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The digestive system of the adult Hermetia illucens (Diptera: Stratiomyidae): morphological features and functional properties

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Abstract

The larvae of the black soldier fly (BSF), Hermetia illucens (Linnaeus, 1758) (Diptera: Stratiomyidae), are considered an efficient system for the bioconversion of organic waste into usable products, such as insect protein for animal feed and bioactive molecules. Despite the great interest toward H. illucens and its biotechnological applications, information on the biology of this insect is still scarce. In particular, no data on the structural and functional properties of the digestive system of the adult insect are available and it is a common belief that the fly does not eat. In the present work, we therefore investigate the remodeling process of the BSF larval midgut during metamorphosis, analyze the morphofunctional properties of the adult midgut, evaluate if the fly is able to ingest and digest food and assess whether the feeding supply influences the adult performances. Our results show that the larval midgut of H. illucens is removed during metamorphosis and a new pupal-adult epithelium, characterized by peculiar features compared to the larval organ, is formed by proliferation and differentiation of midgut stem cells. Moreover, our experiments indicate that the adult insect possesses a functional digestive system and that food administration affects the longevity of the fly. These data not only demonstrate that the adult BSF is able to eat but also open up the possibility to manipulate the feeding substrate of the fly to improve its performances in mass rearing procedures.

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References

  • Amcheslavsky A, Jiang J, Ip YT (2009) Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4:49–61

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benkel BF, Hickey DA (1986) Glucose repression of amylase gene expression in Drosophila melanogaster. Genetics 114:137–144

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bernfeld P (1955) Amylases, α and β. Methods Enzymol 1:149–158

    CAS  Google Scholar 

  • Bertinetti C, Samayoa AC, Hwang SY (2019) Effects of feeding adults of Hermetia illucens (Diptera: Stratiomyidae) on longevity, oviposition, and egg hatchability: insights into optimizing egg production. J Insect Sci 19:19

    PubMed Central  Google Scholar 

  • Billingsley PF, Lehane MJ (1996) Structure and ultrastructure of the insect midgut. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Springer, Dordrecht, pp 3–30

    Google Scholar 

  • Bonelli M, Bruno D, Caccia S, Sgambetterra G, Cappellozza S, Jucker C, Tettamanti G, Casartelli M (2019) Structural and functional characterization of Hermetia illucens larval midgut. Front Physiol 10:204. https://doi.org/10.3389/fphys.2019.00204

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Google Scholar 

  • Bruno D, Bonelli M, De Filippis F, Di Lelio I, Tettamanti G, Casartelli M, Ercolini D, Caccia S (2019) The intestinal microbiota of Hermetia illucens larvae is affected by diet and shows a diverse composition in the different midgut regions. Appl Environ Microbiol 85:e01864–e01818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buchon N, Osman D, David FP, Fang HY, Boquete JP, Deplancke B, Lemaitre B (2013) Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 3:1725–1738

    CAS  PubMed  Google Scholar 

  • Caccia S, Chakroun M, Vinokurov K, Ferre J (2014) Proteolytic processing of Bacillus thuringiensis Vip3A proteins by two Spodoptera species. J Insect Physiol 67:76–84

    CAS  PubMed  Google Scholar 

  • Charney J, Tomarelli RM (1947) A colorimetric method for the determination of the proteolytic activity of duodenal juice. J Biol Chem 171:501–505

    CAS  PubMed  Google Scholar 

  • Chng WA, Sleiman MSB, Schupfer F, Lemaitre B (2014) Transforming growth factor beta/activin signaling functions as a sugar-sensing feedback loop to regulate digestive enzyme expression. Cell Rep 9:336–348

    CAS  PubMed  Google Scholar 

  • Cickova H, Newton GL, Lacy RC, Kozanek M (2015) The use of fly larvae for organic waste treatment. Waste Manag 35:68–80

    CAS  PubMed  Google Scholar 

  • Coch Frugoni JA (1957) Tampone universale di Britton e Robinson a forza ionica costante. Gazz Chim Ital 84:403–407

