Abstract
Bacillus biocontrol agent(s) BCA(s) such as Bacillus cereus, Bacillus thuringiensis and Bacillus subtilis have been widely applied to control insects’ pests of plants and pathogenic microbes, improve plant growth, and facilitate their resistance to environmental stresses. In the last decade, researchers have shown that, the application of Bacillus biocontrol agent(s) BCA(s) optimized agricultural production yield, and reduced disease risks in some crops. However, these bacteria encountered various abiotic stresses, among which ultraviolet (UV) radiation severely decrease their efficiency. Researchers have identified several strategies by which Bacillus biocontrol agents resist the negative effects of UV radiation, including transcriptional response, UV mutagenesis, biochemical and artificial means (addition of protective agents). These strategies are governed by distinct pathways, triggered by UV radiation. Herein, the impact of UV radiation on Bacillus biocontrol agent(s) BCA(s) and their mechanisms of resistance were discussed.
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References
Aboul-Soud MA, Al-Amri MZ, Kumar A, Al-Sheikh YA, Ashour AE, El-Kersh TA (2019) Specific cytotoxic effects of parasporal crystal proteins isolated from native Saudi Arabian Bacillus thuringiensis strains against Cervical cancer cells. Molecules 24(3):506. https://doi.org/10.3390/molecules24030506
Allard-Massicotte R, Tessier L, Lécuyer F, Lakshmanan V, Lucier JF, Garneau D, Caudwell L (2016) Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. mBio 7(6):10–1128. https://doi.org/10.1128/mBio.01664-16
Au N, Kuester-Schoeck E, Mandava V, Bothwell LE, Canny SP, Chachu K, Colavito SA et al (2005) Genetic composition of the Bacillus subtilis sos system. J Bacteriol 187(22):7655–7666. https://doi.org/10.1128/jb.187.22.7655-7666.2005
Baek I, Lee K, Goodfellow M, Chun J (2019) Comparative genomic and phylogenomic analyses clarify relationships within and between Bacillus cereus and Bacillus thuringiensis: Proposal for the recognition of two Bacillus thuringiensis genomovars. Front Microbiol 10:1978. https://doi.org/10.3389/fmicb.2019.01978
Banerjee G, Gorthi S, Chattopadhyay P (2018) Beneficial effects of bio-controlling agent Bacillus cereus ib311 on the Agricultural crop production and its biomass optimization through response surface methodology. An Acad Bras Cienc 90(2 suppl 1):2149–2159. https://doi.org/10.1590/0001-3765201720170362
Batool K, Alam I, Wu S, Liu W, Zhao G, Chen M, Wang J et al (2018) Transcriptomic analysis of Aedes aegypti in response to mosquitocidal Bacillus thuringiensis LLP29 toxin. Sci Rep 8(1):12650. https://doi.org/10.1038/s41598-018-30741-x
Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci 110(17):E1621–E1630. https://doi.org/10.1073/pnas.1218984110
Cao ZL, Tan TT, Jiang K, Mei SQ, Hou XY, Cai J (2018) Complete genome sequence of Bacillus thuringiensis l-7601, a wild strain with high production of melanin. J Biotechnol 275:40–43. https://doi.org/10.1016/j.jbiotec.2018.03.020
Castillo-Hair SM, Baerman EA, Fujita M, Igoshin OA, Tabor JJ (2019) Optogenetic control of Bacillus subtilis gene expression. Nat Commun 10(1):3099. https://doi.org/10.1038/s41467-019-10906-6
Chen Y, Deng Y, Wang J, Cai J, Ren G (2004) Characterization of melanin produced by a wild-type strain of Bacillus thuringiensis. J Gen Appl Microbiol 50(4):183–188. https://doi.org/10.2323/jgam.50.183
Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo JH (2013) Biocontrol of tomato wilt Disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15(3):848–864. https://doi.org/10.1111/j.1462-2920.2012.02860.x
Coohill TP, Sagripanti J-L (2009) Bacterial inactivation by solar ultraviolet radiation compared with sensitivity to 254 nm radiation. Photochem Photobiol 85(5):1043–1052. https://doi.org/10.1111/j.1751-1097.2009.00586.x
Cortesão M, Fuchs FM, Commichau FM, Eichenberger P, Schuerger AC, Nicholson WL, Setlow P, Moeller RJFIM (2019) Bacillus subtilis spore resistance to simulated mars surface conditions. Front Microbiol 10:333. https://doi.org/10.3389/fmicb.2019.00333
Dame ZT, Rahman M, Islam T (2021) Bacilli as sources of agrobiotechnology: recent advances and future directions. Green Chem Lett and Rev 14(2):246–271. https://doi.org/10.1080/17518253.2021.1905080
De Carvalho C (2017) Biofilms: microbial strategies for surviving Uv exposure. Adv Exp Med Biol 996:233–239. https://doi.org/10.1007/978-3-319-56017-5_19
Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97(7):3526–3531. https://doi.org/10.1073/pnas.060023897
Ehling-Schulz M, Lereclus D, Koehler TM (2019) The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.GPP1123-0032-2018
Elham J, Bel Y, Maghsoudi S, Noroozian E, Escriche B (2023) Enhancing insecticidal efficacy of Bacillus thuringiensis Cry1Ab through pH-sensitive encapsulation. Appl Microbiol Biotechnol 107(20):6407–6419. https://doi.org/10.1007/s00253-023-12723-w
Etesami H, Jeong B, Glick B (2023) Potential use of Bacillus spp. As an effective biostimulant against abiotic stresses in crops—a review. Curr Res Biotechn 5:100128. https://doi.org/10.1016/j.crbiot.2023.100128
Fernando RG, Del Rocío BO, Saúl CB, Peter S, Mario PR (2016) The reca-dependent sos response is active and required for processing of DNA damage during Bacillus subtilis sporulation. PLoS ONE 11(3):e0150348. https://doi.org/10.1371/journal.pone.0150348
Gao H, Qi G, Yin R, Zhang H, Li C, Zhao X (2016) Bacillus cereus strain s2 shows high nematicidal activity against Meloidogyne incognita by producing sphingosine. Sci Rep 6(1):28756. https://doi.org/10.1038/srep28756
Ghribi D, Zouari N, Jaoua S (2004) Improvement of bioinsecticides production through mutagenesis of Bacillus thuringiensis by UV and nitrous acid affecting metabolic pathways and/or delta-endotoxin synthesis. J Appl Microbiol 97(2):338–346. https://doi.org/10.1111/j.1365-2672.2004.02323.x
Goranov AI, Kuester-Schoeck E, Wang JD, Grossman AD (2006) Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis. J Bacteriol 188(15):5595–5605. https://doi.org/10.1128/JB.00342-06
Griego VM, Spence KD (1978) Inactivation of Bacillus thuringiensis spores by ultraviolet and visible light. Appl Environ Microbiol 35(5):906–910. https://doi.org/10.1128/aem.35.5.906-910.19
Härtig E, Jahn D (2012) Regulation of the anaerobic metabolism in Bacillus subtilis. Adv Microb Physiol 61:195–216. https://doi.org/10.1016/B978-0-12-394423-8.00005-6
Hashem A, Tabassum B, Fathi Abd_Allah E (2019) Bacillus subtilis: a plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi J Biol Sci 26(6):178. https://doi.org/10.1016/j.sjbs.2019.05.004
Hinarejos E, Castellano MM, Rodrigo I, Bellés JM, Conejero V, López-Gresa MP, Lisón P (2016) Bacillus subtilis IAB/BS03 as a potential biological control agent. Eur J Plant Pathol 146:597–608. https://doi.org/10.1007/s10658-016-0945-3
