Dynamics of the intestinal bacterial community in black soldier fly larval guts and its influence on insect growth and development.
bacterial isolates
germ-free BSF larvae
growth and development; Hermetia illucens
promotive effects
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
revised:
05
06
2022
received:
05
10
2021
accepted:
21
06
2022
medline:
2
8
2023
pubmed:
12
7
2022
entrez:
11
7
2022
Statut:
ppublish
Résumé
Black soldier fly (BSF), Hermetia illucens (Diptera: Stratiomyidae), is a prominent insect for the bioconversion of various organic wastes. As a saprotrophic insect, the BSF inhabits microbe-rich environments. However, the influences of the intestinal microorganisms on BSF growth and development are not very clear. In this study, the dynamics of the intestinal bacterial community of BSF larvae (BSFL) were analyzed using pyrosequencing. Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria were the most prevalent bacterial phyla in the intestines of all larval instars. The dynamic changes in bacterial community compositions among different larval instars were striking at the genus level. Klebsiella, Clostridium, Providencia, and Dysgonomonas were the relatively most abundant bacteria in the 1st- to 4th-instar BSFL, respectively. Dysgonomonas and Providencia also dominated the 5th- and 6th-instar larvae, at ratios of 31.1% and 47.2%, respectively. In total, 148 bacterial strains affiliated with 20 genera were isolated on different media under aerobic and anaerobic conditions. Among them, 6 bacteria, BSF1-BSF6, were selected for further study. The inoculation of the 6 isolates independently into germ-free BSFL feeding on an artificial diet showed that all the bacteria, except BSF4, significantly promoted BSF growth and development compared with the germ-free control. Citrobacter, Dysgonomonas, Klebsiella, Ochrobactrum, and Providencia promoted BSF development significantly by increasing the weight gains of larvae and pupae, as well as increasing the prepupae and eclosion rates. In addition, Citrobacter, Klebsiella and Providencia shortened the BSF life cycle significantly. The results illustrate the promotive effects of intestinal bacteria on BSF growth and development.
Identifiants
pubmed: 35811567
doi: 10.1111/1744-7917.13095
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
947-963Subventions
Organisme : National Natural Science Foundation of China
ID : 31670004
Organisme : the Fundamental Research Funds for the Central Universities, Central China Normal University
ID : CCNU20CG005
Organisme : the Fundamental Research Funds for the Central Universities, Central China Normal University
ID : KJ02072019-0383
Informations de copyright
© 2022 Institute of Zoology, Chinese Academy of Sciences.
Références
Ao, Y., Yang, C., Wang, S., Hu, Q., Yi, L., Zhang, J. et al. (2020) Characteristics and nutrient function of intestinal bacterial communities in black soldier fly (Hermetia illucens L.) larvae in livestock manure conversion. Microbial Biotechnology, 14, 886-896.
Behar, A., Yuval, B. & Jurkevitch, E. (2008) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. Journal of Insect Physiology, 54, 1377-1383.
Boccazzi, I.V., Ottoboni, M., Martin, E., Comandatore, F., Vallone, L., Spranghers, T. et al. (2017) A survey of the mycobiota associated with larvae of the black soldier fly (Hermetia illucens) reared for feed production. PLoS ONE, 12, e0182533.
Brune, A. (2014) Symbiotic digestion of lignocellulose in termite guts. Nature Reviews Microbiology, 12, 168-180.
Bruno, D., Bonelli, M., De Filippis, F., Lelio, D.I., Tettamanti, G., Casartelli, M. et al. (2019) The intestinal microbiota of Hermetia illucens larvae is affected by diet and shows a diverse composition in the different midgut regions. Applied and Environmental Microbiology, 85(2), e01864-e01818.
Cai, Z., Yao, Z., Li, Y., Xi, Z., Bourtzis, K., Zhao, Z. et al. (2018) Intestinal probiotics restore the ecological fitness decline of Bactrocera dorsalis by irradiation. Evolutionary Applications, 11(10), 1946-1963.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K. et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335-336.
Cifuentes, Y., Glaeser, S.P., Mvie, J., Bartz, J.-O., Müller, A., Gutzeit, H.O. et al. (2020) The gut and feed residue microbiota changing during the rearing of Hermetia illucens larvae. Antonie Van Leeuwenhoek, 113, 1323-1344.
Cheng, D., Guo, Z., Riegler, M., Xi, Z., Liang, G. & Xu, Y. (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome, 5(1), 13.
