Bio-larvicidal and Cytotoxic Activity of forest Streptomyces Isolate GA9 Against Some Mosquito Larvae: http://www.doi.org/10.26538/tjnpr/v8i1.33

Abdirasak S.A. Mude; Yahye A. Nageye; Kizito E. Bello

Authors

Abdirasak S.A. Mude Faculty of Medicine and Health Sciences, SIMAD University, Mogadishu, Somalia. 252.
Yahye A. Nageye Faculty of Medicine and Health Sciences, SIMAD University, Mogadishu, Somalia. 252.
Kizito E. Bello Department of Microbiology, Faculty of Natural Science, Kogi State (Prince Abubakar Audu) University, Anyigba. PMB 1008, Anyigba, Kogi State, Nigeria.

Keywords:

soil, Biological control, Cytotoxicity, Streptomyces, Mosquito, Bio-larvicide

Abstract

An antibiotic-producing Streptomyces spp. was isolated from forest soil and assessed for its bio-larvicidal and cytotoxic activity against various mosquito species (Aedes spp, Anopheles spp, Culex spp, and Mansonia spp) and Brime shrimps. Active biocides were extracted using a modified solid state fermentation process. Mosquito larvae were exposed to different concentrations of the ethanolic extract of the Streptomyces exudates for 24 hours. The extract's cytotoxicity was also evaluated using Brime shrimp. The results revealed a significant mortality rate among all four important vector mosquitoes following treatment with the extract. The LC50 and LC90 values of the extract were 0.40 mg/ml and 0.80 mg/ml for Anopheles spp, 0.20 mg/ml and 0.60 mg/ml for Culex spp, 0.40 mg/ml and 0.60 mg/ml for Aedes spp, and 0.20 mg/ml and 0.60 mg/ml for Mansonia spp, respectively. The Minimum larvicidal concentration values were 0.2 mg/ml for Aedes spp, Anopheles spp, Culex spp, and Mansonia spp. The extract showed a low degree of cytotoxicity, with an average mortality rate of only 20% at 0.8 mg/ml of the extract, upon testing with Brime shrimp. In conclusion, the aqueous extract of forest Streptomyces spp. exhibited high bio-larvicidal activity against Aedes spp, Anopheles spp, Culex spp, and Mansonia spp larvae, suggesting its potential as an environmentally friendly approach to mosquito control. This study represents an initial step toward supplementing eco-friendly nontoxic microbe-based bioinsecticides for synthetic insecticides against medically significant mosquitoes.

References

Salam N, Mustafa S, Hafiz A, Chaudhary AA, Deeba F, Parveen S. Global prevalence and distribution of coinfection of malaria, dengue and chikungunya: A systematic review. BMC Public Health. 2018;18:1-20.

Abdullahi IN, Akande AO, Muhammed Y, Rogo LD, Oderinde BS. Prevalence Pattern of Chikungunya Virus Infection in Nigeria: A Four Decade Systematic Review and Meta-analysis. Pathog Glob Health. 2020; 114(3):120-125.

Irekeola AA, Engku Nur Syafirah EAR, Islam MA, Shueb RH. Global prevalence of dengue and chikungunya coinfection: A systematic review and meta-analysis of 43,341 participants. Acta Trop. 2022; 231:106408.

Castellanos JE, Jaimes N, Coronel-Ruiza C, Rojas JP, Mejía LF, Villarreal VH, Maya LE, Claros LM, Orjuela C, Calvo E, Muñoz MV. Dengue-chikungunya coinfection outbreak in children from Cali, Colombia, in 2018–2019. Int J Infect Dis. 2021; 102:97–102.

Higuera A, Ramírez JD. Molecular epidemiology of dengue, yellow fever, Zika and Chikungunya arboviruses: An update. Acta Trop. 2019; 190:99–111.

WHO. World Malaria Report 2016. G. Balint, Antala B, Carty C, Mabieme JMA, Amar IB, Kaplanova A, editors. World Health Organization. 2016 [cited 2023 Apr 29];7(1):343–54. Available from: https://desytamara.blogspot.com/2017/11/sistem-pelayanan-perpustakaan-dan-jenis.html

Feng X, Sun W, Birkhead GS, Wang X, Guo Z, Lu J. The surveillance of four mosquito-borne diseases in international travelers arriving at Guangzhou Baiyun International Airport, China, 2016–2017. Travel Med Infect Dis. 2019; 32:101513.