    Google Scholar 

  • Dow JAT (1986) Insect midgut function. Adv Insect Physiol 19:187–328

    CAS  Google Scholar 

  • Dubreuil RR (2004) Copper cells and stomach acid secretion in the Drosophila midgut. Int J Biochem Cell Biol 36:745–752

    CAS  PubMed  Google Scholar 

  • EFSA Scientific Committee (2015) Scientific opinion on a risk profile related to production and consumption of insects as food and feed. EFSA J 13:4257–4317

    Google Scholar 

  • Endo Y, Nishiitsutsuju-Uwo J (1981) Gut endocrine cells in insects: the ultrastructure of the gut endocrine cells of the lepidopterous species. Biomed Res 2:270–280

    Google Scholar 

  • European Commission (2017) Commission regulation (EU) 2017/893 of 24 May 2017 amending Annexes I and IV to regulation (EC) no 999/2001 of the European Parliament and of the Council and Annexes X, XIV and XV to commission regulation (EU) no 142/2011 as regards the provisions on processed animal protein. Off J Eur Union L138:92–116

    Google Scholar 

  • Franzetti E, Huang ZJ, Shi YX, Xie K, Deng XJ, Li JP, Li QR, Yang WY, Zeng WN, Casartelli M, Deng HM, Cappellozza S, Grimaldi A, Xia Q, Feng Q, Cao Y, Tettamanti G (2012) Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 17:305–324

    CAS  PubMed  Google Scholar 

  • Franzetti E, Romanelli D, Caccia S, Cappellozza S, Congiu T, Rajagopalan M, Grimaldi A, de Eguileor M, Casartelli M, Tettamanti G (2015) The midgut of the silkmoth Bombyx mori is able to recycle molecules derived from degeneration of the larval midgut epithelium. Cell Tissue Res 361:509–528

    CAS  PubMed  Google Scholar 

  • Fujita T, Kobayashi S (1977) Structure and function of gut endocrine cells. Int Rev Cytol Suppl 187–233

  • Giangaspero A, Broce AB (1993) Micromorphology of the prestomal teeth and feeding-behavior of Musca autumnalis, M. larvipara and M. osiris (Diptera, Muscidae). Med Vet Entomol 7:398–400

    CAS  PubMed  Google Scholar 

  • Gobbi P, Martinez-Sanchez A, Rojo S (2013) The effects of larval diet on adult life-history traits of the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). Eur J Entomol 110:461–468

    Google Scholar 

  • Graczyk TK, Knight R, Gilman RH, Cranfield MR (2001) The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3:231–235

    CAS  PubMed  Google Scholar 

  • Graczyk TK, Knight R, Tamang L (2005) Mechanical transmission of human protozoan parasites by insects. Clin Microbiol Rev 18:128–132

    PubMed  PubMed Central  Google Scholar 

  • Gullan PJ, Cranston PS (2014) The insects: an outline of entomology. Wiley-Blackwell, Chichester, pp 156–189

    Google Scholar 

  • Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608

    CAS  PubMed  Google Scholar 

  • Hickey DA, Benkel B (1982) Regulation of amylase activity in Drosophila melanogaster: effects of dietary carbohydrate. Biochem Genet 20:1117–1129

    CAS  PubMed  Google Scholar 

  • Hogsette JA (1992) New diets for production of house flies and stable flies (Diptera, Muscidae) in the laboratory. J Econ Entomol 85:2291–2294

    CAS  PubMed  Google Scholar 

  • Holmes LA, Vanlaerhoven SL, Tomberlin JK (2012) Relative humidity effects on the life history of Hermetia illucens (Diptera: Stratiomyidae). Environ Entomol 41:971–978

    Google Scholar 

  • Holmes LA, Vanlaerhoven SL, Tomberlin JK (2013) Substrate effects on pupation and adult emergence of Hermetia illucens (Diptera: Stratiomyidae). Environ Entomol 42:370–374

    CAS  PubMed  Google Scholar 

  • Kovacs F, Medveczky I, Papp L, Gondar E (1990) Role of prestomal teeth in feeding of the house fly, Musca domestica (Diptera, Muscidae). Med Vet Entomol 4:331–335

