An Enterobacter cloacae strain NG-33 that can solubilize phosphate and promote maize growth

It is critical to identify and evaluate efficient phosphate-solubilizing bacteria (PSB) that enable P uptake from unavailable forms, and therefore improve the phosphorus (P) uptake efficiency of crops. The Enterobacter cloacae strain NG-33, belonging to PSB, was isolated and identified from calcareous rhizosphere soils in Nonggang National Reserve, Guangxi, China. The stain NG-33 could reduce the pH of the medium to below 5.6, and had the ability to release soluble phosphorus (P; 180.7 μg ml−1) during the culture in the National Botanical Research Institute’s Phosphate medium (NBRIP), and produced such organic acids as gluconic acid (4,881 mg L−1), acetic acid (346 mg L−1), and indole-3-acetic acid (20.4 μg ml−1). It could also convert inorganic P in AlPO4 (Al-P) and FePO4 (Fe-P) into soluble P, with conversion efficiencies of 19.2 μg ml−1 and 16.3 μg ml−1, respectively. Under pot experiments and when compared controls without inoculating NG-33, the shoot and root biomass of maize seedlings showed increases by 140% for shoot biomass and by 97% for root biomass in loamy soil (P sufficient) inoculated with NG-33. In sandy soil (P deficit) supplemented with tricalcium phosphate and inoculated with NG-33, the soluble P content was significantly higher, 58.6% in soil and 33.6% in roots, meanwhile, the biomass of shoots and roots increased by 14.9 and 24.9%, respectively. The growth-promoting effects coupled to the significant increase in leaf net photosynthetic rate and stomatal conductance of plants grown in NG-33-inoculated soil. Inoculating NG-33 could significantly improve the diversity and richness of bacterial population and altered the dominant bacterial population in soil.

[1]  R. Çakmakçı,et al.  Isolation and Characterization of Phosphate Solubilizing Bacteria and Effect of Growth and Nutrient Uptake of Maize Under Pot and Field Conditions , 2022 .

[2]  Li Li,et al.  Profound Change in Soil Microbial Assembly Process and Co-occurrence Pattern in Co-inoculation of Bradyrhizobium japonicum 5038 and Bacillus aryabhattai MB35-5 on Soybean , 2022, Frontiers in Microbiology.

[3]  M. Irfan,et al.  Differential Root Exudation and Architecture for Improved Growth of Wheat Mediated by Phosphate Solubilizing Bacteria , 2021, Frontiers in Microbiology.

[4]  C. Crecchio,et al.  Photosynthetic responses of durum wheat to chemical/microbiological fertilization management under salt and drought stresses , 2021, Acta Physiologiae Plantarum.

[5]  Wangxiang Zhang,et al.  Effect of co-inoculation with arbuscular mycorrhizal fungi and phosphate solubilizing fungi on nutrient uptake and photosynthesis of beach palm under salt stress environment , 2021, Scientific Reports.

[6]  Xiwen Chen,et al.  A Bacterium Isolated From Soil in a Karst Rocky Desertification Region Has Efficient Phosphate-Solubilizing and Plant Growth-Promoting Ability , 2021, Frontiers in Microbiology.

[7]  H. Saud,et al.  Characterization of Peat Microbial Functional Diversity in Aerobic Rice Rhizosphere , 2020 .

[8]  Shikha Gupta,et al.  Diversity analysis of ACC deaminase producing bacteria associated with rhizosphere of coconut tree (Cocos nucifera L.) grown in Lakshadweep islands of India and their ability to promote plant growth under saline conditions. , 2020, Journal of biotechnology.

[9]  A. Hidayat,et al.  Shifting of microbial biodiversity and soil health in rhizomicrobiome of natural forest and agricultural soil , 2020 .

[10]  Haijun Yang,et al.  The relative contributions of pH, organic anions, and phosphatase to rhizosphere soil phosphorus mobilization and crop phosphorus uptake in maize/alfalfa polyculture , 2019, Plant and Soil.

[11]  Junsheng Liang,et al.  Effects of Phosphate Solubilizing Bacteria on the Growth, Photosynthesis, and Nutrient Uptake of Camellia oleifera Abel. , 2019, Forests.

[12]  M. S. Anzuay,et al.  Growth promotion of peanut (Arachis hypogaea L.) and maize (Zea mays L.) plants by single and mixed cultures of efficient phosphate solubilizing bacteria that are tolerant to abiotic stress and pesticides. , 2017, Microbiological research.

[13]  D. Dowling,et al.  Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates , 2015, Front. Microbiol..

[14]  Zhi-xing Zhang,et al.  Terminal Restriction Fragment Length Polymorphism Analysis of Soil Bacterial Communities under Different Vegetation Types in Subtropical Area , 2015, PloS one.

[15]  J. Palta,et al.  Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize , 2015, Plant and Soil.

[16]  S. Pereira,et al.  Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils , 2014 .

[17]  L. Hinzman,et al.  Bacterial community structure and soil properties of a subarctic tundra soil in Council, Alaska , 2014, FEMS microbiology ecology.

[18]  A. Brauman,et al.  Bacterial capacities to mineralize phytate increase in the rhizosphere of nodulated common bean (Phaseolus vulgaris) under P deficiency , 2014 .

[19]  G. Tóth,et al.  Phosphorus levels in croplands of the European Union with implications for P fertilizer use , 2014 .

[20]  M. V. D. van der Heijden,et al.  Soil biodiversity and soil community composition determine ecosystem multifunctionality , 2014, Proceedings of the National Academy of Sciences.