Choi, Y.C., Choi, J.Y., Kim, J., Kim, M., Kim, W., Park, K. et al. (2009) Potential usage of food waste as a natural fertilizer after digestion by Hermetia illucens (Diptera: Stratiomyidae). International Journal of Industrial Entomology, 19, 171-174.
Consuegra, J., Grenier, T., Baa-Puyoulet, P., Rahioui, I., Akherraz, H., Gervais, H. et al. (2020) Drosophila-associated bacteria differentially shape the nutritional requirements of their host during juvenile growth. PLoS Biology, 18(3), e3000681.
De Smet, J., Wynants, E., Cos, P. & Campenhout, L.V. (2018) Microbial community dynamics during rearing of black soldier fly larvae (Hermetia illucens) and impact on exploitation potential. Applied and Environmental Microbiology, 84, 2722-2717.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C. & Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194-2200.
Engel, P. & Moran, N.A. (2013) The gut microbiota of insects-diversity in structure and function. FEMS Microbiology Reviews, 37(5), 699-735.
Erickson, M.C., Islam, M., Sheppard, C., Liao, J. & Doyle, M.P. (2004) Reduction of Escherichia coli O157: H7 and Salmonella enterica serovar enteritidis in chicken manure by larvae of the black soldier fly. Journal of Food Protection, 67, 685-690.
Fang, H., Chen, W., Wang, B., Li, X., Liu, S.-J. & Yang, H. (2016) Cultivation and characterization of symbiotic bacteria from the gut of Reticulitermes chinensis. Applied Environmental Biotechnology, 1, 3-12.
Fontes-Perez, H., Olvera-García, M., Chávez-Martínez, A., Rodriguez-Almeida, F.A., Arzola-Alvarez, C.A., Sanchez-Flores, A. et al. (2015) Genome sequence of Citrobacter sp. CtB7.12, isolated from the gut of the desert subterranean termite Heterotermes aureus. Genome Announcements, 3(6), e01290-e01215.
Galac, M.R. & Lazzaro, B.P. (2011) Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes and Infection, 13(7), 673-683.
Gao, S-M., Schippers, A., Chen, N., Yuan, Y., Zhang, M.-M., Li, Q. et al. (2020) Depth-related variability in viral communities in highly stratified sulfidic mine tailings. Microbiome, 8(1), 89.
Generalovic, T.N., McCarthy, S.A., Warren, I.A., Wood, J.M.D., Torrance, J., Sims, Y. et al. (2021) A high-quality, chromosome-level genome assembly of the Black Soldier Fly (Hermetia illucens L.). G3, 11(5), jkab085.
Gold, M., Tomberlin, J.K., Diener, S., Zurbrügg, C. & Mathys, A. (2018) Decomposition of biowaste macronutrients, microbes, and chemicals in black soldier fly larval treatment: a review. Waste Management, 82, 302-318.
Guo, Z., Lu, Y., Yang, F., Zeng, L., Liang, G. & Xu, Y. (2017) Transmission modes of a pesticide-degrading symbiont of the oriental fruit fly Bactrocera dorsalis (Hendel). Applied Microbiology and Biotechnology, 101(23-24), 8543-8556.
Habineza, P., Muhammad, A., Ji, T., Xiao, R., Yin, X., Hou, Y. et al. (2019) The promoting effect of gut microbiota on growth and development of red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by modulating its nutritional metabolism. Frontiers in Microbiology, 10, 1212.
Hamden, H., Guerfali, M.M., Fadhl, S., Saidi, M. & Chevrier, C. (2013) Fitness improvement of mass-reared sterile males of Ceratitis capitata (Vienna 8 strain) (Diptera: Tephritidae) after gut enrichment with probiotics. Journal of Economic Entomology, 106, 641-647.
Hogsette, J.A. (1992) New diets for production of house-flies and stable flies (Diptera, Muscidae) in the laboratory. Journal of Economic Entomology, 85, 2291-2294.
Jiang, C., Jin, W.Z., Tao, X.H., Zhang, Q., Zhu, J., Feng, S.Y. et al. (2019) Black soldier fly larvae (Hermetia illucens) strengthen the metabolic function of food waste biodegradation by gut microbiome. Microbial Biotechnology, 12, 528-543.
Jeon, H., Park, S., Choi, J., Jeong, G., Lee, S.-B., Choi, Y. et al. (2011) The intestinal bacterial community in the food waste-reducing larvae of Hermetia illucens. Current Microbiology, 62, 1390-1399.
