Wang C, Wang S. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol. 2017;62:73–90.
Google Scholar
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS. Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol. 2015;132:1–41.
Google Scholar
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA Entomopathogenic fungi: new insights into host-pathogen interactions. Advances in Genetics. 2016. Elsevier Ltd.
Lu HL, St. Leger RJ. Insect immunity to entomopathogenic fungi. Adv Genet. 2016;94:251–85.
Google Scholar
Yuan S, Tao X, Huang S, Chen S, Xu A. Comparative immune systems in animals. Annu Rev Anim Biosci. 2014;2:235–58.
Google Scholar
Flórez LV, Biedermann PHW, Engl T, Kaltenpoth M. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep. 2015;32:904–36.
Google Scholar
Oliver KM, Smith AH, Russell JA. Defensive symbiosis in the real world – advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol. 2014;28:341–55.
Google Scholar
Scarborough CL, Ferrari J, Godfray HC. Aphid protected from pathogen. Science 2005;310:1781.
Google Scholar
Łukasik P, van Asch M, Guo H, Ferrari J, Charles H. Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett. 2013;16:214–8.
Google Scholar
Flórez LV, Scherlach K, Gaube P, Ross C, Sitte E, Hermes C, et al. Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat Commun. 2017;8:15172.
Google Scholar
Flórez LV, Scherlach K, Miller IJ, Rodrigues A, Kwan JC, Hertweck C, et al. An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles. Nat Commun. 2018;9:2478.
Google Scholar
Kaltenpoth M, Göttler W, Herzner G, Strohm E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol. 2005;15:475–9.
Google Scholar
Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, et al. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol. 2010;6:261–3.
Google Scholar
Kaltenpoth M, Goettler W, Koehler S, Strohm E. Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol Ecol. 2010;24:463–77.
Google Scholar
Wang X, Yang X, Zhou F, Tian ZQ, Cheng J, Michaud JP, et al. Symbiotic bacteria on the cuticle protect the oriental fruit moth Grapholita molesta from fungal infection. Biol Control. 2022;169:104895.
Google Scholar
Wang L, Feng Y, Tian J, Xiang M, Sun J, Ding J, et al. Farming of a defensive fungal mutualist by an attelabid weevil. ISME J. 2015;9:1793–801.
Google Scholar
Currie CR, Stuart AE. Weeding and grooming of pathogens in agriculture by ants. Proc R Soc B Biol Sci. 2001;268:1033–9.
Google Scholar
Currie CR, Scottt JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999;398:701–4.
Google Scholar
Currie CR, Bot ANM, Boomsma JJ. Experimental evidence of a tripartite mutualism: Bacteria protect ant fungus gardens from specialized parasites. Oikos 2003;101:91–102.
Google Scholar
Um S, Fraimout A, Sapountzis P, Oh D-CC, Poulsen M. The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi. Sci Rep. 2013;3:3250.
Google Scholar
Grubbs KJ, Surup F, Biedermann PHW, McDonald BR, Klassen JL, Carlson CM, et al. Cycloheximide-producing streptomyces associated with xyleborinus saxesenii and xyleborus affinis fungus-farming ambrosia beetles. Front Microbiol. 2020;11:1–12.
Google Scholar
Piel J. Metabolites from symbiotic bacteria. Nat Prod Rep. 2009;26:338–62.
Google Scholar
Van Arnam EB, Currie CR, Clardy J. Defense contracts: Molecular protection in insect-microbe symbioses. Chem Soc Rev. 2018;47:1638–51.
Google Scholar
Beemelmanns C, Guo H, Rischer M, Poulsen M. Natural products from microbes associated with insects. Beilstein J Org Chem. 2016;12:314–27.
Google Scholar
Lackner G, Peters EE, Helfrich EJN, Piel J. Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges. Proc Natl Acad Sci USA. 2017;114:E347–E356.
Google Scholar
Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci USA. 2011;108:1955–60.
Google Scholar
Kaltenpoth M, Strupat K, Svatoš A. Linking metabolite production to taxonomic identity in environmental samples by (MA)LDI-FISH. ISME J. 2016;10:527–31.
Google Scholar
Geier B, Sogin EM, Michellod D, Janda M, Kompauer M, Spengler B, et al. Spatial metabolomics of in situ host–microbe interactions at the micrometre scale. Nat Microbiol. 2020;5:498–510.
Google Scholar
De Roode JC, Lefèvre T. Behavioral immunity in insects. Insects 2012;3:789–820.
Google Scholar
Kerwin AH, Gromek SM, Suria AM, Samples RM, Deoss DJ, O’Donnell K, et al. Shielding the next generation: Symbiotic bacteria from a reproductive organ protect bobtail squid eggs from fungal fouling. mBio. 2019;10:e02376-19.
Google Scholar
Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, et al. Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol. 2008;22:864–71.
