Highly specific host-pathogen interactions influence Metarhizium brunneum blastospore virulence against Culex quinquefasciatus larvae

References

• Scholte E-J, Knols BG, Takken W. Autodissemination of the entomopathogenic fungus Metarhizium anisopliae amongst adults of the malaria vector Anopheles gambiae ss. Malar J. 2004;3:45. DOI:10.1186/1475-2875-3-45. PMID:15566626.
   Web of Science ®Google Scholar
• Greenfield BP, Peace A, Evans H, et al. Identification of Metarhizium strains highly efficacious against Aedes, Anopheles and Culex larvae. Biocontrol Sci Technol. 2015;25:487–502.
   Web of Science ®Google Scholar
• Alkhaibari A, Carolino A, Bull J, et al. Differential pathogenicity of Metarhizium blastospores and conidia against larvae of three mosquito species. J Med Entomol. 2017;54:696–704. ; PMID:2839920210.
   PubMed Web of Science ®Google Scholar
• Driver F, Milner RJ, Trueman JW. A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res. 2000;104:134–150.
   Web of Science ®Google Scholar
• Samson RA, Evans HC, Latgé J-P. Atlas of entomopathogenic fungi. New York (NY): Springer Science & Business Media; 2013.
   Google Scholar
• Wang S, Fang W, Wang C, et al. Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathog. 2011;7:e1002097.
   PubMed Web of Science ®Google Scholar
• Scholte E-J, Njiru BN, Smallegange RC, et al. Infection of malaria (Anopheles gambiae ss) and filariasis (Culex quinquefasciatus) vectors with the entomopathogenic fungus Metarhizium anisopliae. Malar J. 2003;2:29.
   PubMed Web of Science ®Google Scholar
• Miranpuri G, Khachatourians G. Larvicidal activity of blastospores and conidiospores of Beauveria bassiana (strain GK 2016) against age groups of Aedes aegypti. Vet Parasitol. 1990;37:155–162.
   PubMed Web of Science ®Google Scholar
• Nadeau M, Boisvert J. Larvicidal activity of the entomopathogenic fungus Tolypocladium cylindrosporum (Deuteromycotina: hyphomycetes) on the mosquito Aedes triseriatus and the black fly Simulium vittatum (Diptera: simuliidae). J Am Mosq Control Assoc. 1994;10:487–491. PMID: 7707051.
   PubMed Web of Science ®Google Scholar
• Riba G, Keita A, Soares G Jr, et al. Comparative studies of Metarhizium anisopliae and Tolypocladium cylindrosporum as pathogens of mosquito larvae. J Am Mosq Control Assoc. 1986;2:469–473.
   PubMed Web of Science ®Google Scholar
• Soarés GG. Pathogenesis of infection by the hyphomycetous fungus, Tolypocladium cylindrosporum in Aedes sierrensis and Culex tarsalis [Dip.: culicidae]. Entomophaga. 1982;27:283–299.
   Google Scholar
• Alkhaibari AM, Carolino AT, Yavasoglu SI, et al. Metarhizium brunneum blastospore pathogenesis in Aedes aegypti larvae: attack on several fronts accelerates mortality. PLoS Pathog. 2016;12:e1005715. . PMID 27389584.
   PubMed Web of Science ®Google Scholar
• Butt TM, Greenfield BP, Greig C, et al. Metarhizium anisopliae pathogenesis of mosquito larvae: a verdict of accidental death. PLoS One. 2013;8:e81686. . PMID:24349111.
   PubMed Web of Science ®Google Scholar
• Greenfield BP, Lord AM, Dudley E, et al. Conidia of the insect pathogenic fungus, Metarhizium anisopliae, fail to adhere to mosquito larval cuticle. Royal Soc Open Sci. 2014;1:140193. . PMID:26064542.
   PubMed Web of Science ®Google Scholar
• Butt T, Coates C, Dubovskiy I, et al. Entomopathogenic Fungi: new Insights into Host–pathogen Interactions. Adv Genet. 2016;94:307–364.
   PubMed Web of Science ®Google Scholar
• Altre J, Vandenberg J, Cantone F. Pathogenicity of Paecilomyces fumosoroseus isolates to diamondback moth, Plutella xylostella: correlation with Spore Size, Germination Speed, and Attachment to Cuticle. J Invertebr Pathol. 1999;73:332–338. . PMID:10222189.
   PubMed Web of Science ®Google Scholar
• Iwase R, Shimizu S. Adhesion and virulence of conidia of Metarhizium anisopliae to Thrips palmi (Thysanoptera: thripidae). Jpn J Appl Entomol Z (Japan). 2004;48:275–280.
   Web of Science ®Google Scholar
• Yaginuma D, Hiromori H, Hatsukade M. Relationship between virulence and adhesion of the entomopathogenic fungus Beauveria amorpha (strain: hpBa-1) to the yellowish elongate chafer, Heptophylla picea (Motschulsky)(Coleoptera: scarabaeidae). Jpn J Appl Entomol Z (Japan). 2004;48:101–108.
