cytology and Genetics. https://doi.org/10.3103/S0095452714050041

McGuire, S. (2015). FAO, IFAD, and WFP. The state of food insecurity in the world 2015: meeting the 2015 international hunger targets: taking stock of uneven progress. Rome: FAO, 2015. Oxford University Press.

Mohamed, H., & Almaroai, Y. (2016). Effect of Inoculated Azotobacter chroococcum and Soil Yeasts on Growth, N-uptake and Yield of Wheat (Triticum aestivum) under Different Levels of Nitrogen Fertilization. International Journal of Soil Science, 11, 102–107. https://doi.org/10.3923/ijss.2016.102.107

Moura, E. G. de, Gehring, C., Braun, H., Ferraz Junior, A. D. S. L., Reis, F. de O., & Aguiar, A. D. C. F. (2016). Improving farming practices for sustainable soil use in the humid tropics and rainforest ecosystem health. Sustainability, 8(9), 841.

Mrkovački, N., Bjelić, D., Đalović, I., Šeremešić, S., Milošev, D., Jocković, Đ., & Jug, I. (2016). Effect of inoculation with Azotobacter chroococcum on dynamics of the number of microorganisms in the rhizosphere of maize. J Agric Biol Sci, 632, 45–53.

Mukhtar, H., Bashir, H., & Nawaz, A. (2018). Optimization of growth conditions for Azotobacter species and their use as biofertilizer. J Bacteriol Mycol Open Access, 6(5), 274–278.

Murumkar, D. R., Borkar, S. G., & Chimote, V. P. (2012). Diversity of cell morphology, nitrogenase activity and dna profile of azotobacter isolates from soils of Maharashtra. BIOINFOLET-A Quarterly Journal of Life Sciences, 9(4b), 851–858.

Nosheen, A., Bano, A., Yasmin, H., Keyani, R., Habib, R., Shah, S. T. A., & Naz, R. (2016). Protein Quantity and Quality of Safflower Seed Improved by NP Fertilizer and Rhizobacteria (Azospirillum and Azotobacter spp.) . Frontiers in Plant Science .

Oelze, J. (2000). Respiratory protection of nitrogenase in Azotobacter species: Is a widely held hypothesis unequivocally supported by experimental evidence? FEMS Microbiology Reviews. https://doi.org/10.1016/S0168-6445(00)00029-2

Patil, V. (2011). Production of indole acetic acid by Azotobacter sp. Recent research in Science and Technology.

Paungfoo-Lonhienne, C., Lonhienne, T. G. A., Yeoh, Y. K., Donose, B. C., Webb, R. I., Parsons, J., … Ragan, M. A. (2016). Crosstalk between sugarcane and a plant-growth promoting Burkholderia species. Scientific Reports, 6(1), 37389. https://doi.org/10.1038/srep37389

Ponmurugan, K., Sankaranarayanan, A., & Al-Dharbi, N. A. (2012). Biological activities of plant growth promoting Azotobacter sp. isolated from vegetable crops rhizosphere soils. Journal of Pure and Applied Microbiology, 6(4), 1–10.

Qessaoui, R., Bouharroud, R., Furze, J. N., El Aalaoui, M., Akroud, H., Amarraque, A., … Chebli, B. (2019). Applications of New Rhizobacteria Pseudomonas Isolates in Agroecology via Fundamental Processes Complementing Plant Growth. Scientific Reports, 9(1), 12832. https://doi.org/10.1038/s41598-019-49216-8

Rahmayani, S., Hindersah, R., & Fitriatin, B. N. (2017). Role of Azotobacter sp. on nitrogen uptake and growth of soybean (Glycine max (L.) Merrill) on saline soil. International Journal of Scientific & Engineering Research, 8(6), 1214–1220.

Reddy, S., Singh, A. K., Masih, H., Benjamin, J. C., Ojha, S. K., Ramteke, P. W., & Singla, A. (2018). Effect of Azotobacter sp and Azospirillum sp on vegetative growth of Tomato (Lycopersicon esculentum). Journal of Pharmacognosy and Phytochemistry, 7(4), 2130–2137.