Kešnerová, L., Mars, R., Ellegaard, K.M., Troilo, M., Sauer, U. & Engel, P. (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biology, 15(12), e2003467.
Klammsteiner, T., Walter, A., Bogataj, T., Heussler, C.D., Stres, B., Steiner, F.M. et al. (2020) The core gut microbiome of black soldier fly (Hermetia illucens) larvae raised on low-bioburden diets. Frontiers in Microbiology, 11, 993.
Klammsteiner, T., Walter, A., Bogataj, T., Heussler, C.D., Stres, B., Steiner, F.M. et al. (2021) Impact of processed food (canteen and oil wastes) on the development of black soldier fly (Hermetia illucens) larvae and their gut microbiome functions. Frontiers in Microbiology, 12, 619112.
Lam, K., Babor, D., Duthie, B., Babor, E.M., Moore, M. & Gries, G. (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Animal Behaviour, 74, 81-92.
Lam, K., Geisreiter, C. & Gries, G. (2009) Ovipositing female house flies provision offspring larvae with bacterial food. Entomologia Experimentalis et Applicata, 133, 292-295.
Li, H., Ren, L., Xie, M., Gao, Y., He, M., Hassan, B. et al. (2020) Egg-surface bacteria are indirectly associated with oviposition aversion in Bactrocera dorsalis. Current Biology, 30(22), 4432-4440.e4.
Liang, Z., Fang, W., Luo, Y., Lu, Q., Juneau, P., He, Z. et al. (2021) Mechanistic insights into organic carbon-driven water blackening and odorization of urban rivers. Journal of Hazardous Materials, 405, 124663.
Liu, J.H., Zhang, M.L., Zhang, R.Y., Zhu, W.Y. & Mao, S.Y. (2016) Comparative studies of the composition of bacterial microbiota associated with the ruminal content, ruminal epithelium and in the feces of lactating dairy cows. Microbial Biotechnology, 9(2), 257-268.
Liu, N., Li, H., Chevrette, M.G., Zhang, L., Cao, L., Zhou, H. et al. (2019) Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite. The ISME Journal, 13, 104-117.
Liu, Q.L., Tomberlin, J.K., Brady, J.A., Sanford, M.R. & Yu, Z.N. (2008) Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environmental Entomology, 37, 1525-1530.
Lymar, E.S., Li, B. & Renganathan, V. (1995) Purification and characterization of a cellulose-binding (beta)-glucosidase from cellulose-degrading cultures of Phanerochaete chrysosporium. Applied and Environmental Microbiology, 61, 2976-2980.
Mazza, L., Xiao, X., Rehman, K., Cai, M., Zhang, D., Fasulo, S. et al. (2020) Management of chicken manure using black soldier fly (Diptera:Stratiomyidae) larvae assisted by companion bacteria. Waste Management, 102, 312-318.
McManus, R., Ravenscraft, A. & Moore, W. (2018) Bacterial associates of a gregarious riparian beetle with explosive defensive chemistry. Frontiers in Microbiology, 9, 2361.
Minami, Y., Shigeta, Y., Tokumoto, U., Tanaka, Y., Yonekura-Sakakibara, K., Oh-oka, H. & Matsubara, H. (1999) Cloning, sequencing, characterization, and expression of a beta-glucosidase cDNA from the indigo plant. Plant Science, 142, 219-226.
Newton, L., Sheppard, C., Watson, D.W., Burtle, G. & Dove, R. (2005) Using the black soldier fly, Hermetia illucens, as a value-added tool for the management of swine manure. Countryside & Small Stock Journal, 36(12), 17.
Park, S.I., Kim, J.W. & Yoe, S.M. (2015) Purification and characterization of a novel antibacterial peptide from black soldier fly (Hermetia illucens) larvae. Devlopmental and Comparative Immunology, 52, 98-106.
Ponnusamy, L., Xu, N., Nojima, S., Wesson, D.M., Schal, C. & Apperson, C.S. (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proceedings of the National Academy of Sciences USA, 105, 9262-9267.
Roque-Romero, L., Hernándes, E., Aceituno-Medina, M., Ventura, C., Toledo, J. & Malo, E.A. (2020) Attractiveness and sexual competitiveness of Anastrepha obliqua males (Diptera: Tephritidae) fed on a diet enriched with Providencia rettgeri. Frontiers in Microbiology, 11, 1777.
Sheppard, D.C., Newton, G.L. & Thompson, S.A. (1994) A value added manure management system using the black soldier fly. Bioresource Technology, 50, 275-279.
