Skip to main content
SpringerLink
Log in

Harnessing the saline soil-inhabiting bacteria for antagonistic, antibiotic resistance, and plant growth-promoting attributes

  • Research Articles
  • Published:
Vegetos Aims and scope Submit manuscript

Abstract

Biological control of soil-borne plant infections is sorely needed since they are challenging to treat with conventional fungicides. This fundamental research was aimed to find bacteria that live in saline soils (halophilic or halotrophic) and have antagonistic activity against Sclerotium oryzae and Ralstonia solani. A total of fifty bacterial strains were recovered from the saline soils of Gangavathi, Karnataka, India. Eight of the fifty bacterial strains in the dual culture approach demonstrated antibiosis against S. oryzae and R. solani. The isolates that produced HCN, siderophore, and hydrolytic enzymes strongly correlated with their biocontrol activity. Arnow’s and Csaky’s methods were used for testing the types of siderophores formed, and only a few isolates produced both catecholate and hydroxamate types. In Arnow’s and Csaky’s assays, the isolate Bacillus albus (HB-17) showed catechol and hydroxamate type siderophores. These prospective isolates’ identity was previously confirmed using 16 S rRNA analysis of Bacillus cereus, Bacillus albus, Bacillus safensis, Staphylococcus xylosus, Lysinibacillus sphaericus, and Pseudomonas stutzeri. Antibiotic resistance testing revealed that the isolates were resistant to Penicillin, Ofloxacin, and Vancomycin. Furthermore, the strains were tested for their plant growth-promoting properties, such as phosphorous (P) and zinc (Zn) solubilization, and potassium (K) release, at three NaCl concentrations (3, 6, and 10% w/v). At a concentration of 6% NaCl, the solubilization zones of zinc carbonate (ZnCO3), zinc oxide (ZnO), and phosphorous (Ca3PO4) were 5.20–9.0 mm, 6.06–13.20 mm, and 6.30–9.70 mm, respectively. Finally, we investigated the isolation of new bacterial strains with antifungal activity from saline soils in Gangavathi, Karnataka, India’s untapped agro-ecological habitats. This research also provides the path for further characterization of these isolates to maximize their antifungal potential.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andersson DI, Hughes D (2012) Evolution of antibiotic resistance at non-lethal drug concentration. Drug Resist Updat 15:162–172. doi: https://doi.org/10.1016/j.drup.2012.03.005

    Article  CAS  PubMed  Google Scholar 

  • Andersson DI, Hughes D (2014) Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 12:465–478. doi: https://doi.org/10.1038/nrmicro3270

    Article  CAS  PubMed  Google Scholar 

  • Arnow LE (1937) Colorimetric determination of the components of 3,4-dihy droxyphenylalanine-tyrosine mixtures. J Biol Chem 118:531–537

    CAS  Google Scholar 

  • Bahlm MI, Sørensen SJ, Hansen LH, Licht TR (2004) Effect of tetracycline on transfer and establishment of the tetracycline-inducible conjugative transposon Tn916 in the guts of gnotobiotic rats. Appl Environ Microbiol 70:758–764. doi: https://doi.org/10.1128/AEM.70.2.758-764.2004

    Article  CAS  Google Scholar 

  • Barthalomew JW, Mittewar T (1950) A simplified bacterial strain. Strain Tech 25:153

    Google Scholar 

  • Berrada I, Anne W, Paul DV, ElMostafa EF, Jean S, Najib B, Marouane M, Mohamed A (2012) Diversity of culturable moderately halophilic and halotolerant bacteria in a marsh and two salterns a protected ecosystem of Lower Loukkos (Morocco). Afr J Microbiol Res 6(10):2419–2434

    CAS  Google Scholar 

  • BhaskarRao T, Ramakrishna C, Ramesh M, Punniakotti E, Venkatesh V, Sailaja B, Raghurami RM, Arra Y, Laha GS, Sheshu M, Sundaram RM, Ladhalakshmi D, Balachandran SM, Satendra KM (2019) Pectin induced transcriptome of a Rhizoctonia solani strain causing sheath blight disease in rice reveals insights on key genes and RNAi machinery for development of pathogen derived resistance. Plant Mol Biol 100:59–71

    Google Scholar 

  • Cappuccino JC, Sherman N (2013) Microbiology: a laboratory manual, 10th edn. Pearson Pub. Co., New York, Harlow, Essex

