in

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

  • 1.

    Sikorski, J. A. & Gruys, K. J. Understanding glyphosate’s molecular mode of action with EPSP synthase: evidence favoring an allosteric inhibitor model. Acc. Chem. Res. 30, 2–8 (1997).

    CAS 
    Article 

    Google Scholar 

  • 2.

    Duke, S. O. & Powles, S. B. Glyphosate: a once‐in‐a‐century herbicide. Pest Manag. Sci. 64, 319–325 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 3.

    Siehl, D. L. Inhibitors of EPSP synthase, glutamine synthetase and histidine synthesis. In Herbicide Activity: Toxicology, Biochemistry and Molecular Biology, vol. 1 (eds. Michael Roe, R., Burton, J. D. & Kuhr, R. J.) 37 (IOS Press, 1997).

  • 4.

    Shilo, T., Zygier, L., Rubin, B., Wolf, S. & Eizenberg, H. Mechanism of glyphosate control of Phelipanche aegyptiaca. Planta 244, 1095–1107 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 5.

    Tzin, V. & Galili, G. New Insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol. Plant 3, 956–972 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 6.

    McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110, 3229–3236 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 7.

    Hacker, S. D. & Gaines, S. D. Some implications of direct positive interactions for community species diversity. Ecology 78, 1990–2003 (1997).

    Article 

    Google Scholar 

  • 8.

    van den Bosch, T. J. M. & Welte, C. U. Detoxifying symbionts in agriculturally important pest insects. Microb. Biotechnol. 10, 531–540 (2017).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 9.

    Lemoine, M. M., Engl, T. & Kaltenpoth, M. Microbial symbionts expanding or constraining abiotic niche space in insects. Curr. Opin. Insect Sci. 39, 14–20 (2020).

    PubMed 
    Article 

    Google Scholar 

  • 10.

    Feldhaar, H. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36, 533–543 (2011).

    Article 

    Google Scholar 

  • 11.

    Moran, N. A. Symbiosis. Curr. Biol. 16, R866–R871 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 12.

    Moran, N. A. & Telang, A. Bacteriocyte-associated symbionts of insects. Bioscience 48, 295–304 (1998).

    Article 

    Google Scholar 

  • 13.

    Oliver, K. M. & Martinez, A. J. How resident microbes modulate ecologically-important traits of insects. Curr. Opin. Insect Sci. 4, 1–7 (2014).

    PubMed 
    Article 

    Google Scholar 

  • 14.

    Douglas, A. E. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38–47 (2009).

    Article 

    Google Scholar 

  • 15.

    Douglas, A. E. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Curr. Opin. Insect Sci. 23, 65–69 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 16.

    Vigneron, A. et al. Insects recycle endosymbionts when the benefit is over. Curr. Biol. 24, 2267–2273 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 17.

    Andersen, S. O. Cuticular sclerotization and tanning. In Insect Molecular Biology and Biochemistry (ed. Gilbert, L. I.) 167–192 (Elsevier, 2012).

  • 18.

    Anbutsu, H. & Fukatsu, T. Symbiosis for insect cuticle formation. In Cellular Dialogues in the Holobiont (eds. Bosch, T. C. G. & Hadfield, M. G.) 201–216 (CRC Press, 2020).

  • 19.

    Anbutsu, H. et al. Small genome symbiont underlies cuticle hardness in beetles. Proc. Natl. Acad. Sci. USA 114, E8382–E8391 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 20.

    Li, A. P. & Long, T. J. An evaluation of the genotoxic potential of glyphosate. Fundam. Appl. Toxicol. 10, 537–546 (1988).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 21.

    Smith, E. A. & Oehme, F. W. The biological activity of glyphosate to plants and animals: a literature review. Vet. Hum. Toxicol. 34, 531–543 (1992).

    CAS 
    PubMed 

    Google Scholar 

  • 22.

    Smith, D. F. Q. et al. Glyphosate inhibits melanization and increases insect susceptibility to infection. bioRxiv (2020).

  • 23.

