Abstract
Whitefly Bemisia tabaci, a carrier of cassava mosaic disease (CMD), poses a significant threat to cassava crops. Investigating culturable bacteria and their impact on whiteflies is crucial due to their vital role in whitefly fitness and survival. The whitefly biotype associated with cassava and transmitting CMD in India has been identified as Asia II 5 through partial mitochondrial cytochrome oxidase I gene sequencing. In this study, bacteria associated with adult B. tabaci feeding on cassava were extracted using seven different media. Nutrient Agar (NA), Soyabean Casein Digest Medium (SCDM), Luria Bertani agar (LBA), and Reasoner’s 2A agar (R2A) media resulted in 19, 6, 4, and 4 isolates, respectively, producing a total of 33 distinct bacterial isolates. Species identification through 16SrRNA gene sequencing revealed that all isolates belonged to the Bacillota and Pseudomonadota phyla, encompassing 11 genera: Bacillus, Cytobacillus, Exiguobacterium, Terribacillus, Brevibacillus, Enterococcus, Staphylococcus, Brucella, Novosphingobium, Lysobacter, and Pseudomonas. All bacterial isolates were tested for chitinase, protease, siderophore activity, and antibiotic sensitivity. Nine isolates exhibited chitinase activity, 28 showed protease activity, and 23 displayed siderophore activity. Most isolates were sensitive to antibiotics such as Vancomycin, Streptomycin, Erythromycin, Kanamycin, Doxycycline, Tetracycline, and Ciprofloxacin, while they demonstrated resistance to Bacitracin and Colistin. Understanding the culturable bacteria associated with cassava whitefly and their functional significance could contribute to developing effective cassava whitefly and CMD control in agriculture.
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References
Abraham A (1956) Tapioca cultivation in India. Indian Council of Agricultural Research, New Delhi
Akintola AA, Hwang H-S, Khatun MF, Ande AT, Lee K-Y (2020) Genetic diversity of Bemisia tabaci cryptic species in Nigeria and their relationships with endosymbionts and acquired begomoviruses. J Asia–pacific Entomol 23(4):1003–1009. https://doi.org/10.1016/j.aspen.2020.08.007
Akman Gündüz E, Douglas A (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc B Biol Sci 276(1658):987–991. https://doi.org/10.1098/rspb.2008.1476
APEDA (2022) https://agriexchange.apeda.gov.in/India%20Production/India_Productions.aspx?cat=Vegetables&hscode=1087
Apte-Deshpande A, Paingankar M, Gokhale MD, Deobagkar DN (2012) Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS ONE. https://doi.org/10.1371/journal.pone.0040401
Ashfaq M, Hebert PD, Mirza MS, Khan AM, Mansoor S, Shah GS, Zafar Y (2014) DNA barcoding of Bemisia tabaci complex (Hemiptera: Aleyrodidae) reveals southerly expansion of the dominant whitefly species on cotton in Pakistan. PLoS ONE 9(8):e104485. https://doi.org/10.1371/journal.pone.0104485
Ashwathappa K, Venkataravanappa V, Reddy CL, Reddy MK (2020) Association of tomato leaf curl New Delhi virus with mosaic and leaf curl disease of Chrysanthemum and its whitefly cryptic species. Indian Phytopathol 73:533–542. https://doi.org/10.1007/s42360-020-00214-1
Ateyyat MA, Shatnawi M, Al-Mazraawi M (2010) Isolation and identification of culturable forms of bacteria from the sweet potato whitefly Bemesia tabaci Genn. (Homoptera: Aleyrodidae) in Jordan. Turk J Agric for 34(3):225–234. https://doi.org/10.3906/tar-0902-35
Banerjee S, Maiti TK, Roy RN (2022) Enzyme producing insect gut microbes: an unexplored biotechnological aspect. Crit Rev Biotechnol 42(3):384–402. https://doi.org/10.1080/07388551.2021.1942777
Basu A (2019) Bemisia tabaci (Gennadius): crop pest and the principal whitefly vector of plant viruses. CRC Press
Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. https://doi.org/10.1146/annurev.micro.59.030804.121041
Beier S, Bertilsson S (2013) Bacterial chitin degradation—mechanisms and ecophysiological strategies. Front Microbiol 4:149. https://doi.org/10.3389/fmicb.2013.00149
Bhattacharya D, Nagpure A, Gupta RK (2007) Bacterial chitinases: properties and potential. Crit Rev Biotechnol 27(1):21–28. https://doi.org/10.1080/07388550601168223
Bing X-L, Yang J, Zchori-Fein E, Wang X-W, Liu S-S (2013) Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79(2):569–575. https://doi.org/10.1128/AEM.03030-12
Brown JK, Czosnek H (2002) Whitefly transmission of plant viruses. https://doi.org/10.1016/S0065-2296(02)36059-2
Casteel CL, Hansen AK (2014) Evaluating insect-microbiomes at the plant-insect interface. J Chem Ecol 40:836–847. https://doi.org/10.1007/s10886-014-0475-4
Cattelan A, Hartel P, Fuhrmann J (1999) Screening for plant growth–promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63(6):1670–1680. https://doi.org/10.2136/sssaj1999.6361670x
Chakraborty U, Chakraborty B, Dey P, Chakraborty A, Sarkar J (2019) Biochemical responses of wheat plants primed with Ochrobactrum pseudogrignonense and subjected to salinity stress. Agric Res 8:427–440. https://doi.org/10.1007/s40003-018-0394-7
Chandrasekaran R, Revathi K, Nisha S, Kirubakaran SA, Sathish-Narayanan S, Senthil-Nathan S (2012) Physiological effect of chitinase purified from Bacillus subtilis against the tobacco cutworm Spodoptera litura Fab. Pestic Biochem Physiol 104(1):65–71. https://doi.org/10.1016/j.pestbp.2012.07.002
Chen W, Hasegawa DK, Kaur N, Kliot A, Pinheiro PV, Luan J, Stensmyr MC, Zheng Y, Liu W, Sun H (2016) The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol 14(1):1–15. https://doi.org/10.1186/s12915-016-0321-y#article-info
Chen W, Wosula EN, Hasegawa DK, Casinga C, Shirima RR, Fiaboe KK, Hanna R, Fosto A, Goergen G, Tamò M (2019) Genome of the African cassava whitefly Bemisia tabaci and distribution and genetic diversity of cassava-colonizing whiteflies in Africa. Insect Biochem Mol Biol 110:112–120. https://doi.org/10.1016/j.ibmb.2019.05.003
Chi Y, Pan L-L, Bouvaine S, Fan Y-Y, Liu Y-Q, Liu S-S, Seal S, Wang X-W (2020) Differential transmission of Sri Lankan cassava mosaic virus by three cryptic species of the whitefly Bemisia tabaci complex. Virology 540:141–149. https://doi.org/10.1016/j.virol.2019.11.013
Chiza Chikoti P, Tembo M, Peter Legg J, Rufini Shirima R, Mugerwa H, Sseruwagi P (2020) Genetic diversity of mitochondrial DNA of Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae) associated with cassava and the occurrence of cassava mosaic disease in Zambia. InSects 11(11):761. https://doi.org/10.3390/insects11110761
Chowda-Reddy R, Kirankumar M, Seal SE, Muniyappa V, Valand GB, Govindappa M, Colvin J (2012) Bemisia tabaci phylogenetic groups in India and the relative transmission efficacy of Tomato leaf curl Bangalore virus by an indigenous and an exotic population. J Integr Agric 11(2):235–248. https://doi.org/10.1016/S2095-3119(12)60008-2
Ciche TA, Blackburn M, Carney JR, Ensign JC (2003) Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogen mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 69(8):4706–4713. https://doi.org/10.1128/AEM.69.8.4706-4713.2003
Cody R (1989) Distribution of chitinase and chitobiase in Bacillus. Curr Microbiol 19:201–205. https://doi.org/10.1007/BF01570162
Colman DR, Toolson EC, Takacs-Vesbach C (2012) Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 21(20):5124–5137. https://doi.org/10.1111/j.1365-294X.2012.05752.x
Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71:773–782. https://doi.org/10.1007/s00253-005-0183-7