[21]  FangChun Liu,et al.  Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings , 2013, Applied Microbiology and Biotechnology.

[22]  T. Kirikae,et al.  Multilocus Sequence Typing (MLST) for Characterization of Enterobacter cloacae , 2013, PloS one.

[23]  You-Zhi Li,et al.  Characterization of Plant-Growth-Promoting Effects and Concurrent Promotion of Heavy Metal Accumulation in the Tissues of the Plants Grown in The Polluted Soil by Burkholderia Strain LD-11 , 2013, International journal of phytoremediation.

[24]  Y. Bashan,et al.  Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure , 2013, Biology and Fertility of Soils.

[25]  A. Imran,et al.  Root colonization and growth promotion of sunflower (Helianthus annuus L.) by phosphate solubilizing Enterobacter sp. Fs-11 , 2012, World Journal of Microbiology and Biotechnology.

[26]  Lin Wenxiong,et al.  Effects of Sugarcane Ratooning Cultivation on the Alteration of Bacterial Communities in the Rhizosphere Soil , 2012, Sugar Tech.

[27]  S. K. Pandian,et al.  Evaluation of Bacterial Diversity in Palk Bay Sediments Using Terminal-Restriction Fragment Length Polymorphisms (T-RFLP) , 2012, Applied Biochemistry and Biotechnology.

[28]  Bruno Lima Soares,et al.  Biological nitrogen fixation and phosphate solubilization by bacteria isolated from tropical soils , 2012, Plant and Soil.

[29]  P. Gunasekaran,et al.  Root colonization of a rice growth promoting strain of Enterobacter cloacae , 2011, Journal of basic microbiology.

[30]  C. Calheiros,et al.  Bacterial community dynamics in horizontal flow constructed wetlands with different plants for high salinity industrial wastewater polishing. , 2010, Water research.

[31]  A. Godeas,et al.  Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilization , 2010, Biology and Fertility of Soils.

[32]  Chengrong Chen,et al.  Citric acid enhances the mobilization of organic phosphorus in subtropical and tropical forest soils , 2010, Biology and Fertility of Soils.

[33]  Allan Konopka,et al.  What is microbial community ecology? , 2009, The ISME Journal.

[34]  N. Carneiro,et al.  Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. , 2009 .

[35]  J. Ramos,et al.  New molecular tools for enhancing methane production, explaining thermodynamically limited lifestyles and other important biotechnological issues , 2009, Microbial biotechnology.

[36]  B. Wang,et al.  Effects of soil microarthropods on plant litter decomposition across an elevation gradient in the Wuyi Mountains. , 2009 .

[37]  J. Tarafdar,et al.  Hydrolysis of Organic Phosphate Forms by Phosphatases and Phytase Producing Fungi of Arid and Semi Arid Soils of India , 2009 .

[38]  T. Junier,et al.  TRiFLe, a Program for In Silico Terminal Restriction Fragment Length Polymorphism Analysis with User-Defined Sequence Sets , 2008, Applied and Environmental Microbiology.

[39]  G. Reddy,et al.  Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. , 2008, Microbiological research.

[40]  T. Sa,et al.  Pseudomonas corrugata (NRRL B-30409) Mutants Increased Phosphate Solubilization, Organic Acid Production, and Plant Growth at Lower Temperatures , 2008, Current Microbiology.

[41]  L. Yarzábal,et al.  Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region , 2007 .

[42]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[43]  K. Huddersman,et al.  Novel ion chromatography technique for the rapid identification and quantification of saturated and unsaturated low molecular weight organic acids formed during the Fenton oxidation of organic pollutants. , 2007, Journal of Chromatography A.

[44]  R. Coico,et al.  Gram Staining , 2005, Current protocols in microbiology.

[45]  N. Ayub,et al.  Organic Acids Production and Phosphate Solubilization by Phosphate Solubilizing Microorganisms (PSM) Under in vitro Conditions , 2004 .

[46]  E. Temminghoff,et al.  Plant Analysis Procedures , 2004, Springer Netherlands.

[47]  J. Tarafdar,et al.  Phytase and phosphatase producing fungi in arid and semi-arid soils and their efficiency in hydrolyzing different organic P compounds , 2003 .

[48]  H. Rodríguez,et al.  Phosphate solubilizing bacteria and their role in plant growth promotion. , 1999, Biotechnology advances.

[49]  C. Nautiyal An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. , 1999, FEMS microbiology letters.

[50]  D. Schachtman,et al.  Phosphorus Uptake by Plants: From Soil to Cell , 1998, Plant physiology.

[51]  H. Krishnan,et al.  Rahnella aquatilis, a bacterium isolated from soybean rhizosphere, can solubilize hydroxyapatite , 1997 .

[52]  V. J. G. Houba,et al.  A novel digestion technique for multi-element plant analyses , 1983 .

[53]  I. Rose The Bacterium. , 1965, Canadian Medical Association journal.

[54]  H. Katznelson,et al.  PHOSPHATE-DISSOLVING MICROORGANISMS ON SEED AND IN THE ROOT ZONE OF PLANTS , 1962 .

[55]  S. R. Olsen,et al.  Estimation of available phosphorus in soils by extraction with sodium bicarbonate , 1954 .

[56]  S. T. Cowan Bergey's Manual of Determinative Bacteriology , 1948, Nature.

[57]  J. Brown Bergey's Manual of Determinative Bacteriology (5th ed.) , 1939 .