    Torretta, V., Katsoyiannis, I., Viotti, P. & Rada, E. Critical review of the effects of glyphosate exposure to the environment and humans through the food supply chain. Sustainability 10, 950 (2018).

    Article 
    CAS 

    Google Scholar 

  • 24.

    Snyder, A. K. & Rio, R. V. M. “Wigglesworthia morsitans” folate (Vitamin B 9) biosynthesis contributes to tsetse host fitness. Appl. Environ. Microbiol. 81, 5375–5386 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 25.

    Motta, E. V. S., Raymann, K. & Moran, N. A. Glyphosate perturbs the gut microbiota of honey bees. Proc. Natl. Acad. Sci. USA 115, 10305–10310 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 26.

    Motta, E. V. S. et al. Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Appl. Environ. Microbiol. 86, e01150–20 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 27.

    Klein, A. et al. A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior. ISME J 10, 376–388 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 28.

    Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 29.

    Dunne, J. A. & Williams, R. J. Cascading extinctions and community collapse in model food webs. Philos. Trans. R. Soc. B Biol. Sci 364, 1711–1723 (2009).

    Article 

    Google Scholar 

  • 30.

    Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002).

    Article 

    Google Scholar 

  • 31.

    Memmott, J. et al. Biodiversity loss and ecological network structure. In Ecological Networks: Linking Structure to Dynamics in Food Webs (eds Pascual, M. & Dunne, J. A.) 325–347 (Oxford University Press, 2005).

  • 32.

    Liao, C., Upadhyay, A., Liang, J., Han, Q. & Li, J. 3,4-Dihydroxyphenylacetaldehyde synthase and cuticle formation in insects. Dev. Comp. Immunol. 83, 44–50 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 33.

    Muthukrishnan, S., Merzendorfer, H., Arakane, Y. & Kramer, K. J. Chitin metabolism in insects. In Insect Molecular Biology and Biochemistry (ed. Gilbert, L. I.) 193–235 (Elsevier, 2012).

  • 34.

    Wirtz, R. A. & Hopkins, T. L. Tyrosine and phenylalanine concentrations in haemolymph and tissues of the American cockroach, Periplaneta americana, during metamorphosis. J. Insect Physiol. 20, 1143–1154 (1974).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 35.

    Gibbs, A. G. & Rajpurohit, S. Cuticular lipids and water balance. In Insect Hydrocarbons (eds Blomquist, G. J. & Bagneres, A. -G.) 100–120 (Cambridge University Press, 2010).

  • 36.

    Hackman, R. H. Chemistry of the insect cuticle. in The Physiology of Insecta (ed. Rodstein, M.) 215–270 (Academic Press, 1974).

  • 37.

    Mattson, W. J. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11, 119–161 (1980).

    Article 

    Google Scholar 

  • 38.

    Kumar, V. et al. Amino acids distribution in economical important plants: a review. Biotechnol. Res. Innov 3, 197–207 (2019).

    Article 

    Google Scholar 

  • 39.

    Noh, M. Y., Muthukrishnan, S., Kramer, K. J. & Arakane, Y. Cuticle formation and pigmentation in beetles. Curr. Opin. Insect Sci. 17, 1–9 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 40.

    Sterkel, M. et al. Tyrosine detoxification is an essential trait in the life history of blood-feeding arthropods. Curr. Biol. 26, 2188–2193 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 41.

    Herrmann, K. M. & Weaver, L. M. The shikimate pathway. Annu. Rev. Plant Biol. 50, 473–503 (1999).

    CAS 
    Article 

    Google Scholar 

  • 42.

    Engl, T. et al. Ancient symbiosis confers desiccation resistance to stored grain pest beetles. Mol. Ecol. 27, 2095–2108 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 43.

    Hirota, B. et al. A novel, extremely elongated, and endocellular bacterial symbiont supports cuticle formation of a grain pest beetle. MBio 8, 1–16 (2017).

    Article 

    Google Scholar 

  • 44.

    Boyer, S., Zhang, H. & Lempérière, G. A review of control methods and resistance mechanisms in stored-product insects. Bull. Entomol. Res. 102, 213 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 45.

    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 46.

    Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 47.

