[en] Plant growth-promoting rhizobacteria (PGPR) are considered environmentally sound option to reduce chemical fertilizer inputs, improve soil quality and increase crop yields. The objective of this study was to isolate an effective PGPR strain and investigate its effects on soybean growth and soil bacterial community composition. A total of 163 bacterial isolates were obtained from rhizospheres of plants in four provinces of China. According to capacities for mineral potassium and phosphate solubilization, the best strain (designated 3016) was selected and identified as Paenibacillus mucilaginosus based on biochemical characterization and phylogenetic analysis. Moreover, strain 3016 showed a higher capacity for nitrogen fixation and phytohormone production than commercial strains. In a field experiment, P. mucilaginosus 3016 was used as an inoculant for seed dressing survived in the soybean rhizosphere as revealed by a species-specific PCR method. Inoculation significantly improved symbiotic nodulation, soybean growth parameters, nutrient contents and yields. The number of nodules was increased by 31.8% for the inoculation treatment compared with CK. Soybean height, pods and seeds per plant and dry weight of nodules were also significantly higher for the inoculation, as well as nutrient contents. Regarding yields, the highest of 3191.4 kg hm-2 was obtained under inoculation regime. Moreover, numerous bacterial classes and genera, which were associated with symbiotic nitrogen-fixation, plant growth promotion, biological control and soil catalase activity improvement, were also overrepresented in the inoculation treatment. Some taxa with negative impacts on soil quality decreased. In conclusion, inoculation with P. mucilaginosus 3016 had beneficial effects on both soybean growth and soil quality, and is a potential candidate for developing commercial inoculants of PGPR to be used as a bio-fertilizer.
Research Center/Unit :
Microbial Processes and Interactions Research Unit
Basak, B.B. and D.R. Biswas, 2012. Co-inoculation of potassium solubilizing and nitrogen fixing bacteria on solubilization of waste mica and their effect on growth promotion and nutrient acquisition by a forage crop. Biol. Fert. Soils, 46: 641-648
Basak, B.B. and D.R. Biswas, 2009. Influence of potassium solubilizing microorganism (Bacillus mucilaginosus) and waste mica on potassium uptake dynamics by sudan grass (Sorghum vulgare Pers.) grown under two Alfisols. Plant Soil, 317: 235-255
Cao, F., D. Shen, J. Li, D. Guan, X. Jiang, L. Li, R. Feng, X. Yang, H. Chen and Y. Ge, 2008. Multiplex-PCR approach to identify Bacillus species applied in microbial fertilizers. Acta Microbiol. Sin., 48: 651-656
Caporaso, J.G., C.L. Lauber, W.A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S.M. Owens, J. Betley, L. Fraser, M. Bauer and R. Rormley, 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J., 6: 1621
Chromy, V., B. Vinklárková, L. Šprongl and M. Bittová, 2015. The Kjeldahl method as a primary reference procedure for total protein in certified reference materials used in clinical chemistry. I. A review of Kjeldahl methods adopted by laboratory medicine. Crit. Rev. Anal. Chem., 45: 106-111
Claus, D. and R.C.W. Berkeley, 1986. Genus Bacillus Cohn 1872, pp: 1105-1140. Murray, R.G.E., P.H.A. Sneath, M.E. Sharpe and J.G. Holt (eds.). Bergey's Manual of Systematic Bacteriology, Springer
Collins, L.A. and S.G. Franzblau, 1997. Microplate alamar blue assay versus BACTEC 460 system for high-throughput screening of compounds against Mycobacterium tuberculosis and Mycobacterium avium. Antimicrob. Agents C., 41: 1004-1009
