Control Potentials of Three Entomopathogenic Bacterial Isolates for the Carob Moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae) in Pomegranates
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains
2.2. Insects
2.3. Bioassay for Larvicidal Activity
2.4. Gas Chromatography–Mass Spectrometry (GC-MS) Analysis
2.5. Statistical Analysis
3. Results
3.1. Larvicidal Activity of Bacterial Filtrates on E. ceratoniae
3.2. Larvicidal Activity of Bacterial Cells on E. ceratoniae
3.3. Comparison of the Effect of the Bacterial Filtrate and Bacterial Cells on the Larval Mortality of E. ceratoniae
3.4. Lethal Concentration and Time of the Bacterial Filtrate and Cells in the Larval Mortality of E. ceratoniae
3.5. GC-MS Analysis of the Bacterial Cell-Free Supernatant
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Day, K.R.; Wilkins, E.D. Commercial Pomegranate (Punica granatum L.) Production in California. Acta Hort. 2011, 890, 275–286. [Google Scholar] [CrossRef]
- Braham, M. Insect Larvae Associated with Dropped Pomegranate Fruits in an Organic Orchard in Tunisia. J. Entomol. Nematol. 2015, 7, 5–10. [Google Scholar]
- Hoseini, S.A.; Goldansaz, S.H.; Sadeghhasani, S.; Mousavi, S.G. A Field Screening of 10 High Yield Pomegranate Cultivars for Resistance to the Carob Moth, Ectomyelois ceratoniae, in the Climate Condition of Karaj, Alborz, Iran. In Proceedings of the 21st Iranian Plant Protection Congress, Urmia, Iran, 23–26 August 2014. [Google Scholar]
- Dhouibi, M.H. Lutte Intégrée Pour la Protection du Palmier Dattier en Tunisie; Centre de Publication Universitaire: Tunis, Tunisia, 2000. [Google Scholar]
- Shakeri, M. Carob Moth and Its Control Methods; Yazd Utilization Publishing: Yazd, Iran, 2005. [Google Scholar]
- Pertot, I.; Caffi, T.; Rossi, V.; Mugnai, L.; Hoffmann, C.; Grando, M.S.; Gary, C.; Lafond, D.; Duso, C.; Thiery, D.; et al. A Critical Review of Plant Protection Tools for Reducing Pesticide Use on Grapevine and New Perspectives for the Implementation of IPM in Viticulture. Crop Prot. 2017, 97, 70–84. [Google Scholar] [CrossRef]
- Brivio, M.F.; Mastore, M. Nematobacterial Complexes and Insect Hosts: Different Weapons for the Same War. Insects 2018, 9, 117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grewal, P.S.; Ehlers, R.U.; Shapiro-Ilan, D.I. Nematodes as Biological Control Agents. CABI Publishing: Wallingford, UK, 2005. [Google Scholar]
- Koppenhofer, A.M. Nematodes. In Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests, 3rd ed.; Lacey, L.A., Kaya, H.K., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 249–264. [Google Scholar]