Amelia-Yap ZH, Chen CD, Sofian-Azirun M, Lau KW, Suana IW, Syahputra E, Razak A, Low VL. Efficacy of mosquito coils: cross-resistance to pyrethroids in Aedes aegypti (Diptera: Culicidae) from Indonesia. J Econ Entomol. 2018;111(6):2854–2860.

Tanvir R, Sajid I, Hasnain S. Larvicidal potential of Asteraceae family endophytic actinomycetes against Culex quinquefasciatus mosquito larvae. Nat Prod Res. 2014; 28(22):2048–2052.

Ansari MS, Moraiet MA, Ahmad S. Insecticides: Impact on the environment and human health. 2014. In: Malik, A., Grohmann, E., Akhtar, R. (eds) Environmental Deterioration and Human Health. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7890-0_6

Tsetsarkin KA, McGee CE, Volk SM. Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS One. 2009; 4:e6835.

Dawson D, Salice CJ, Subbiah S. The efficacy of the Bacillus thuringiensis israelensis larvicide against Culex tarsalis in municipal wastewater and water from natural wetlands. J Am Mosq Control Assoc. 2019; 35(2):97–106.

Karthik L, Gaurav K, Rao KVB, Rajakumar G, Rahuman AA. Larvicidal, repellent, and ovicidal activity of marine actinobacteria extracts against Culex tritaeniorhynchus and Culex gelidus. Parasitol Res. 2011;108(6):1447–1455.

Amuthavalli P, Hwang JS, Dahms HU, Wang L, Anitha J, Vasanthakumaran M, Gandhi AD, Murugan K, Subramaniam J, Paulpandi M, Chandramohan B. Zinc oxide nanoparticles using plant Lawsonia inermis and their mosquitocidal, antimicrobial, anticancer applications showing moderate side effects. Sci Rep. 2021;11(1):8837.

Sivarajan A, Shanmugasundaram T, Sangeetha M, Radhakrishnan M, Balagurunathan R. Screening, production, and characterization of biologically active secondary metabolite(s) from marine Streptomyces sp. PA9 for antimicrobial, antioxidant, and mosquito larvicidal activity. Indian J Mar Sci. 2019; 48(8):1319–1326.

Ramya S, Shanmugasundaram T, Balagurunathan R. Actinobacterial enzyme mediated synthesis of selenium nanoparticles for antibacterial, mosquito larvicidal and anthelminthic applications. Part. Sci. Technol. 2020; 38(1):63–72.

de Lima Procópio RE, da Silva IR, Martins MK, de Azevedo JL, de Araújo JM. Antibiotics produced by Streptomyces. Braz J Infect Dis. 2012;16(5):466–471.

Law JW, Chan KG, He YW, Khan TM, Ab Mutalib NS, Goh BH, Lee LH. Diversity of Streptomyces spp. from mangrove forest of Sarawak (Malaysia) and screening of their antioxidant and cytotoxic activities. Sci Rep. 2019; 9(1):15262.

Quinn GA, Banat AM, Abdelhameed AM, Banat IM. Streptomyces from traditional medicine: Sources of new innovations in antibiotic discovery. J Med Microbiol. 2020; 69(8):1040–1048.

Bello K, and Nwankwo E.O. Antibiotic Activity of Streptomyces Isolates Collected from Soil of Kogi Central, Nigeria. IOSR J Pharm Biol Sci. 2013; 8(4):78–84.

Shanmugasundaram T, Balagurunathan R. Mosquito larvicidal activity of silver nanoparticles synthesised using actinobacterium, Streptomyces sp. M25 against Anopheles subpictus, Culex quinquefasciatus and Aedes aegypti. J Par Dis. 2015; 39(4):677–684.

Salwan R, Sharma V. Bioactive products from Streptomyces. Adv Appl Microbiol. 2000; 47:113–156.

Sumithra D, Bharathi S, Kaviyarasan P, Suresh G. Biofabrication of Selenium Nanoparticles Using Marine Streptomyces sp. and Assessment of Its Antibacterial, Antibiofilm, Antioxidant, and In Vivo Cytotoxic Potential. Geomicrobiol J. 2023; 40(5): 485-492.

Ambarwati A, Wahyuono S, Moeljopawiro S, Yuwono T. Antimicrobial activity of ethyl acetate extracts of Streptomyces sp. CRB46 and the prediction of their bioactive compounds chemical structure. Biodiversitas. 2020; 21(7):3380–3390.

Wang XJ, Zhang J, Liu CX, Gong DL, Zhang H, Wang JD, Yan YJ, Xiang WS. A novel macrocyclic lactone with insecticidal bioactivity from Streptomyces microflavus neau3. Biorg Med Chem Lett. 2011; 21(18):5145–5148.