    McCutcheon, J. P. & Moran, N. A. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26 (2012).

    CAS 
    Article 

    Google Scholar 

  • 48.

    Van Leuven, J. T., Meister, R. C., Simon, C. & McCutcheon, J. P. Sympatric speciation in a bacterial endosymbiont results in two genomes with the functionality of one. Cell 158, 1270–1280 (2014).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 49.

    Campbell, M. A., Łukasik, P., Simon, C. & McCutcheon, J. P. Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas. Curr. Biol. 27, 3568–3575.e3 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 50.

    Campbell, M. A. et al. Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia. Proc. Natl. Acad. Sci. USA 112, 10192–10199 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 51.

    Chen, Y. C., Liu, T., Yu, C. H., Chiang, T. Y. & Hwang, C. C. Effects of GC bias in next-generation-sequencing data on de novo genome assembly. PLoS ONE 8, e62856 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 52.

    Kozarewa, I. et al. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+ C)-biased genomes. Nat. Methods 6, 291–295 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Quail, M. A. et al. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 13, 1–13 (2012).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 54.

    Treangen, T. J. & Salzberg, S. L. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat. Rev. Genet. 13, 36–46 (2012).

    CAS 
    Article 

    Google Scholar 

  • 55.

    Sloan, D. B. et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31, 857–871 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 56.

    Zucko, J. et al. Global genome analysis of the shikimic acid pathway reveals greater gene loss in host-associated than in free-living bacteria. BMC Genomics 11, 628 (2010).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Tokuda, G. et al. Maintenance of essential amino acid synthesis pathways in the Blattabacterium cuenoti symbiont of a wood-feeding cockroach. Biol. Lett. 9, 20121153 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Kinjo, Y. et al. Parallel and gradual genome erosion in the Blattabacterium endosymbionts of Mastotermes darwiniensis and Cryptocercus Wood Roaches. Genome Biol. Evol. 10, 1622–1630 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 59.

    Menzel, R. & Roth, J. Purification of the putA gene product. A bifunctional membrane-bound protein from Salmonella typhimurium responsible for the two-step oxidation of proline to glutamate. J. Biol. Chem. 256, 9755–9761 (1981).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 60.

    Zhou, Y., Zhu, W., Bellur, P. S., Rewinkel, D. & Becker, D. F. Direct linking of metabolism and gene expression in the proline utilization a protein from Escherichia coli. Amino Acids 35, 711–718 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 61.

    Sabree, Z. L., Kambhampati, S. & Moran, N. A. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc. Natl. Acad. Sci. USA 106, 19521–19526 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 62.

    McCutcheon, J. P., McDonald, B. R. & Moran, N. A. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. USA 106, 15394–15399 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 63.

    Sabree, Z. L., Huang, C. Y., Okusu, A., Moran, N. A. & Normark, B. B. The nutrient supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environ. Microbiol. 15, 1988–1999 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 64.

    Rosas-Pérez, T., Rosenblueth, M., Rincón-Rosales, R., Mora, J. & Martínez-Romero, E. Genome Sequence of “Candidatus Walczuchella monophlebidarum” the Flavobacterial endosymbiont of Llaveia axin axin (Hemiptera: Coccoidea: Monophlebidae). Genome Biol. Evol. 6, 714–726 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 65.

    Kuriwada, T. et al. Biological role of Nardonella endosymbiont in its weevil host. PLoS ONE 5, e13101 (2010).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 66.

    Okude, G. et al. Novel bacteriocyte-associated pleomorphic symbiont of the grain pest beetle Rhyzopertha dominica (Coleoptera: Bostrichidae). Zool. Lett. 3, 13 (2017).

    Article 

    Google Scholar 

  • 67.

    Hirota, B., Meng, X.-Y. & Fukatsu, T. Bacteriome-sssociated rndosymbiotic bacteria of Nosodendron tree sap beetles (Coleoptera: Nosodendridae). Front. Microbiol. 11, 2556 (2020).

    Article 

    Google Scholar 

  • 68.

    Hopkins, T. L. & Kramer, K. J. Insect cuticle sclerotization. Annu. Rev. Entomol. 37, 273–302 (1992).