- Nour El-Deen, A.H.; Al-Barty, A.F.; Darwesh, H.Y.; Al-Ghamdi, A.S. Eco-Friendly Management of Root-Knot Nematode, Meloidogyne incognita Infecting Pomegranate at Taif Governorate, KSA. Res. J. Pharm. Biol. Chem. Sci. 2016, 7, 1070–1076. [Google Scholar]
- Akhurst, R.; Bedding, R.A. Natural Occurrence of Insect Pathogenic Nematodes (Steinernematidae and Heterorhabditidae) in Soil in Australia. J. Austr. Entomol. Soc. 1986, 25, 241–244. [Google Scholar] [CrossRef]
- Koppler, K.; Peters, A.; Vogt, H. Initial Results in the Application of Entomopathogenic Nematodes against the European Cherry Fruit Fly Rhagoletis cerasi L. (Diptera: Tephritidae). IOBC/WPRS Bull. 2003, 23, 13–18. [Google Scholar]
- Herz, A.; Koppler, K.; Vogt, H.; Elias, E.; Katz, P.; Peters, A. Biological Control of the Cherry Fruit Fly, Rhagoletis cerasi L. (Diptera, Tephritidae) by Use of Entomopathogenic Nematodes: First Experiences Towards Practical Implementation. In Proceedings of the 12th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit Growing (Eco-fruit), Weinsberg, Germany, 18–20 February 2006; Boos, M., Ed.; Foerdergemeinschaft Oekologischer Obstbau: Weinsberg, Germany; Kernen, Germany; pp. 67–72. [Google Scholar]
- Alghamdi, A.S.; Nour El-Deen, A.H.; Al-Barty, A.F.; Hassan, M.M. Toxicity of Some Plant Extracts and Entomopathogenic Nematode against Pomegranate Aphid, Aphis punicae under Laboratory Condition. Annu. Res. Rev. Biol. 2017, 21, 1–6. [Google Scholar] [CrossRef]
- Fuchs, S.W.; Grundmann, F.; Kurz, M.; Kaiser, M.; Bode, H.B. Fabclavines: Bioactive Peptide–Polyketide-Polyamino Hybrids from Xenorhabdus. Chembiochem 2014, 15, 512–516. [Google Scholar] [CrossRef] [PubMed]
- Abbott, W.S. A Method of Computing the Effectiveness Insecticides. J. Econ. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
- Finney, D.J. Probit Analysis; University Press: Cambridge, UK, 1971. [Google Scholar]
- Yooyangket, T.; Muangpat, P.; Polseela, R.; Tandhavanant, S.; Thanwisai, A.; Vitta, A. Identification of Entomopathogenic Nematodes and Symbiotic Bacteria from Nam Nao National Park in Thailand and Larvicidal Activity of Symbiotic Bacteria against Aedes aegypti and Aedes albopictus. PLoS ONE 2018, 13, e0195681. [Google Scholar] [CrossRef]
- Memari, Z.; Javad, K.; Shokoofeh, K.; Seyed, H.G.; Mojtaba, H. Are Entomopathogenic Nematodes Effective Biological Control Agents against the Carob Moth, Ectomyelois ceratoniae? J. Nematol. 2016, 48, 261–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elbrense, H.; Elmasry, A.M.; Seleiman, M.F.; AL-Harbi, M.S.; Abd El-Raheem, A.M. Can Symbiotic Bacteria (Xenorhabdus and Photorhabdus) Be More Efficient than Their Entomopathogenic Nematodes against Pieris rapae and Pentodon algerinus Larvae? Biology 2021, 10, 999. [Google Scholar] [CrossRef] [PubMed]
