The symbiotic bacterium Serratia liquefaciens enhances the development of Bacillus thuringiensis bacteriosis in Colorado potato beetle larvae by alkalinization of pH in the midgut
- 作者: Artemchenko A.S.1,2, Klementeva T.N.1, Khodyrev V.P.1, Sitnikov V.N.3, Glupov V.V.1, Polenogova O.V.1
-
隶属关系:
- Institute of Animal Systematics and Ecology SB RAS
- Novosibirsk State University
- Stavropol State Agrarian University
- 期: 卷 94, 编号 2 (2025)
- 页面: 185–194
- 栏目: EXPERIMENTAL ARTICLES
- URL: https://gynecology.orscience.ru/0026-3656/article/view/680840
- DOI: https://doi.org/10.31857/S0026365625020077
- ID: 680840
如何引用文章
详细
Abstarct. Invasion by pathogens is accompanied by competitive interactions between the pathogens and the microbiota, by the allocation of a niche in the intestine for the pathogen, and induction of immune processes in the host organism. These processes are accompanied by the accumulation of microbiota secondary metabolites, which may result in alterations of physicochemical characteristics of the host gut. These events may affect the speed of progression of bacterial infections, including secondary bacterial infections. In this study, experimental evidence showed that within the initial 24-h period, both in vitro and in vivo, interaction between Bacillus thuringiensis (Bt) and the symbiotic bacterium Serratia liquefaciens caused alkalization of the medium: both the culture fluid and the midgut contents of the Colorado potato beetle (CPB). Combined oral administration of S. liquefaciens and Bt resulted in 83% mortality of CPB larvae as early as 48 h after the inoculation. This mortality rate was 8.3-fold higher than that (<10%) observed in individuals infected with Bt alone. Provision of food treated with Bt and a peptide fraction of S. liquefaciens metabolites to CPB larvae had analogous synergistic effects on mortality. It is possible that during an invasion by pathogens under conditions of the gut microbiota, there is an increase in the production of metabolites that can result in a release of inhibitors into the local medium. These inhibitors may then act as activators of Bt endotoxins (Cry toxins). This hypothesis requires further research.
全文:

作者简介
A. Artemchenko
Institute of Animal Systematics and Ecology SB RAS; Novosibirsk State University
Email: ovp0408@yandex.ru
俄罗斯联邦, Novosibirsk, 630091; Novosibirsk, 630090
T. Klementeva
Institute of Animal Systematics and Ecology SB RAS
Email: ovp0408@yandex.ru
俄罗斯联邦, Novosibirsk, 630091
V. Khodyrev
Institute of Animal Systematics and Ecology SB RAS
Email: ovp0408@yandex.ru
俄罗斯联邦, Novosibirsk, 630091
V. Sitnikov
Stavropol State Agrarian University
Email: ovp0408@yandex.ru
俄罗斯联邦, Stavropol, 355035
V. Glupov
Institute of Animal Systematics and Ecology SB RAS
Email: ovp0408@yandex.ru
俄罗斯联邦, Novosibirsk, 630091
O. Polenogova
Institute of Animal Systematics and Ecology SB RAS
编辑信件的主要联系方式.
Email: ovp0408@yandex.ru
俄罗斯联邦, Novosibirsk, 630091
参考
- Akiba Y., Sekijima,Y., Aizawa K., Fujiyoshi N. Microbial ecological studies on Bacillus thuringiensis III. Effect of pH on the growth of Bacillus thuringiensis in soil extracts // Jpn. J. Appl. Entomol. Zool. 1979. V. 23. P. 220–223. https://doi.org/10.1303/jjaez.23.220
- Alyokhin A. Y., Chen H., Udalov M., Benkovskaya G., Lindstrom L. Evolutionary considerations in potato pest management // Insect pests of potato: global perspectives on biology and management / Eds. Giordanengo P., Vincent C., Alyokhin A. Oxford, UK: Academic Press, 2013. P. 543–571. https://doi.org/10.1016/B978-0-12-386895-4.00019-3
- Arzumanov E. N. Effect of pH on the growth of Bacillus thuringiensis // Mikrobiologiia. 1979. V. 48. P. 65–69.