    CAS  PubMed  Google Scholar 

  • Lee CY, Cooksey BA, Baehrecke EH (2002) Steroid regulation of midgut cell death during Drosophila development. Dev Biol 250:101–111

    CAS  PubMed  Google Scholar 

  • Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550

    CAS  PubMed  Google Scholar 

  • Lemaitre B, Miguel-Aliaga I (2013) The digestive tract of Drosophila melanogaster. Annu Rev Genet 47:377–404

    CAS  PubMed  Google Scholar 

  • Lemos FJA, Terra WR (1991) Digestion of bacteria and the role of midgut lysozyme in some insect larvae. Comp Biochem Physiol 100:265–268

    CAS  Google Scholar 

  • Li YB, Yang T, Wang JX, Zhao XF (2018) The steroid hormone 20-hydroxyecdysone regulates the conjugation of autophagy-related proteins 12 and 5 in a concentration and time-dependent manner to promote insect midgut programmed cell death. Front Endocrinol (Lausanne) 9:28

    Google Scholar 

  • Lii CY, Chang SM, Young YL (1982) Investigation of the physical and chemical properties of banana starches. J Food Sci 47:1493–1497

    CAS  Google Scholar 

  • Makkar HPS, Tran G, Henze V, Ankers P (2014) State-of-the-art on use of insects as animal feed. Anim Feed Sci Technol 197:1–33

    CAS  Google Scholar 

  • Marianes A, Spradling AC (2013) Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2:e00886

    PubMed  PubMed Central  Google Scholar 

  • McNulty M, Puljung M, Jefford G, Dubreuil RR (2001) Evidence that a copper-metallothionein complex is responsible for fluorescence in acid-secreting cells of the Drosophila stomach. Cell Tissue Res 304:383–389

    CAS  PubMed  Google Scholar 

  • Meneguz M, Schiavone A, Gai F, Dama A, Lussiana C, Renna M, Gasco L (2018) Effect of rearing substrate on growth performance, waste reduction efficiency and chemical composition of black soldier fly (Hermetia illucens) larvae. J Sci Food Agric

  • Micchelli CA, Perrimon N (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475–479

    CAS  PubMed  Google Scholar 

  • Montali A, Romanelli D, Cappellozza S, Grimaldi A, de Eguileor M, Tettamanti G (2017) Timing of autophagy and apoptosis during posterior silk gland degeneration in Bombyx mori. Arthropod Struct Dev 46:518–528

    PubMed  Google Scholar 

  • Muller A, Wolf D, Gutzeit HO (2017) The black soldier fly, Hermetia illucens—a promising source for sustainable production of proteins, lipids and bioactive substances. Z Naturforsch C 72:351–363

    PubMed  Google Scholar 

  • Nakamura S, Ichiki RT, Shimoda M, Morioka S (2016) Small-scale rearing of the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae), in the laboratory: low-cost and year-round rearing. Appl Entomol Zool 51:161–166

    Google Scholar 

  • Nguyen TTX, Tomberlin JK, Vanlaerhoven S (2013) Influence of resources on Hermetia illucens (Diptera: Stratiomyidae) larval development. J Med Entomol 50:898–906

    PubMed  Google Scholar 

  • Nguyen TTX, Tomberlin JK, Vanlaerhoven S (2015) Ability of black soldier fly (Diptera: Stratiomyidae) larvae to recycle food waste. Environ Entomol 44:406–410

    CAS  PubMed  Google Scholar 

  • Nishiitsutsuju-Uwo J, Endo Y (1981) Gut endocrine cells in insects: the ultrastructure of the gut endocrine cells of the cockroach midgut. Biomed Res 2:30–44

    Google Scholar 

  • Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474

    CAS  PubMed  Google Scholar 

  • Ohlstein B, Spradling A (2007) Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315:988–992

    CAS  PubMed  Google Scholar 

  • Padilha MH, Pimentel AC, Ribeiro AF, Terra WR (2009) Sequence and function of lysosomal and digestive cathepsin D-like proteinases of Musca domestica midgut. Insect Biochem Mol Biol 39:782–791