    CAS 
    Article 

    Google Scholar 

  • 69.

    Andersen, S. O. Insect cuticular sclerotization: a review. Insect Biochem. Mol. Biol. 40, 166–178 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 70.

    Cao, G. et al. A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. PLoS ONE 7, e38718 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 71.

    Moran, N. A. & Bennett, G. M. The tiniest tiny genomes. Annu. Rev. Microbiol. 68, 195–215 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 72.

    McCutcheon, J. P., Boyd, B. M. & Dale, C. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol. 29, R485–R495 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 73.

    Salem, H. et al. Drastic genome reduction in an herbivore’s pectinolytic symbiont. Cell 171, 1520–1531 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 74.

    Reis, F. et al. Bacterial symbionts support larval sap feeding and adult folivory in (semi-) aquatic reed beetles. Nat. Commun. 11, 1–15 (2020).

    Google Scholar 

  • 75.

    Salem, H., Florez, L., Gerardo, N. & Kaltenpoth, M. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. B Biol. Sci. 282, 20142957 (2015).

    Article 

    Google Scholar 

  • 76.

    Salem, H. et al. Symbiont digestive range reflects host plant breadth in herbivorous beetles. Curr. Biol. 30, 2875–2886 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 77.

    Hansen, A. K., Pers, D. & Russell, J. A. Symbiotic solutions to nitrogen limitation and amino acid imbalance in insect diets. In Mechanisms Underlying Microbial Symbiosis, vol. 58 (ed. Kerry M. Oliver, J. A. R.) 161–205 (Academic Press, 2020).

  • 78.

    Tanner, J. J. Structural biology of proline catabolism. Amino Acids 35, 719–730 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 79.

    Adams, E. & Frank, L. Metabolism of proline and the hydroxyprolines. Annu. Rev. Biochem. 49, 1005–61 (1980).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 80.

    Bursell, E. The role of proline in energy metabolism.In Energy Metabolism in Insects (ed. Downer R.G.H.) 135–154 (Springer, Boston, 1981).

  • 81.

    Engl, T., Schmidt, T. H. P., Kanyile, S. N. & Klebsch, D. Metabolic cost of a nutritional symbiont manifests in delayed reproduction in a grain pest beetle. Insects 11, 717 (2020).

    PubMed Central 
    Article 
    PubMed 

    Google Scholar 

  • 82.

    José de Souza, D., Devers, S. & Lenoir, A. Blochmannia endosymbionts and their host, the ant Camponotus fellah: cuticular hydrocarbons and melanization. C. R. Biol. 334, 737–741 (2011).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 83.

    Zientz, E., Beyaert, I., Gross, R. & Feldhaar, H. Relevance of the endosymbiosis of Blochmannia floridanus and carpenter ants at different stages of the life cycle of the host. Appl. Environ. Microbiol. 72, 6027–6033 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 84.

    Oakeson, K. F. et al. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol. Evol. 6, 76–93 (2013).

    Article 

    Google Scholar 

  • 85.

    Chong, R. A. & Moran, N. A. Evolutionary loss and replacement of Buchnera, the obligate endosymbiont of aphids. ISME J 12, 898–908 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 86.

    McCutcheon, J. P. & Moran, N. A. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2, 708–718 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 87.

    Gerth, M., Gansauge, M. T., Weigert, A. & Bleidorn, C. Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat. Commun. 5, 1–7 (2014).

    Article 
    CAS 

    Google Scholar 

  • 88.

    Santos-Garcia, D., Silva, F. J., Morin, S., Dettner, K. & Kuechler, S. M. The all-rounder Sodalis: a new bacteriome-associated endosymbiont of the Lygaeoid bug Henestaris halophilus (Heteroptera: Henestarinae) and a critical examination of its evolution. Genome Biol. Evol. 9, 2893–2910 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 89.

    Motta, E. V. S. & Moran, N. A. Impact of glyphosate on the honey bee gut microbiota: effects of intensity, duration, and timing of exposure. Msystems 5, e00268–20 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 90.

