Abstract
Prospective plant growth promoting rhizobacteria isolated from the rhizosphere of Vigna radiata was identified as Acinetobacter sp. SK2 that solubilized 682 μg ml−1 of tricalcium phosphate (TCP) and 86 μg ml−1 of rock phosphate (RP) with concomitant decrease in pH up to 4 due to the production of gluconate. The biochemical basis of the P solubilization suggested that the gluconate production was mediated by mGDH and sGDH enzymes. Our results illustrate the role of succinate in repression of P solubilization via suppression of mGDH and sGDH activity which correlated with repression of expression of respective genes, gdhA and gdhB. SK2 also produced IAA (117 μg ml−1), siderophore (87% units), HCN, ammonia and solubilized minerals of Zn and K. Our findings imply that it is important to understand the cause of failure of several phosphate solubilizing bacteria in field conditions where catabolite repression may control the expression of several genes and pathways including that of mineral phosphate solubilization. Furthermore, Acinetobacter sp. SK2 bearing two glucose dehydrogenase (gdhA and gdhB) genes was recognized as promising strain for P biofortification and enhanced plant growth promotion.
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References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Method Enzymol 8:115–118. https://doi.org/10.1016/0076-6879(66)08014-5
An R, Moe LA (2016) Regulation of pyrroloquinoline quinone-dependent glucose dehydrogenase activity in the model rhizosphere-dwelling bacterium Pseudomonas putida KT2440. Appl Environ Microbiol 82(16):4955–4964. https://doi.org/10.1128/aem.00813-16
Basu A, Apte SK, Phale PS (2006) Preferential utilization of aromatic compounds over glucose by Pseudomonas putida CSV86. Appl Environ Microbiol 72(3):2226–2230. https://doi.org/10.1128/aem.72.3.2226-2230.2006
Bergey DH, Krieg NR, Holt JG (eds) (1984) Bergey’s manual of systematic bacteriology. Williams and Wilkins, Baltimore
Duine JA, Jzn JF, Van der Meer R (1982) Different forms of quinoprotein aldose-(glucose-) dehydrogenase in Acinetobacter calcoaceticus. Arch Microbiol 131(1):27–31
Etesami H, Emami S, Alikhani HA (2017) Potassium solubilizing bacteria (KSB): mechanisms, promotion of plant growth, and future prospects—a review. J Soil Sci Plant Nutr 17(4):897–911. https://doi.org/10.4067/S0718-95162017000400005
Flexer V, Mano N (2014) Wired pyrroloquinoline quinone soluble glucose dehydrogenase enzyme electrodes operating at unprecedented low redox potential. Anal Chem 86(5):2465–2473. https://doi.org/10.1021/ac403334w
Goldstein AH (1995) recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram negative bacteria. Biol Agric Hortic 12(2):185–193. https://doi.org/10.1080/01448765.1995.9754736
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26(1):192–195. https://doi.org/10.1104/pp.26.1.192
Gulati A, Sharma N, Vyas P, Sood S, Rahi P, Pathania V, Prasad R (2010) Organic acid production and plant growth promotion as a function of phosphate solubilization by Acinetobacter rhizosphaerae strain BIHB 723 isolated from the cold deserts of the trans-Himalayas. Arch Microbiol 192(11):975–983. https://doi.org/10.1007/s00203-010-0615-3
Gyaneshwar P, Parekh LJ, Archana G, Poole PS, Collins MD, Hutson RA, Kumar GN (1999) Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilization by Enterobacter asburiae. FEMS Microbiol Lett 171(2):223–229. https://doi.org/10.1111/j.1574-6968.1999.tb13436.x
Hansen PA (1930) The detection of ammonia production by bacteria in agar slants. J Bacteriol 19(3):223
Iyer B, Rajkumar S (2019) Succinate irrepressible periplasmic glucose dehydrogenase of Rhizobium sp. Td3 and SN1 contributes to its phosphate solubilization ability. Arch Microbiol 201(5):649–659. https://doi.org/10.1007/s00203-019-01630-2
Iyer B, Rajput MS, Rajkumar S (2017) Effect of succinate on phosphate solubilization in nitrogen fixing bacteria harbouring chick pea and their effect on plant growth. Microbiol Res 202:43–50. https://doi.org/10.1016/j.micres.2017.05.005
Joshi E, Iyer B, Rajkumar S (2019) Glucose and arabinose dependent mineral phosphate solubilization and its succinate-mediated catabolite repression in Rhizobium sp. J Biosci Bioeng, RM RS. https://doi.org/10.1016/j.jbiosc.2019.04.020
Jung J, Park W (2015) Acinetobacter species as model microorganisms in environmental microbiology: current state and perspectives. Appl Microbiol Biotechnol 99(6):2533–2548. https://doi.org/10.1007/s00253-015-6439-y
Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593. https://doi.org/10.3389/fmicb.2017.02593
Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Khan MS, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms: principles and application of microphos technology. Springer International Publishing, Cham, pp 31–62. https://doi.org/10.1007/978-3-319-08216-5_2
Kravchenko LV, Azarova TS, Leonova-Erko EI, Shaposhnikov AI, Makarova NM, Tikhonovich IA (2003) Tomato root exudates and their effect on the growth and antifungal activity of Pseudomonas strains. Mikrobiologiia 72(1):48–53
