Abstract
Volatile compounds emitted by bacteria can play a significant role in interacting with microorganisms, plants, and other organisms. In this work, we studied the effect of total gaseous mixtures of organic as well as inorganic volatile compounds (VCs) and individual pure volatile organic compounds (VOCs: ketones 2-nonanone, 2-heptanone, 2-undecanone, a sulfur-containing compound dimethyl disulfide) synthesized by the rhizosphere Pseudomonas chlororaphis 449 and Serratia plymuthica IC1270 strains, the soil-borne strain P. fluorescens B-4117, and the spoiled meat isolate S. proteamaculans 94 strain on Arabidopsis thaliana plants (on growth and germination of seeds). We demonstrated that total mixtures of volatile compounds emitted by these strains grown on Luria–Bertani agar, Tryptone Soya Agar, and Potato Dextrose Agar media inhibited the A. thaliana growth. When studied bacteria grew on Murashige and Skoog (MS) agar medium, volatile mixtures produced by bacteria could stimulate the growth of plants. Volatile compounds of bacteria slowed down the germination of plant seeds; in the presence of volatile mixtures of P. fluorescens B-4117, the seeds did not germinate. Of the individual VOCs, 2-heptanone had the most potent inhibitory effect on seed germination. We also showed that the tested VOCs did not cause oxidative stress in Escherichia coli cells using specific lux-biosensors. VOCs reduced the expression of the lux operon from the promoters of the katG, oxyS, and soxS genes (whose products involved in the protection of cells from oxidative stress) caused by the action of hydrogen peroxide and paraquat, respectively.
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References
Ahmad A, Viljoen AM, Chenia HY (2014) The impact of plant volatiles on bacterial quorum sensing. Lett Appl Microbiol 60:8–19. https://doi.org/10.1111/lam.12343
Audrain B, Farag MA, Ryu C-M, Ghigo J-M (2015a) Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Revs 39:222–233. https://doi.org/10.1093/femsre/fuu013
Audrain B, Letoffe S, Ghigo JM (2015b) Airborne bacterial interactions: functions out of thin air? Front Microbiol 6:1476. https://doi.org/10.3389/fmicb.2015.01476
Avalos M, van Wezel GP, Raaijmakers JM, Garbeva P (2018) Healthy scents: microbial volatiles as new frontier in antibiotic research? Curr Opin Microbiol 45:84–91. https://doi.org/10.1016/j.mib.2018.02.011
Bailly A, Weisskopf L (2012) The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal Behav 7:79–85. https://doi.org/10.4161/psb.7.1.18418
Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338. https://doi.org/10.1128/AEM.68.7.3328-3338.2002
Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011a) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058. https://doi.org/10.1111/j.1462-2920.2011.02582.x
Blom D, Fabbri C, Eberl L, Weisskopf L (2011b) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microbiol 77(3):1000–1008. https://doi.org/10.1128/AEM.01968-10
Chernin L, Toklikishvili N, Ovadis M, Kim S, Ben-Ari J, Khmel I, Vainstein A (2011) Quorum-sensing quenching by rhizobacterial volatiles. Environ Microbiol Rep 3:698–704. https://doi.org/10.1111/j.1758-2229.2011.00284.x
Chung J, Song GC, Ryu CM (2016) Sweet scents from good bacteria: Case studies on bacterial volatile compounds for plant growth and immunity. Plant Mol Biol 90:677–687. https://doi.org/10.1007/s11103-015-0344-8
Cordovez V, Mommer L, Moisan K, Lucas-Barbosa D, Pierik R, Mumm R, Carrion VJ, Raaijmakers JM (2017) Plant phenotypic and transcriptional changes induced by volatiles from the fungal root pathogen Rhizoctonia solani. Front Plant Sci 8:1262. https://doi.org/10.3389/fpls.2017.01262