Davidson EW, Rosell RC, Hendrix DL (2000) Culturable bacteria associated with the whitefly, Bemisia argentifolii (Homoptera: Aleyrodidae). Florida Entomol 83:159–159
De Barro PJ, Liu S-S, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. https://doi.org/10.1146/annurev-ento-112408-085504
de Vries EJ, Breeuwer JA, Jacobs G, Mollema C (2001) The association of western flower thrips, Frankliniella occidentalis, with a near Erwinia species gut bacteria: transient or permanent? J Invertebr Pathol 77(2):120–128. https://doi.org/10.1006/jipa.2001.5009
Dillon RJ, Dillon V (2004) The gut bacteria of insects: nonpathogenic interactions. Ann Rev Entomol 49(1):71–92. https://doi.org/10.1146/annurev.ento.49.061802.123416
Dinsdale A, Cook L, Riginos C, Buckley Y, De Barro P (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103(2):196–208. https://doi.org/10.1603/AN09061
Drewnowska J, Fiodor A, Barboza-Corona J, Swiecicka I (2020) Chitinolytic activity of phylogenetically diverse Bacillus cereus sensu lato from natural environments. Syst Appl Microbiol 43(3):126075. https://doi.org/10.1016/j.syapm.2020.126075
Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37(5):699–735. https://doi.org/10.1111/1574-6976.12025
Essghaier B, Zouaoui M, Najjari A, Sadfi N (2021) Potentialities and characterization of an antifungal chitinase produced by a halotolerant Bacillus licheniformis. Curr Microbiol 78:513–521. https://doi.org/10.1007/s00284-020-02329-0
Everett KD, Thao M, Horn M, Dyszynski GE, Baumann P (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts ‘Candidatus Fritschea bemisiae’strain Falk and ‘Candidatus Fritschea eriococci’strain Elm. Int J Syst Evol Microbiol 55(4):1581–1587. https://doi.org/10.1099/ijs.0.63454-0
FAOSTAT (2022) Food and agriculture organization statistical data. https://www.fao.org/faostat/en/#data/
Fiallo-Olivé E, Pan L-L, Liu S-S, Navas-Castillo J (2020) Transmission of begomoviruses and other whitefly-borne viruses: dependence on the vector species. Phytopathology 110(1):10–17. https://doi.org/10.1094/PHYTO-07-19-0273-FI
Furukawa K, Matsumura F, Tonomura K (1978) Alcaligenes and Acinetobacter strains capable of degrading polychlorinated biphenyls. Agric Biol Chem 42(3):543–548. https://doi.org/10.1080/00021369.1978.10863017
Gao H, Cui C, Wang L, Jacobs-Lorena M, Wang S (2020) Mosquito microbiota and implications for disease control. Trends Parasitol 36(2):98–111. https://doi.org/10.1016/j.pt.2019.12.001
Genta FA, Dillon RJ, Terra WR, Ferreira C (2006) Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. J Insect Physiol 52(6):593–601. https://doi.org/10.1016/j.jinsphys.2006.02.007
Ghosh S, Bouvaine S, Richardson SC, Ghanim M, Maruthi M (2018) Fitness costs associated with infections of secondary endosymbionts in the cassava whitefly species Bemisia tabaci. J Pest Sci 91:17–28. https://doi.org/10.1007/s10340-017-0910-8
Gnankine O, Mouton L, Henri H, Terraz G, Houndete T, Martin T, Vavre F, Fleury F (2013) Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6(3):411–421. https://doi.org/10.1111/j.1752-4598.2012.00206.x
Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72(5):3646–3652. https://doi.org/10.1128/AEM.72.5.3646-3652.2006
Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19(19):4365–4376. https://doi.org/10.1111/j.1365-294X.2010.04775.x
Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48(1):743–772. https://doi.org/10.1146/annurev.mi.48.100194.003523
Gupta A, Nair S (2020) Dynamics of insect–microbiome interaction influence host and microbial symbiont. Front Microbiol 11:1357. https://doi.org/10.3389/fmicb.2020.01357
Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23(6):1473–1496. https://doi.org/10.1111/mec.12421