    CAS  PubMed  Google Scholar 

  • Parthasarathy R, Palli SR (2008) Proliferation and differentiation of intestinal stem cells during metamorphosis of the red flour beetle, Tribolium castaneum. Dev Dyn 237:893–908

    CAS  PubMed  Google Scholar 

  • Pimentel AC, Montali A, Bruno D, Tettamanti G (2017) Metabolic adjustment of the larval fat body in Hermetia illucens to dietary conditions. J Asia Pac Entomol 20:1307–1313

    Google Scholar 

  • Pimentel AC, Barroso IG, Ferreira JMJ, Dias RO, Ferreira C, Terra WR (2018) Molecular machinery of starch digestion and glucose absorption along the midgut of Musca domestica. J Insect Physiol 109:11–20

    CAS  PubMed  Google Scholar 

  • Rivers D, Geiman T (2017) Insect artifacts are more than just altered bloodstains. Insects 8

  • Romanelli D, Casartelli M, Cappellozza S, de Eguileor M, Tettamanti G (2016) Roles and regulation of autophagy and apoptosis in the remodelling of the lepidopteran midgut epithelium during metamorphosis. Sci Rep 6:32939

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sehnal F, Zitnan D (1996) Midgut endocrine cells. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Springer, Dordrecht, pp 55–85

    Google Scholar 

  • Shanbhag S, Tripathi S (2009) Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J Exp Biol 212:1731–1744

    CAS  PubMed  Google Scholar 

  • Sheppard DC, Newton GL, Thompson SA, Savage S (1994) A value-added manure management-system using the black soldier fly. Bioresour Technol 50:275–279

    CAS  Google Scholar 

  • Sheppard DC, Tomberlin JK, Joyce JA, Kiser BC, Sumner SM (2002) Rearing methods for the black soldier fly (Diptera: Stratiomyidae). J Med Entomol 39:695–698

    PubMed  Google Scholar 

  • Shina M (1975) Amylase activity in the midgut of Sarcophaga ruficornis and Musca domestica. Entomol Exp Appl 18:290–296

    Google Scholar 

  • Stoffolano JG Jr, Haselton AT (2013) The adult Dipteran crop: a unique and overlooked organ. Annu Rev Entomol 58:205–225

    CAS  PubMed  Google Scholar 

  • Stoffolano JG, Acaron A, Conway M (2008) “Bubbling” or droplet regurgitation in both sexes of adult Phormia regina (Diptera: Calliphoridae) fed various concentrations of sugar and protein solutions. Ann Entomol Soc Am 101:964–970

    CAS  Google Scholar 

  • Takashima S, Younossi-Hartenstein A, Ortiz PA, Hartenstein V (2011) A novel tissue in an established model system: the Drosophila pupal midgut. Dev Genes Evol 221:69–81

    PubMed  PubMed Central  Google Scholar 

  • Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200

    Google Scholar 

  • Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol B 109:1–62

    Google Scholar 

  • Terra WR, Ferreira C (2005) Biochemistry of digestion. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 4. Elsevier Pergamon Press, Oxford, pp 171–224

    Google Scholar 

  • Terra WR, Espinoza-Fuentes FP, Ferreira C (1988a) Midgut amylase, lysozyme, aminopeptidase, and trehalase from larvae and adults of Musca domestica. Arch Insect Biochem 9:283–297

    CAS  Google Scholar 

  • Terra WR, Espinoza-Fuentes FP, Ribeiro BM, Ferreira C (1988b) The larval midgut of the housefly (Musca domestica): ultrastructure, fluid fluxes and ion secretion in relation to the organization of digestion. J Insect Physiol 34:463–472

    CAS  Google Scholar 

  • Terra WR, Ferreira C, Baker JE (1996a) Compartmentalization of digestion. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Springer, Dordrecht, pp 206–235

    Google Scholar 

  • Terra WR, Ferreira C, Jordão BP, Dillon RJ (1996b) Digestive enzymes. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Springer, Dordrecht, pp 153–194

