Abstract
This study investigated the pathogenic potential of Pseudomonas protegens on mosquito larvae of the two species Culex pipiens and Aedes albopictus, representing major threats for disease transmission in the Mediterranean area and worldwide. The bacterium achieved to kill over 90% of the mosquito larvae within 72 h after exposition to a bacterial concentration of 100 million CFU/ml. These lethal effects were concentration dependent and a significantly higher susceptibility was associated with younger larvae of both mosquito species. Significant slowdown of immature (larval and pupal) development and decrease in adult emergence rate after treatment with sub-lethal doses of the bacterium were also detected. This study reports for the first time the insecticidal activity of a root-associated biocontrol bacterium against aquatic mosquito larvae.
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Data generated and analysed during this study are available from authors under reasonable request.
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References
Ruiu L (2020) Plant-growth-promoting bacteria (PGPB) against insects and other agricultural pests. Agronomy 10:861. https://doi.org/10.3390/agronomy10060861
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319. https://doi.org/10.1038/nrmicro1129
Philmus B, Shaffer BT, Kidarsa TA, Yan Q, Raaijmakers JM, Begley TP, Loper JE (2015) Investigations into the Biosynthesis, Regulation, and Self-Resistance of Toxoflavin in Pseudomonas protegens Pf-5. ChemBioChem 16:1782–1790. https://doi.org/10.1002/cbic.201500247
Ramette A, Frapolli M, Fischer-Le Saux M, Gruffaz C, Meyer JM, Défago G et al (2011) Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2, 4-diacetylphloroglucinol and pyoluteorin. Syst Appl Microbiol 34:180–188. https://doi.org/10.1016/j.syapm.2010.10.005
Flury P, Aellen N, Ruffner B, Péchy-Tarr M, Fataar S, Metla Z, Dominguez-Ferreras A, Bloemberg G, Frey J, Goesmann A et al (2016) Insect pathogenicity in plant-beneficial pseudomonads: Phylogenetic distribution and comparative genomics. ISME J 10:2527–2542. https://doi.org/10.1038/ismej.2016.5
Vesga P, Flury P, Vacheron J, Keel C, Croll D, Maurhofer M (2020) Transcriptome plasticity underlying plant root colonization and insect invasion by Pseudomonas protegens. ISME J 14:2766–2782. https://doi.org/10.1038/s41396-020-0729-9
Ruiu L, Marche MG, Mura ME, Tarasco E (2022) Involvement of a novel Pseudomonas protegens strain associated with entomopathogenic nematode infective juveniles in insect pathogenesis. Pest Manag Sci 78:5437–5443. https://doi.org/10.1002/ps.7166
Ruiu L, Mura ME (2021) Oral toxicity of Pseudomonas protegens against muscoid flies. Toxins 13:772. https://doi.org/10.3390/toxins13110772
Flury P, Vesga P, Dominguez-Ferreras A, Tinguely C, Ullrich CI, Kleespies RG et al (2019) Persistence of root-colonizing Pseudomonas protegens in herbivorous insects throughout different developmental stages and dispersal to new host plants. ISME J 13:860–872. https://doi.org/10.1038/s41396-018-0317-4
Thomas WE, Ellar DJ (1983) Mechanism of action of Bacillus thuringiensis var israelensis insecticidal delta-endotoxin. FEBS Lett 154:362–368. https://doi.org/10.1016/0014-5793(83)80183-5
Darboux I, Nielsen-LeRoux C, Charles JF, Pauron D (2001) The receptor of Bacillus sphaericus binary toxin in Culex pipiens (Diptera: Culicidae) midgut: molecular cloning and expression. Insect Biochem Mol Biol 31:981–990. https://doi.org/10.1016/S0965-1748(01)00046-7
Paul A, Harrington LC, Zhang L, Scott JG (2005) Insecticide resistance in Culex pipiens from New York. J Am Mosq Control Assoc 21:305–309. https://doi.org/10.2987/8756-971X(2005)21[305:IRICPF]2.0.CO;2
Su T, Thieme J, Ocegueda C, Ball M, Cheng ML (2018) Resistance to Lysinibacillus sphaericus and other commonly used pesticides in Culex pipiens (Diptera: Culicidae) from Chico. California J Med Entomol 55:423–428. https://doi.org/10.1093/jme/tjx235
Myasnik M, Manasherob R, Ben-Dov E, Zaritsky A, Margalith Y, Barak Z (2001) Comparative sensitivity to UV-B radiation of two Bacillus thuringiensis subspecies and other Bacillus sp. Curr Microbiol 43:140–143. https://doi.org/10.1007/s002840010276
Ruiu L, Virdis B, Mura ME, Floris I, Satta A, Tarasco E (2017) Oral insecticidal activity of new bacterial isolates against insects in two orders. Biocontrol Sci Technol 2:886–902. https://doi.org/10.1080/09583157.2017.1355964
