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The effect of NaCl on growth and volatile metabolites produced by antagonistic endophytic bacteria isolated from Prosopis cineraria

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Abstract

Previously, we reported that endophytic Pseudomonas aeruginosa PC5 isolated from Prosopis cineraria, abundantly produced antimicrobial volatile organic compounds (VOCs) and significantly suppressed the growth of Pythium aphanidermatum which causes damping-off in cucumber in in vitro assays. However, under pot culture conditions, no significant effect of this bacterium on cucumber damping-off was noticed under salt water irrigation (100 mM NaCl), while the antagonistic bacterium Acinetobacter johnsonii PC3 isolated from the same host which produced low levels of antimicrobial VOCs was effective in reducing the disease incidence under salt water irrigation. In this in vitro study, the effect of NaCl on the growth P. aphanidermatum and VOC composition of these two endophytic bacterial strains was evaluated. NaCl had inhibitory effects on the growth of both P. aeruginosa PC5 and A. johnsonii PC3. Gas chromatography-mass spectrometry analysis of the VOCs produced by these endophytes revealed that dimethyl disulfide (DMDS), a well-known antimicrobial compound, was the major compound (33.82%) released by P. aeruginosa PC5 in the absence of NaCl, whereas the production of DMDS was completely inhibited when it was cultured in a medium containing high concentrations of NaCl. Trimethylsilanol was released abundantly by A. johnsonii PC3 when grown in the salt-amended medium compared to control, suggesting possible involvement of this compound in the suppression of P. aphanidermatum by this bacterium under salt-stress conditions.

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References

  • Agisha VN, Kumar A, Eapen SJ, Sheoran N, Suseelabhai R (2019) Broad-spectrum antimicrobial activity of volatile organic compounds from endophytic Pseudomonas putida BP25 against diverse plant pathogens. Biocontrol Sci Technol 29:1069–1089

    Article  Google Scholar 

  • Al-Rashdi A, Al-Hinai FS, Al-Harrasi MMA, Al-Sabahi JN, Al-Badi RS, Al-Mahmooli IH, Al-Sadi AM, Velazhahan R (2023) The potential of endophytic bacteria from Prosopis cineraria for the control of Pythium aphanidermatum-induced damping-off in cucumber under saline water irrigation. J Plant Pathol 105:39–56

    Article  Google Scholar 

  • Alabouvette C, Olivain C, Migheli Q, Steinberg C (2009) Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt‐inducing Fusarium oxysporum. New Phytol 184:529–544

    Article  PubMed  CAS  Google Scholar 

  • Albdaiwi RN, Khyami-Horani H, Ayad JY, Alananbeh KM, Al-Sayaydeh R (2019) Isolation and characterization of halotolerant plant growth promoting rhizobacteria from durum wheat (Triticum turgidum subsp. durum) cultivated in saline areas of the dead sea region. Front Microbiol 10:1639

    Article  PubMed  PubMed Central  Google Scholar 

  • Bal HB, Nayak L, Das S, Adhya TK (2013) Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366:93–105

    Article  CAS  Google Scholar 

  • Bennett DR, Staratt WH (1973) Primate absorption and elimination balance studies including pulmonary, urinary, biliary and fecal excretion of t-butanol, trimethylsilanol, dimethylsilanediol and hexamethyldisiloxane. Toxicol Appl Pharmacol 25:445

    Google Scholar 

  • Bonaterra A, Badosa E, Daranas N, Francés J, Roselló G, Montesinos E (2022) Bacteria as biological control agents of plant diseases. Microorganisms 10:1759

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cam S, Kucuk C (2020) The Effect of salinity on growth, antagonistic potential, protease activity, and proline content of Trichoderma harzianum. Comm J Biol 4:62–66

    Google Scholar 

  • Christakis CA, Daskalogiannis G, Chatzaki A, Markakis EA, Mermigka G, Sagia A, Rizzo GF, Catara V, Lagkouvardos I, Studholme DJ, Sarris PF (2021) Endophytic bacterial isolates from halophytes demonstrate phytopathogen biocontrol and plant growth promotion under high salinity. Front Microbiol 12:681567

