Abstract
Black soldier fly, Hermetia illucens (Linnaeus, 1758), is an important economic fly as its larvae can be used for recycling organic waste, such as food waste and manure. H. illucens larvae (BSFL) could uptake Cd from substrates and accumulate it inside bodies, which need to be monitored during waste treatment. Metallothionein (MT) usually serve as biomarker because of its role in metal homeostasis, detoxification, and dose response of heavy metals. Therefore, a MT gene was cloned from H. illucens (HIMT) that encoded 40 amino acids with typical cysteine rich features, which had a high sequence identity with other insect MTs. The expression of HIMT and total MT protein was measured in BSFL fed by meals spiked with gradient dose of Cd (0, 5, 50, 500 mg/kg) for 24, 48, 72, and 96 h, respectively. Dose-associated response of HIMT and total MT were found and the possible correlative range of Cd was from 5 to 50 mg/kg. The expression of HIMT might be a potential biomarker for monitoring Cd contamination by H. illucens in terrestrial organic matters, which might further apply in waste transformation system.
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References
Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF (2000) The genome sequence of Drosophila melanogaster. Science 287(5461):2185–2196. https://doi.org/10.1126/science.287.5461.2185
Amiard-Triquet C, Rainglet F, Larroux C, Regoli F, Hummel H (1998) Metallothioneins in arctic bivalves. Ecotoxicol Environ Saf 41(2):96–102. https://doi.org/10.1016/j.aquatox.2005.08.015
Asselman J, Shaw JR, Glaholt SP, Colbourne JK, De Schamphelaere KAC (2013) Transcription patterns of genes encoding four metallothionein homologs in Daphnia pulex exposed to copper and cadmium are time- and homolog- dependent. Aquat Toxicol 142-143:422–430. https://doi.org/10.1016/j.aquatox.2013.09.010
Badiou-Bénéteau A, Benneveau A, Géret F, Delatte H, Becker N, Brunet JL, Reynaud B, Belzunces LP (2013) Honeybee biomarkers as promising tools to monitor environmental quality. Environ Int 60:31–41. https://doi.org/10.1016/j.envint.2013.07.002
Chen X, Wang X, Gu X, Jiang Y, Ji R (2017) Oxidative stress responses and insights into the sensitivity of the earthworms Metaphire guillelmi and Eisenia fetida to soil cadmium. Sci Total Environ 574:300–306. https://doi.org/10.1016/j.scitotenv.2016.09.059
Cummins VC Jr, Rawles SD, Thompson KR, Velasquez A, Kobayashi Y, Hager J, Webster CD (2017) Evaluation of black soldier fly (Hermetia illucens) larvae meal as partial or total replacement of marine fish meal in practical diets for Pacific white shrimp (Litopenaeus vannamei). Aquaculture 473:337–344. https://doi.org/10.1016/j.aquaculture.2017.02.022
Diener S, Solano NMS, Gutiérrez FR, Zurbrügg C, Tockner K (2011) Biological treatment of municipal organic waste using black soldier fly larvae. Waste Biomass Valori 2:357–363. https://doi.org/10.1007/s12649-011-9079-1
Diener S, Zurbrügg C, Tockner K (2015) Bioaccumulation of heavy metals in the black soldier fly, Hermetia illucens and effects on its life cycle. J Insect Food Feed 1:261–270. https://doi.org/10.3920/JIFF2015.0030
Gao Q, Wang X, Wang W, Lei C, Zhu F (2017) Influences of chromium and cadmium on the development of black soldier fly larvae. Environ Sci Pollut Res 24(9):8637–8644. https://doi.org/10.1007/s11356-017-8550-3
Gauthier M, Aras P, Jumarie C, Boily M (2016) Low dietary levels of Al, Pb and Cd may affect the non-enzymatic antioxidant capacity in caged honey bees (Apis mellifera). Chemosphere 144:848–854. https://doi.org/10.1016/j.chemosphere.2015.09.057
Guirola M, Naranjo Y, Capdevila M, Atrian S (2011) Comparative genomics analysis of metallothioneins in twelve Drosophila species. J Inorg Biochem 105(8):1050–1059. https://doi.org/10.1016/j.jinorgbio.2011.05.004
Hamer DH (1986) Metallothionein. Annu Rev Biochem 55(1):913–951. https://doi.org/10.1146/annurev.bi.55.070186.004405
Kenis M, Kone N, Chrysostome CAAM, Devic E, Koko GKD, Clottey VA, Nacambo S, Mensah GA (2014) Insects used for animal feed in West Africa. Entomologia 2(2):107–114. https://doi.org/10.4081/entomologia.2014.218
Liu Y, Wu H, Yu Z, Guo Y, Zhang J, Zhu KY, Ma E (2015) Transcriptional response of two metallothionein genes (OcMT1 and OcMT2) and histological changes in Oxya chinensis (Orthoptera: Acridoidea) exposed to three trace metals. Chemosphere 139:310–317. https://doi.org/10.1016/j.chemosphere.2015.06.043
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Marono S, Loponte R, Lombardi P, Vassalotti G, Pero ME, Russo F, Gasco L, Parisi G, Piccolo G, Nizza S, Di Meo C, Attia YA, Bovera F (2017) Productive performance and blood profiles of laying hens fed Hermetia illucens larvae meal as total replacement of soybean meal from 24 to 45 weeks of age. Poult Sci 96(6):1783–1790. https://doi.org/10.3382/ps/pew461
