真菌在蚊虫防控中的应用研究进展

doi:10.11853/j.issn.1003.8280.2023.06.021

摘要/Abstract

摘要： 蚊虫是疟疾、登革热等传染病的重要传播媒介,对人类健康造成严重威胁。基于杀虫剂的化学防治是当前蚊媒疾病媒介控制的主要策略之一,但杀虫剂抗药性的威胁日益严重,迫切需要开发更多的蚊虫控制工具。昆虫病原真菌可作为化学杀虫剂的一种环保替代品,能够通过影响蚊虫的寿命和媒介能力等达到防控蚊虫和蚊媒传染病的目的,也能通过转基因技术对真菌进行改造间接发挥作用。该文对绿僵菌、白僵菌和大链壶菌等主要杀蚊真菌进行介绍,并对其在蚊虫防控中的研究进展进行综述和展望。

关键词: 真菌, 蚊虫防控, 绿僵菌, 白僵菌, 大链壶菌

Abstract: Mosquitoes are important vectors of infectious diseases such as malaria and dengue fever, posing a serious threat to human health. Insecticide-based chemical control is currently one of the main strategies for vector control of mosquito-borne diseases, but the growing threat of insecticide resistance has created an urgent need for the development of additional mosquito control tools. Entomopathogenic fungi can be used as an environmentally friendly alternative to chemical insecticides, because they can control mosquitoes and mosquito-borne infectious diseases by affecting the life span and vector ability of mosquitoes and play an indirect role by modifying fungi through transgenic technology. This review provides an introduction to the main mosquito-killing fungi, such as Metarhizium anisopliae, Beauveria bassiana, and Lagenidium giganteum, and summarizes the progress of their research in mosquito control.

Key words: Fungus, Mosquito control, Metarhizium anisopliae, Beauveria bassiana, Lagenidium giganteum

中图分类号:

邓思佳, 胡鞠萍, 朱国鼎. 真菌在蚊虫防控中的应用研究进展[J]. 中国媒介生物学及控制杂志, 2023, 34(6): 819-823.

DENG Si-jia, HU Ju-ping, ZHU Guo-ding. Research progress of the application of fungi in mosquito control[J]. Chinese Journal of Vector Biology and Control, 2023, 34(6): 819-823.

