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Analysis of the effects of nanosilver on bacterial community in the intestinal fluid of silkworms using high-throughput sequencing

Published online by Cambridge University Press:  27 September 2019

Chen Lin Open the ORCID record for Chen Lin [Opens in a new window] ,
Zhou Wei ,
Zhou Yi ,
Tan Tingting ,
Du Huamao  and
Feng Lichun
Chen Lin
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing400715, China
Zhou Wei
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing400715, China
Zhou Yi
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing400715, China
Tan Tingting
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing400715, China
Feng Lichun*
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing400715, China
*
Author for correspondence: Feng Lichun, Email: [email protected]
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Abstract

Nanosilver is an environment-friendly, harmless alternative of traditional disinfectants which can be potentially applied in the sericulture industry. However, the effects of nanosilver on the intestinal bacterial community of the silkworms (Bombyx mori L.) are unclear. In this study, Illumina MiSeq high-throughput sequencing technology was used to assess the intestinal bacterial community in both male and female silkworms while treated with different concentrations of nanosilver. We found that nanosilver significantly influenced the composition of silkworm intestinal bacterial community on the different taxonomic levels. Most conspicuously, the abundance of Firmicutes was increased by the treatment of 20 mg L−1 nanosilver but decreased by that of 100 mg L−1 nanosilver at the phylum level. The same trend was observed in Bacilli at the class level and in Enterococcus at the genus level. In some extreme cases, application of nanosilver eliminated the bacterium, e.g., Brevibacillus, but increased the population of several other bacteria in the host intestine, such as Blautia, Terrisporobacter, Faecalibacterium, and some bacteria could only be found in nanosilver treatment groups, e.g., Dialister. In addition, although nanosilver generally showed negative effects on the cocooning rate in a dose-dependent manner, we found that 20 mg L−1 nanosilver treatment significantly increased the body weight of silkworms and did not show negative effects on the survival rate. These results indicated that the intestinal bacteria community of silkworm larvae was significantly changed after nanosilver treatment which might consequently influence host growth and development.

Keywords

Bacterial communityhigh-throughput sequencingnanosilversilkworm
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 3 , June 2020 , pp. 309 - 320
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Copyright
Copyright © Cambridge University Press 2019