- Salvadori, J.D.; Defferrari, M.S.; Ligabue-Braun, R.; Lau, E.Y.; Salvadori, J.R.; Carlini, C.R. Characterization of Entomopathogenic Nematodes and Symbiotic Bacteria Active Against Spodoptera frugiperda (Lepidoptera: Noctuidae) and Contribution of Bacterial Urease to the Insecticidal Effect. Biol. Control 2012, 63, 253–263. [Google Scholar] [CrossRef] [Green Version]
- Fukruksa, C.; Yimthin, T.; Suwannaroj, M.; Muangpat, P.; Tandhavanant, S.; Thanwisai, A.; Vitta, A. Isolation and Identification of Xenorhabdus and Photorhabdus Bacteria Associated with Entomopathogenic Nematodes and Their Larvicidal Activity against Aedes aegypti. Parasit Vectors 2017, 10, 440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dillman, A.R.; Guillermin, M.L.; Lee, J.H.; Kim, B.; Sternberg, P.W.; Hallem, E.A. Olfaction Shapes Host-Parasite Interactions in Parasitic Nematodes. Proc. Natl. Acad. Sci. USA 2012, 109, E2324–E2333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Daborn, P.J.; Waterfield, N.; Silva, C.P.; Au, C.P.Y.; Sharma, S.; Ffrench-Constant, R.H. A Single Photorhabdus Gene, Makes Caterpillars Floppy (mcf), Allows Escherichia coli to Persist within and Kill Insects. Proc. Natl. Acad. Sci. USA 2002, 99, 10742–10747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dowling, A.J.; Waterfield, N.R.; Hares, M.C.; Le Goff, G.; Streuli, C.H.; Ffrench-Constant, R.H. The Mcf1 Toxin Induces Apoptosis via the Mitochondrial Pathway and Apoptosis is Attenuated by Mutation of the BH3-like Domain. Cell. Microbiol. 2007, 9, 2470–2484. [Google Scholar] [CrossRef] [PubMed]
- Tobias, N.J.; Wolff, H.; Djahanschiri, B.; Grundmann, F.; Kronenwerth, M.; Shi, Y.M.; Simonyi, S.; Grün, P.; Shapiro-Ilan, D.; Pidot, S.J.; et al. Natural Product Diversity Associated with the Nematode Symbionts Photorhabdus and Xenorhabdus. Nat Microbiol. 2017, 2, 1676–1685. [Google Scholar] [CrossRef]
- Kegler, C.; Bode, H.B. Artificial Splitting of a Non-Ribosomal Peptide Synthetase by Inserting Natural Docking Domains. Angew. Chem. 2020, 59, 13463–13467. [Google Scholar] [CrossRef]
- Wolff, H.; Bode, H.B. The Benzodiazepine-like Natural Product Tilivalline is Produced by the Entomopathogenic Bacterium Xenorhabdus eapokensis. PLoS ONE 2018, 13, e0194297. [Google Scholar]
- Eom, S.; Park, Y.; Kim, Y. Sequential Immunosuppressive Activities of Bacterial Secondary Metabolites From the Entomopahogenic Bacterium Xenorhabdus nematophila. J. Microbiol. 2014, 529, 161–168. [Google Scholar] [CrossRef] [PubMed]
- Rodou, A.; Ankrah, D.O.; Stathopoulos, C. Toxin and Secretion Systems of Photorhabdus luminescens. Toxins 2010, 2, 1250–1264. [Google Scholar] [CrossRef] [PubMed]