参考文献

[1] Lee JY,Woo RM,Choi CJ,et al. Beauveria bassiana for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults shows high conidia persistence and productivity[J]. AMB Express,2019,9（1）:206. DOI:10.1186/s13568-019-0933-z.
[2] Grubaugh ND,Fauver JR,Rückert C,et al. Mosquitoes transmit unique West Nile virus populations during each feeding episode[J]. Cell Rep,2017,19（4）:709-718. DOI:10.1016/j.celrep. 2017.03.076.
[3] Cui CL,Wang Y,Li YF,et al. Expression of mosquito miRNAs in entomopathogenic fungus induces pathogen-mediated host RNA interference and increases fungal efficacy[J]. Cell Rep,2022,41（4）:111527. DOI:10.1016/j.celrep.2022.111527.
[4] Weaver SC,Charlier C,Vasilakis N,et al. Zika,chikungunya,and other emerging vector-borne viral diseases[J]. Annu Rev Med,2018,69:395-408. DOI:10.1146/annurev-med-050715-105122.
[5] Wang Y,Cui CL,Wang GD,et al. Insects defend against fungal infection by employing microRNAs to silence virulence-related genes[J]. Proc Natl Acad Sci USA,2021,118（19）:e2023802118. DOI:10.1073/pnas.2023802118.
[6] Lopez-Perez M,Rodriguez-Gomez D,Loera O. Production of conidia of Beauveria bassiana in solid-state culture:Current status and future perspectives[J]. Crit Rev Biotechnol,2015,35（3）:334-341. DOI:10.3109/07388551.2013.857293.
[7] Hemingway J,Ranson H. Insecticide resistance in insect vectors of human disease[J]. Annu Rev Entomol,2000,45:371-391. DOI:10.1146/annurev.ento.45.1.371.
[8] Damalas CA,Eleftherohorinos IG. Pesticide exposure,safety issues,and risk assessment indicators[J]. Int J Environ Res Public Health,2011,8（5）:1402-1419. DOI:10.3390/ijerph 8051402.
[9] de Oliveira Barbosa Bitencourt R,Corrêa TA,Santos-Mallet J,et al. Beauveria bassiana interacts with gut and hemocytes to manipulate Aedes aegypti immunity[J]. Parasit Vectors,2023,16（1）:17. DOI:10.1186/s13071-023-05655-x.
[10] Nakahara Y,Shimura S,Ueno C,et al. Purification and characterization of silkworm hemocytes by flow cytometry[J]. Dev Comp Immunol,2009,33（4）:439-448. DOI:10.1016/j.dci.2008.09.005.
[11] Vivekanandhan P,Kavitha T,Karthi S,et al. Toxicity of Beauveria bassiana-28 mycelial extracts on larvae of Culex quinquefasciatus mosquito （Diptera:Culicidae）[J]. Int J Environ Res Public Health,2018,15（3）:440. DOI:10.3390/ijerph 15030440.
[12] Chelico L,Khachatourians GG. Isolation and characterization of nucleotide excision repair deficient mutants of the entomopathogenic fungus,Beauveria bassiana[J]. J Invertebr Pathol,2008,98（1）:93-100. DOI:10.1016/j.jip.2007.10.006.
[13] Bartholomay LC,Michel K. Mosquito immunobiology:The intersection of vector health and vector competence[J]. Annu Rev Entomol,2018,63:145-167. DOI:10.1146/annurev-ento-010715-023530.
[14] Garza-Hernández JA,Rodríguez-Pérez MA,Salazar MI,et al. Vectorial capacity of Aedes aegypti for dengue virus type 2 is reduced with co-infection of Metarhizium anisopliae[J]. PLoS Negl Trop Dis,2013,7（3）:e2013. DOI:10.1371/journal.pntd. 0002013.
[15] Clark TB,Kellen WR,Fukuda T,et al. Field and laboratory studies on the pathogenicity of the fungus Beauveria bassiana to three genera of mosquitoes[J]. J Invertebr Pathol,1968,11（1）:1-7. DOI:10.1016/0022-2011（68）90047-5.
[16] Lai YL,Chen H,Wei G,et al. In vivo gene expression profiling of the entomopathogenic fungus Beauveria bassiana elucidates its infection stratagems in Anopheles mosquito[J]. Sci China Life Sci,2017,60（8）:839-851. DOI:10.1007/s11427-017-9101-3.
[17] Howard AF,N’guessan R,Koenraadt CJ,et al. The entomopathogenic fungus Beauveria bassiana reduces instantaneous blood feeding in wild multi-insecticide-resistant Culex quinquefasciatus mosquitoes in Benin,West Africa[J]. Parasit Vectors,2010,3（1）:87. DOI:10.1186/1756-3305-3-87.