Harrison RL, Bonning BC (2010) Proteases as insecticidal agents. Toxins 2(5):935–953. https://doi.org/10.3390/toxins2050935
He Y-Z, Wang Y-M, Yin T-Y, Cuellar WJ, Liu S-S, Wang X-W (2021) Gut-expressed vitellogenin facilitates the movement of a plant virus across the midgut wall in its insect vector. Msystems 6(3):00581–01521. https://doi.org/10.1128/msystems.00581-21
Hogenhout SA, van der Wilk F, Verbeek M, Goldbach RW, van den Heuvel JF (1998) Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog. J Virol 72(1):358–365. https://doi.org/10.1128/jvi.72.1.358-365.1998
Hudzicki J (2009) Kirby-Bauer disk diffusion susceptibility test protocol. Am Soc Microbiol 15:55–63
Hue KT, Van DTT, Spörndly E, Ledin I, Wredle E (2012) Effect of adaptation strategies when feeding fresh cassava foliage on intake and physiological responses of lambs. Trop Anim Health Prod 44:267–276. https://doi.org/10.1007/s11250-011-0013-0
Indiragandhi P, Anandham R, Madhaiyan M, Poonguzhali S, Kim G, Saravanan V, Sa T (2007) Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos-susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for, antagonism towards entomopathogenic fungi and host insect nutrition. J Appl Microbiol 103(6):2664–2675
Indiragandhi P, Yoon C, Yang JO, Cho S, Sa TM, Kim GH (2010) Microbial communities in the developmental stages of B and Q biotypes of sweetpotato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). J Korean Soc Appl Biol Chem 53:605–617. https://doi.org/10.1111/j.1365-2672.2007.03506.x
Jia D, Mao Q, Chen Y, Liu Y, Chen Q, Wu W, Zhang X, Chen H, Li Y, Wei T (2017) Insect symbiotic bacteria harbour viral pathogens for transovarial transmission. Nat Microbiol 2(5):1–7
Joyce JD, Nogueira JR, Bales AA, Pittman KE, Anderson JR (2011) Interactions between La Crosse virus and bacteria isolated from the digestive tract of Aedes albopictus (Diptera: Culicidae). J Med Entomol 48(2):389–394. https://doi.org/10.1603/ME09268
Kanakala S, Ghanim M (2019) Global genetic diversity and geographical distribution of Bemisia tabaci and its bacterial endosymbionts. PLoS ONE 14(3):e0213946. https://doi.org/10.1371/journal.pone.0213946
Karunya SK, Reetha D, Saranraj P, Milton DJ (2011) Optimization and purification of chitinase produced by Bacillus subtilis and its antifungal activity against plant pathogens. Int J Pharm Biol Arch 2(6):1680–1685
Kliot A, Kontsedalov S, Lebedev G, Czosnek H, Ghanim M (2019) Combined infection with Tomato yellow leaf curl virus and Rickettsia influences fecundity, attraction to infected plants and expression of immunity-related genes in the whitefly Bemisia tabaci. J General Virol 100(4):721–731. https://doi.org/10.1099/jgv.0.001233
Krishnamoorthy R, Arul Jose P, Janahiraman V, Indira Gandhi P, Gandhi Gracy R, Jalali SK, Senthil Kumar M, Malathi V, Anandham R (2020) Function and insecticidal activity of bacteria associated with papaya mealybug, Paracoccus marginatus Williams & Granara de Willink (Hemiptera: Pseudococcidae). Biocontrol Sci Tech 30(8):762–778. https://doi.org/10.1080/09583157.2020.1765983
Kuddus M, Ahmad I (2013) Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. J Genetic Eng Biotechnol 11(1):39–46. https://doi.org/10.1016/j.jgeb.2013.03.001
Latif S, Müller J (2015) Potential of cassava leaves in human nutrition: a review. Trends Food Sci Technol 44(2):147–158. https://doi.org/10.1016/j.tifs.2015.04.006
Lee W, van Baalen M, Jansen VA (2012) An evolutionary mechanism for diversity in siderophore-producing bacteria. Ecol Lett 15(2):119–125. https://doi.org/10.1111/j.1461-0248.2011.01717.x