Google Scholar
Bunker ME, Elliott G, Martin MO, Arnold AE, Weiss SL. Vertically transmitted microbiome protects eggs from fungal infection and egg failure. Anim Microbiome. 2021;3:43.
Google Scholar
Nyholm SV. In the beginning: Egg-microbe interactions and consequences for animal hosts: Egg microbiomes in animals. Philos Trans R Soc B Biol Sci. 2020;375:20190593.
Google Scholar
Smith DFQ, Dragotakes Q, Kulkarni M, Hardwick M, Casadevall A, Microbiology M, et al. Melanization is an important antifungal defense mechanism in Galleria mellonella hosts. bioRxiv 2022.04.02.486843.
Yokoi K, Hayakawa Y, Kato D, Minakuchi C, Tanaka T, Ochiai M, et al. Prophenoloxidase genes and antimicrobial host defense of the model beetle, Tribolium castaneum. J Invertebr Pathol. 2015;132:190–200.
Google Scholar
Zhang J, Huang W, Yuan C, Lu Y, Yang B, Wang CY, et al. Prophenoloxidase-mediated ex vivo immunity to delay fungal infection after insect ecdysis. Front Immunol. 2017;8:1–14.
Zhang J, Lu A, Kong L, Zhang Q, Ling E. Functional analysis of insect molting fluid proteins on the protection and regulation of ecdysis. J Biol Chem. 2014;289:35891–906.
Google Scholar
Soluk DA. Postmolt susceptibility of ephemerella larvae to predatory stoneflies: constraints on defensive armour. Oikos 1990;58:336.
Google Scholar
Kanyile SN, Engl T, Kaltenpoth M. Nutritional symbionts enhance structural defence against predation and fungal infection in a grain pest beetle. J Exp Biol. 2022;225:1–9.
Google Scholar
Flórez LV, Kaltenpoth M. Symbiont dynamics and strain diversity in the defensive mutualism between Lagria beetles and Burkholderia. Environ Microbiol. 2017;19:3674–88.
Google Scholar
Uberti A, Smaniotto MA, Giacobbo CL, Lovatto M, Lugaresi A, Girardi GC. Novo inseto praga na cultura do pessegueiro: biologia de Lagria villosa Fabricius, 1783 (Coleoptera: Tenebrionidae) alimentados com pêssego. Sci Electron Arch. 2017;10:72–76.
Stammer HJ. Die Symbiose der Lagriiden (Coleoptera). Z für Morphol und Ökologie der Tiere. 1929;15:1–34.
Google Scholar
Boucias DG, Pendland JC Principles of Insect Pathology. 1998. Springer Science + Business Media, LLC, New York.
Garcia MA, Pierozzi IJ. Aspectos da biologia e ecologia de Lagria villosa Fabricius, 1781 (Coleoptera, Lagriidae). Rev Bras Biol. 1982;42:415–20.
Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner SA. Entomopathogenic fungal endophytes. Biol Control. 2008;46:72–82.
Google Scholar
Kabaluk JT, Ericsson JD. Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agron J. 2007;99:1377–81.
Google Scholar
Hallouti A, Ait Hamza M, Zahidi A, Ait Hammou R, Bouharroud R, Ait Ben Aoumar A, et al. Diversity of entomopathogenic fungi associated with Mediterranean fruit fly (Ceratitis capitata (Diptera: Tephritidae)) in Moroccan Argan forests and nearby area: impact of soil factors on their distribution. BMC Ecol. 2020;20:1–13.
Google Scholar
Iwanicki NS, Pereira AA, Botelho ABRZ, Rezende JM, Moral RDA, Zucchi MI, et al. Monitoring of the field application of Metarhizium anisopliae in Brazil revealed high molecular diversity of Metarhizium spp in insects, soil and sugarcane roots. Sci Rep. 2019;9:1–12.
Google Scholar
Roberts DW, St. Leger RJ. Metarhizium spp., cosmopolitan insect-pathogenic fungi: Mycological aspects. Adv Appl Microbiol. 2004;54:1–70.
Google Scholar
Wierz JC, Gaube P, Klebsch D, Kaltenpoth M, Flórez LV. Transmission of bacterial symbionts with and without genome erosion between a beetle host and the plant environment. Front Microbiol. 2021;12:715601.
Google Scholar
Gillespie JP, Bailey AM, Cobb B, Vilcinskas A. Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol. 2000;44:49–68.
Google Scholar
Ortiz-Urquiza A, Keyhani NO. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 2013;4:357–74.
Google Scholar
Grizanova EV, Coates CJ, Dubovskiy IM, Butt TM. Metarhizium brunneum infection dynamics differ at the cuticle interface of susceptible and tolerant morphs of Galleria mellonella. Virulence 2019;10:999–1012.