    Article  PubMed  PubMed Central  Google Scholar 

  • Chuankun X, Minghe M, Leming Z, Keqin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004

    Article  Google Scholar 

  • Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703

    Article  PubMed  CAS  Google Scholar 

  • Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571

    Article  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Pare PW (2006) GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268

    Article  PubMed  CAS  Google Scholar 

  • Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

    Article  CAS  Google Scholar 

  • Giorgio A, De Stradis A, Lo Cantore P, Iacobellis NS (2015) Biocide effects of volatile organic compounds produced by potential biocontrol rhizobacteria on Sclerotinia sclerotiorum. Front Microbiol 6:1056

    Article  PubMed  PubMed Central  Google Scholar 

  • Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schulz S, Weisskopf L (2013) Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 39:892–906

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Leon R, Rojas-Solis D, Contreras-Perez M, del Carmen Orozco-Mosqueda M, Macias-Rodriguez LI, Reyes-de la Cruz H, Valencia-Cantero E, Santoyo G (2015) Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Control 81:83–92

    Article  CAS  Google Scholar 

  • Huang CJ, Tsay JF, Chang SY, Yang HP, Wu WS, Chen CY (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310

    Article  PubMed  CAS  Google Scholar 

  • Jayakumar V, Sundar AR, Viswanathan R (2021) Biocontrol of Colletotrichum falcatum with volatile metabolites produced by endophytic bacteria and profiling VOCs by headspace SPME coupled with GC-MS. Sugar Tech 23:94–107

    Article  CAS  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360

    Article  PubMed  CAS  Google Scholar 

  • Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012

    Article  PubMed  CAS  Google Scholar 

  • Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F (2013) Plant growth-promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria× ananassa). HortScience 48:563–567

    Article  CAS  Google Scholar 

  • Karunasinghe TG, Al-Mahmooli IH, Al-Sadi AM, Velazhahan R (2020) The effect of salt-tolerant antagonistic bacteria from tomato rhizosphere on plant growth promotion and damping-off disease suppression under salt-stress conditions. Acta Agric Scand B- Soil Plant Sci 70:69–75

    Google Scholar 

  • Khruengsai S, Pripdeevech P, Tanapichatsakul C, Srisuwannapa C, D’Souza PE, Panuwet P (2021) Antifungal properties of volatile organic compounds produced by Daldinia eschscholtzii MFLUCC 19-0493 isolated from Barleria prionitis leaves against Colletotrichum acutatum and its post-harvest infections on strawberry fruits. PeerJ 9:e11242

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim YM, Farrah S, Baney RH (2006) Silanol-A novel class of antimicrobial agent. Electron J Biotechnol 9:176–180

    Article  CAS  Google Scholar 

  • Kohl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845

    Article  PubMed  PubMed Central  Google Scholar 

  • Kol S, Merlo ME, Scheltema RA, de Vries M, Vonk RJ, Kikkert NA, Dijkhuizen L, Breitling R, Takano E (2010) Metabolomic characterization of the salt stress response in Streptomyces coelicolor. Appl Environ Microbiol 76:2574–2581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin YT, Lee CC, Leu WM, Wu JJ, Huang YC, Meng M (2021) Fungicidal activity of volatile organic compounds emitted by Burkholderia gladioli strain BBB-01. Molecules 26:745

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meldau DG, Meldau S, Hoang LH, Underberg S, Wunsche H, Baldwin IT (2013) Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25:2731–2747

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohamed HALA, Haggag WM (2006) Biocontrol potential of salinity tolerant mutants of Trichoderma harzianum against Fusarium oxysporum. Braz J Microbiol 37:181–191

    Article  Google Scholar 

  • Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83

    Article  Google Scholar 

  • Mu J, Li X, Jiao J, Ji G, Wu J, Hu F, Li H (2017) Biocontrol potential of vermicompost through antifungal volatiles produced by indigenous bacteria. Biol Control 112:49–54