Lei T, Zhao J, Wang HL, Liu YQ, Liu SS (2021) Impact of a novel Rickettsia symbiont on the life history and virus transmission capacity of its host whitefly (Bemisia tabaci). Insect Sci 28(2):377–391. https://doi.org/10.1111/1744-7917.12797
Leiva AM, Chittarath K, Lopez-Alvarez D, Vongphachanh P, Gomez MI, Sengsay S, Wang X-W, Rodriguez R, Newby J, Cuellar WJ (2022) Mitochondrial genetic diversity of Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae) associated with cassava in Lao PDR. InSects 13(10):861. https://doi.org/10.3390/insects13100861
Liu R, Wang W, Liu X, Lu Y, Xiang T, Zhou W, Wan Y (2018) Characterization of a lipase from the silkworm intestinal bacterium Bacillus pumilus with antiviral activity against Bombyx mori (Lepidoptera: Bombycidae) nucleopolyhedrovirus in vitro. J Insect Sci 18(6):3. https://doi.org/10.1093/jisesa/iey111
Lv J, Zhang Y, Ma M, Oh D-H, Fu X (2022) Characterization of chitinase from Exiguobacterium antarcticum and its bioconversion of crayfish shell into chitin oligosaccharides. Food Res Int 158:111517. https://doi.org/10.1016/j.foodres.2022.111517
Ma E, Zhu Y, Liu Z, Wei T, Wang P, Cheng G (2021) Interaction of viruses with the insect intestine. Ann Rev Virol 8:115–131. https://doi.org/10.1146/annurev-virology-091919-100543
Milagres AM, Machuca A, Napoleao D (1999) Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J Microbiol Methods 37(1):1–6. https://doi.org/10.1016/S0167-7012(99)00028-7
Misaka BC, Wosula EN, Marchelo-d’Ragga PW, Hvoslef-Eide T, Legg JP (2020) Genetic diversity of Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae) colonizing sweet potato and cassava in South Sudan. InSects 11(1):58. https://doi.org/10.3390/insects11010058
Morin S, Ghanim M, Zeidan M, Czosnek H, Verbeek M, van den Heuvel JF (1999) A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology 256(1):75–84. https://doi.org/10.1006/viro.1999.9631
Moussian B (2019) Chitin: structure, chemistry and biology. Target Chitin-Contain Organ. https://doi.org/10.1007/978-981-13-7318-3_2
Mugerwa H, Rey ME, Alicai T, Ateka E, Atuncha H, Ndunguru J, Sseruwagi P (2012) Genetic diversity and geographic distribution of Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae) genotypes associated with cassava in East Africa. Ecol Evol 2(11):2749–2762. https://doi.org/10.1002/ece3.379
Muzzarelli RA (2011) Chitin nanostructures in living organisms. Chitin Format Diagen. https://doi.org/10.1007/978-90-481-9684-5_1
Nirgianaki A, Banks GK, Frohlich DR, Veneti Z, Braig HR, Miller TA, Bedford ID, Markham PG, Savakis C, Bourtzis K (2003) Wolbachia infections of the whitefly Bemisia tabaci. Curr Microbiol 47:0093–0101. https://doi.org/10.1007/s00284-002-3969-1
Nishimura T, Tanaka N, Umezawa H (1962) Inhibition of protein synthesis by kanamycin. J Antibio Ser A 15(5):210–215. https://doi.org/10.11554/antibioticsa.15.5_210
Okongo RN, Puri AK, Wang Z, Singh S, Permaul K (2019) Comparative biocontrol ability of chitinases from bacteria and recombinant chitinases from the thermophilic fungus Thermomyces lanuginosus. J Biosci Bioeng 127(6):663–671. https://doi.org/10.1016/j.jbiosc.2018.11.007
Patel S, Preuss CV, Bernice F (2022) Vancomycin. In: StatPearls. StatPearls Publishing
Pinheiro PV, Kliot A, Ghanim M, Cilia M (2015) Is there a role for symbiotic bacteria in plant virus transmission by insects? Curr Opin Insect Sci 8:69–78. https://doi.org/10.1016/j.cois.2015.01.010
Raina HS, Rawal V, Singh S, Daimei G, Shakarad M, Rajagopal R (2015) Elimination of Arsenophonus and decrease in the bacterial symbionts diversity by antibiotic treatment leads to increase in fitness of whitefly, Bemisia tabaci. Infect Genet Evol 32:224–230. https://doi.org/10.1016/j.meegid.2015.03.022
Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62(3):597–635. https://doi.org/10.1128/MMBR.62.3.597-635.1998