    Helander, M., Pauna, A., Saikkonen, K. & Saloniemi, I. Glyphosate residues in soil affect crop plant germination and growth. Sci. Rep. 9, 19653 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 91.

    Kiers, E. T., Rousseau, R. A., West, S. A. & Denlson, R. F. Host sanctions and the legume-rhizobium mutualism. Nature 425, 78–81 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 92.

    Whiteside, M. D., Digman, M. A., Gratton, E. & Treseder, K. K. Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biol. Biochem. 55, 7–13 (2012).

    CAS 
    Article 

    Google Scholar 

  • 93.

    Faita, M. R., Cardozo, M. M., Amandio, D. T. T., Orth, A. I. & Nodari, R. O. Glyphosate-based herbicides and Nosema sp. microsporidia reduce honey bee (Apis mellifera L.) survivability under laboratory conditions. J. Apic. Res. 59, 1–11 (2020).

    Article 

    Google Scholar 

  • 94.

    Wilson, A. C. C. et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19, 249–258 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 95.

    Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232, 8–27 (2019).

    Article 

    Google Scholar 

  • 96.

    Wagner, D. L. Insect declines in the anthropocene. Annu. Rev. Entomol. 65, 457–480 (2020).

    CAS 
    Article 

    Google Scholar 

  • 97.

    Desneux, N., Decourtye, A. & Delpuech, J.-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007).

    CAS 
    Article 

    Google Scholar 

  • 98.

    Goulson, D. The insect apocalypse, and why it matters. Curr. Biol. 29, R967–R971 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 99.

    Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 100.

    Hayes, T. B. & Hansen, M. From silent spring to silent night: agrochemicals and the anthropocene. Elem. Sci. Anthropol. 5, (2017).

  • 101.

    Bowler, D. E., Heldbjerg, H., Fox, A. D., Jong, M. & Böhning‐Gaese, K. Long‐term declines of European insectivorous bird populations and potential causes. Conserv. Biol. 33, 1120–1130 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 102.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 103.

    Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, 1–12 (2014).

    Article 

    Google Scholar 

  • 104.

    Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 105.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2015).

    Article 
    CAS 

    Google Scholar 

  • 106.

    Laczny, C. C. et al. BusyBee Web: metagenomic data analysis by bootstrapped supervised binning and annotation. Nucleic Acids Res. 45, W171–W179 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 107.

    Aziz, R. K. et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 1–15 (2008).

    Article 
    CAS 

    Google Scholar 

  • 108.

    Arkin, A. P. et al. KBase: The United States department of energy systems biology knowledgebase. Nat. Biotechnol. 36, 566 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 109.

    Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 110.

    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 111.

    Tatusov, R. L., Galperin, M. Y., Natale, D. A. & Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 112.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 113.

    Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 114.

    Brettin, T. et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci. Rep. 5, 8365 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 115.

    Li, L., Stoeckert, C. J. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 116.

    Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 117.

    Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–14 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 118.

    Weiss, B. & Kaltenpoth, M. Bacteriome-localized intracellular symbionts in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). Front. Microbiol. 7, 1486 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 119.

    Dunn, O. J. Multiple comparisons using rank sums. Technometrics 6, 241–252 (1964).

    Article 

    Google Scholar 

  • 120.

    Tanahashi, M. Natsumushi: Image measuring software for entomological studies. Entomol. Sci. 21, 347–360 (2018).

    Article 

    Google Scholar 

  • 121.

    Pérez-Palacios, T., Barroso, M. A., Ruiz, J. & Antequera, T. A rapid and accurate extraction procedure for analysing free amino acids in meat samples by GC–MS. Int. J. Anal. Chem. 2015, 209214 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 122.

    Miller, R. G. Simultaneous Statistical Inference (Springer, 1981).

  • 123.

    Engl, T., Kiefer, J.S.T. Data from: Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamenis. Max Planck Soc. https://doi.org/10.17617/3.5l (2021).


  • Source: Ecology - nature.com

    Analytics platform for coastal desalination plants wins 2021 Water Innovation Prize

    Supplementation of Lactobacillus early in life alters attention bias to threat in piglets