Sheppard, D.C., Tomberlin, J.K., Joyce, J.A., Kiser, B.C. & Sumner, S.M. (2002) Rearing methods for the black soldier fly (Diptera: Stratiomyidae). Journal of Medcial Entomology, 39, 695-698.
Singh, A. & Kumari, K. (2019) An inclusive approach for organic waste treatment and valorisation using black soldier fly larvae: a review. Journal of Environmental Management, 251, 109569.
Smetana, S., Palanisamy, M., Mathys, A. & Heinz, V. (2016) Sustainability of insect use for feed and food: life cycle assessment perspective. Journal of Cleaner Production, 137, 741-751.
Tegtmeler, D., Thompson, C.L., Schauer, C. & Brune, A. (2016) Oxygen affects gut bacterial colonization and metabolic activities in a gnotobiotic cockroach model. Applied and Environmental Microbiology, 82, 1080-1089.
Tomberlin, J.K., Sheppard, D.C. & Joyce, J.A. (2005) Black soldier fly (Diptera: Stratiomyidae) colonization of pig carrion in South Georgia. Journal of Forensic Sciences, 50, 152-153.
Tomberlin, J.K., Adler, P.H. & Myers, H.M. (2009) Development of the black soldier fly (Diptera: Stratiomyidae) in relation to temperature. Environmental Entomology, 38, 930-934.
Tomberlin, J.K. & van Huis, A. (2020) Black soldier fly from pest to “crown jewel” of the insects as feed industry: an historical perspective. Journal of Insects as Food and Feed, 6, 1-4.
Vacchini, V., Gonella, E., Crotti, E., Prosdocimi, E.M., Mazzetto, F., Chouaia, B. et al. (2017) Bacterial diversity shift determined by different diets in the gut of the spotted wing fly Drosophila suzukii is primarily reflected on acetic acid bacteria. Environmental Microbiology Report, 9, 91-103.
Wang, X.M., Ma, S., Yang, S.Y., Peng, R., Zheng, Y. & Yang, H. (2016) Paenibacillus nasutitermitis sp. nov. isolated from a termite gut. International Journal of Systematic and Evolutionary Microbiology, 66, 901-905.
Weisburg, W.G., Barns, S.M., Pelletier, D.A. & Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173, 697-703.
Yang, Y.-J., Zhang, N., Ji, S.-Q., Lan, X., Zhang, K.-D., Shen, Y.-L. et al. (2014) Dysgonomonas macrotermitis sp. nov., isolated from the hindgut of a fungus-growing termite. International Journal of Systematic and Evolutionary Microbiology, 64, 2956-2961.
Yu, G., Cheng, P., Chen, Y., Li, Y., Yang, Z., Chen, Y. et al. (2011) Inoculating poultry manure with companion bacteria influences growth and development of black soldier fly (Diptera: Stratiomyidae) larvae. Environmental Entomology, 40, 30-35.
Zhan, S., Fang, G., Cai, M., Kou, Z., Xu, J., Cao, Y. et al. (2020) Genomic landscape and genetic manipulation of the black soldier fly Hermetia illucens, a natural waste recycler. Cell Research, 30, 50-60.
Zhang, J., Huang, L., He, J., Tomberlin, J.K., Li, J., Lei, C. et al. (2010) An artificial light source influences mating and oviposition of black soldier flies, Hermetia illucens. Journal of Insect Science, 10(202), 1-7.
Zheng, H., Powell, J.E., Steele, M.I., Dietrich, C. & Moran, N.A. (2017) Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences USA, 114, 4775-4780.
Zheng, L.Y., Crippen, T.L., Singh, B., Tarone, A.M., Dowd, S., Yu, Z.N. et al. (2013a) A survey of bacterial diversity from successive life stages of black soldier fly (Diptera: Stratiomyidae) by using 16S rDNA pyrosequencing. Journal of Medical Entomology, 50, 647-658.
Zheng, L.Y., Crippen, T.L., Holmes, L., Singh, B., Pimsler, M.L., Benbow, M.E. et al. (2013b) Bacteria mediate oviposition by the black soldier fly, Hermetia illucens (L.), (Diptera: Stratiomyidae). Scientific Reports, 3, 2563.
Zhou, N., Sun, Y.T., Chen, D.W., Du, W., Yang, H. & Liu, S.J. (2019) Harnessing microfluidic streak plate technique to investigate the gut microbiome of Reticulitermes chinensis. Microbiology Open, 8(3), e654.