Mokdad R, Debec A, Wegnez M (1987) Metallothionein genes in Drosophila melanogaster constitute a dual system. P Natl Acad Sci USA 84(9):2658–2662. https://doi.org/10.1073/pnas.84.9.2658
Nguyen AH, Altomare LE, McElwain MC (2014) Decreased accumulation of cadmium in drosophila selected for resistance suggests a mechanism independent of metallothionein. Biol Trace Elem Res 160(2):245–249. https://doi.org/10.1007/s12011-014-0037-1
Nguyen TTX, Tomberlin JK, Vanlaerhoven S (2015) Ability of black soldier fly (Diptera: Stratiomyidae) larvae to recycle food waste. Environ Entomol 44(2):406–410. https://doi.org/10.1093/ee/nvv002
Polykretis P, Delfino G, Petrocelli I, Cervo R, Tanteri G, Montori G, Perito B, Branca JJV, Morucci G, Gulisano M (2016) Evidence of immunocompetence reduction induced by cadmium exposure in honey bees (Apis mellifera). Environ Pollut 218:826–834. https://doi.org/10.1016/j.envpol.2016.08.006
Purschke B, Scheibelberger R, Axmann S, Adler A, Jager H (2017) Impact of substrate contamination with mycotoxins, heavy metals and pesticides on growth performance and composition of black soldier fly larvae (Hermetia illucens) for use in the feed and food value chain. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. https://doi.org/10.1080/19440049.2017.1299946
Ren XY, Zhou Y, Zhang JP, Feng WH, Jiao BH (2003) Expression of metallothionein gene at different time in testicular interstitial cells and liver of rats treated with cadmium. World J Gastroentero 9(7):1554–1558. https://doi.org/10.3748/wjg.v9.i7.1554
Ren F, Jiang H, Sun J, He L, Li W, Wang Y, Wang Q (2011) Cloning, characterization, expression, and copper sensitivity of the metallothionein-1 gene in the Chinese mitten crab, Eriocheir sinensis. Mol Biol Rep 38(4):2383–2393. https://doi.org/10.1007/s11033-010-0372-z
Sheppard DC, Tomberlin JK, Joyce JA, Kiser BC, Sumner SM (2002) Rearing methods for the black soldier fly (Diptera : Stratiomyidae). J Med Entomol 39(4):695–698. https://doi.org/10.1603/0022-2585-39.4.695
Shu Y, Zhang G, Wang J (2012) Response of the common cutworm Spodoptera litura to zinc stress: Zn accumulation, metallothionein and cell ultrastructure of the midgut. Sci Total Environ 438:210–217. https://doi.org/10.1016/j.scitotenv.2012.06.065
Somparn A, Iwai CB, Noller B (2015) Potential use of acetylcholinesterase, glutathione-S-transferase and metallothionein for assessment of contaminated sediment in tropical chironomid, Chironomus javanus. J Environ Biol 36:1355
Stamer A (2015) Insect proteins-a new source for animal feed: the use of insect larvae to recycle food waste in high-quality protein for livestock and aquaculture feeds is held back largely owing to regulatory hurdles. EMBO Rep 16(6):676–680. https://doi.org/10.15252/embr.201540528
Sterenborg I, Roelofs D (2003) Field-selected cadmium tolerance in the springtail Orchesella cincta is correlated with increased metallothionein mRNA expression. Insect Biochem Mol Biol 33(7):741–747. https://doi.org/10.1016/S0965-1748(03)00070-5
Tang T, Huang DW, Zhang D, YJ W, Murphy RW, Liu FS (2011) Identification of two metallothionein genes and their roles in stress responses of Musca domestica toward hyperthermy and cadmium tolerance. Comp Biochem Physiol B Biochem Mol Biol 160(2-3):81–88. https://doi.org/10.1016/j.cbpb.2011.06.008
Van Der Fels-Klerx HJ, Camenzuli L, Van Der Lee MK, Oonincx DG (2016) Uptake of cadmium, lead and arsenic by Tenebrio molitor and Hermetia illucens from contaminated substrates. PLoS One 11(11):166–186. https://doi.org/10.1371/journal.pone.0166186
Won E-J, Rhee J-S, Ra K, Kim K-T, Au DWT, Shin K-H, Lee J-S (2011) Molecular cloning and expression of novel metallothionein (MT) gene in the polychaete Perinereis nuntia exposed to metals. Environ Sci Pollut R 19(7):2606–2618. https://doi.org/10.1007/s11356-012-0905-1
Zheng L, Hou Y, Li W, Yang S, Li Q, Yu Z (2012) Biodiesel production from rice straw and restaurant waste employing black soldier fly assisted by microbes. Energy 47(1):225–229. https://doi.org/10.1016/j.energy.2012.09.006
Zhou F, Tomberlin JK, Zheng L, Yu Z, Zhang J (2013) Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. J Med Entomol 50(6):1224–1230. https://doi.org/10.1603/ME13021
Funding
This study was funded by the Agricultural Technology Transfer Research Challenge Fund, (No. 9321301), the EU-funded project PROteINSECT (No. 034082), and the Fundamental Research Funds for the Central Universities (No. 2014PY059).
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Wang, X., Gao, Q., Liu, X. et al. Metallothionein in Hermetia illucens (Linnaeus, 1758) larvae (Diptera: Stratiomyidae), a potential biomarker for organic waste system. Environ Sci Pollut Res 25, 5379–5385 (2018). https://doi.org/10.1007/s11356-017-0856-7
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DOI: https://doi.org/10.1007/s11356-017-0856-7