Lareen A, Burton F, Schafer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90(6):575–587. https://doi.org/10.1007/s11103-015-0417-8
Long MH, McGlathery KJ, Zieman JC, Berg P (2008) The role of organic acid exudates in liberating phosphorus from seagrass-vegetated carbonate sediments. Limnol Oceanogr 53(6):2616–2626. https://doi.org/10.4319/lo.2008.53.6.2616
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Mahjoubi M, Jaouani A, Guesmi A, Ben Amor S, Jouini A, Cherif H, Najjari A, Boudabous A, Koubaa N, Cherif A (2013) Hydrocarbonoclastic bacteria isolated from petroleum contaminated sites in Tunisia: isolation, identification and characterization of the biotechnological potential. N Biotechnol 30(6):723–733. https://doi.org/10.1016/j.nbt.2013.03.004
Mandal NC, Chakrabartty PK (1993) Succinate-mediated catabolite repression of enzymes of glucose metabolism in root-nodule bacteria. Curr Microbiol 26(5):247–251. https://doi.org/10.1007/bf01575912
Matsushita K, Shinagawa E, Adachi O, Ameyama M (1989) Quinoprotein d-glucose dehydrogenase of the Acinetobacter calcoaceticus respiratory chain: membrane-bound and soluble forms are different molecular species. Biochemistry 28(15):6276–6280
Matsushita K, Toyama H, Ameyama M, Adachi O, Dewanti A, Duine JA (1995) Soluble and membrane-bound quinoprotein d-glucose dehydrogenases of the Acinetobacter calcoaceticus: the binding process of PQQ to the apoenzymes. Biosci Biotechnol Biochem 59(8):1548–1555. https://doi.org/10.1271/bbb.59.1548
Miller SH, Browne P, Prigent-Combaret C, Combes-Meynet E, Morrissey JP, O’Gara F (2010) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2(3):403–411. https://doi.org/10.1111/j.1758-2229.2009.00105.x
Moreno R, Ruiz-Manzano A, Yuste L et al (2007) The Pseudomonas putida Crc global regulator is an RNA binding protein that inhibits translation of the AlkS transcriptional regulator. Mol Microbiol 64:665–675. https://doi.org/10.1111/j.1365-2958.2007.05685.x
Patel DK, Murawala P, Archana G, Kumar GN (2011) Repression of mineral phosphate solubilizing phenotype in the presence of weak organic acids in plant growth promoting fluorescent pseudomonads. Biores Technol 102(3):3055–3061. https://doi.org/10.1016/j.biortech.2010.10.041
Rajput MS, Naresh Kumar G, Rajkumar S (2013) Repression of oxalic acid-mediated mineral phosphate solubilization in rhizospheric isolates of Klebsiella pneumoniae by succinate. Arch Microbiol 195(2):81–88. https://doi.org/10.1007/s00203-012-0850-x
Rammachandran S, Fontanille P, Pandey A, Larroche C (2006) Gluconic acid: properties, applications and microbial production. Food Technol Biotechnol 44:185–195
Rentz JA, Alvarez PJ, Schnoor JL (2004) Repression of Pseudomonas putida phenanthrene-degrading activity by plant root extracts and exudates. Environ Microbiol 6(6):574–583. https://doi.org/10.1111/j.1462-2920.2004.00589.x
Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321(1):305–339. https://doi.org/10.1007/s11104-009-9895-2
Rijavec T, Lapanje A (2016) Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol 7:1785. https://doi.org/10.3389/fmicb.2016.01785
Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17(4–5):319–339. https://doi.org/10.1016/S0734-9750(99)00014-2
Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S, Dhakephalkar PK, Chopade BA (2011) Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J Microbiol Biotechnol 21(6):556–566. https://doi.org/10.4014/jmb.1012.12006
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Setiawati TC, Mutmainnah L (2016) Solubilization of potassium containing mineral by microorganisms from sugarcane rhizosphere. Agric Agric Sci Procedia 9:108–117. https://doi.org/10.1016/j.aaspro.2016.02.134
Sharma SK, Sharma MP, Ramesh A, Joshi OP (2012) Characterization of zinc-solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds. J Microbiol Biotechnol 22(3):352–359. https://doi.org/10.4014/jmb.1106.05063
Suzuki W, Sugawara M, Miwa K, Morikawa M (2014) Plant growth-promoting bacterium Acinetobacter calcoaceticus P23 increases the chlorophyll content of the monocot Lemna minor (duckweed) and the dicot Lactuca sativa (lettuce). J Biosci Bioeng 118(1):41–44. https://doi.org/10.1016/j.jbiosc.2013.12.007
Acknowledgements
The authors greatfully acknowledge the financial grant received by SR from Science and Engineering Research Board (SERB), Department of Sciences and Technology (DST), Government of India (SERB/EMR/2017/001464). Authors would also like to acknowledge Nirma University for providing infrastructure facility for the research work.
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Bharwad, K., Rajkumar, S. Modulation of PQQ-dependent glucose dehydrogenase (mGDH and sGDH) activity by succinate in phosphate solubilizing plant growth promoting Acinetobacter sp. SK2. 3 Biotech 10, 5 (2020). https://doi.org/10.1007/s13205-019-1991-2
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DOI: https://doi.org/10.1007/s13205-019-1991-2