Dhami, N. and B.N. Prasad, 2010. Increase in root nodulation and crop yield of soybean by native Bradyrhizobium japonicum strains. Bot. Orient. J. Plant. Sci., 6: 1-3
Ding, J., X. Jiang, M. Ma, B. Zhou, D. Guan, B. Zhao, J. Zhou, F. Cao, L. Li and J. Li, 2016. Effect of 35 years inorganic fertilizer and manure amendment on structure of bacterial and archaeal communities in black soil of northeast China. Appl. Soil Ecol., 105: 187-195
Edgar, R.C., B.J. Haas, J.C. Clemente, C. Quince and R. Knight, 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27: 2194-2200
Fankem, H., D. Nwaga, A. Deubel, L. Dieng, W. Merbach and F.X. Etoa, 2006. Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr. J. Biotechnol., 5: 2450-2460
Figueiredo, M.D.V.B., L. Seldin, F.F. de Araujo and R.D.L.R. Mariano, 2010. Plant growth promoting rhizobacteria: fundamentals and applications, In: Plant Growth and Health Promoting Bacteria, pp: 21-43. Springer Berlin Heidelberg, Germany
Galiana, A., P. Balle, A. Kanga and A.M. Domenach, 2002. Nitrogen fixation estimated by the 15 N natural abundance method in Acacia mangium Willd. inoculated with Bradyrhizobium sp. and grown in silvicultural conditions. Soil Biol. Biochem., 34: 251-262
Gao, M., J. Zhou, E. Wang, C. Qian, X.U. Jing and J. Sun, 2015. Multiphasic characterization of a plant growth promoting bacterial strain, Burkholderia sp. 7016 and its effect on tomato growth in the field. J. Integr. Agric., 14: 1855-1863
Gao, M., H. Yang, J. Zhao, J. Liu, Y. Sun, Y. Wang and J. Sun, 2013. Paenibacillus brassicae sp. nov., isolated from cabbage rhizosphere in Beijing, China. Antonie. Van. Leeuwenhoek, 103: 647-653
Geisseler, D. and K.M. Scow, 2014. Long-term effects of mineral fertilizers on soil microorganisms-A review. Soil Biol. Biochem., 75: 54-63
Gomez, J.P., G.A. Bravo, R.T. Brumfield, J.G. Tello and C.D. Cadena, 2010. A phylogenetic approach to disentangling the role of competition and habitat filtering in community assembly of Neotropical forest birds. J. Anim. Ecol., 79: 1181-1192
Govindasamy, V., M. Senthilkumar, V. Magheshwaran, U. Kumar, P. Bose, V. Sharma and K. Annapurna, 2010. Bacillus and Paenibacillus spp.: potential PGPR for sustainable agriculture, In: Plant Growth and Health Promoting Bacteria, pp: 333-364. Springer
Green, S.J., O. Prakash, P. Jasrotia, W.A. Overholt, E. Cardenas, D. Hubbard, J.M. Tiedje, D.B. Watson, C.W. Schadt and S.C. Brooks, 2012. Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Appl. Environ. Microbiol., 78: 1039-1047
Hadas, A. and R. Portnoy, 1997. Rates of decomposition in soil and release of available nitrogen from cattle manure and municipal waste composts. Compost Sci. Util., 5: 48-54
Hamilton, H.A., E. Brod, O. Hanserud, B.M. Danielüller, H. Brattebø and T.K. Haraldsen, 2017. Recycling potential of secondary phosphorus resources as assessed by integrating substance flow analysis and plant-availability. Sci. Total Envion., 575: 1546-1555
Hart, S.C., J.M. Stark., E.A. Davidson and M.K. Firestone, 1994. Nitrogen mineralization, immobilization, and nitrification. Methods Soil Anal. Part 2. Microbiol. Biochem., 985-1018
He, L.Y., Y.X. Yin and W.Y. Huang, 2003. Characterization and Phylogenetic Analysis of a Strain of Silicate Baterium. Acta Microbiol. Sin. Chin. Ed., 43: 162-168
Hou, S., J. Zhu, M. Ding and G. Lv, 2008. Simultaneous determination of gibberellic acid, indole-3-acetic acid and abscisic acid in wheat extracts by solid-phase extraction and liquid chromatography-electrospray tandem mass spectrometry. Talanta, 76: 798-802
Hu, X.F., S.X. Li, J.G. Wu, J.F. Wang, Q.L. Fang and J.S. Chen, 2010. Transfer of Bacillus mucilaginosus and Bacillus edaphicus to the genus Paenibacillus as Paenibacillus mucilaginosus comb. nov. and Paenibacillus edaphicus comb. nov. Int. J. Syst. Evol. Microbiol., 60: 8-14