Hmani M, Boukedi H, Ben Khedher S, Elleuch A, Tounsi S, Abdelkefi-Mesrati L (2018) Improvement of Vip3Aa16 toxin production and efficiency through nitrous acid and uv mutagenesis of Bacillus thuringiensis (Bacillales: Bacillaceae). J Econ Entomol 111(1):108–111. https://doi.org/10.1093/jee/tox328
Hoti SL, Balaraman K (1993) Formation of melanin pigment by a mutant of Bacillus thuringiensis H-14. J Gen Microbiol 139(10):2365–2369. https://doi.org/10.1099/00221287-139-10-2365
Huang T, Zhang X, Pan J, Su X, Jin X, Guan X (2016) Purification and characterization of a novel cold shock protein-like bacteriocin synthesized by Bacillus thuringiensis. Sci Rep 6(1):35560. https://doi.org/10.1038/srep35560
Huang T, Lin Q, Qian X, Zheng Y, Yao J, Wu H, Li M et al (2018) Nematicidal activity of Cry1Ea11 from Bacillus thuringiensis BRC-XQ12 against the pine wood nematode (Bursaphelenchus Xylophilus). Phytopathol 108(1):44–51. https://doi.org/10.1094/phyto-05-17-0179-r
Hullo MF, Moszer I, Danchin A, Martin-Verstraete I (2001) Cota of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 183(18):5426–5430. https://doi.org/10.1128/jb.183.18.5426-5430.2001
Ibrahim MA, Griko N, Junker M, Bulla LA (2010) Bacillus thuringiensis: a genomics and proteomics perspective. Bioeng Bugs 1(1):31–50. https://doi.org/10.4161/bbug.1.1.10519
Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A et al (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nat 423(6935):87–91. https://doi.org/10.1038/nature01582
Jalali E, Maghsoudi S, Noroozian E (2020) A novel method for biosynthesis of different polymorphs of TiO2 nanoparticles as a protector for Bacillus thuringiensis from ultra violet. Sci Rep 10(1):426. https://doi.org/10.1038/s41598-019-57407-6
Jallouli W, Sellami S, Sellami M, Tounsi S (2014) Efficacy of olive mill wastewater for protecting Bacillus thuringiensis formulation from UV radiations. Acta Trop 140:19–25. https://doi.org/10.1016/j.actatropica.2014.07.016
Jianping Z, Jun C, Yinyue D, Yuehua C, Gaixin R (2007) Characterization of melanin produced by a wild-type strain of Bacillus cereus. Front Biol China 2(1):26–29. https://doi.org/10.1007/s11515-007-0004-8
Katrien B, Dongmin KT, Marc H, Chris M, Abram A, Andreja R, Frank D (2020) Directed evolution by uv-c treatment of Bacillus cereus spores. Int J Food Microbiol 317:108424. https://doi.org/10.1016/j.ijfoodmicro.2019.108424
Kim SS, Kim SH, Park SH, Kang DH (2020) Inactivation of Bacillus cereus spores on stainless steel by combined superheated steam and UV-C irradiation treatment. J Food Prot 83(1):13–16. https://doi.org/10.4315/0362-028x.jfp-19-133
Lin F, Mao Y, Zhao F, Idris AL, Liu Q, Zou S, Guan X, Huang T (2023) Towards sustainable green adjuvants for microbial pesticides: recent progress, upcoming challenges, and future perspectives. Microorganisms 11(2):364. https://doi.org/10.3390/microorganisms11020364
Liu N, Zhang T, Wang YJ, Huang YP, Ou JH, Shen P (2004) A heat inducible tyrosinase with distinct properties from Bacillus thuringiensis. Lett Appl Microbiol 39(5):407–412. https://doi.org/10.1111/j.1472-765X.2004.01599.x
Lv J, Zhang X, Gao T, Cui T, Peng Q, Zhang J, Song F (2019) Effect of the spoIIID mutation on mother cell lysis in Bacillus thuringiensis. Appl Microbiol Biotechnol 103(10):4103–4112. https://doi.org/10.1007/s00253-019-09722-1
Maghsoudi S, Jalali E (2017) Noble UV protective agent for Bacillus thuringiensis based on a combination of graphene oxide and olive oil. Sci Rep 7(1):11019. https://doi.org/10.1038/s41598-017-11080-9