[18] Hajek AE,Wraight SP,Vandenberg JD. Control of arthropods using pathogenic fungi[M]//Pointing SB,Hyde KD. Bio-exploitation of filamentous fungi. Hong Kong,China:Fungal Diversity Press,2001:309-347.
[19] St Leger RJ,Wang JB. Metarhizium:Jack of all trades,master of many[J]. Open Biol,2020,10（12）:200307. DOI:10.1098/rsob.200307.
[20] Aw KMS,Hue SM. Mode of infection of Metarhizium spp. fungus and their potential as biological control agents[J]. J Fungi,2017,3（2）:30. DOI:10.3390/jof3020030.
[21] Wu CC,Tang D,Dai J,et al. Bioremediation of mercury-polluted soil and water by the plant symbiotic fungus Metarhizium robertsii[J]. Proc Natl Acad Sci USA,2022,119（47）:e2214513119. DOI:10.1073/pnas.2214513119.
[22] Nong XQ,Wang GJ,Cai N,et al. Multiple association of Metarhizium with plants and the application potential in plant protection[J]. Plant Prot,2022,48（3）:22-30,54. DOI:10.16688/j.zwbh.2022215.（in Chinese）农向群,王广君,蔡霓,等. 绿僵菌与植物的多重关系及其在植物保护中的应用潜力[J]. 植物保护,2022,48（3）:22-30,54. DOI:10.16688/j.zwbh.2022215
[23] Scholte EJ,Ng’habi K,Kihonda J,et al. An entomopathogenic fungus for control of adult African malaria mosquitoes[J]. Science,2005,308（5728）:1641-1642. DOI:10.1126/science. 1108639.
[24] Lai LY,Cao X,Chen JJ,et al. Coordinated regulation of infection-related morphogenesis by the KMT2-Cre1-Hyd4 regulatory pathway to facilitate fungal infection[J]. Sci Adv,2020,6（13）:eaaz1659. DOI:10.1126/sciadv.aaz1659.
[25] Wang LL,Lai YL,Chen JJ,et al. The ASH1-PEX16 regulatory pathway controls peroxisome biogenesis for appressorium-mediated insect infection by a fungal pathogen[J]. Proc Natl Acad Sci USA,2023,120（4）:e2217145120. DOI:10.1073/pnas.2217145120.
[26] Butt TM,Greenfield BP,Greig C,et al. Metarhizium anisopliae pathogenesis of mosquito larvae:A verdict of accidental death[J]. PLoS One,2013,8（12）:e81686. DOI:10.1371/journal.pone.0081686.
[27] Golkar L,LeBrun RA,Ohayon H,et al. Variation of larval susceptibility to Lagenidium giganteum in three mosquito species[J]. J Invertebr Pathol,1993,62（1）:1-8. DOI:10.1006/jipa.1993.1066.
[28] Kramer VI. Laboratory evaluation of Lagenidium giganteum （Oomycetes:Lagenidiales） in water from Contra Costa county,California,mosquito sources[J]. J Am Mosq Control Assoc,1990,6（1）:79-83.
[29] Patel KJ,Rueda LM,Axtell RC,et al. Temperature-dependent development of the fungal pathogen Lagenidium giganteum （Oomycetes:Lagenidiales） in larvae of Culex quinquefasciatus （Diptera:Culicidae）[J]. J Med Entomol,1991,28（1）:95-100. DOI:10.1093/jmedent/28.1.95.
[30] Grooters AM. Pythiosis,lagenidiosis,and zygomycosis in small animals[J]. Vet Clin North Am Small Anim Pract,2003,33（4）:695-720. DOI:10.1016/s0195-5616（03）00034-2.
[31] Vilela R,Taylor JW,Walker ED,et al. Lagenidium giganteum pathogenicity in mammals[J]. Emerg Infect Dis,2015,21（2）:290-297. DOI:10.3201/eid2102.141091.
[32] Su XQ. A new species of Pythium isolated from mosquito lavae and its ITS region of rDNA[J]. Mycosystema,2006,25（4）:523-528. DOI:10.3969/j.issn.1672-6472.2006.04.004.（in Chinese）苏晓庆. 分离自蚊幼虫的腐霉一新种及其rDNA的ITS区段分析[J]. 菌物学报,2006,25（4）:523-528. DOI:10.3969/j.issn.1672-6472.2006.04.004.
[33] Su XQ. An introduction to a new type of mosquito-biological control agent against mosquito larvae[J]. Chin J Hyg Insect Equip,2016,22（4）:401-404. DOI:10.19821/j.1671-2781. 2016.04.029.（in Chinese）苏晓庆. 一种新型的真菌灭蚊幼剂[J]. 中华卫生杀虫药械,2016,22（4）:401-404. DOI:10.19821/j.1671-2781.2016.04.029.