Dandurishvili N, Toklikishvili N, Ovadis M, Eliashvili P, Giorgobiani N, Keshelava R, Tediashvili M, Vainshtein A, Khmel I, Szegedi E, Chernin L (2011) Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J Appl Microbiol 110:341–352. https://doi.org/10.1111/j.1365-2672.2010.04891.x
Demidyuk IV, Kalashnikov AE, Gromova TY, Gasanov EV, Safina DR, Zabolotskaya MV, Rudenskaya GN, Kostrov SV (2006) Cloning, sequencing, expression, and characterization of protealysin, a novel neutral proteinase from Serratia proteamaculans representing a new group of thermolysin-like proteases with short N-terminal region of precursor. Protein Expr Purif 47(2):551–561. https://doi.org/10.1016/j.pep.2005.12.005
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. https://doi.org/10.1007/s10886-012-0135-5
Farr SB, Kogoma T (1991) Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Revs 55:561–585. https://doi.org/10.1128/mr.55.4.561-585.1991
Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75. https://doi.org/10.1016/j.micres.2018.01.002
Imlay JA (2015) Transcription factors that defend bacteria against reactive oxygen species. Annu Rev Microbiol 69:93–108. https://doi.org/10.1146/annurev-micro-091014-104322
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. https://doi.org/10.1007/s00253-008-1760-3
Kang BR, Anderson AJ, Kim YC (2019) Hydrogen cyanide produced by Pseudomonas chlororaphis O6 is a key aphicidal metabolite. Can J Microbiol 65(3):185–190. https://doi.org/10.1139/cjm-2018-0372
Kotova VY, Manukhov IV, Zavilgelskii GB (2010) Lux-biosensors for detection of SOS-response, heat shock, and oxidative stress. Appl Biochem Microbiol 46:781–788. https://doi.org/10.1134/S0003683810080089
Moisan K, Cordovez V, van de Zande EM, Raaijmakers JM, Dicke M, Lucas-Barbosa D (2019) Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects. Oecologia 190:589–604. https://doi.org/10.1007/s00442-019-04433-w
Ovadis M, Liu X, Gavriel S, Ismailov Z, Chet I, Chernin L (2004). The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing, and functional studies. J Bacteriol 186(15):4986–4993. https://doi.org/10.1128/JB.186.15.4986-4993.2004
Piechulla B, Lemfack MC, Kai M (2017) Effects of discrete bioactive microbial volatiles on plants and fungi. Plant, Cell Environ 40:2042–2067. https://doi.org/10.1111/pce.13011
Piechulla B, Lemfack MC, Magnus N (2020) Chapter 2. Bioactive bacterial volatiles: an overview and critical comments. In: Ryu C-M, Weisskopf L, Piechulla B (eds) Bacterial volatile compounds as mediators of airborne interactions. Springer Nature Singapore Pte Ltd, pp 39–92. https://doi.org/10.1007/978-981-15-7293-7_2
Plyuta V, Lipasova V, Popova A, Koksharova O, Kuznetsov A, Szegedi E, Chernin L, Khmel I (2016) Influence of volatile organic compounds emitted by Pseudomonas and Serratia strains on Agrobacterium tumefaciens biofilms. APMIS 124:586–594. https://doi.org/10.1111/apm.12547
Plyuta VA, Chernikova AS, Sidorova DE, Kupriyanova EV, Koksharova OA, Chernin LS, Khmel IA (2021) Modulation of Arabidopsis thaliana growth by volatile substances emitted by Pseudomonas and Serratia strains. World J Microbiol Biotechnol 37:82. https://doi.org/10.1007/s11274-021-03047-w
Popova AA, Koksharova OA, Lipasova VA, Zaitseva JV, Katkova-Zhukotskaya OA, Eremina SI, Mironov AS, Chernin LS, Khmel IA (2014) Inhibitory and toxic effects of volatiles emitted by strains of Pseudomonas and Serratia on growth and survival of selected microorganisms, Caenorhabditis elegans and Drosophila melanogaster. BioMed Res Int Article ID 125704, 11 pages. https://doi.org/10.1155/2014/125704
Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Pare´ PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932. https://doi.org/10.1073/pnas.0730845100