Manasherob R, Ben-Dov E, Xiaoqiang W, Boussiba S, Zaritsky A (2002) Protection from UV-B damage of mosquito larvicidal toxins from Bacillus thuringiensis subsp. Israelensis expressed in Anabaena Pcc 7120. Curr Microbiol 45(3):217–220. https://doi.org/10.1007/s00284-001-0106-5
Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13(6):614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
Martinez-Garcia M, Sauceda-Gálvez JN, Codina-Torrella I, Hernández-Herrero MM, Gervilla R, Roig-Sagués AX (2019) Evaluation of continuous UV-C treatments and its combination with Uhph on spores of Bacillus subtilis in whole and skim milk. Foods (Basel Switzerland) 8(11):539. https://doi.org/10.3390/foods8110539
Mehraj I, Latha CN (2010) Effect of UV rays (265nm) to determine the minimum amount of exposure required to effect a 100% kill of the organism. Bacillus cereus, an endospore-former, and Staphylococcus aureus, a non-endospore-former will be used to provide a comparison of the related resistances of vegetative and spore types. Biomed Pharmacol J 3(2):431–434
Moeller R, Setlow P, Reitz G, Nicholson WL (2009) Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl Environ Microbiol 75(16):5202–5208. https://doi.org/10.1128/aem.00789-09
Moeller VlašićI, Reitz G, Nicholson WL (2012) Role of altered rpoB alleles in Bacillus subtilis sporulation and spore resistance to heat, hydrogen peroxide, formaldehyde, and glutaraldehyde. Arch Microbiol 194(9):759–767. https://doi.org/10.1007/s00203-012-0811-4
Mohamed H-LA, Abd El-Fatah MR, Sabbour MM, El-Sharkawey AZ, El-Sayed RS (2010) Genetic modification of Bacillus thuringiensis var. Kurstaki HD-73 to overproduce melanin, UV resistance and their insecticidal potentiality against potato tuber moth. Intl J Acad Res, 2(6)
Muhammad MH, Idris AL, Fan X, Guo Y, Yu Y, Jin X, Qiu J, Guan X, Huang T (2020) Beyond risk: Bacterial biofilms and their regulating approaches. Front Microbiol 11:928. https://doi.org/10.3389/fmicb.2020.00928
Nicholson, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64(3):548–572. https://doi.org/10.1128/mmbr.64.3.548-572.2000
Nishiwaki H, Ito K, Otsuki K, Yamamoto H, Komai K, Matsuda K (2004) Purification and functional characterization of insecticidal sphingomyelinase C produced by Bacillus cereus. Eur J Biochem 271(3):601–606. https://doi.org/10.1111/j.1432-1033.2003.03962.x
Nowell RW, Laue BE, Sharp PM, Green S (2016) Comparative genomics reveals genes significantly associated with woody hosts in the plant pathogen Pseudomonas syringae. Mol Plant Pathol 17(9):1409–1424. https://doi.org/10.1111/mpp.12423
Omotade TO, Bernhards RC, Klimko CP, Matthews ME, Hill AJ, Hunter MS, Webster WM et al (2014) The impact of inducing germination of Bacillus anthracis and Bacillus thuringiensis spores on potential secondary decontamination strategies. J Appl Microbiol 117(6):1614–1633. https://doi.org/10.1111/jam.12644
Pan X, Xu Z, Li L, Shao E, Chen S, Huang T, Chen Z et al (2017) Adsorption of insecticidal crystal protein Cry11Aa onto nano-Mg(OH)2: effects on bioactivity and anti-ultraviolet ability. J Agric Food Chem 65(43):9428–9434. https://doi.org/10.1021/acs.jafc.7b03410
Patil SV, Patil CD, Narkhede CP, Suryawanshi R, Koli SH, Shinde LV, Mohite BV (2018) Phytosynthesized Gold nanoparticles-Bacillus thuringiensis (Bt-GNP) formulation: a novel photo stable preparation against mosquito larvae. J Clust Sci 29:577–583. https://doi.org/10.1007/s10876-018-1368-4
Pezzoni M, Pizarro RA, Costa CS (2018) Exposure to low doses of UV-A increases biofilm formation in Pseudomonas aeruginosa. Biofouling 34(6):673–684. https://doi.org/10.1080/08927014.2018.1480758