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References

Bannoehr, J and Guardabassi, L (2012) Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Veterinary Dermatology 23, 253–266.CrossRefGoogle ScholarPubMed
Biswas, N, Rahman, A, Datta, A, Goswami, A and Bramhachary, RL (2010) Nanoparticle surface as activation site. Journal Nanoscience Nanotechnology 10, 1–5.CrossRefGoogle ScholarPubMed
Brisse, S, Grimont, F, Grimont, PAD, Dworkin, M, Falkow, S, Rosenberg, E, Schleifer, K-H and Stackebrandt, E (2006) The Prokaryotes-A Handbook on the Biology of Bacteria, vol. 95. New York: Springer, pp. 6578–6583.Google Scholar
Brisse, S, Fevre, C, Passet, V, Issenhuth-Jeanjean, S, Tournebize, R, Diancourt, L and Grimont, P (2009) Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 4, e4982.CrossRefGoogle ScholarPubMed
Cao, GT, Zeng, XF, Chen, AG, Zhou, L, Zhang, L, Xiao, YP and Yang, CM (2013) Effects of a probiotic, Enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poultry Science 92, 2949–2955.CrossRefGoogle ScholarPubMed
Chao, A and Lee, SM (1992) Estimating population size for capture-recapture data when capture probabilities vary by time and individual animal. Biometrics 48, 201–216.CrossRefGoogle ScholarPubMed
Clavijo, V and Flórez, MJV (2018) The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: a review. Poultry Science 97, 1006–1021.CrossRefGoogle ScholarPubMed
Colman, DR, Toolson, EC and Takacs-Vesbach, CD (2012) Do diet and taxonomy influence insect gut bacterial communities? Molecular Ecology 21, 5124–5137.CrossRefGoogle ScholarPubMed
Dai, ZL, Wu, ZL, Hang, SQ, Zhu, WY and Wu, GY (2015) Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction. Molecular Human Reproduction 21, 389–409.CrossRefGoogle ScholarPubMed
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C and Knight, R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200.CrossRefGoogle ScholarPubMed
Farzi, A, Fröhlich, EE and Holzer, P (2018) Gut microbiota and the neuroendocrine system. Neurotherapeutics 15, 5–22.CrossRefGoogle ScholarPubMed
Gao, C, Cui, CF, Zhang, GF, Ren, GW, Wu, JJ and Yu, DH (2014) Influences of different kinds of disinfection methods on the germination and sterilization effects of tobacco seeds. Journal of Anhui Agricultural Sciences 43, 44–49.Google Scholar
Gao, K, Mu, CL, Yu, KF and Zhu, WY (2016) Enteroendocrine and nutrient sensing system. Chinese Journal of Animal Nutrition 28, 1633–1640, (in Chinese).Google Scholar
Gray, JS (2000) The measurement of marine species diversity, with an application to the benthic fauna of the Norwegian continental shelf. Journal of Experimental Marine Biology Ecology 250, 23–49.CrossRefGoogle ScholarPubMed
Grimont, PAD, Grimont, F, Brenner, DJ, Krieg, NR and Staley, JT (2005) Bergey's Manual of Systematic Bacteriology, vol. 2 The Proteobacteria, Part B: The Gammaproteobacteria. New York: Springer-Verlag, pp. 685–693.Google Scholar
Huang, Y, Li, Y, Huang, Q, Cui, Z, Yu, D and Rajput, IR (2012) Effect of orally administered Enterococcus faecium EF1 on intestinal cytokines and chemokines production of suckling piglets. Pakeran Veteran Journal 32, 81–84.Google Scholar
Insuk, S, Keun-Tae, P, Gayeung, K, Jong-Ho, K and Young-Hee, L (2018) Probiotic potential of Enterococcus faecium isolated from chicken cecum with immunomodulating activity and promoting longevity in Caenorhabditis elegans. Journal Microbiology Biotechnology 28, 883–892.Google Scholar
Jeng, HA and Swanson, J (2006) Toxicity of metal oxide nanoparticles in mammalian cells. Journal of Environment Science Health 41, 2699–2711.CrossRefGoogle ScholarPubMed
Jregory, C, Justin, K, Jesse, S, Kyle, B, Frederic, DB, Elizabeth, KC, Noah, F, Antonio, GP, Julia, KG, Jeffrey, IG, Gavin, AH, Scott, TK, Dan, K, Jeremy, EK, Ruth, EL, Catherine, AL, Daniel, M, Brian, DM, Meg, P, Jens, R, Joel, RS, Peter, JT, William, AW, Jeremy, W, Tanya, Y, Jesse, Z and Rob, K (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.Google Scholar
Kalliokoski, O, Jacobsen, KR, Darusman, HS, Henriksen, T, Weimann, A, Poulsen, HE, Hau, J and Abelson, K (2013) Mice do not habituate to metabolism cage housing – a three week study of male BALB/c mice. PLoS One 8, 584–560.CrossRefGoogle ScholarPubMed
Lembo, D and Cavalli, R (2010) Nanoparticulate delivery systems for antiviral drugs. Antiviral Chemistry and Chemotherapy 21, 53–70.CrossRefGoogle ScholarPubMed
Li, C, Zhou, Y, Zhang, YQ, Chen, L, Yang, RK and Feng, LC (2019) Effects of bleach powder on the midgut digestive enzymes of silkworms. Chinese Journal of Applied Entomology 42, 142–149.Google Scholar
Liu, W (2015) Method of using lime powder disinfection in sericulture production. Farmers’ Friends of Riches 13, 12–113.Google Scholar
Ma, ML, He, XY and Zhu, WY (2016) Metabolic pattern of pig hindgut bacteria on aromatic amino acids by an in vitro fermentation method. Acta Microbiologica Sinica 56, 1786–1793, (in Chinese).Google ScholarPubMed
Mikkelsen, L, Sheykhzade, M, Jensen, KA, Saber, AT, Jacobsen, NR, Vogel, U, Wallin, H, Loft, S and Møller, P (2011) Modest effect on plaque progression and vasodilatory function in atherosclerosis-prone mice exposed to nanosized TiO2. Particle and Fibre Toxicology 10, 8–32.Google Scholar
Mu, CL, Yang, YX and Zhu, WY (2016) Gut microbiota: the brain peacekeeper. Frontiers in Microbiology 7, 345–153.CrossRefGoogle ScholarPubMed