    Google Scholar 

  • Castric KF, Castric PA (1983) Method for rapid detection of cyanogenic bacteria. Appl Environ Microbiol 45:700–702

    Google Scholar 

  • Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants–with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513

    CAS  PubMed  Google Scholar 

  • Coleman MB, Owen HH, Dacey HG (1930) Fermentation of monosaccharides by organisms of the Abortus melitensis group. J Lab Clin Med 15:641–642

    Google Scholar 

  • Cother E, Nicol H (1999) Susceptibility of Australian rice cultivars to stem rot fungus Sclerotium oryzae. Austra Plant Path 28:85–91

    Google Scholar 

  • Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moënne-Loccoz Y (2009) Pseudomonas fluorecens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48:505–512

    CAS  PubMed  Google Scholar 

  • Cowan ST, Steel KJ (1965) Manual for the identification of medical bacteria. J Clin Pathol 46:975

    Google Scholar 

  • Cray JA, Connor MC, Stevenson A, Houghton JDR, Rangel DEN, Cooke LR, Hallsworth JE (2015) Biocontrol agents promote growth of potato pathogens, depending on environmental conditions. Microb Biotech 9:330–354. https://doi.org/10.1111/1751-7915.12349

    Article  CAS  Google Scholar 

  • Csaky TZ (1948) On the estimation of bound hydroxylamine in biological materials. Acta Chem Scand 2:450–454

    CAS  Google Scholar 

  • Dave BP, Kena A, Puja H (2006) Siderophores of halophilic archaea and their chemical characterization. Indian J Exp Biol 44:340–344

    CAS  PubMed  Google Scholar 

  • Eynard A, Lal R, Wiebe K (2005) Crop response in salt-affected soils. J Sustain Agric 27:5–50. https://doi.org/10.1300/J064v27n01_03

    Article  Google Scholar 

  • Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol Lett 213:1–6

    CAS  PubMed  Google Scholar 

  • Ferris H, Tuomisto H (2015) Unearthing the role of biological diversity in soil health. Soil Biol Biochem 85:101–109

    CAS  Google Scholar 

  • Fich EA, Segerson NA, Rose JK (2016) The plant polyester cutin: biosynthesis, structure, and biological roles. Annu Rev Plant Biol 67:207–233

    CAS  PubMed  Google Scholar 

  • Franco N, Jayleen D, Jose R, Karlo ML (2018) Assessment of halophilic bacteria in the salt flats and wildlife refuge in Cabo Rojo, Puerto Rico and their antibiotic resistance pattern. EC Microbiol 14(10):707–714

    Google Scholar 

  • Gillican CA (2008) Sustainable agriculture and plant diseases: An epidemiological perspective. Phil Trans R Soc B 27:741–756

    Google Scholar 

  • Gopika K, Jagadeeswar R, Krishna rao V, Vijayalakshmi K (2017) Isolation, identification and evaluation of native antagonists microflora from stem rot infected rice plants against Sclerotium oryzae. Bull Env Pharmacol Life sci 6(2):349–353

    Google Scholar 

  • Graham EB (2016) Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol 7:214

    PubMed  PubMed Central  Google Scholar 

  • Guerin E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, Da Re S (2009) The SOS response controls integron recombination. Science 324:1034. doi: https://doi.org/10.1126/science.1172914

    Article  CAS  PubMed  Google Scholar 

  • Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB (2014) Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet 10:1004281

    Google Scholar 

  • JL  (1975) Powdered chitin agar as a selective medium for enumeration of Actinomycetes in water and soil. 29:422–426 3

  • Jackson LF, Webster RK, Wick CM, Bolstad J, Wilkerson JA (1977) Chemical control of stem rot of Rice in California. Phytopathology 67:1155–1158

    CAS  Google Scholar 

  • Kushner DJ (1993) Growth and nutrition of halophilic bacteria. In: Vreeland RH, Hochstein L (eds) The biology of halophilic bacteria. CRC Press, Boca Raton, pp 87–103

    Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Path 132:1–41

    CAS  Google Scholar 

  • Liu Y (2017) Ethylene signaling is important for isofavonoid-mediated resistance to Rhizoctonia solani in roots of Medicago truncatula. Mol Plant Microbe Interact 30:691–700