Poopathi S, Mani C, Thirugnanasambantham K, Praba VL, Ahangar NA, Balagangadharan K (2014) Identification and characterization of a novel marine Bacillus cereus for mosquito control. Parasitol Res 113(1):323–332. https://doi.org/10.1007/s00436-013-3658-y
Pozo-Antonio JS, Sanmartín P (2018) Exposure to artificial daylight or uv irradiation (A, B or C) prior to chemical cleaning: an effective combination for removing phototrophs from granite. Biofouling 34(8):851–869. https://doi.org/10.1080/08927014.2018.1512103
Radhakrishnan R, Hashem A, Abd_Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 6(8):667. https://doi.org/10.3389/fphys.2017.00667
Ralf M, Gerda H, Rainer F, Erko S (2005) Role of pigmentation in protecting Bacillus sp. endospores against environmental UV radiation. FEMS Microbiol Ecol 51(2):231–236. https://doi.org/10.1016/j.femsec.2004.08
Ralf M, Douki T, Cadet J, Stackebrandt E, Wayne LN, Rettberg P, Reitz G, Horneck G (2007a) UV-radiation-induced formation of DNA bipyrimidine photoproducts in Bacillus subtilis endospores and their repair during germination. Intl Microbiol 10(1):39–46
Ralf M, Erko S, Günther R, Thomas B, Petra R, Aidan JD, Gerda H, Wayne NL (2007b) Role of DNA repair by nonhomologous-end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV, and ionizing radiation. J Bacteriol 189(8):3306–3311. https://doi.org/10.1128/JB.00018-07
Ralf M, Thierry D, Petra R, Günther R, Jean G, Wayne LN, Gerda H (2010) Genomic bipyrimidine nucleotide frequency and microbial reactions to germicidal uv radiation. Arch Microbiol 192(7):521–529. https://doi.org/10.1007/s00203-010-0579-3
Ralf M, Wassmann M, Reitz G, Setlow P (2011) Effect of radioprotective agents in sporulation medium on Bacillus subtilis spore resistance to hydrogen peroxide, wet heat and germicidal and environmentally relevant UV radiation. J Appl Microbiol 110(6):1485–1494. https://doi.org/10.1111/j.1365-2672.2011.05004.x
Ramírez-Guadiana FH, Barraza-Salas M, Ramírez-Ramírez N, Ortiz-Cortés M, Setlow P, Pedraza-Reyes M (2012) Alternative excision repair of ultraviolet B- and C-induced DNA damage in dormant and developing spores of Bacillus subtilis. J Bacteriol 194(22):6096–6104. https://doi.org/10.1128/jb.01340-12
Ramírez-Guadiana FH, Del Barajas-Ornelas C, Ayala-García R, Yasbin VM, Robleto RE E, Pedraza-Reyes M (2013) Transcriptional coupling of DNA repair in sporulating Bacillus subtilis cells. Mol Microbiol 90(5):1088–1099. https://doi.org/10.1111/mmi.12417
Rivas-Castillo AM, Yasbin RE, Robleto E, Nicholson WL, Pedraza-Reyes M (2010) Role of the y-family DNA polymerases yqjh and yqjw in protecting sporulating Bacillus subtilis cells from DNA damage. Curr Microbiol 60(4):263–267. https://doi.org/10.1007/s00284-009-9535-3
Ruan L, Yu Z, Fang B, He W, Wang Y, Shen P (2004) Melanin pigment formation and increased UV resistance in Bacillus thuringiensis following high temperature induction. Syst Appl Microbiol 27(3):286–289. https://doi.org/10.1078/0723-2020-00265
Ruiu L, Falchi G, Floris I, Marche MG, Mura ME, Satta A (2015) Pathogenicity and characterization of a novel Bacillus cereus sensu lato isolate toxic to the mediterranean fruit fly ceratitis capitata wied. J Invertebr Pathol 126:71–77. https://doi.org/10.1016/j.jip.2015.01.010
Saoussen BK, Boutheina MT, Slim T (2021) Biological potential of Bacillus subtilis V26 for the control of Fusarium wilt and tuber dry rot on potato caused by Fusarium species and the promotion of plant growth. Biolog Contrl 152:104444. https://doi.org/10.1016/j.biocontrol.2020.104444