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding // Anal. Biochem. 1976. V. 72. P. 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
- Bravo A., Gill S. S., Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control // Toxicon. 2007. V. 49. P. 423–435. https://doi.org/10.1016/j.toxicon.2006.11.022
- Broderick N. A., Raffa K. F., Handelsman J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity // Proc. Natl. Acad. Sci. USA. 2006. V. 103. P. 15196–15199. https://doi.org/10.1073/pnas.0604865103
- Broderick N. A., Robinson C. J., McMahon M.D., Holt J., Handelsman J., Raffa K. F. Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera // BMC Biology. 2009. V. 7. P. 1–9. https://doi.org/10.1186/1741-7007-7-11
- Caccia S., Di Lelio I., La Storia A., Marinelli A., Varricchio P., Franzetti E., Banyuls N., Tettamanti G., Casartelli M., Giordana B., Ferré J., Gigliotti S., Ercolini D., Pennacchio F. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism // Proc. Natl. Acad. Sci. USA. 2016. V. 113. P. 9486–9491. https://doi.org/10.1073/pnas.1521741113
- Chowdhury N., Hazarika D. J., Goswami G., Sarmah U., Borah S., Boro R. C., Barooah M. Acid tolerant bacterium Bacillus amyloliquefaciens MBNC retains biocontrol efficiency against fungal phytopathogens in low pH // Arch. Microbiol. 2022. V. 204. Art. 124. https://doi.org/10.1007/s00203-021-02741-5
- Chung S. H., Scully E. D., Peiffer M., Geib S. M., Rosa C., Hoover K., Felton G. W. Host plant species determines symbiotic bacterial community mediating suppression of plant defenses // Sci. Rep. 2017. V. 7. Art. 39690. https://doi.org/10.1038/srep39690
- Dawson R. M.C., Elliott D. C., Elliot W. H., Jones K. M. (Eds.). Data for Biochemical Research. London: Oxford University Press, 1969. P. 670. ISBN-10: 0198553382. ISBN-13: 978-0198553380.
- Dias S., Sagardoy M. A. Influence of pH on the toxicity and survival of total cells and spores of Bacillus thuringiensis // Rev. Argent. Microbiol. 1998. V. 30. P. 122–129.
- Eida A. A., Bougouffa S., L’Haridon F., Alam I., Weisskopf L., Bajic V. B., Saad M. M., Hirt H. Genome insights of the plant-growth promoting bacterium Cronobacter muytjensii JZ38 with volatile-mediated antagonistic activity against Phytophthora infestans // Front. Microbiol. 2020. V. 11. Art. 369. https://doi.org/10.3389/fmicb.2020.00369
- Gayatri Priya N., Ojha A., Kajla M. R., Raj A., Rajagopal R. Host plant induced variation in gut bacteria of Helicoverpa armigera // PloS One. 2012. V. 7. Art. e30768. https://doi.org/10.1371/journal.pone.0030768
- Göldel B., Lemic D., Bažok R. Alternatives to synthetic insecticides in the control of the Colorado potato beetle (Leptinotarsa decemlineata Say) and their environmental benefits // Agriculture. 2020. V. 10. Art. 611. https://doi.org/10.3390/agriculture10120611
- Green E. R., Mecsas J. Bacterial secretion systems: an overview // Virulence Mechanisms of Bacterial Pathogens / Eds. Kudva I. T., Cornick N. A., Plummer P. J., Zhang Q., Nicholson T. L., Bannantine J. P., Bellaire B. H. USA: ASM Press, 2016. P. 213–239. https://doi.org/10.1128/9781555819286.ch8
- Grimont F., Grimont P. A. The genus Serratia // Prokaryotes / Eds. Dworkin M., Falkow S., Rosenberg E., Schleifer K. H., Stackebrandt E. New York: Springer, 2006. https://doi.org/10.1007/0-387-30746-X_11