    Google Scholar 

  • Tettamanti G, Grimaldi A, Casartelli M, Ambrosetti E, Ponti B, Congiu T, Ferrarese R, Rivas-Pena ML, Pennacchio F, Eguileor M (2007) Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tissue Res 330:345–359

    PubMed  Google Scholar 

  • Tettamanti G, Salo E, Gonzalez-Estevez C, Felix DA, Grimaldi A, de Eguileor M (2008) Autophagy in invertebrates: insights into development, regeneration and body remodeling. Curr Pharm Des 14:116–125

    CAS  PubMed  Google Scholar 

  • Tettamanti G, Cao Y, Feng Q, Grimaldi A, de Eguileor M (2011) Autophagy in Lepidoptera: more than old wine in new bottle. Invertebr Surviv J 8:5–14

    Google Scholar 

  • Tomberlin JK, Sheppard DC (2002) Factors influencing mating and oviposition of black soldier flies (Diptera: Stratiomyidae) in a colony. J Entomol Sci 37:345–352

    Google Scholar 

  • Tomberlin JK, Sheppard DC, Joyce JA (2002) Selected life-history traits of black soldier flies (Diptera: Stratiomyidae) reared on three artificial diets. Ann Entomol Soc Am 95:379–386

    Google Scholar 

  • Tomberlin JK, Adler PH, Myers HM (2009) Development of the black soldier fly (Diptera: Stratiomyidae) in relation to temperature. Environ Entomol 38:930–934

    PubMed  Google Scholar 

  • Villalon JM, Ghosh A, Jacobs-Lorena M (2003) The peritrophic matrix limits the rate of digestion in adult Anopheles stephensi and Aedes aegypti mosquitoes. J Insect Physiol 49:891–895

    CAS  PubMed  Google Scholar 

  • Vinokurov KS, Elpidina EN, Oppert B, Prabhakar S, Zhuzhikov DP, Dunaevsky YE, Belozersky MA (2006) Diversity of digestive proteinases in Tenebrio molitor (Coleoptera: Tenebrionidae) larvae. Comp Biochem Physiol B Biochem Mol Biol 145:126–137

    CAS  PubMed  Google Scholar 

  • Vogel H, Muller A, Heckel DG, Gutzeit H, Vilcinskas A (2018) Nutritional immunology: diversification and diet-dependent expression of antimicrobial peptides in the black soldier fly Hermetia illucens. Dev Comp Immunol 78:141–148

    CAS  PubMed  Google Scholar 

  • Wang YS, Shelomi M (2017) Review of black soldier fly (Hermetia illucens) as animal feed and human food. Foods 6

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Acknowledgements

This work was supported by Fondazione Cariplo (grant no. 2014-0550). Daniele Bruno is a PhD student of the “Biotechnology, Biosciences and Surgical Technology” course at University of Insubria. Marco Bonelli is a PhD student of the “Environmental Sciences” course at the University of Milano. We thank Prof. Pietro Brandmayr for the identification of mouthparts and Sherryl Sundell for English editing.

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  1. Daniele Bruno and Marco Bonelli contributed equally to this work.

Authors and Affiliations

  1. Department of Biotechnology and Life Sciences, University of Insubria, Via J. H. Dunant, 3, 21100, Varese, Italy

    Daniele Bruno, Agustin G. Cadamuro, Annalisa Grimaldi & Gianluca Tettamanti

  2. Department of Biosciences, University of Milano, Via G. Celoria, 26, 20133, Milan, Italy

    Marco Bonelli & Morena Casartelli

  3. Department of Medicine and Surgery, University of Insubria, Via F. Guicciardini, 9, 21100, Varese, Italy

    Marcella Reguzzoni

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  1. Daniele Bruno
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Bruno, D., Bonelli, M., Cadamuro, A.G. et al. The digestive system of the adult Hermetia illucens (Diptera: Stratiomyidae): morphological features and functional properties. Cell Tissue Res 378, 221–238 (2019). https://doi.org/10.1007/s00441-019-03025-7

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