Stutz EW, Défago G, Kern H (1986) Naturally occurring fluorescent Pseudomonads involved in suppression. Phytopathology 76:181–185. https://doi.org/10.1094/Phyto-76-181
Ledda S, Foxi C, Puggioni G, Bechere R, Rocchigiani AM, Scivoli R et al (2023) Experimental infection of Aedes (Stegomyia) albopictus and Culex pipiens mosquitoes with Bluetongue virus. Med Vet Entomol 37:105–110. https://doi.org/10.1111/mve.12613
Bedini S, Muniz ER, Tani C, Conti B, Ruiu L (2020) Insecticidal potential of Brevibacillus laterosporus against dipteran pest species in a wide ecological range. J Invertebr Pathol 177:107493. https://doi.org/10.1016/j.jip.2020.107493
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Keel C (2016) A look into the toolbox of multi-talents: insect pathogenicity determinants of plant-beneficial pseudomonads. Environ Microbiol 18:3207–3209. https://doi.org/10.1111/1462-2920.13462
Kupferschmied P, Maurhofer M, Keel C (2013) Promise for plant pest control: root-associated pseudomonads with insecticidal activities. Front Plant Sci 4:287. https://doi.org/10.3389/fpls.2013.00287
Ruffner B, Péchy-Tarr M, Höfte M, Bloemberg G, Grunder J, Keel C, Maurhofer M (2015) Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus. BMC Genomics 16:1–14. https://doi.org/10.1186/s12864-015-1763-2
Jurat-Fuentes JL, Jackson TA (2012) Bacterial entomopathogens. In: Tanada Y, Kaya HK (eds) Insect pathology. Academic press Inc., San Diego, pp 265–349
Job V, Gomez-Valero L, Renier A, Rusniok C, Bouillot S, Chenal-Francisque V, Gueguen E, Adrait A, Robert-Genthon M, Jeannot K, Panchev P, Elsen S, Fauvarque M-O, Couté Y, Buchrieser C, Attrée I (2022) Genomic erosion and horizontal gene transfer shape functional differences of the ExlA toxin in Pseudomonas spp. Iscience 25:104596. https://doi.org/10.1016/j.isci.2022.104596
Bedini S, Conti B, Hamze R, Muniz ER, Fernandes ÉK, Ruiu L (2021) Lethal and sub-lethal activity of Brevibacillus laterosporus on the mosquito Aedes albopictus and side effects on non-target water-dwelling invertebrates. J Invertebr Pathol 184:107645. https://doi.org/10.1016/j.jip.2021.107645
Hamze R, Nuvoli MT, Pirino C, Ruiu L (2022) Compatibility of the bacterial entomopathogen Pseudomonas protegens with the natural predator Chrysoperla carnea (Neuroptera: Chrysopidae). J Invertebr Pathol 194:107828. https://doi.org/10.1016/j.jip.2022.107828
Preethi SV, Pandian RS (2009) Evaluation of the larvicidal and pupicidal activities of the exotoxin of Pseudomonas fluorescens Migula against Aedes aegypti (L.) and Culex quinquefasciatus Say. Curr Biot 3:416–438
Roy M, Chatterjee SN, Roy P, Dangar TK (2010) Significance of the midgut bacterium Pseudomonas fluorescens on Culex vishnui (Diptera: Culicidae) larval development. Int J Trop Insect Sci 30:182–185. https://doi.org/10.1017/S1742758410000366
Wang YT, Shen RX, Xing D, Zhao CP, Gao HT, Wu JH et al (2021) Metagenome sequencing reveals the midgut microbiota makeup of Culex pipiens quinquefasciatus and its possible relationship with insecticide resistance. Front Microbiol 12:625539. https://doi.org/10.3389/fmicb.2021.625539
Agaras BC, Wall LG, Valverde C (2017) Pseudomonas communities in soil agroecosystems. In: Singh HB, Sarma BK, Keswani C (eds) Advances in PGPR Research, 1st edn. CAB International, Boston, pp 126–147
Acknowledgements
We would like to warmly thank Dr Christoph Keel from Université de Lausanne (Switzerland) for kindly providing the Pseudomonas protegens strain CHA0.
Funding
This study was supported by Fondazione di Sardegna, grant 2017, project “Insect Microbiome Resources” and by Department of Hygiene and Health and Social Welfare, Autonomous Region of Sardinia, RAS AOO 12-01-00 Convention n. 21 Prot. n. 22656 of 10/10/2022.
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RH and LR: carried out the laboratory investigation, data curation, and wrote the original manuscript. CF, SL, and GS: conducted insect rearing and contributed to investigation. All authors reviewed and approved the final version of the paper.
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Hamze, R., Foxi, C., Ledda, S. et al. Pseudomonas protegens Affects Mosquito Survival and Development. Curr Microbiol 80, 172 (2023). https://doi.org/10.1007/s00284-023-03291-3
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DOI: https://doi.org/10.1007/s00284-023-03291-3