[34] Lei JJ,Gong MQ,Liu LJ. Research progress in the mechanisms and effects of biological insecticides for mosquitoes[J]. J Trop Dis Parasitol,2022,20（4）:235-240. DOI:10.3969/j.issn.1672-2302.2022.04.012.（in Chinese）类晶晶,公茂庆,刘丽娟. 媒介蚊虫生物杀虫剂杀虫机制及效果研究进展[J]. 热带病与寄生虫学,2022,20（4）:235-240. DOI:10.3969/j.issn.1672-2302.2022.04.012.
[35] de Paula AR,LEI Silva,Ribeiro A,et al. Metarhizium anisopliae blastospores are highly virulent to adult Aedes aegypti,an important arbovirus vector[J]. Parasit Vectors,2021,14（1）:555. DOI:10.1186/s13071-021-05055-z.
[36] de Faria MR,Wraight SP. Mycoinsecticides and mycoacaricides:A comprehensive list with worldwide coverage and international classification of formulation types[J]. Biol Control,2007,43（3）:237-256. DOI:10.1016/j.biocontrol.2007.08.001.
[37] Kanzok SM,Jacobs-Lorena M. Entomopathogenic fungi as biological insecticides to control malaria[J]. Trends Parasitol,2006,22（2）:49-51. DOI:10.1016/j.pt.2005.12.008.
[38] Rodrigues J,Bergamini C,Montalva C,et al. Simple method to detect and to isolate entomopathogenic fungi （Hypocreales） from mosquito larvae[J]. J Invertebr Pathol,2021,182:107581. DOI:10.1016/j.jip.2021.107581.
[39] Reyes-Villanueva F,Garza-Hernandez JA,Garcia-Munguia AM,et al. Dissemination of Metarhizium anisopliae of low and high virulence by mating behavior in Aedes aegypti[J]. Parasit Vectors,2011,4（1）:171. DOI:10.1186/1756-3305-4-171.
[40] Darbro JM,Thomas MB. Spore persistence and likelihood of aeroallergenicity of entomopathogenic fungi used for mosquito control[J]. Am J Trop Med Hyg,2009,80（6）:992-997. DOI:10.4269/ajtmh.2009.80.992.
[41] Morales-Rodriguez A,Peck DC. Synergies between biological and neonicotinoid insecticides for the curative control of the white grubs Amphimallon majale and Popillia japonica[J]. Biol Control,2009,51（1）:169-180. DOI:10.1016/j.biocontrol.2009. 06.008.
[42] Vivekanandhan P,Swathy K,Murugan AC,et al. Insecticidal efficacy of Metarhizium anisopliae derived chemical constituents against disease-vector mosquitoes[J]. J Fungi,2022,8（3）:300. DOI:10.3390/jof8030300.
[43] Samish M,Rot A,Ment D,et al. Efficacy of the entomopathogenic fungus Metarhizium brunneum in controlling the tick Rhipicephalus annulatus under field conditions[J]. Vet Parasitol,2014,206（3/4）:258-266. DOI:10.1016/j.vetpar.2014.10.019.
[44] Alkhaibari AM,Carolino AT,Yavasoglu SI,et al. Metarhizium brunneum blastospore pathogenesis in Aedes aegypti larvae:Attack on several fronts accelerates mortality[J]. PLoS Pathog,2016,12（7）:e1005715. DOI:10.1371/journal.ppat.1005715.
[45] Jackson MA. Optimizing nutritional conditions for the liquid culture production of effective fungal biological control agents[J]. J Ind Microbiol Biotechnol,1997,19（3）:180-187. DOI:10.1038/sj.jim.2900426.
[46] Stone LBL,Bidochka MJ. The multifunctional lifestyles of Metarhizium:Evolution and applications[J]. Appl Microbiol Biotechnol,2020,104（23）:9935-9945. DOI:10.1007/s00253-020-10968-3.
[47] Leão MPC,Tiago PV,Andreote FD,et al. Differential expression of the pr1A gene in Metarhizium anisopliae and M. acridum across different culture conditions and during pathogenesis[J]. Genet Mol Biol,2015,38（1）:86-92. DOI:10.1590/S1415-475738138120140236.
[48] de Sousa NA,Rodrigues J,Arruda W,et al. Development of Metarhizium humberi in Aedes aegypti eggs[J]. J Invertebr Pathol,2021,184:107648. DOI:10.1016/j.jip.2021.107648.
[49] Greenfield BPJ,Lord AM,Dudley E,et al. Conidia of the insect pathogenic fungus,Metarhizium anisopliae,fail to adhere to mosquito larval cuticle[J]. Roy Soc Open Sci,2014,1（2）:140193. DOI:10.1098/rsos.140193.
[50] Renuka S,Vani HC,Alex E. Entomopathogenic fungi as a potential management tool for the control of urban malaria vector,Anopheles stephensi （Diptera:Culicidae）[J]. J Fungi,2023,9（2）:223. DOI:10.3390/jof9020223.