Packia Jacob, SJ, Finub, JS and Narayanan, A (2012) Synthesis of silver nanoparticles using Piper longum leaf extracts and its cytotoxic activity against Hep-2 cell line. Colloids and Surfaces B Biointerfaces 9, 212–214.CrossRefGoogle Scholar
Park, SH, Lee, SI, Kim, SA, Christensen, K and Ricke, SC (2017) Comparison of antibiotic supplementation versus a yeast-based prebiotic on the cecal microbiome of commercial broilers. PLoS One 12, 182–805.Google ScholarPubMed
Pitta, DW, Parmar, N, Patel, AK, Indugu, N, Kumar, S, Prajapathi, KB, Patel, AB, Reddy, B and Joshi, C (2014) Bacterial diversity dynamics associated with different diets and different primer pairs in the rumen of kankrej cattle. PLoS One 9, 11–13.CrossRefGoogle ScholarPubMed
Rahman, A, Biswas, N, Ulrichs, C, Büttner, C, Bramhachary, RL, Goswami, A and Datta, A (2009 a) Nanoparticle–virus complex shows enhanced immunological effect against baculovirus. Journal Nanoscience Nanotechnology 9, 5567–5571.CrossRefGoogle ScholarPubMed
Robinson, CJ and Young, VB (2010) Antibiotic administration alters the community structure of the gastrointestinal microbiota. Gut Microbes 1, 279–284.CrossRefGoogle Scholar
Scharek, L, Guth, J, Reiter, K, Weyrauch, KD, Taras, D, Schwerk, P, Schierack, P, Schmidt, MF, Wieler, LH and Tedin, K (2005) Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Veterinary Immunology and Immunopathology 105, 151–161.CrossRefGoogle ScholarPubMed
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH, Robinson, CJ, Sahl, JW, Stres, B, Thallinger, GG, Van Horn, DJ and Weber, CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.CrossRefGoogle ScholarPubMed
Stanley, D, Geier, MS, Denman, SE, Haring, VR, Crowley, TM, Hughes, RJ and Moore, RJ (2013) Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Veterinary Microbiology 164, 85–92.CrossRefGoogle ScholarPubMed
Sun, Z, Lu, Y, Zhang, H, Kumar, D, Liu, B, Gong, Y, Zhu, M, Zhu, L, Liang, Z, Kuang, S, Chen, F, Hu, X, Cao, G, Xue, R and Gong, C (2016) Effects of BmCPV infection on silkworm Bombyx mori intestinal bacteria. PLoS One 11, 146–313.Google ScholarPubMed
Tamburini, S, Shen, N, Wu, HC and Clemente, JC (2016) The microbiome in early life: implications for health outcomes. Nature Medicine 22, 713–722.CrossRefGoogle ScholarPubMed
Thakur, A, Dhammi, P, Saini, HS and Kaur, S (2015) Pathogenicity of bacteria isolated from gut of Spodoptera litura (Lepidoptera: Noctuidae) and fitness costs of insect associated with consumption of bacteria. Journal of Invertebrate Pathology 127, 38–46.CrossRefGoogle Scholar
Wang, A, Yao, Z, Zheng, W and Zhang, H (2014 a) Bacterial communities in the gut and reproductive organs of Bactrocera minax (Diptera: Tephritidae) based on 454 pyrosequencing. PLoS One 9, 106–988.Google ScholarPubMed
Willing, BP, Russell, SL and Finlay, BB (2011) Shifting the balance: antibiotic effects on host-microbiota mutualism. Nature Reviews Microbiology 9, 233–243.CrossRefGoogle ScholarPubMed
Xiao, LB, Joseph, G, Gregory, L and Nicolas, B (2018) Nutrient-dependent impact of microbes on Drosophila suzukii development. American Society for Microbiology 9, 2199–2117.Google Scholar
Xiong, BH, Chen, LF, Chen, L, Cheng, GT, Tan, WH, Tang, YJ, Chai, CL and Du, HM (2018) A preliminary experiment of nanosilver for disinfection and disease prevention in sericultural production. Newsletter of Sericultural Science 38, 7–9.Google Scholar
Xue, SZ, Zhu, L, Tian, SY, Lang, YP and Li, Y (2008) Toxicity effect of three kinds of carbon nanomaterials on aquatic organisms. China Environmental Science 28, 269–273.Google Scholar
Xue, L, Fu, YM, Tong, L and Liu, H (2014) Microbial shifts of the silkworm larval gut in response to lettuce leaf feeding. Applied Microbiology and Biotechnology 25, 3769–3776.Google Scholar
Yang, YX, Dai, ZL and Zhu, WY (2014) Important impacts of intestinal bacteria on utilization of dietary amino acids in pigs. Amino Acids 46, 2489–2501.CrossRefGoogle ScholarPubMed
Yegani, M and Korver, DR (2008) Factors affecting intestinal health in poultry. Poultry Science 87, 2052–2063.CrossRefGoogle ScholarPubMed
Yeh, KM, Lin, JC, Yin, FY, Fung, CP, Hung, HC, Siu, LK and Chang, FY (2010) Revisiting the importance of virulence determinant magA and its surrounding genes in Klebsiella pneumoniae causing pyogenic liver abscesses: exact role in serotype K1 capsule formation. The Journal of Infectious Diseases 15, 1259–1267.CrossRefGoogle Scholar
Yun, JH, Roh, SW, Whon, TW, Jung, MJ, Kim, MS, Park, DS, Yoon, C, Nam, YD, Kim, YJ, Choi, JH, Kim, JY, Shin, NR, Kim, SH, Lee, WJ and Bae, JW (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied of Environmental Microbiology 80, 5254–5264.CrossRefGoogle ScholarPubMed
Ze, J (2019) Anti-breast disinfection test report of silkworm cocoon. Journal of Agricultural Science 32, 528–9017.Google Scholar
Zen, TT, Gao, X, Mo, GH, Wang, GH, Liu, HY, Liao, W and Xie, SB (2018) Characterization of microbial community succession for uranium removal under different temperature. China Environmental Science 11, 4261–4268.Google Scholar
Zhang, H, Ni, M, Li, F, Xu, K, Wang, B, Hong, F, Shen, W and Li, B (2014) Effects of feeding silkworm with nanoparticulate anatase TiO2 (TiO2 NPs) on its feed efficiency. Biological Trace Element Research 159, 224–232.CrossRefGoogle ScholarPubMed
Zhang, C, Zhu, SR, Tian, F, Dai, LJ and Chen, W (2016) Effects of different green manure on bacterial community structure and diversity in tobacco-planting field in Xiangxi. Guizhou Agricultural Sciences 44, 43–46.Google Scholar