- Gupta U., Dey P. Rise of the guardians: gut microbial maneuvers in bacterial infections // Life Sci. 2023. V. 330. Art. 121993. https://doi.org/10.1016/j.lfs.2023.121993
- Höfte H., Whiteley H. R. Insecticidal crystal proteins of Bacillus thuringiensis // Microbiol. Rev. 1989. V. 53. P. 242–255. https://doi.org/10.1128/mr.53.2.242-255.1989
- Kamada N., Chen G. Y., Inohara N., Núñez G. Control of pathogens and pathobionts by the gut microbiota // Nat. Immunol. 2013. V. 14. P. 685–690. https://doi.org/10.1038/ni.2608
- Keswani C., Singh H. B., García-Estrada C., Caradus J., He Y. W., Mezaache-Aichour S., Borris R. Sansinenea E. Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides // Appl. Microbiol. Biotechnol. 2020. V. 104. P. 1013–1034. https://doi.org/10.1007/s00253-019-10300-8
- Koller C. N., Bauer L. S., Hollingworth R. M. Characterization of the pH-mediated solubility of Bacillus thuringiensis var. san diego native δ-endotoxin crystals // Biochem. Biophys. Res. Commun. 1992. V. 184. P. 692–699. https://doi.org/10.1016/0006-291x(92)90645-2
- Li S., De Mandal S., Xu X., Jin F. The tripartite interaction of host immunity–Bacillus thuringiensis infection–gut microbiota // Toxins. 2020. V. 12. Art. 514. https://doi.org/10.3390/toxins12080514
- Maal K. B., Emtiazi G., Nahvi I. Increasing the alkaline protease activity of Bacillus cereus and Bacillus polymyxa simultaneously with the start of sporulation phase as a defense mechanism // Afr. J. Biotechnol. 2011. V. 10. P. 3894–3901. https://doi.org/10.5897/AJB10.774
- Mai A. G.M. Serratia a novel source of secondary metabolites // Adv. Biotechnol. Microbiol. 2018. V. 11. P. 83–87. https://doi.org/10.19080/AIBM.2018.11.555814
- Malovichko Y. V., Nizhnikov A. A., Antonets K. S. Repertoire of the Bacillus thuringiensis virulence factors unrelated to major classes of protein toxins and its role in specificity of host-pathogen interactions // Toxins. 2019. V. 11. Art. 347. https://doi.org/10.3390/toxins11060347
- Melo A. L.A., Soccol V. T., Soccol C. R. Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review // Crit. Rev. Biotechnol. 2016. V. 36. P. 317–326. https://doi.org/10.3109/07388551.2014.960793
- Michaud D., Bernier-Vadnais N., Overney S., Yelle S. Constitutive expression of digestive cysteine proteinase forms during development of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) // Insect Biochem. Mol. Biol. 1995. V. 25. P. 1041–1048. https://doi.org/10.1016/0965-1748(95)00044-V
- Muratoglu H., Demirbag Z., Sezen K. The first investigation of the diversity of bacteria associated with Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) // Biologia. 2011. V. 66. P. 288–293. https://doi.org/10.2478/s11756-011-0021-6
- Obeidat M., Khyami-Horani H., Al-Momani F. Toxicity of Bacillus thuringiensis β-exotoxins and δ-endotoxins to Drosophila melanogaster, Ephestia kuhniella and human erythrocytes // Afr. J. Biotechnol. 2012. V. 11. P. 10504–10512. https://doi.org/10.5897/AJB11.2260
- Palma L., Muñoz D., Berry C., Murillo J., Caballero P. Bacillus thuringiensis toxins: an overview of their biocidal activity // Toxins. 2014. V. 6. P. 3296–3325. https://doi.org/10.3390/toxins6123296
- Polenogova O. V., Noskov Y. A., Yaroslavtseva O. N., Kryukova N. A., Alikina T., Klementeva T. N., Andrejeva J., Khodyrev V. P., Kabilov M. R., Kryukov V. Y., Glupov V. V. Influence of Bacillus thuringiensis and avermectins on gut physiology and microbiota in Colorado potato beetle: impact of enterobacteria on susceptibility to insecticides // PLoS One. 2021. V. 16. Art. e0248704. https://doi.org/10.1371/journal.pone.0248704
