HomeScienceBacterial ectosymbionts in cuticular organs chemically protect a beetle during molting stages

Bacterial ectosymbionts in cuticular organs chemically protect a beetle during molting stages

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  • Wang C, Wang S. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol. 2017;62:73–90.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    PubMed 
    Article 

    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.

    Article 

    Google Scholar
     

  • Scarborough CL, Ferrari J, Godfray HC. Aphid protected from pathogen. Science 2005;310:1781.

    CAS 
    PubMed 
    Article 

    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.

    PubMed 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • Kaltenpoth M, Göttler W, Herzner G, Strohm E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol. 2005;15:475–9.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    Article 

    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.

    CAS 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    Article 

    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.

    CAS 
    Article 

    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.

    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    Article 

    Google Scholar
     

  • Piel J. Metabolites from symbiotic bacteria. Nat Prod Rep. 2009;26:338–62.

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Van Arnam EB, Currie CR, Clardy J. Defense contracts: Molecular protection in insect-microbe symbioses. Chem Soc Rev. 2018;47:1638–51.

    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • De Roode JC, Lefèvre T. Behavioral immunity in insects. Insects 2012;3:789–820.

    PubMed 
    PubMed Central 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.


    Google Scholar
     

  • 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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Soluk DA. Postmolt susceptibility of ephemerella larvae to predatory stoneflies: constraints on defensive armour. Oikos 1990;58:336.

    Article 

    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.

    Article 

    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.

    PubMed 
    Article 
    CAS 

    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.


    Google Scholar
     

  • Stammer HJ. Die Symbiose der Lagriiden (Coleoptera). Z für Morphol und Ökologie der Tiere. 1929;15:1–34.

    Article 

    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.


    Google Scholar
     

  • Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner SA. Entomopathogenic fungal endophytes. Biol Control. 2008;46:72–82.

    Article 

    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.

    Article 

    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.

    Article 
    CAS 

    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.

    CAS 
    Article 

    Google Scholar
     

  • Roberts DW, St. Leger RJ. Metarhizium spp., cosmopolitan insect-pathogenic fungi: Mycological aspects. Adv Appl Microbiol. 2004;54:1–70.

    CAS 
    PubMed 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Ortiz-Urquiza A, Keyhani NO. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 2013;4:357–74.

    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    Article 

    Google Scholar
     

  • Threlkeld ST, Chiavelli DA, Willey RL. The organization of zooplankton epibiont communities. Trends Ecol Evol. 1993;8:317–21.

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Duneau D, Ebert D. The role of moulting in parasite defence. Proc R Soc B Biol Sci. 2012;279:3049–54.

    Article 

    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.

    Article 

    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.

    Article 

    Google Scholar
     

  • Reynolds SE, Samuels RI. Physiology and biochemistry of insect moulting fluid. Adv Insect Phys. 1996;26:157–232.

    CAS 
    Article 

    Google Scholar
     

  • Lopanik NB. Chemical defensive symbioses in the marine environment. Funct Ecol. 2014;28:328–40.

    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Gil-Turnes MS, Fenical W. Embryos of Homarus americanus are protected by epibiotic bacteria. Biol Bull. 1992;182:105–8.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    PubMed 
    PubMed Central 
    Article 

    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.

    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    Article 
    CAS 

    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.

    Article 
    CAS 

    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.

    Article 

    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.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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.

    CAS 
    PubMed 
    Article 

    Google Scholar
     


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