Saxena D, Ben-Dov E, Manasherob R, Barak Z, Boussiba S, Zaritsky A (2002) A UV tolerant mutant of Bacillus thuringiensis subsp. Kurstaki producing melanin. Curr Microbiol 44(1):25–30. https://doi.org/10.1007/s00284-001-0069-6
Schünemann R, Knaak N (2014) Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean culture. ISRN MIcrobiol 20:135675. https://doi.org/10.1155/2014/135675
Setlow P (2001) Resistance of spores of Bacillus species to ultraviolet light. Environ Mol Mutagen 38(2–3):97–104. https://doi.org/10.1002/em.1058
Setlow P (2007) I will survive: DNA protection in bacterial spores. Trends Microbiol 15(4):172–180. https://doi.org/10.1016/j.tim.2007.02.004
Setlow, Setlow P (1996) Role of DNA repair in Bacillus subtilis spore resistance. J Bacteriol 178(12):3486–3495. https://doi.org/10.1128/jb.178.12.3486-3495.1996
Setlow PS, Zhang P, Li YQ, Neely W, Setlow P (2014) Mechanism of killing of spores of Bacillus anthracis in a high-temperature gas environment, and analysis of DNA damage generated by various decontamination treatments of spores of Bacillus anthracis, Bacillus subtilis and Bacillus thuringiensis. J Appl Microbiol 116(4):805–814. https://doi.org/10.1111/jam.12421
Shen L, Griffith TM, Nyangaresi PO, Qin Y, Pang X, Chen G-L, Li M, Lu Y, Zhang B (2019) Efficacy of UVC-led in water disinfection on Bacillus species with consideration of antibiotic resistance issue. J Hazard Mater 386:121968. https://doi.org/10.1016/j.jhazmat.2019.121968
Siddiqui ZA, Mahmood I (1999) Role of bacteria in the management of plant parasitic nematodes: a review. Bioresour Technol 69:167–179. https://doi.org/10.1016/S0960-8524(98)00122-9
Su X, Li L, Pan J, Fan X, Ma S, Guo Y, Idris AL et al (2020) Identification and partial purification of thuricin 4AJ1 produced by Bacillus thuringiensis. Arch Microbiol 202(4):755–763. https://doi.org/10.1007/s00203-019-01782-1
Subramoni S, Nathoo N, Klimov E, Yuan Z-C (2014) Agrobacterium tumefaciens responses to plant-derived signaling molecules. Front Plant sci 5:322–322. https://doi.org/10.3389/fpls.2014.00322
Tan TT, Zhang XD, Miao Z, Yu Y, Du SL, Hou XY, Cai J (2019) A single point mutation in hmgA leads to melanin accumulation in Bacillus thuringiensis BMB181. Enzyme Microb Technol 120:91–97. https://doi.org/10.1016/j.enzmictec.2018.10.007
Taylor W, Camilleri E, Craft DL, Korza G, Granados MR, Peterson J, Szczpaniak R et al (2020) DNA damage kills bacterial spores and cells exposed to 222-nanometer UV radiation. Appl Environ Microbiol 86(8):e03039–e03019. https://doi.org/10.1128/AEM.03039-19
Tian B, Yang J, Zhang KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61(2):197–213. https://doi.org/10.1111/j.1574-6941.2007.00349.x
Wassmann M, Moeller R, Reitz G, Rettberg PJA (2010) Adaptation of Bacillus subtilis cells to archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiol 10(6):605–615. https://doi.org/10.1089/ast.2009.0455
Wayne LN, Galeano B (2003) UV resistance of Bacillus anthracis spores revisited: validation of Bacillus subtilis spores as UV surrogates for spores of Bacillus anthracis sterne. Appl Environ Microbiol 69(2):1327–1330. https://doi.org/10.1128/AEM.69.2.1327-1330.2003
Wayne LN, Schuerger AC, Setlow P (2005) The solar UV environment and bacterial spore UV resistance: considerations for earth-to-mars transport by natural processes and human spaceflight. Mutat Res 571(1–2):249–264. https://doi.org/10.1016/j.mrfmmm.2004.10.012