Hu, X., J. Chen and J. Guo, 2006. Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J. Microbiol. Biotechnol., 22: 983-990
Janczarek, M., J. Jaroszuk-Scisel and A. Skorupska, 2009. Multiple copies of rosR and pssA genes enhance exopolysaccharide production, symbiotic competitiveness and clover nodulation in Rhizobium leguminosarum bv. trifolii. Anton Leeuw. Int. J.G., 96: 471-486
Khosravi, A. and M.R.A. Zarei, 2017. Influence of biofertilizers and phosphate sources on the phosphorus uptake of lettuce and chemical forms of phosphorus in Soil. Commun. Soil. Sci. Plant. Anal., 48: 2701-2714
Kundim, B.A., Y. Itou, Y. Sakagami, R. Fudou, T. Iizuka, S. Yamanaka and M. Ojika, 2003. New haliangicin isomers, potent antifungal metabolites produced by a marine myxobacterium. J. Antibiot. (Tokyo), 56: 630-638
Lauber, C.L., K.S. Ramirez, Z. Aanderud, J. Lennon and N. Fierer, 2013. Temporal variability in soil microbial communities across land-use types. ISME J., 7: 1641-1650
Li, X., Z. Wu, W. Li, R. Yan, L. Li, Y. Li and M. Li, 2007. Growth promoting effect of a transgenic Bacillus mucilaginosus on tobacco planting. Appl. Microbiol. Biotechnol., 74: 1120-1125
Linu, M.S., J. Stephen and M.S. Jisha, 2009. Phosphate solubilizing Gluconacetobacter sp., Burkholderia sp. and their potential interaction with cowpea (Vigna unguiculata (L.) Walp.). Int. J. Agric. Res., 4: 79-87
Liu, H., D. Chen, R. Zhang, X. Hang, R. Li and Q. Shen, 2016. Amino acids hydrolyzed from animal carcasses are a good additive for the production of bio-organic fertilizer. Front. Microbiol., 7: 1290
Liu, H.U.I., X.Q. WU, J.H. Ren and J.R. Ye, 2011. Isolation and identification of phosphobacteria in poplar rhizosphere from different regions of China. Pedosphere, 21: 90-97
Lu, J.J., J.F. Wang and X.F. Hu, 2013. Genome sequence of growth-improving Paenibacillus mucilaginosus strain KNP414. Genom. Announc., 1: 13
Ma, M., X. Jiang, L. Li and J. Li, 2014. Function and genomics of Paenibacillus mucilaginosus. Chin. Bull. Life Sci., 26: 1038-1045
Ma, M., Z. Wang, L. Li, X. Jiang, D. Guan, F. Cao, H. Chen, X. Wang, D. Shen and B. Du, 2012. Complete genome sequence of Paenibacillus mucilaginosus 3016, a bacterium functional as microbial fertilizer. J. Bacteriol., 194: 2777-2778
Masciarelli, O., A. Llanes and V. Luna, 2014. A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol. Res., 169: 609-615
McGill, B.J., R.S. Etienne, J.S. Gray, D. Alonso, M.J. Anderson, H.K. Benecha, M. Dornelas, B.J. Enquist, J.L. Green and F. He, 2007. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett., 10: 995-1015
Mendes, R., M. Kruijt, I. de Bruijn, E. Dekkers, M. van der Voort, J.H.M. Schneider, Y.M. Piceno, T.Z. DeSantis, G.L. Andersen, P.A.H.M. Bakker and J.M. Raaijmakers, 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332: 1097-1100
Monib, M., M.K. Zahra, S.I. Abdel el-Al and A. Heggo, 1984. Role of silicate bacteria in releasing K and Si from biotite and orthoclase. In: Soil biology and Conservation of the Biosphere, pp: 733-743. Szegi, J. (ed.). Budapest: Akademiai Kiado. ISBN 9630537001
Nastasijevic, B., 2006. Influence of Silicate Substrate on Growth and Production of Macrocapsules of Certain Strains of Bacillus Circulans. Mikrobiol
Nosheen, A., A. Bano, H. Yasmin, R. Keyani, R. Habib, S.T.A. Shah and R. Naz, 2016. Protein quantity and quality of safflower seed improved by NP fertilizer and Rhizobacteria (Azospirillum and Azotobacter spp.). Front. Plant Sci., 7: 104
Nosratabad, A.R.F., H. Etesami and S. Shariati, 2017. Integrated use of organic fertilizer and bacterial inoculant improves phosphorus use efficiency in wheat (Triticum aestivum L.) fertilized with triple superphosphate. Rhizosphere, 3: 109-111