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. https://doi.org/10.1104/pp.103.026583
Sanchez LA, Gomez FF, Delgado OD (2009) Cold-adapted microorganisms as a source of new antimicrobials. Extremophiles 13:111–120. https://doi.org/10.1007/s00792-008-0203-5
Schmidt R, Cordovez V, de Boer W, Raaijmakers J, Garbeva P (2015) Volatile affairs in microbial interactions. ISME J 9:1–7. https://doi.org/10.1038/ismej.2015.42
Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842. https://doi.org/10.1039/B507392H
Schulz S, Dickschat JS, Kunze B, Wagner-Dobler I, Diestel R, Sasse F (2010) Biological activity of volatiles from marine and terrestrial bacteria. Mar Drugs 8:2976–2987. https://doi.org/10.3390/md8122976
Schulz-Bohm K, Martín-Sánchez L, Garbeva P (2017) Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front Microbiol 8:2484. https://doi.org/10.3389/fmicb.2017.02484
Sharifi R, Ryu CM (2018) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 122:349–358. https://doi.org/10.1093/aob/mcy108
Sharifi R, Ryu C-M (2020) Chapter 14. Formulation and agricultural application of bacterial volatile compounds. In: Ryu C-M, Weisskopf L, Piechulla B (eds) Bacterial volatile compounds as mediators of airborne interactions. Springer Nature Singapore Pte Ltd, pp 317–336
Tyc O, Song C, Dickschat JS, Vos M, Garbeva P (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25:280–292. https://doi.org/10.1016/j.tim.2016.12.002
Veselova M, Lipasova V, Protsenko MA, Buza N, Khmel IA (2009) GacS-dependent regulation of enzymic and antifungal activities and synthesis of N-acylhomoserine lactones in rhizospheric strain Pseudomonas chlororaphis 449. Folia Microbiol (Praha) 54(5):401–408. https://doi.org/10.1007/s12223-009-0056-z
Weisskopf L, Schulz S, Garbeva P (2021) Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions. Nat Rev Microbiol 19:391–404. https://doi.org/10.1038/s41579-020-00508-1
Zavilgelsky GB, Zarubina AP, Manukhov IV (2002) Sequencing and comparative analysis of the lux operon of Photorhabdus luminescens Strain Zm1: ERIC Elements as Putative Recombination Hot Spots. Mol Biol 36:637–647. https://doi.org/10.1023/A:1020663128043
Zhang C, Zhang M, Yan Z, Wang F, Yuan X, Zhao S, Zhang L, Tian H, Ding Z (2021) CO2 is a key constituent of the plant growth-promoting volatiles generated by bacteria in a sealed system. Plant Cell Rep 40:59–68. https://doi.org/10.1007/s00299-020-02610-3
Acknowledgements
The authors are grateful to Dr. Kupriyanova E.V. for providing the collection seeds of Arabidopsis thaliana.
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This study was funded partially within the state assignment of the NRC “Kurchatov Institute” — IMG for 2021–2022 (no. 121030200227-6).
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Conceptualization, I. A. K. and V. A. P; methodology, I. A. K., V. A. P., D. E. S.; formal analysis, D. E. S., V. A. P., I. A. K.; investigation, D. E. S., A. S. C., T. A. C.; writing — original draft preparation, I. A. K. and D. E. S., A. S. C., T. A. C.; writing — review and editing, V. A. P., I. A. K., D. E. S.; funding acquisition, I. A. K.; resources, I. A. K. and V. A. P.; supervision, I. A. K. and V. A. P.; project administration, I. A. K. and D. E. S. All authors have read and agreed to the published version of the manuscript.
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Sidorova, D.E., Khmel, I.A., Chernikova, A.S. et al. Biological activity of volatiles produced by the strains of two Pseudomonas and two Serratia species. Folia Microbiol 68, 617–626 (2023). https://doi.org/10.1007/s12223-023-01038-y
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DOI: https://doi.org/10.1007/s12223-023-01038-y