    CAS  PubMed  Google Scholar 

  • Maclean JL, Dawe DC, Hardy B, Hettel GP (2002) Rice Almanac. Los Banos, Phillippines. International Rice research Institute; West Africa Rice Development Association; International center for tropical agriculture; Food and Agriculture Organization, Bouake; Cali; Rome, p 253

    Google Scholar 

  • Manwar AV, Khandelwal SR, Chaudhari BL, Meyer JM, Chincholkar SB (2004) Siderophore production by a marine Pseudomonas aeruginosa and its antagonistic action against phytopathogenic fungi. Appl Biochem Biotechnol 118:243–251

    CAS  PubMed  Google Scholar 

  • Martins JG, Martin C, Hernández-Apaolaza L, Barros MT, Soares HMVM, Lucena JJ (2018) Azotochelin and N-dihydroxy-N, N’-diisopropylhex anediamide as Fe sources to cucumber plants in hydroponic cultures. Emirates J Food Agric 30:65–76. https://doi.org/10.9755/ejfa.2018.v30. i1.1586

    Article  Google Scholar 

  • Menasria T, Monteoliva-Sánchez M, Benammar L, Benhadj M, Ayachi A, Hacène H, Gonzalez-Paredes A, Aguilera M (2019) Culturable halophilic bacteria inhabiting Algerian saline ecosystems: a source of promising features and potentialities. World J Microb Biotech 35(9):1–6

    CAS  Google Scholar 

  • Nagaraju Y, Gundappagol RC, Mahadevaswamy (2020) Mining saline soils to manifest plant stress-alleviating halophilic bacteria. Curr Microbiol 77:2265–2278. https://doi.org/10.1007/s00284-020-02028-w

    Article  CAS  PubMed  Google Scholar 

  • Nieto JJ, Fernandez CR, Garcia MT, Mellado E, Ventos A (1993) Survey of antimicrobial suceptability of moderately halophilic eubacteria and extremely halophilic aerobic arcahaeobacteria: utilization of antibiotic resistance as a genetic marker. Syst Appl Microbiol 16:352–360

    CAS  Google Scholar 

  • Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834

    CAS  PubMed  Google Scholar 

  • Pan M, Chu LM (2016) Adsorption and degradation of five selected antibiotics in agricultural soil. Sci Total Environ 545–546:48–56. doi: https://doi.org/10.1016/j.scitotenv.2015.12.040

    Article  CAS  PubMed  Google Scholar 

  • Payne SM (1994) Detection, isolation and characterization of siderophores. Methods Enzymol 235:329–344

    CAS  PubMed  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologiya 17:362–370

    CAS  Google Scholar 

  • Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie V Leeuwen 81:537–547

    CAS  Google Scholar 

  • Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in vertisols of central India. Appl Soil Ecol 73:87–96

    Google Scholar 

  • Reetha S, Bhuvaneswari G, Thamizhiniyan P, Mycin TR (2014) Isolation of indole acetic acid (IAA) producing rhizobacteria of Pseudomonas fluorescens and Bacillus subtilis and enhance growth of onion (Allim cepa. L). Int J Curr Microbiol App Sci 3:568–574

    Google Scholar 

  • Richa K, Tiwari IM, Kumari M, Devanna BN, Sonah H, Kumari A, Nagar R, Sharma V, Botel JR, Tilakr STR (2016) Functional characterization of novel chitinase genes present in the sheath blight resistance QTL: qSBR11-1in rice line tetep. Front Plant Sci 7:1–10

    Google Scholar 

  • Sambrook J, Fritsch ER, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Saravanan VS, Subramoniam SR, Raj SA (2003) Assessing in vitro solubilization of different zinc solubilizing bacterial (ZBS) strains. Braz J Microbiol 34:121–125

    Google Scholar 

  • Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439

    PubMed  Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56

    CAS  PubMed  Google Scholar 

  • Sengupta S, Chattopadhyay MK, Grossart HP (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4:47. doi: https://doi.org/10.3389/fmicb.2013.00047

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahab S, Ahmed N (2008) Effect of various parameters on the efficiency of zinc phosphate solubilization by indigenous bacterial isolates. Afr J Biotechnol 7(10):1543–1549

    Google Scholar 

  • Shawish R, Tarabees R (2017) Prevalence and antimicrobial resistance of Bacillus cereus isolated from beef products in Egypt Reyad. O Vet J 7(4):337–341