   Web of Science ®Google Scholar
• Inglis GD, Goettel MS, Butt TM, et al. Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N, editors. Fungi as biocontrol agents: progress, problems and potential. Wallingford (UK): CAB International; 2001. p. 23–69.
   Google Scholar
• Butt TM. Use of entomogenous fungi for the control of insect pests. In: Esser K, Bennett JW, Kempken F, editors. Agricultural Applications: Mycota. Berlin: Springer; 2002. p. 111–134.
   Google Scholar
• Boucias D, Pendland J, Latge J. Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol. 1988;54:1795–1805. PMCID: PMC202748.
   PubMed Web of Science ®Google Scholar
• Holder DJ, Keyhani NO. Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Appl Environ Microbiol. 2005;71:5260–5266. . PMCID: PMC1214598.
   PubMed Web of Science ®Google Scholar
• Paterson IC, Charnley AK, Cooper RM, et al. Partial characterization of specific inducers of a cuticle-degrading protease from the insect pathogenic fungus Metarhizium anisopliae. Microbiology. 1994;140:3153–3159.
   PubMed Web of Science ®Google Scholar
• St Leger R. Integument as a barrier to microbial infections. In: Binnington K, Retnakaran A, editors. Physiology of the insect epidermis. Canberra: CSIRO; 1991. p. 284–306.
   Google Scholar
• Sosa-Gomez D, Boucias D, Nation J. Attachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. J Invertebr Pathol. 1997;69:31–39.
   PubMed Web of Science ®Google Scholar
• Epstein L, Nicholson R. Adhesion and adhesives of fungi and oomycetes. In: Smith AM, Callow JA, editors. Biological adhesives. Berlin: Springer; 2016. p. 25–55.
   Google Scholar
• Wang C, St Leger RJ. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot Cell. 2007;6:808–816. . PMCID: PMC1899246.
   PubMedGoogle Scholar
• Hillyer JF, Strand MR. Mosquito hemocyte-mediated immune responses. Curr Opin Immunol. 2014;3:14–21. . PMCID: PMC4190037.
   Google Scholar
• Lavine M, Strand M. Insect hemocytes and their role in immunity. Insect Biochem Mol Biol. 2002;32:1295–1309.
   PubMed Web of Science ®Google Scholar
• Yassine H, Kamareddine L, Osta MA. The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog. 2012;8:e1003029. . PMCID: PMC3499577.
   PubMed Web of Science ®Google Scholar
• Charroux B, Royet J. Drosophila immune response: from systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract. Fly. 2010;4:40–47. DOI:10.4161/fly.4.1.10810
   PubMed Web of Science ®Google Scholar
• Müller U, Vogel P, Alber G, et al. The innate immune system of mammals and insects. Trends in Innate Immunity. 2008;15:21–44. Karger Publishers. .
   Google Scholar
• Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008;29:263–271.
   PubMed Web of Science ®Google Scholar
• Tsakas S, Marmaras V. Insect immunity and its signalling: an overview. Invertebrate Surviv J. 2010;7:228–238.
   Web of Science ®Google Scholar
• Dubovskii I, Grizanova E, Chertkova E, et al. Generation of reactive oxygen species and activity of antioxidants in hemolymph of the moth larvae Galleria mellonella (L.) (Lepidoptera: piralidae) at development of the process of encapsulation. J Evol Biochem Physiol. 2010;46:35–43.
   Web of Science ®Google Scholar
• Felton GW, Summers CB. Antioxidant systems in insects. Arch Insect Biochem Physiol. 1995;29:187–197.
   PubMed Web of Science ®Google Scholar
• Lyakhovich V, Vavilin V, Zenkov N, et al. Active defense under oxidative stress. The antioxidant responsive element. Biochemistry (Moscow). 2006;71:962–974.
   PubMed Web of Science ®Google Scholar
• Dubovskiy I, Kryukov VY, Benkovskaya G, et al. Activity of the detoxificative enzyme system and encapsulation rate in the Colorado potato beetle Leptinotarsa decemlineata (Say) larvae under organophosphorus insecticide treatment and entomopathogenic fungus Metharizium anisopliae (Metsch.) infection. Euroasian Entomol J. 2010;9:577–582.
   Google Scholar
• Dubovskiy I, Slyamova N, Kryukov VY, et al. The activity of nonspecific esterases and glutathione-S-transferase in Locusta migratoria larvae infected with the fungus Metarhizium anisopliae (Ascomycota, Hypocreales). Entomol Rev. 2012;92:27–31.
   Google Scholar
• Serebrov V, Gerber O, Malyarchuk A, et al. Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biol Bull. 2006;33:581–586.
   Web of Science ®Google Scholar
• Shah FA, Allen N, Wright CJ, et al. Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiol Lett. 2007;276:60–66.