- Polenogova O. V., Noskov Y. A., Artemchenko A. S., Zhangissina S., Klementeva T. N., Yaroslavtseva O. N., Khodyrev V. P., Kruykova N. A., Glupov V. V. Citrobacter freundii, a natural associate of the Colorado potato beetle, increases larval susceptibility to Bacillus thuringiensis // Pest. Manag. Sci. 2022. V. 78. P. 3823–3835. https://doi.org/10.1002/ps.6856
- Robertson J. L., Preisler H. K. Pesticide bioassays with arthropods. Boca Raton: CRC, 1992. https://doi.org/10.1201/9781315373775
- Sablon L., Haubruge E., Verheggen F. J. Consumption of immature stages of Colorado potato beetle by Chrysoperla carnea (Neuroptera: Chrysopidae) larvae in the laboratory // Am. J. Potato Res. 2013. V. 90. P. 51–57. https://doi.org/10.1007/s12230-012-9275-y
- Sánchez-Clemente R., Igeño M., Población A. G., Guijo M. I., Merchán F., Blasco R. Study of pH changes in media during bacterial growth of several environmental strains // Proceedings. 2018. V. 2. Art. 1297. https://doi.org/10.3390/PROCEEDINGS2201297
- Tran P., Lander S. M., Prindle A. Active pH regulation facilitates Bacillus subtilis biofilm development in a minimally buffered environment // mBio. 2024. V. 15. Art. e0338723. https://doi.org/10.1128/mbio.03387-23
- Waites W., Kay D., Dawes I., Wood D., Warren S. C., Mandelstam J. Sporulation in Bacillus subtilis. Correlation of biochemical events with morphological changes in asporogenous mutants // Biochem. J. 1970. V. 118. P. 667–676. https://doi.org/10.1042/BJ1180667
- Weiss B. L. Maltz M. A., Vigneron A., Wu Y., Walter K. S., O’Neill M.B., Wang J., Aksoy S. Colonization of the tsetse fly midgut with commensal Kosakonia cowanii Zambiae inhibits trypanosome infection establishment // PLoS Pathog. 2019. V. 15. Art. e1007470. https://doi.org/10.1371/journal.ppat.1007470
- West A. W., Burges H. D., Dixon T. J., Wyborn C. H. Survival of Bacillus thuringiensis and Bacillus cereus spore inocula in soil: effects of pH, moisture, nutrient availability and indigenous microorganisms // Soil Biol. Biochem. 1985. V. 17. P. 657–665. https://doi.org/10.1016/0038-0717(85)90043-4
- Xiang Q., Zhu D., Chen Q.-L., Delgado-Baquerizo M., Su J.-Q., Qiao M., Yang X.-R., Zhu Y.-G. Effects of diet on gut microbiota of soil collembolans // Sci. Total Environ. 2019. V. 676. P. 197–205. https://doi.org/10.1016/j.scitotenv.2019.04.104
- Yu Y., Wang Y., Li H., Yu X., Shi W., Zhai J. Comparison of microbial communities in Colorado potato beetles (Leptinotarsa decemlineata say) collected from different sources in China // Front. Microbiol. 2021. V. 12. Art. 639913. https://doi.org/10.3389/fmicb.2021.639913
- Yun J. H., Roh S. W., Whon T. W., Jung M. J., Kim M. S., Park D. S., Yoon C., Nam Y. D., Kim Y. J., Choi J. H., Kim J. Y., Shin N. R., Kim S. H., Lee W. J., Bae J. W. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host // Appl. Environ. Microbiol. 2014. V. 80. P. 5254–5264. https://doi.org/10.1128/AEM.01226-14
- Zheng H., Powell J. E., Steele M. I., Dietrich C., Moran N. A. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling // Proc. Natl. Acad. Sci. USA. 2017. V. 114. P. 4775–4780. https://doi.org/10.1073/pnas.1701819114
补充文件