Arasu MV, Al-Dhabi NA, Saritha V, Duraipandiyan V, Muthukumar C, Kim SJ. Antifeedant, larvicidal and growth inhibitory bioactivities of novel polyketide metabolite isolated from Streptomyces sp. AP-123 against Helicoverpa armigera and Spodoptera litura. BMC Microbiol. 2013;13:105.

Ganesan P. Larvicidal, ovicidal and repellent activities of Streptomyces enissocaesilis (S12–17) isolated from Western Ghats of Tamil Nadu India. J Entomol Zool Stud. 2018; 6:1828–1835.

Usman HS, Sallau AB, Salihu A, Nok AJ. Larvicidal Assessment of Fractions of Aristolochia albida Rhizome on Culex quinquefasciatus: Trop J Nat Prod Res. 2018; 2(5):227-234.

Nwagwu CS, Ogbonna JD, Nwobi LG, Echezona AC, Ugwu CN, Ezeibe EN, Ozioko AC, Nnamani PO, Attama AA. Design, development and evaluation of the repellent activity of Azadirachta indica oil-based solid lipid microparticles against Aedes aegypti (Linn). Trop J Nat Prod Res. 2020; 4(8):471–478.

Karthik L, Gaurav K, Rao KVB, Rajakumar G, Rahuman AA. Larvicidal, repellent, and ovicidal activity of marine actinobacteria extracts against Culex tritaeniorhynchus and Culex gelidus. Parasitol Res. 2011;108(6):1447–1455.

Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol. 1966;16(3):313–340.

Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B, Vanncanneyt M, Swings J, Kim SB, Liu Z, Chun J, Tamura T, Oguchi A, Kikuchi T, Kikuchi H, Nishii T, Tsuji K, Yamaguchi Y, Tase A, Takahashi M, Sakane T, Suzuki KI, Hatano K. Phylogenetic study of the species within the family Streptomycetaceae. Antonie van Leeuwenhoek. 2012;101(1):73–104.

Arogba SS. Phenolics, Antiradical Assay and Cytotoxicity of Processed Mango (Mangifera indica) and Bush Mango (Irvingia gabonensis) Kernels. Nig Fd J. 2014;32(1):62–72.

Prashith Kekuda TR, Onkarappa R. Bioactivities of streptomyces species from soils of western ghats of Karnataka, India. J Chem Pharm Res. 2015; 7(11):181–189.

Jakubiec-Krzesniak K, Rajnisz-Mateusiak A, Guspiel A, Ziemska J, Solecka J. Secondary metabolites of actinomycetes and their antibacterial, antifungal and antiviral properties. Pol J Microbiol. 2018; 67(3):259–272.

Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clément C, Ouhdouch Y, van Wezel GP. Taxonomy, Physiology, and Natural Products of Actinobacteria. Microbiol and Mol Biol Rev. 2016; 80(1):1–43.

Njoku IS, Ichide MU, Rahman NU, Khan MA, Chibuko NA, Asekun OT, Familoni OB. Extraction, Characterization and Larvicidal Activity of Essential Oil and Hydrosol from Sida acuta Burm. f. Leaves Grown in Nigeria. Trop J Nat Prod Res. 2021: 5(1):211–216.

Pridham TG, Gottlieb D. The Utilization of Carbon Compounds by Some Actinomycetales as an Aid for Species Determination. J Bacteriol. 1948; 56(1):107–114.

Vijayakumar R, Murugesan S, Cholarajan A, Sakthi V. Larvicidal potentiality of marine actinomycetes isolated from Muthupet Mangrove, Tamilnadu India. Int J Microbiol Res. 2010; 1:179–183.

al-Doori M, al-Tae AA, Jalil S, Hassan SA. Larvicidal activity of actinomycete isolate against Toxocara canis. Folia Parasitol (Praha). 1991; 38(4):379–382.

Tantithanagorngul W, Sujitwanit A, Piluk J, Tolieng V, Petsom A, Sangvanich P, Palaga T, Puthong S, Thamchaipenet A, Pinphanichakarn P. Screening for brine shrimp larvicidal activity of Streptomyces isolated from soil and anti-tumor activity of the active isolates. Aust J Basic Appl Sci. 2011; 5(7):15–22.

Isman MB. Botanical insecticides: for richer, for poorer. Pest Manag Sci. 2008; 64(1):8–11.