Ravindran V (1993) Cassava leaves as animal feed: potential and limitations. J Sci Food Agric 61(2):141–150. https://doi.org/10.1002/jsfa.2740610202
Roopa H, Rebijith K, Asokan R, Mahmood R, Nk KK (2014) Isolation and identification of culturable bacteria from honeydew of whitefly, Bemisia tabaci (G.)(Hemiptera: Aleyrodidae). Meta Gene 2:114–122. https://doi.org/10.1016/j.mgene.2013.11.002
Saranya M, Kennedy J, Anandham R (2022a) Functional characterization of cultivable gut bacterial communities associated with rugose spiralling whitefly Aleurodicus rugioperculatus Martin. Biotech 12(1):14. https://doi.org/10.1007/s13205-021-03081-3
Saranya M, Kennedy J, Anandham R, Manikandan A (2022b) Characterization and functional significance of bacteria associated with rugose spiralling whitefly, Aleurodicus rugioperculatus Martin (Hemiptera: Aleyrodidae) reared on guava plants. Appl Entomol Zool 57(4):323–331. https://doi.org/10.1007/s13205-021-03081-3
Shan HW, Zhang CR, Yan TT, Tang HQ, Wang XW, Liu SS, Liu YQ (2016) Temporal changes of symbiont density and host fitness after rifampicin treatment in a whitefly of the Bemisia tabaci species complex. Insect Sci 23(2):200–214. https://doi.org/10.1111/1744-7917.12276
Sharma R (2021) Kirby Bauer disc diffusion method for antibiotic susceptibility testing.
Skujins J, Potgieter H, Alexander M (1965) Dissolution of fungal cell walls by a streptomycete chitinase and β-(1→ 3) glucanase. Arch Biochem Biophys 111(2):358–364. https://doi.org/10.1016/0003-9861(65)90197-9
Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Let 8(6):986–989. https://doi.org/10.1098/rsbl.2012.0664
Sonawane M, Chaudhary R, Shouche Y, Sayyed R (2018) Insect gut bacteria: a novel source for siderophore production. Proc Natl Acad Sci India Sect B Biol Sci 88:567–572. https://doi.org/10.1007/s40011-016-0785-0
Souza CP, Burbano-Rosero EM, Almeida BC, Martins GG, Albertini LS, Rivera IN (2009) Culture medium for isolating chitinolytic bacteria from seawater and plankton. World J Microbiol Biotechnol 25:2079–2082. https://doi.org/10.1007/s11274-009-0098-z
Spotts CR, Stanier R (1961) Mechanism of streptomycin action on bacteria: a unitary hypothesis. Nature 192:633–637
Subbanna A, Rajasekhara H, Stanley J, Mishra K, Pattanayak A (2018) Pesticidal prospectives of chitinolytic bacteria in agricultural pest management. Soil Biol Biochem 116:52–66. https://doi.org/10.1016/j.soilbio.2017.09.019
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/molbev/msab120
Thao ML, Baumann P (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70(6):3401–3406. https://doi.org/10.1128/AEM.70.6.3401-3406.2004
Tocko-Marabena BK, Silla S, Simiand C, Zinga I, Legg J, Reynaud B, Delatte H (2017) Genetic diversity of Bemisia tabaci species colonizing cassava in Central African Republic characterized by analysis of cytochrome c oxidase subunit I. PLoS ONE 12(8):e0182749. https://doi.org/10.1371/journal.pone.0182749
Uke A, Tokunaga H, Utsumi Y, Vu NA, Nhan PT, Srean P, Hy NH, Ham LH, Lopez-Lavalle LAB, Ishitani M (2022) Cassava mosaic disease and its management in Southeast Asia. Plant Mol Biol. https://doi.org/10.1007/s11103-021-01168-2
Varma A, Mandal B, Singh MK (2011) Global emergence and spread of whitefly (Bemisia tabaci) transmitted geminiviruses. The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivirus-Infected Host Plants: Bemisia tabaci, Host Plants and Geminiviruses. https://doi.org/10.1007/978-94-007-1524-0_10
Veliz EA, Martínez-Hidalgo P, Hirsch AM (2017) Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiol 3(3):689
Visôtto L, Oliveira M, Guedes R, Ribon A, Good-God P (2009) Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. J Insect Physiol 55(3):185–191. https://doi.org/10.1016/j.jinsphys.2008.10.017
Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex–ratio–distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270(1526):1857–1865. https://doi.org/10.1098/rspb.2003.2425
Wu P, Sun P, Nie K, Zhu Y, Shi M, Xiao C, Liu H, Liu Q, Zhao T, Chen X (2019a) A gut commensal bacterium promotes mosquito permissiveness to arboviruses. Cell Host Microbe 25(1):101–112. https://doi.org/10.1016/j.chom.2018.11.004
Wu W, Huang L, Mao Q, Wei J, Li J, Zhao Y, Zhang Q, Jia D, Wei T (2019b) Interaction of viral pathogen with porin channels on the outer membrane of insect bacterial symbionts mediates their joint transovarial transmission. Philos Trans R Soc B 374(1767):20180320. https://doi.org/10.3389/fmicb.2022.805352
Wu W, Shan H-W, Li J-M, Zhang C-X, Chen J-P, Mao Q (2022) Roles of bacterial symbionts in transmission of plant virus by hemipteran vectors. Front Microbiol 13:805352. https://doi.org/10.1098/rspb.2003.2425
Yin C, Sun P, Yu X, Wang P, Cheng G (2020) Roles of symbiotic microorganisms in arboviral infection of arthropod vectors. Trends Parasitol 36(7):607–615. https://doi.org/10.1016/j.pt.2020.04.009
Zchori-Fein E, Brown J (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae). Ann Entomol Soc Am 95(6):711–718. https://doi.org/10.1603/0013-8746(2002)095[0711:DOPAWB]2.0.CO;2
Zhang C-R, Shan H-W, Xiao N, Zhang F-D, Wang X-W, Liu Y-Q, Liu S-S (2015a) Differential temporal changes of primary and secondary bacterial symbionts and whitefly host fitness following antibiotic treatments. Sci Rep 5(1):1–12. https://doi.org/10.1038/srep15898
Zhang C-R, Shan H-W, Xiao N, Zhang F-D, Wang X-W, Liu Y-Q, Liu S-S (2015b) Differential temporal changes of primary and secondary bacterial symbionts and whitefly host fitness following antibiotic treatments. Sci Rep 5(1):15898. https://doi.org/10.1038/srep15898
Zhang G-F, Liu X, Zhang S, Pan B, Liu M-L (2018) Ciprofloxacin derivatives and their antibacterial activities. Eur J Med Chem 146:599–612. https://doi.org/10.1016/j.ejmech.2018.01.078
Zhao M, Lin X, Guo X (2022) The role of insect symbiotic bacteria in metabolizing phytochemicals and agrochemicals. InsEcts 13(7):583. https://doi.org/10.3390/insects13070583
Zhu-Salzman K, Zeng R (2015) Insect response to plant defensive protease inhibitors. Annu Rev Entomol 60:233–252. https://doi.org/10.1146/annurev-ento-010814-020816
Acknowledgements
KV acknowledges the Department of Biotechnology, Government of India, New Delhi, India, for the Junior Research Fellowship (DBT-JRF) financial support during the doctoral program under grant DBT/2021-22/TNAU/1691. The Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India, is acknowledged for providing research facilities and funding. All authors accepted the final version of manuscript submitted to the journal.
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KV conducted all the laboratory experiments and manuscript drafting. SJ and MM conceived the hypothesis, designed the experiment, and corrected the manuscript. SM, RV, GK, and AM assisted in laboratory experiments and drafted the manuscript. All authors have seen and approved the manuscript and its contents, and that they are aware of the responsibilities connected to the authorship.
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Kumar, V., Subramanian, J., Marimuthu, M. et al. Diversity and functional characteristics of culturable bacterial endosymbionts from cassava whitefly biotype Asia II-5, Bemisia tabaci. 3 Biotech 14, 100 (2024). https://doi.org/10.1007/s13205-024-03949-0
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DOI: https://doi.org/10.1007/s13205-024-03949-0