- Jallouli, W.; Zouari, N.; Jaoua, S. Involvement of Oxidative Stress and Growth at High Cell Density in the Viable but Nonculturable State of Photorhabdus temperata ssp. temperata Strain K122. Process Biochem. 2010, 45, 706–713. [Google Scholar] [CrossRef]
- Hasana, A.; Ahmeda, S.; Mollaha, M.M.; Leeb, D.; Kima, Y. Variation in Pathogenicity of Different Strains of Xenorhabdus nematophila: Differential Immunosuppressive Activities and Secondary Metabolite Production. J. Invertebr. Pathol. 2019, 166, 107221. [Google Scholar] [CrossRef] [PubMed]
- Mollah, M.I.; Kim, Y. Virulent Secondary Metabolites of Entomopathogenic Bacteria Genera, Xenorhabdus and Photorhabdus, Inhibit Phospholipase A2 to Suppress Host Insect Immunity. BMC Microbiol. 2020, 20, 359. [Google Scholar] [CrossRef] [PubMed]
Bacterial Species | Concentration (µL mL−1) | a Corrected Mortality % | Bacterial Species Means | |||
---|---|---|---|---|---|---|
12 h | 24 h | 48 h | 72 h | |||
EMA | 600 | b 80 ± 0 | 88 ± 4.9 | 95.7 ± 4.34 | 100 ± 0 | 53.7 a |
400 | 64 ± 4 | 72 ± 4.9 | 78.3 ± 0 | 86.98 ± 5.3 | ||
200 | 48 ± 4.9 | 56 ± 4 | 60.86 ± 4.36 | 73.92 ± 8.14 | ||
150 | 40 ± 0 | 47.82 ± 5.3 | 48 ± 4.9 | 56.5 ± 0 | ||
75 | 26.1 ± 5.3 | 28 ± 4.9 | 30.4 ± 4.35 | 32 ± 4.9 | ||
25 | 8 ± 4.9 | 21.7 ± 5.3 | 21.7 ± 5.3 | 24 ± 4 | ||
EMC | 600 | 64 ± 4 | 72 ± 4.9 | 86.98 ± 5.3 | 91.32 ± 5.3 | 43.9 b |
400 | 48 ± 4.9 | 60 ± 0 | 65.2 ± 5.34 | 78.3 ± 6.88 | ||
200 | 36 ± 4 | 48 ± 4.9 | 52.2 ± 4.34 | 69.6 ± 5.34 | ||
150 | 32 ± 4.9 | 40 ± 0 | 47.82 ± 5.3 | 47.82 ± 5.3 | ||
75 | 16 ± 4 | 21.7 ± 5.3 | 24 ± 4 | 26.1 ± 5.3 | ||
25 | 0 ± 0 | 7.8 ± 3.2 | 8 ± 4.9 | 13.04 ± 0 | ||
TT01 | 600 | 36 ± 7.5 | 48 ± 4.9 | 65.2 ± 5.34 | 78.3 ± 0 | 26.7 c |
400 | 20 ± 0 | 32 ± 4.9 | 34.8 ± 0 | 56.5 ± 6.88 | ||
200 | 20 ± 0 | 26.1 ± 5.3 | 28 ± 4.9 | 34.8 ± 0 | ||
150 | 16 ± 4 | 17.4 ± 4.35 | 20 ± 6.3 | 34.8 ± 0 | ||
75 | 8 ± 4.9 | 12 ± 4.9 | 13.04 ± 0 | 21.7 ± 5.3 | ||
25 | 0 ± 0 | 4 ± 4 | 5.2 ± 3.2 | 7.8 ± 3.2 | ||
LB | 0 ± 0 | 0 ± 0 | 0.87 ± 0.53 | 0.87 ± 0.53 | 0.43 d | |
Exposure duration Means | 23.5 d | 29.8 c | 32.5 b | 38.9 a |
Bacterial Species | Concentration (CFU mL−1) | a Corrected Mortality % | Bacterial Species Means | |||
---|---|---|---|---|---|---|
12 h | 24 h | 48 h | 72 h | |||
EMA | 108 | b 84 ± 4 | 88 ± 4.9 | 100 ± 0 | 100 ± 0 | 81.6 a |
106 | 72 ± 4.9 | 80 ± 0 | 88 ± 4.9 | 92 ± 4.9 | ||
104 | 56 ± 4 | 60 ± 0 | 71.3 ± 4.6 | 87.7 ± 5.05 | ||
EMC | 108 | 72 ± 4.9 | 80 ± 0 | 83.7 ± 4.1 | 88 ± 4.9 | 67.4 b |
106 | 52 ± 4.9 | 60 ± 8.9 | 66.96 ± 5.02 | 79.3 ± 0.4 | ||
104 | 48 ± 4.9 | 52 ± 4.9 | 54.96 ± 7.1 | 71.3 ± 4.6 | ||
TT01 | 108 | 40 ± 6.3 | 40 ± 0 | 67.3 ± 4.5 | 79.3 ± 0.4 | 42.8 c |