    Article  CAS  Google Scholar 

  • Nakata K, Yoshimoto A, Yamada Y (1999) Promotion of antibiotic production by high ethanol, high NaCl concentration, or heat shock in Pseudomonas fluorescens S272. Biosci Biotechnol Biochem 63:293–297

    Article  PubMed  CAS  Google Scholar 

  • Ng YK, Hodson MP, Hewavitharana AK, Bose U, Shaw PN, Fuerst JA (2014) Effects of salinity on antibiotic production in sponge-derived Salinispora actinobacteria. J Appl Microbiol 117:109–125

    Article  PubMed  CAS  Google Scholar 

  • Palmieri D, Ianiri G, Del Grosso C, Barone G, De Curtis F, Castoria R, Lima G (2022) Advances and perspectives in the use of biocontrol agents against fungal plant diseases. Horticulturae 8:577

    Article  Google Scholar 

  • Paul D, Dineshkumar N, Nair S (2006) Proteomics of a plant growth-promoting rhizobacterium, Pseudomonas fluorescens MSP-393, subjected to salt shock. World J Microbiol Biotechnol 22:369–374

    Article  CAS  Google Scholar 

  • Pennerman KK, Al-Maliki HS, Lee S, Bennett JW (2016) Fungal volatile organic compounds (VOCs) and the genus Aspergillus. In: Gupta V. (ed.): New and future developments in microbial biotechnology and bioengineering: Aspergillus system properties and applications, 1st Edition. Elsevier, pp. 95–115. ISBN: 978-0-444-63505-1

  • Phour M, Sindhu SS (2020) Amelioration of salinity stress and growth stimulation of mustard (Brassica juncea L.) by salt-tolerant Pseudomonas species. Appl Soil Ecol 149:103518

    Article  Google Scholar 

  • Raza W, Ling N, Liu D, Wei Z, Huang Q, Shen Q (2016) Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol Res 192:103–113

    Article  PubMed  CAS  Google Scholar 

  • Rybakova D, Rack-Wetzlinger U, Cernava T, Schaefer A, Schmuck M, Berg G (2017) Aerial warfare: a volatile dialogue between the plant pathogen verticillium longisporum and its antagonist Paenibacillus polymyxa. Front Plant Sci 8:1294

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927–4932

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sapre S, Gontia-Mishra I, Tiwari S (2018) Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol Res 206:25–32

    Article  PubMed  CAS  Google Scholar 

  • Shukla PS, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J Plant Growth Regul 31:195–206

    Article  CAS  Google Scholar 

  • Tyagi S, Lee KJ, Shukla P, Chae JC (2020) Dimethyl disulfide exerts antifungal activity against Sclerotinia minor by damaging its membrane and induces systemic resistance in host plants. Sci Rep 10:1–12

    Google Scholar 

  • Vedamurthy AB, Bhattacharya S, Das A, Shruthi SD (2021) Exploring nanomaterials with rhizobacteria in current agricultural scenario. In: Jogaiah S, Singh HB, Fraceto LF, de Lima R (eds.) Advances in Nano-Fertilizers and Nano-Pesticides in Agriculture, Woodhead Publishing, pp. 487–503. ISBN: 978-0-12-820092-6

  • Vega C, Rodriguez M, Llamas I, Bejar V, Sampedro I (2020) Silencing of phytopathogen communication by the halotolerant PGPR Staphylococcus equorum strain EN21. Microorganisms 8:42

    Article  CAS  Google Scholar 

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Acknowledgements

This work was funded by Sultan Qaboos University, Sultanate of Oman (RF/AGR/CROP/21/02).

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Correspondence to Rethinasamy Velazhahan.

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Al-Rashdi, A., Al-Sadi, A.M., Al-Harrasi, M.A. et al. The effect of NaCl on growth and volatile metabolites produced by antagonistic endophytic bacteria isolated from Prosopis cineraria. Australasian Plant Pathol. 52, 377–384 (2023). https://doi.org/10.1007/s13313-023-00922-y

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