Romero-Perdomo, F., Abril, J., Camelo, M., Moreno-Galván, A., Pastrana, I., Rojas-Tapias, D., & Bonilla, R. (2017). Azotobacter chroococcum as a potentially useful bacterial biofertilizer for cotton (Gossypium hirsutum): Effect in reducing N fertilization. Revista Argentina de Microbiología, 49(4), 377–383. https://doi.org/https://doi.org/10.1016/j.ram.2017.04.006

Rubio, E. J., Montecchia, M. S., Tosi, M., Cassán, F. D., Perticari, A., & Correa, O. S. (2013). Genotypic Characterization of Azotobacteria Isolated from Argentinean Soils and Plant-Growth-Promoting Traits of Selected Strains with Prospects for Biofertilizer Production. The Scientific World Journal, 2013. https://doi.org/10.1155/2013/519603

Sabra, W., Zeng, A. P., Lunsdorf, H., & Deckwer, W. D. (2000). Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role in protecting nitrogenase. Applied and Environmental Microbiology. https://doi.org/10.1128/AEM.66.9.4037-4044.2000

San Yu, S., & Ullrich, M. (2018). Interaction of Nitrogen Fixation and Alginate Synthesis of Azotobacter vinelandii Isolated from Myanmar Mangrove. International Journal of Plant Biology & Research.

Santana, E. B., Marques, E. L. S., & Dias, J. C. T. (2016). Effects of phosphate-solubilizing bacteria, native microorganisms, and rock dust on Jatropha curcas L. growth. Genetics and Molecular Research, 15(4).

Sebilo, M., Mayer, B., Nicolardot, B., Pinay, G., & Mariotti, A. (2013). Long-term fate of nitrate fertilizer in agricultural soils. Proceedings of the National Academy of Sciences of the United States of America, 110(45), 18185–18189. https://doi.org/10.1073/pnas.1305372110

Sethi, S. K., & Adhikary, S. P. (2012). Azotobacter: a plant growth-promoting rhizobacteria used as biofertilizer. Dynamic Biochemistry, Process Biotechnology and Molecular Biology, 6(1), 68–74.

Setiawati, M. R., Sofyan, E. T., Nurbaity, A., Suryatmana, P., & Marihot, G. P. (2018). Pengaruh Aplikasi Pupuk Hayati, Vermikompos Dan Pupuk Anorganik Terhadap Kandungan N, Populasi Azotobacter sp. Dan Hasil Kedelai Edamame (Glycine max (L.) Merill) Pada Inceptisols Jatinangor. Agrologia. https://doi.org/10.30598/a.v6i1.174

Seyed Sharifi, R., Khalilzadeh, R., & Jalilian, J. (2017). Effects of biofertilizers and cycocel on some physiological and biochemical traits of wheat (Triticum aestivum L.) under salinity stress. Archives of Agronomy and Soil Science, 63(3), 308–318. https://doi.org/10.1080/03650340.2016.1207242

Shah, K., Chaudhary, I., Rana, D., & Singh, V. (2019). Effectiveness of combined dose of organic manure and fertilizer on Knol-khol (Brassica oleracea var. gongylodes) vegetable crop. Fundamental and Applied Agriculture, 4(3), 959–969.

Sharma, P., Verma, P. P., & Kaur, M. (2017). Phytohormones production and phosphate solubilization capacities of fluorescent Pseudomonas sp. isolated from Shimla Dist. of Himachal Pradesh. IJCMAS, 6, 2447–2454.

Singh, S. (2011). Selection of Effective Azotobacter Isolates for Tomato (Lycopersicon esculentum Mill.). Indira Gandhi Krshi Vishwavidyalaya, Raipur (CG).

Sivapriya, S. L., & Priya, P. R. (2017). Selection of Hyper Exopolysaccharide Producing and Cyst Forming Azotobacter Isolates for Better Survival under Stress Conditions. International Journal of Current Microbiology and Applied Sciences. https://doi.org/10.20546/ijcmas.2017.606.274

Sivasakthi, S., Saranraj, P., & Sivasakthivelan, P. (2017). Biological nitrogen fixation by Azotobacter sp.—a review. Indo Asian J Multidiscip Res, 3, 1274–1284.