Google Scholar
Eaton WD, Love DC, Botelho C, Meyers TR, Imamura K, Koeneman T. Preliminary results on the seasonality and life cycle of the parasitic dinoflagellate causing bitter crab disease in Alaskan Tanner crabs (Chionoecetes bairdi). J Invertebr Pathol. 1991;57:426–34.
Google Scholar
Field RH, Chapman CJ, Taylor AC, Neil DM, Vickerman K. Infection of the Norway lobster Nephrops norvegicus by a Hematodinium-like species of dinoflagellate on the west coast of Scotland. Dis Aquat Organ. 1992;13:1–15.
Google Scholar
Threlkeld ST, Chiavelli DA, Willey RL. The organization of zooplankton epibiont communities. Trends Ecol Evol. 1993;8:317–21.
Google Scholar
Duneau D, Ebert D. The role of moulting in parasite defence. Proc R Soc B Biol Sci. 2012;279:3049–54.
Google Scholar
Vandenberg JD, Ramos M, Altre JA. Dose-Response and Age- and Temperature-Related Susceptibility of the Diamondback Moth (Lepidoptera: Plutellidae) to Two Isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environ Entomol. 1998;27:1017–21.
Google Scholar
Vey A, Fargues J. Histological and ultrastructural studies of Beauveria bassiana infection in Leptinotarsa decemlineta larvae during ecdysis. J Invertebr Pathol. 1977;30:207–15.
Google Scholar
Reynolds SE, Samuels RI. Physiology and biochemistry of insect moulting fluid. Adv Insect Phys. 1996;26:157–232.
Google Scholar
Lopanik NB. Chemical defensive symbioses in the marine environment. Funct Ecol. 2014;28:328–40.
Google Scholar
Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, Mueller UG. Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci USA. 2009;106:17805–10.
Google Scholar
Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 2006;311:81–3.
Google Scholar
Li H, Sosa-Calvo J, Horn HA, Pupo MT, Clardy J, Rabeling C, et al. Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. Proc Natl Acad Sci USA. 2018;115:10720–5.
Google Scholar
Kaltenpoth M, Roeser-Mueller K, Koehler S, Peterson A, Nechitaylo TY, Stubblefield JW, et al. Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis. Proc Natl Acad Sci. 2014;111:6359–64.
Google Scholar
Engl T, Kroiss J, Kai M, Nechitaylo TY, Svatoš A, Kaltenpoth M. Evolutionary stability of antibiotic protection in a defensive symbiosis. Proc Natl Acad Sci USA. 2018;115:E2020–E2029.
Google Scholar
Gil-Turnes MS, Hay ME, Fenical W. Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 1989;246:116–8.
Google Scholar
Gil-Turnes MS, Fenical W. Embryos of Homarus americanus are protected by epibiotic bacteria. Biol Bull. 1992;182:105–8.
Google Scholar
Hoffmann KH Insect Molecular Biology and Ecology. 2015. CRC Press.
Eisner T, Morgan RC, Attygalle AB, Smedley SR, Herath KB, Meinwald J. Defensive production of quinoline by a phasmid insect (Oreophoetes peruana). J Exp Biol. 1997;200:2493–2500.
Google Scholar
Waterworth SC, Flórez LV, Rees ER, Hertweck C, Kaltenpoth M, Kwan JC. Horizontal gene transfer to a defensive symbiont with a reduced genome in a multipartite beetle microbiome. mBio. 2020;11:e02430-19.
Google Scholar
Niehs SP, Kumpfmüller J, Dose B, Little RF, Ishida K, Flórez LV, et al. Insect‐associated bacteria assemble the antifungal butenolide gladiofungin by non‐canonical polyketide chain termination. Angew Chem. 2020;132:23322–6.
Google Scholar
Dose B, Niehs SP, Scherlach K, Flórez LV, Kaltenpoth M, Hertweck C. Unexpected bacterial origin of the antibiotic icosalide: two-tailed depsipeptide assembly in multifarious Burkholderia symbionts. ACS Chem Biol. 2018;13:2414–20.
Google Scholar
Parada AE, Needham DM, Fuhrman JA. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.
Google Scholar
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.
Google Scholar
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA. 2011;108:4516–22.
Google Scholar
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
Google Scholar
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.
Google Scholar
Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and ‘all-species Living Tree Project (LTP)’ taxonomic frameworks. Nucleic Acids Res. 2014;42:643–8.
Google Scholar
Weiss B, Kaltenpoth M. Bacteriome-localized intracellular symbionts in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). Front Microbiol. 2016;7:1–10.
Google Scholar
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990;56:1919–25.
Google Scholar
Paschke C, Leisner A, Hester A, Maass K, Guenther S, Bouschen W, et al. Mirion – A software package for automatic processing of mass spectrometric images. J Am Soc Mass Spectrom. 2013;24:1296–306.
Google Scholar
Source: Ecology - nature.com