    Google Scholar 

  • Shirling ET, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Google Scholar 

  • Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22(2):123–131

    CAS  PubMed  Google Scholar 

  • Simine CDD, Sayer JA, Gadd GM (1998) Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from a forest soil. Biol Fertil Soils 28:87–94

    Google Scholar 

  • Skidmore AM, Dickinson CH (1976) Colony interaction and hyphal interference between Septoria nodorum and phylloplane fungi. Trans J Br Ceramic Soc 66:57–74

    Google Scholar 

  • Smibert R, Krieg N, Gerhardt P, Murray R, Wood W (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC

    Google Scholar 

  • Song F, Goodman RM (2001) Molecular biology of disease resistance in rice. Physiol Mol Plant Pathol 59:1–11. DOI:https://doi.org/10.1006/pmpp.2001.0353

    Article  CAS  Google Scholar 

  • Tan WZ, Zhang W, Ou ZQ, Li CW, Zhou GJ, Wang ZK, Yin LL (2011) Analyses of the temporal development and yield losses due to sheath blight of Rice (Rhizoctonia solani AG1IA). Agric Sci China 6:1074–1081. https://doi.org/10.1016/S1671-2927(07)60149-7

    Article  Google Scholar 

  • Tango MSA, Islam MR (2002) Potential of extremophiles for biotechnological and petroleum applications. Energy Sourc 24:543–559

    CAS  Google Scholar 

  • Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49:195–204. doi: https://doi.org/10.1002/jobm.200800090

    Article  CAS  PubMed  Google Scholar 

  • Thamthiankul S, Suan-ngay S, Tantimavanich S, Panbangered W (2001) Chitinase from Bacillus thuringiensis subsp. pakistani. Appl Microbi Biotech 56:395–401  https://doi.org/10.1007/s002530100630

  • VanderHeijden MGA, de Bruin S, Luckerhoff L, van Logtestijn RSP, Schlaeppi KA (2016) widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399

    CAS  Google Scholar 

  • Vora JU, Jain NK, Modi HA (2014) Extraction, characterization and application studies of red pigment of halophile Serratia marcescens KH1R KM035849 isolated from Kharaghoda soil. Int J Pure App Biosci 2(6):160–168

    Google Scholar 

  • Yandigeri MS, Meena KK, Singh D, Malviya N, Singh DP, Solanki MK, Yadav AK, Arora DK (2012) Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul 68(3):411–420. https://doi.org/10.1007/s10725-012-9730-2

    Article  CAS  Google Scholar 

  • Yellareddygari SK, Reddy MS, Kloepper JW, Lawrence KS, Fadamiro H (2014) Rice sheath blight: a review of disease and pathogen management approaches. J Plant Pathol Microbiol 5(4):241. https://doi.org/10.4172/2157-7471.1000241

    Article  Google Scholar 

  • Zhao LJ, Liang H, Huang J, Chen Z, Nie Y (2018) Manipulation of the rhizosphere microbial community through applying a new bio-organic fertilizer improves watermelon quality and health. PLoS ONE 13(2):e0192967. doi: https://doi.org/10.1371/journal.pone.0192967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University of Agricultural Sciences, Raichur, India

    Yalavarthi Nagaraju &  Mahadevaswamy

  2. College of Agriculture, Gangavathi, Karnataka, India

    S. B. Gowder

Authors
  1. Yalavarthi Nagaraju
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahadevaswamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. B. Gowder
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YN experimented with M, and SBG helped prepare the manuscript and synthesize the hypothesis.

Corresponding author

Correspondence to Yalavarthi Nagaraju.

Ethics declarations

Conflict of interest

The subject matter and materials presented in this work are entirely free of any financial or other conflicts of interest, according to all of the writers. They do not belong to or participate in any groups or businesses that have a stake in the topics or resources covered in this work, whether such interests be pecuniary or not.

Ethics approval and consent to participate

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nagaraju, Y., Mahadevaswamy & Gowder, S.B. Harnessing the saline soil-inhabiting bacteria for antagonistic, antibiotic resistance, and plant growth-promoting attributes. Vegetos 36, 907–919 (2023). https://doi.org/10.1007/s42535-022-00466-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42535-022-00466-4

Keywords

Search

Navigation