   PubMed Web of Science ®Google Scholar
• Farrar J, Hotez P, Junghanss T, et al. Manson’s tropical diseases e-book. London: Elsevier Health Sciences; 2013.
   Google Scholar
• Lord JC, Howard RW. A proposed role for the cuticular fatty amides of Liposcelis bostrychophila (Psocoptera: liposcelidae) in preventing adhesion of entomopathogenic fungi with dry-conidia. Mycopathol. 2004;158:211–217.
   PubMed Web of Science ®Google Scholar
• Boucias DG, Pendland JC. Attachment of mycopathogens to cuticle: the initial event of mycosis in arthropod hosts. In: Gt C, Hc H, editors. The fungal spore and disease initiation in plants and animals. New York (NY): Plenum Press; 1991. p. 101–127.
   Google Scholar
• Pendland J, Hung S, Boucias D. Evasion of host defense by in vivo-produced protoplast-like cells of the insect mycopathogen Beauveria bassiana. J Bacteriol. 1993;175:5962–5969.
   PubMed Web of Science ®Google Scholar
• Fargues J. Adhesion of the fungal spore to the insect cuticle in relation to pathogenicity. In: J. Aist and D. W. Roberts, editors, Infection processes of fungi. Bellagio: Rockefeller Foundation Study Center; 1984.
   Google Scholar
• James R, Buckner J, Freeman T. Cuticular lipids and silverleaf whitefly stage affect conidial germination of Beauveria bassiana and Paecilomyces fumosoroseus. J Invertebr Pathol. 2003;84:67–74.
   PubMed Web of Science ®Google Scholar
• Freimoser FM, Hu G, St Leger RJ. Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiol. 2005;151:361–371.
   PubMed Web of Science ®Google Scholar
• Vizioli J, Bulet P, Hoffmann JA, et al. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc Natl Acad Sci. 2001;98:12630–12635. . PMCID: PMC60105.
   PubMed Web of Science ®Google Scholar
• Dimopoulos G. Insect immunity and its implication in mosquito–malaria interactions. Cell Microbiol. 2003;5:3–14.
   PubMed Web of Science ®Google Scholar
• Kumar B, Paily K. Identification of immune‐responsive genes in the mosquito Culex quinquefasciatus infected with the filarial parasite Wuchereria bancrofti. Med Vet Entomol. 2008;22:394–398.
   PubMed Web of Science ®Google Scholar
• Nichol H, Law JH, Winzerling JJ. Iron metabolism in insects. Annu Rev Entomol. 2002;47:535–559.
   PubMed Web of Science ®Google Scholar
• Yoshiga T, Hernandez VP, Fallon AM, et al. Mosquito transferrin, an acute-phase protein that is up-regulated upon infection. Proc Natl Acad Sci. 1997;94:12337–12342. PMCID: PMC24933.
   PubMed Web of Science ®Google Scholar
• Bull JC, Ryabov EV, Prince G, et al. A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees. PLoS Pathog. 2012;8:e1003083. PMCID: PMC3531495.
   PubMed Web of Science ®Google Scholar
• Zhao L, Jones W. Expression of heat shock protein genes in insect stress responses. Invertebrate Surviv J. 2012;90:93–101.
   Google Scholar
• Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999;61:243–282.
   PubMed Web of Science ®Google Scholar
• Mayer M, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci. 2005;62:670. DOI:10.1007/s00018-004-4464-6.
   Web of Science ®Google Scholar
• Castillo JC, Creasy T, Kumari P, et al. Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq. BMC Genomics. 2015;16:519. PMCID: PMC4499211.
   PubMed Web of Science ®Google Scholar
• Dubovskiy I, Whitten M, Kryukov V, et al. More than a colour change: insect melanism, disease resistance and fecundity. Proceedings of the Royal Society of London B. 2013;280:20130584.
   Web of Science ®Google Scholar
• Dubovskiy IM, Whitten MM, Yaroslavtseva ON, et al. Can insects develop resistance to insect pathogenic fungi? PloS One. 2013;8:e60248. PMCID: PMC3613352.
   PubMed Web of Science ®Google Scholar
• Dubovskiy I, Martemyanov V, Vorontsova Y, et al. Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 2008;148:1–5.
   PubMed Web of Science ®Google Scholar
• Finney DJ, Tattersfield F. Probit analysis. Cambridge: Cambridge University Press; 1952.
   Google Scholar
• Eastwood DC, Mead A, Sergeant MJ, et al. Statistical modelling of transcript profiles of differentially regulated genes. BMC Mol Biol. 2008;9:66. PMCID: PMC2525656.
   PubMed Web of Science ®Google Scholar
• Morgan GA, Leech NL, Gloeckner GW, et al. IBM SPSS for introductory statistics: use and interpretation. New York (NY): Routledge; 2012.
   Google Scholar
• R Core Team. A language and environment for statistical computing. ISBN 3-900051-07-0. Vienna, Austria: R Foundation for Statistical Computing; 2014. Available from: http://www.R-project.prg
   Google Scholar