106 | 28 ± 4.9 | 44 ± 7.5 | 50.96 ± 7.5 | 58.96 ± 6.1 | ||
104 | 8 ± 4.9 | 20 ± 8.9 | 34.3 ± 6.8 | 42.3 ± 3.7 | ||
Exposure duration Means | 51.1 d | 58.2 c | 68.6 b | 77.6 a |
Bacterial Species | a LC50 | LT50 (h) | ||
---|---|---|---|---|
Filtrate (µL mL−1) | Cells (CFU mL−1) | Filtrate | Cells | |
EMA | 125.9 | 2.14 × 102 | 19.95 | 5.25 |
EMC | 204.2 | 1.78 × 103 | 52.48 | 7.36 |
TT01 | 575.4 | 8.13 × 106 | 208.93 | 44.57 |
No. | R. Time (min) | Name | Formula |
1 | 9.265 | 3.beta.,17.beta.-dihydroxyestr-4-ene | C18H28O2 |
2 | 9.670 | 1-Methylcyclopropanemethanol Heptanal, 2-methylPiperazine, 2-methyl | C5H10O C8H16O C5H12N2 |
3 | 9.973 | 1-Propanol, 3-ethoxy | C5H12O2 |
4 | 10.295 | Oxirane, tetramethyl- | C6H12O |
5 | 10.424 | Cyclohexanol, 4-methyl-, cis | C7H14O |
6 | 11.478 | 1-Methoxy-3-hydroxymethylheptane | C9H20O2 |
7 | 12.900 | Nonanal | C9H18O |
8 | 13.524 | 4,4-Dimethoxy-2-methyl-2-butanol | C7H16O3 |
9 | 17.035 | N-(4-Methylcyclohexyl)acetamide | C9H17NO |
10 | 17.277 | 4-Cyclohexene-1,2-diol | C6H10O2 |
11 | 18.257 | Thiirane | C2H4S |
12 | 19.717 | Oleic Acid $$ 9-Octadecenoic acid (Z) | C18H34O2 |
13 | 20.052 | 2-Decenal, (Z)- | C10H18O |
14 | 22.714 | E-2-Tetradecen-1-ol | C14H28O |
15 | 23.156 | 1,1-Dodecanediol, diacetate | C16H30O4 |
16 | 25.945 | Hexadecanal | C16H32O |
17 | 29.306 | Octadecanal $$ Stearaldehyde | C18H36O |
18 | 41.858 | 1-Formyl-3-methylaziridine-2-carbonitrile | C5H6N2O |
No. | R. Time (min) | Name | Formula |
1 | 9.25 | 3.beta.,17.beta.-dihydroxyestr-4-ene | C18H28O2 |
2 | 9.669 | 1-Methylcyclopropanemethanol Heptanal, 2-methylPiperazine, 2-methyl | C5H10O C8H16O C5H12N2 |
3 | 9.97 | 4,4-Dimethoxy-2-methyl-2-butanol 2-Butanol, 1-methoxy | C7H16O3 C5H12O2 |
4 | 10.294 | Oxirane, 3-ethyl-2,2-dimethyl Oxirane, tetramethyl | C6H12O C6H12O |
5 | 10.424 | Heptanal $$ n-Heptaldehyde | C7H14O |
6 | 11.476 | Octanal $$ n-Caprylaldehyde | C8H16O |
7 | 12.896 | Nonanal | C9H18O |
8 | 13.523 | 4,4-Dimethoxy-2-methyl-2-butanol Cycloserine | C7H16O3 C3H6N2O2 |
9 | 17.022 | N-(4-Methylcyclohexyl)acetamide | C9H17NO |
10 | 17.277 | 4-Cyclohexene-1,2-dio | C6H10O2 |
11 | 19.706 | Oleic Acid | C18H34O2 |
12 | 20.047 | 2-Decenal, (Z)- | C10H18O |
13 | 22.703 | Pentadecanoic acid | C15H33O2 |
14 | 23.151 | 2-Undecenal | C11H20O |
15 | 25.942 | 10-Methyl-E-11-tridecen-1-ol propionate | C17H32O2 |
16 | 26.461 | Z-8-Methyl-9-tetradecenoic acid | C15H28O2 |
17 | 26.753 | Cyclopentaneundecanoic acid | C16H30O2 |
18 | 29.3 | Tetradecanal | C14H28O2 |
19 | 29.781 | 3-Acetoxydodecane | C14H28O2 |
20 | 38.122 | 12-Methyl-E,E-2,13-octadecadien-1-ol 8-Hexadecenal, 14-methyl-, (Z)- | C19H36O C17H32O |