[51] Shoukat RF,Zafar J,Shakeel M,et al. Assessment of lethal,sublethal,and transgenerational effects of Beauveria bassiana on the demography of Aedes albopictus （Culicidae:Diptera）[J]. Insects,2020,11（3）:178. DOI:10.3390/insects11030178.
[52] Paula AR,Carolino AT,Paula CO,et al. The combination of the entomopathogenic fungus Metarhizium anisopliae with the insecticide imidacloprid increases virulence against the dengue vector Aedes aegypti （Diptera:Culicidae）[J]. Parasit Vectors,2011,4（1）:8. DOI:10.1186/1756-3305-4-8.
[53] Paula AR,Ribeiro A,Lemos FJA,et al. Neem oil increases the persistence of the entomopathogenic fungus Metarhizium anisopliae for the control of Aedes aegypti （Diptera:Culicidae） larvae[J]. Parasit Vectors,2019,12（1）:163. DOI:10.1186/s13071-019-3415-x.
[54] de Oliveira Barbosa Bitencourt R,de Souza Faria F,Marchesini P,et al. Entomopathogenic fungi and Schinus molle essential oil:The combination of two eco-friendly agents against Aedes aegypti larvae[J]. J Invertebr Pathol,2022,194:107827. DOI:10.1016/j.jip.2022.107827.
[55] Wei G,Lai YL,Wang GD,et al. Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality[J]. Proc Natl Acad Sci USA,2017,114（23）:5994-5999. DOI:10.1073/pnas.1703546114.
[56] Ji YN,Lu TF,Zou Z,et al. Aedes aegypti CLIPB9 activates prophenoloxidase-3 in the presence of CLIPA14 after fungal infection[J]. Front Immunol,2022,13:927322. DOI:10.3389/fimmu.2022.927322.
[57] Cui CL,Wang Y,Liu JN,et al. A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection[J]. Nat Commun,2019,10（1）:4298. DOI:10.1038/s41467-019-12323-1.
[58] Lovett B,Bilgo E,Diabate A,et al. A review of progress toward field application of transgenic mosquitocidal entomopathogenic fungi[J]. Pest Manag Sci,2019,75（9）:2316-2324. DOI:10.1002/ps.5385.
[59] St Leger RJ,Wang CS. Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests[J]. Appl Microbiol Biotechnol,2010,85（4）:901-907. DOI:10.1007/s00253-009-2306-z.
[60] Fang WG,Vega-Rodríguez J,Ghosh AK,et al. Development of transgenic fungi that kill human malaria parasites in mosquitoes[J]. Science,2011,331（6020）:1074-1077. DOI:10.1126/science.1199115.
[61] Lovett B,Bilgo E,Millogo SA,et al. Transgenic Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso[J]. Science,2019,364（6443）:894-897. DOI:10.1126/science.aaw8737.
[62] Vogel G. Fungus with a venom gene could be new mosquito killer[J]. Science,2019,364（6443）:817. DOI:10.1126/science. 364.6443.817.
[63] Deng SQ,Zou WH,Li DL,et al. Expression of Bacillus thuringiensis toxin Cyt2Ba in the entomopathogenic fungus Beauveria bassiana increases its virulence towards Aedes mosquitoes[J]. PLoS Negl Trop Dis,2019,13（7）:e0007590. DOI:10.1371/journal.pntd.0007590.
[64] Lu JC,Shen FH,Lei Y,et al. Progress of researches on symbionts in the management of mosquito-borne infectious diseases[J]. Chin J Schistosomiasis Control,2021,33（5）:544-550. DOI:10.16250/j.32.1374.2020333.（in Chinese）陆佳晨,沈飞虎,雷瑶,等. 共生菌在控制蚊媒传染病中的研究进展[J]. 中国血吸虫病防治杂志,2021,33（5）:544-550. DOI:10.16250/j.32.1374.2020333.
[65] Jupatanakul N,Sim S,Dimopoulos G. The insect microbiome modulates vector competence for arboviruses[J]. Viruses,2014,6（11）:4294-4313. DOI:10.3390/v6114294.
[66] Dong YM,Morton JCJr,Ramirez JL,et al. The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti[J]. Insect Biochem Mol Biol,2012,42（2）:126-132. DOI:10.1016/j.ibmb.2011.11.005.
[67] Wang YH,Chang MM,Wang M,et al. OTU7B modulates the mosquito immune response to Beauveria bassiana infection via deubiquitination of the toll adaptor TRAF4[J]. Microbiol Spectr,2023,11（1）:e0312322. DOI:10.1128/spectrum.03123-22.