Wayne LN, Schuerger AC, Douki T (2018) The photochemistry of unprotected DNA and DNA inside Bacillus subtilis spores exposed to simulated martian surface conditions of atmospheric composition, temperature, pressure, and solar radiation. Astrobiol 18(4):393–402. https://doi.org/10.1089/ast.2017.1721
Wood JP, Meyer KM, Kelly TJ, Choi YW, Rogers JV, Riggs KB, Willenberg ZJ (2015) Environmental persistence of Bacillus anthracis and Bacillus subtilis spores. PLoS ONE 10(9):e0138083. https://doi.org/10.1371/journal.pone.0138083
Xihua L, Zhang Y, Du X, Luo X, Tan W, Guan X, Zhang L (2023) Effect of yhfs gene on Bt LLP29 antioxidant and UV ray resistance. Pest Manag Sci 79(6):2087–2097. https://doi.org/10.1002/ps.7385
Xu J, Wu C, Yang Z, Liu W, Chen H, Batool K, Yao J et al (2020) For: Pesticide biochemistry and physiology recG is involved with the resistance of Bt to UV. Pestic Biochem Physiol 167:104599. https://doi.org/10.1016/j.pestbp.2020.104599
Yuan S, Liu C, Fang H, Zhang D (2020) Bacillus subtilis: a universal cell factory for industry, agriculture, biomaterials and medicine. Microb Cell Factories 19(1):173. https://doi.org/10.1186/s12934-020-01436-8
Zhang, Huang E, Lin J, Gelbič I, Zhang Q, Guan Y, Huang T, Guan X (2010) A novel mosquitocidal Bacillus thuringiensis strain LLP29 isolated from the phylloplane of Magnolia denudata. Microbiol Res 165(2):133–141. https://doi.org/10.1016/j.micres.2009.03.002
Zhang, Yan JP, Zheng DS, Sun YJ, Yuan ZM (2008) Expression of mel gene improves the UV resistance of Bacillus thuringiensis. J Appl Microbiol 105(1):151–157. https://doi.org/10.1111/j.1365-2672.2008.03729.x
Zhang, Zhang X, Zhang Y, Wu S, Gelbič I, Xu L, Guan X (2016) A new formulation of Bacillus thuringiensis: UV protection and sustained release mosquito larvae studies. Sci Rep 6(1):39425. https://doi.org/10.1038/srep39425
Zhang, Zhang X, Batool K, Hu X, Chen M, Xu J, Wang J et al (2018) Comparison and mechanism of the UV-resistant mosquitocidal bt mutant LLP29-m19. J Med Entomol 55(1):210–216. https://doi.org/10.1093/jme/tjx192
Zhu L, Chu Y, Zhang B, Yuan X, Wang K, Liu Z, Sun M (2022) Creation of an industrial Bacillus thuringiensis strain with high melanin production and UV tolerance by gene editing. Front Microbiol 13:913715. https://doi.org/10.3389/fmicb.2022.913715
Funding
This project was supported by the Fujian Science and Technology Projects (No. 2020N5014 and No. 2023XQ019), the Fujian Agriculture and Forestry University Construction Project for Technological Innovation and Service System of Tea Industry Chain (No. K1520005A03), and the National Natural Science Foundation of China (No. 31672084). We thank the members of the Biopesticide Research Center at Fujian Agriculture and Forestry University for its help. Thanks, were also extended to the referees for their productive comments.
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HT and ALI conceived the study. ALI reviewed the Literature and wrote the manuscript. WL, FH, and FL help in searching for the Literature. HT and XG reviewed the manuscript and offer funding support. All authors read and approved the final version of the manuscript.
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Idris, A.L., Li, W., Huang, F. et al. Impacts of UV radiation on Bacillus biocontrol agents and their resistance mechanisms. World J Microbiol Biotechnol 40, 58 (2024). https://doi.org/10.1007/s11274-023-03856-1
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DOI: https://doi.org/10.1007/s11274-023-03856-1