21 | 41.872 | 1-Formyl-3-methylaziridine-2-carbonitrile | C5H6N2O |
No. | R. Time min | Name | Formula |
1 | 9.29 | 3.beta.,17.beta.-dihydroxyestr-4-ene | C18H28O2 |
2 | 9.698 | 1-Methylcyclopropanemethanol Heptanal, 2-methylPiperazine, 2-methyl | C5H10O C8H16O C5H12N2 |
3 | 10.00 | 4,4-Dimethoxy-2-methyl-2-butanol 2-Butanol, 1-methoxy | C7H16O3 C5H12O2 |
4 | 10.325 | Oxirane, 3-ethyl-2,2-dimethyl Oxirane, tetramethyl | C6H12O C6H12O |
5 | 10.452 | Heptanal | C7H14O |
6 | 11.507 | Octanal $$ n-Caprylaldehyde | C8H16O |
7 | 12.923 | Nonanal | C9H18O |
8 | 13.55 | 2-Amino-1,3-propanediol | C3H9NO2 |
9 | 16.206 | Propanamide, 2-hydroxy-N-methyl- | C4H9NO2 |
10 | 17.045 | Cyclopentaneundecanoic acid N-Cyclododecylacetamide | C16H30O2 C14H27O2 |
11 | 17.229 | 2-Nonenal, (E)-9-Octadecenoic acid (Z)-, hexyl ester | C9H16O C24H46O2 |
12 | 18.066 | 6-(Hydroxy-phenyl-methyl)-2,2-dimethylcyclohexanone | C15H20O2 |
13 | 20.066 | 2-Decenal, (Z) | C10H18O |
14 | 23.164 | 2-Undecenal | C11H20O |
15 | 25.957 | E-2-Tetradecen-1-o | C14H28O2 |
16 | 26.487 | Z-10-Tetradecen-1-ol acetate | C16H30O2 |
17 | 26.763 | Cyclopentaneundecanoic acid 1-Hexadecyne | C16H30O2 C16H30O |
18 | 29.313 | Octadecanal $$ Stearaldehyde | C18H36O |
19 | 29.760 | Octanoic acid, 7-oxo- | C8H14O3 |
20 | 36.091 | 9-Hexadecenoic acid | C16H30O2 |
21 | 38.166 | 12-Methyl-E,E-2,13-octadecadien-1-ol | C19H36O |
22 | 38.469 | 7-Methyl-Z-tetradecen-1-ol acetate | C17H32O2 |
23 | 41.836 | 1-Formyl-3-methylaziridine-2-carbonitrile | C5H6N2O |
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Alotaibi, S.S.; Darwish, H.; Alharthi, S.; Alghamdi, A.; Noureldeen, A.; Fallatah, A.M.; Fodor, A.; Al-Barty, A.; Albogami, B.; Baazeem, A. Control Potentials of Three Entomopathogenic Bacterial Isolates for the Carob Moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae) in Pomegranates. Agriculture 2021, 11, 1256. https://doi.org/10.3390/agriculture11121256
Alotaibi SS, Darwish H, Alharthi S, Alghamdi A, Noureldeen A, Fallatah AM, Fodor A, Al-Barty A, Albogami B, Baazeem A. Control Potentials of Three Entomopathogenic Bacterial Isolates for the Carob Moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae) in Pomegranates. Agriculture. 2021; 11(12):1256. https://doi.org/10.3390/agriculture11121256
Chicago/Turabian StyleAlotaibi, Saqer S., Hadeer Darwish, Sarah Alharthi, Akram Alghamdi, Ahmed Noureldeen, Ahmed M. Fallatah, András Fodor, Amal Al-Barty, Bander Albogami, and Alaa Baazeem. 2021. "Control Potentials of Three Entomopathogenic Bacterial Isolates for the Carob Moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae) in Pomegranates" Agriculture 11, no. 12: 1256. https://doi.org/10.3390/agriculture11121256