Rajendran K, Krishnamoorthy M, Karuppiah K, Ethiraj K, Sekar S. Chitinase from Streptomyces mutabilis as an Effective Eco-friendly Biocontrol Agent. Appl Biochem Biotechnol. 2023. https://doi.org/10.1007/s12010-023-04489-8

Arasu MV, Al-Dhabi NA, Saritha V, Duraipandiyan V, Muthukumar C, Kim SJ. Antifeedant, larvicidal and growth inhibitory bioactivities of novel polyketide metabolite isolated from Streptomyces sp. AP-123 against Helicoverpa armigera and Spodoptera litura. BMC Microbiol. 2013;13:105.

Raguvaran K, Kalpana M, Manimegalai T, Maheswaran R. Larvicidal, antibacterial, antibiofilm, and anti-quorum sensing activities of silver nanoparticles biosynthesized from Streptomyces sclerotialus culture filtrate. Mater Lett. 2022; 316:132000.

Ganesan P. Larvicidal, ovicidal and repellent activities of Streptomyces enissocaesilis (S12–17) isolated from Western Ghats of Tamil Nadu India. J Entomol Zool Stud. 2018; 6:1828–1835.

El-Bendary MA, Rifaat HM, Keera AA. Larvicidal activity of extracellular secondary metabolites of Streptomyces microflavus against Culex pipiens. Can J Pure App Sci. 2010; 4:1021–1026.

Fouda A, Hassan SED, Abdo AM, El-Gamal MS. Antimicrobial, Antioxidant and Larvicidal Activities of Spherical Silver Nanoparticles Synthesized by Endophytic Streptomyces spp. Biol Trace Elem Res. 2020; 195(2):707–724.

Sanjenbam P, Kannabiran K. Antimicrobial and larvicidal activity of Streptomyces sp. VITPK9 isolated from a brine spring of Manipur, India. Der Pharm Lett. 2013; 5:65–70.

Mio JB, Mohamed MO, Osman YO, Abukar MD, Karama NY, Nurani OM. Mapping of Main Mosquitoes in Mogadishu-Somalia. Indiana J. Agric. Life Sci. 2022; 2(4):8-19.

Abok JI, Ombugadu A, Angbalaga GA. Hyptis suaveolens Extract Exhibits Larvicidal Activity Against Anopheles gambiae Larvae. Trop J Nat Prod Res. 2018; 2(5):245-249.

Saurav K, Rajakumar G, Kannabiran K, Rahuman AA, Velayutham K, Elango G, Kamaraj C, Zahir AA. Larvicidal activity of isolated compound 5-(2,4-dimethylbenzyl) pyrrolidin-2-one from marine Streptomyces VITSVK5 sp. against Rhipicephalus (Boophilus) microplus, Anopheles stephensi, and Culex tritaeniorhynchus. Parasitol Res. 2013; 112(1):215–226.

Deepika TL, Kannabiran K, Khanna VG, Rajakumar G, Jayaseelan C, Santhoshkumar T, Rahuman AA. Isolation and characterisation of acaricidal and larvicidal novel compound (2S,5R,6R)-2-hydroxy-3,5,6-trimethyloctan-4-one from Streptomyces sp. against blood-sucking parasites. Parasitol Res. 2012;111(3):1151–1163.

Ganesan P, Jackson A, David RH, Sivanandhan S, Gandhi MR, Paulraj MG, Al-Dhabi NA, Ignacimuthu S. Mosquito (Diptera: Culicidae) larvicidal and ovicidal properties of extracts from Streptomyces vinaceusdrappus (S12–4) isolated from soils. J Entomol Sci. 2018; 53(1):17–26.

Balakrishnan S, Santhanam P, Srinivasan M. Larvicidal potency of marine actinobacteria isolated from mangrove environment against Aedes aegypti and Anopheles stephensi. J Parasit Dis. 2017; 41(2):387–394.

Shanmugasundaram T, Balagurunathan R. Mosquito larvicidal activity of silver nanoparticles synthesised using actinobacterium, Streptomyces sp. M25 against Anopheles subpictus, Culex quinquefasciatus and Aedes aegypti. J Parasit Dis. 2015; 39(4):677–684.

Naine SJ, Devi CS. Larvicidal and repellent properties of streptomyces sp. VITJS4 crude extract against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Pol J Microbiol. 2014; 63(3):341–348.

Reegan AD, Kumar PS, Asharaja AC, Devi C, Jameela S, Balakrishna K, Ignacimuthu S. Larvicidal and ovicidal activities of phenyl acetic acid isolated from Streptomyces collinus against Culex quinquefasciatus Say and Aedes aegypti L. (Diptera: Culicidae). Exp Parasitol. 2021; 226-227:108120.