Ovreås, L., L. Forney, F.L. Daae and V. Torsvik, 1997. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol., 63: 3367-3373
Peiffer, J.A., A. Spor, O. Koren, Z. Jin, S.G. Tringe, J.L. Dangl, E.S. Buckler and R.E. Ley, 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci., 110: 6548-6553
Perrig, D., M.L. Boiero, O.A. Masciarelli, C. Penna, O.A. Ruiz, F.D. Cassán and M.V. Luna, 2007. Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl. Microbiol. Biotechnol., 75: 1143-1150
Piromyou, P., B. Buranabanyat, P. Tantasawat, P. Tittabutr, N. Boonkerd and N. Teaumroong, 2011. Effect of plant growth promoting rhizobacteria (PGPR) inoculation on microbial community structure in rhizosphere of forage corn cultivated in Thailand. Eur. J. Soil Biol., 47: 44-54
Prakamhang, J., K. Minamisawa, K. Teamtaisong, N. Boonkerd and N. Teaumroong, 2009. The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Appl. Soil Ecol., 42: 141-149
Saharan, B.S. and V. Nehra, 2011. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res., 21: 30
Saitou, N. and M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4: 406-425
Sakai, M., A. Hosoda, K. Ogura and M. Ikenaga, 2014. The growth of Steroidobacter agariperforans sp. nov., a novel agar-degrading bacterium isolated from soil, is enhanced by the diffusible metabolites produced by bacteria belonging to Rhizobiales. Microb. Environ., 29: 89-95
Schloss, P.D., D. Gevers and S.L. Westcott, 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One, 6: e27310
Sheng, X.F. and L.Y. He, 2006. Solubilization of potassium-bearing minerals by a wild-type strain of Bacillus edaphicus and its mutants and increased potassium uptake by wheat. Can. J. Microbiol., 52: 66-72
Singh, S. and K.K. Kapoor, 1998. Effects of inoculation of phosphate-solubilizing microorganisms and an arbuscular mycorrhizal fungus on mungbean grown under natural soil conditions. Mycorrhiza, 7: 249-253
Srinivasan, S., J. Kim, S.R. Kang, W.H. Jheong and S.S. Lee, 2013. Burkholderia humi sp. nov., isolated from peat soil. Curr. Microbiol., 66: 300-305
Stamenov, A.D.R., S.S. Djuric and T.H. Jafari, 2018. Effect of Plant Growth Promoting Rhizobacteria on the Germination and Early Growth of Onion (Allium Cepa). Int. J. Agric. Biol. Eng., 12: 80321
Strickland, T.C. and P. Sollins, 1987. Improved method for separating light-and heavy-fraction organic material from soil. Soil Sci. Soc. Amer. J., 51: 1390-1393
Wang, X., M. Ma, D. Guan, X. Jiang, L. Li, Y. Ding and J. Li, 2011. Rapid identification for Paenibacillus mucilaginosus by PCR. Acta Microbiol. Sin., 51: 1485-1493
Watanabe, T., M. Urayama, T. Shinano, R. Okada and M. Osaki, 2015. Application of ionomics to plant and soil in fields under long-term fertilizer trials. SpringerPlus, 4: 781
Watve, M.G., R. Tickoo, M.M. Jog and B.D. Bhole, 2001. How many antibiotics are produced by the genus Streptomyces? Arch. Microbiol., 176: 386-390
Wayne, L.G., D.J. Brenner, R.R. Colwell, P.A.D. Grimont, O. Kandler, M.I. Krichevsky, L.H. Moore, W.E.C. Moore, R. Murray and E. Stackebrandt, 1987. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Evol. Microbiol., 37: 463-464
Wu, J.G., J.F. Wang, X.H. Zhang, S.S. Zhang, X.F. Hu and J.S. Chen, 2010. A gyrB-targeted PCR for rapid identification of Paenibacillus mucilaginosus. Appl. Microbiol. Biotechnol., 87: 739-747
Zeng, J., X. Liu, L. Song, X. Lin, H. Zhang, C. Shen and H. Chu, 2016. Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol. Biochem., 92: 41-49
Zhou, J., D. Guan, B. Zhou, B. Zhao, M. Ma, J. Qin, X. Jiang, S. Chen, F. Cao, D. Shen and J. Li, 2015. Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol. Biochem., 90: 42-51