Sobariu, D. L., Fertu, D. I. T., Diaconu, M., Pavel, L. V., Hlihor, R.-M., Drăgoi, E. N., … Gavrilescu, M. (2017). Rhizobacteria and plant symbiosis in heavy metal uptake and its implications for soil bioremediation. New Biotechnology, 39(Pt A), 125–134. https://doi.org/10.1016/j.nbt.2016.09.002

Subedi, R., Khanal, A., Aryal, K., Chhetri, L., & Kandel, B. (2019). RESPONSE OF AZOTOBACTER IN CAULIFLOWER (BRASSICA OLERACEA L. VAR. BOTRYTIS) PRODUCTION AT LAMJUNG, NEPAL. Acta Scientifica Malaysia, 3, 17–20. https://doi.org/10.26480/asm.01.2019.17.20

Taller, B. J., & Wong, T.-Y. (1989). Cytokinins in Azotobacter vinelandii culture medium. Applied and environmental microbiology, 55(1), 266–267.

Upadhyay, S., Kumar, N., Singh, V. K., & Singh, A. (2015). Isolation, characterization and morphological study of Azotobacter isolates. Journal of Applied and Natural Science, 7(2 SE-), 984–990. https://doi.org/10.31018/jans.v7i2.718

Uttari, N. I. N. D., Nyana, I. D. N., & Astiningsih, A. A. M. (2016). Efektivitas Penggunaan Pupuk Hayati (Enterobacter cloacae) untuk Meningkatkan Hasil dan Mutu Benih Padi Varietas Cigeulis. Agroekoteknologi Tropika, 5(1), 83–92.

Ventorino, V., Nicolaus, B., Di Donato, P., Pagliano, G., Poli, A., Robertiello, A., … Pepe, O. (2019). Bioprospecting of exopolysaccharide-producing bacteria from different natural ecosystems for biopolymer synthesis from vinasse. Chemical and Biological Technologies in Agriculture, 6(1), 18.

Vermani, M. V, Kelkar, S. M., & Kamat, M. Y. (1997). Studies in polysaccharide production and growth of Azotobactervinelandii MTCC 2459, a plant rhizosphere isolate. Letters in applied microbiology, 24(5), 379–383.

Vikhe, P. S. (2014). Azotobacter species as a Natural Plant Hormone Synthesizer. Research Journal of Recent Sciences.

Viscardi, S., Ventorino, V., Duran, P., Maggio, A., De Pascale, S., Mora, M. L., & Pepe, O. (2016). Assessment of plant growth promoting activities and abiotic stress tolerance of Azotobacter chroococcum strains for a potential use in sustainable agriculture. Journal of soil science and plant nutrition, 16(3), 848–863.

Wang, H., Gao, J., Li, X., Zhang, S., & Wang, H. (2015). Nitrate accumulation and leaching in surface and groundwater based on simulated rainfall experiments. PLoS One, 10(8), e0136274.

Widawati, S. S. (2017). The effect of Azotobacter inoculation on Shallot plants (Allium cepa) and availability of phosphate in the saline soil. Biodiversitas, 8(1), 86–94. https://doi.org/10.13057/biodiv/d180113

Yoneyama, F., Yamamoto, M., Hashimoto, W., & Murata, K. (2015). Production of polyhydroxybutyrate and alginate from glycerol by Azotobacter vinelandii under nitrogen-free conditions. Bioengineered, 6(4), 209–217.

Yousaf, M., Li, J., Lu, J., Ren, T., Cong, R., Fahad, S., & Li, X. (2017). Effects of fertilization on crop production and nutrient-supplying capacity under rice-oilseed rape rotation system. Scientific reports, 7(1), 1–9.

Zeffa, D. M., Perini, L. J., Silva, M. B., de Sousa, N. V., Scapim, C. A., Oliveira, A. L. M. de, … Azeredo Goncalves, L. S. (2019). Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes. PLoS One, 14(4), e0215332.

Zhengtao, Z., Wenge, H., Di, Y., Yuan, H., & Tingting, Z. (2019). Diversity of Azotobacter in relation to soil environment in Ebinur Lake wetland. Biotechnology and Biotechnological Equipment. https://doi.org/10.1080/13102818.2019.1659181

Zulaika, E., Solikhah, F., Alami, N. H., Kuswytasari, N. D., & Shovitri, M. (2017). Viability of Azotobacter consortium in auxin production. In AIP Conference Proceedings (Vol. 1854, hal. 20041). AIP Publishing LLC.

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