Skip to main content
Log in

Selenium-enriched Bacillus subtilis reduces the effects of mercury-induced on inflammation and intestinal microbes in carp (Cyprinus carpio var. specularis)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Mercury (Hg) is a global pollutant that affects the health of humans and ecosystems. Selenium (Se) is an essential trace element for many organisms including humans. Bacillus subtilis is one of the main probiotics used in aquaculture, and has a certain adsorption effect on heavy metals. The interaction between Hg and Se was rigorously studied, especially due to the observation of the protective effect of Se on Hg toxicity. The objective of this study was to research the effects of Hg, Se, and B. subtilis on inflammation and intestinal microbes in common carp. The common carp was exposed to Hg (0.03 mg/L), and 105 cfu/g Se-rich B. subtilis was added to the feed. After 30 days of feeding, samples were taken to evaluate the growth performance, serological response, inflammatory response, and intestinal microbial changes. In this study, when fish were exposed to Hg, the growth performance of the Se-rich B. subtilis plus 0.03 mg/L Hg fish group was lower than that of the control group and higher than 0.03 mg/L Hg; The levels of serum immunoglobulin M (IgM) and lysozyme (LZM) decreased, but after supplementation with Se-rich B. subtilis, the levels of LZM and IgM increased; Hg treatment significantly upregulated the mRNA expression of interleukin-1β (IL-1β), interleukin-8 (IL-8), tumor necrosis factor-α (TNF-α), and nuclear factor-kB (NF-κB P65), but downregulated the mRNA expression of interleukin-10 (IL-10), transforming growth factor-β (TGF-β) and NF-kappa-B inhibitor alpha (IkBα). However, compared with the Hg group, the Se-rich B. subtilis plus Hg group can significantly increase the mRNA expression levels of IL-1β, IL-8, TNF-α, and NF-κB P65, but reduce the regulation of IL-10, TGF-β, and IkBα expression. Through the analysis of the microbiological, we found that the Hg group was mainly composed of Aeromonas sobria and Aeromonas hydrophila. However, in the Se-rich B. subtilis treatment group, we found that Aeromonas sobria was significantly less than the Hg group. Se-rich B. subtilis improves Hg-induced intestinal microbial changes, alleviates the abundance of Aeromonas, and alleviates the inflammation of the fish. The results of this study show that Se-rich B. subtilis dietary supplements can effectively protect common carp against Hg toxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP (2001) TNFa promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4:1116–1122

    CAS  PubMed  Google Scholar 

  • AlexandrovPogueLukiw PeterNAileenIWalterJ (2018) Synergism in aluminum and mercury neurotoxicity. Integr Food Nutr Metab 5:1–10

    Google Scholar 

  • Adegoke EO, Xue W, Machebe NS, Adeniran SO, Hao W, Chen W (2018) Sodium selenite inhibits mitophagy, downregulation and mislocalization of blood-testis barrier proteins of bovine Sertoli cell exposed to microcystin-leucine arginine (MC-LR) via TLR4/NF-kB and mitochondrial signaling pathways blockage. Ecotoxicol Environ Saf 166:165–175

    CAS  PubMed  Google Scholar 

  • Beaz-Hidalgo R, Figueras MJ (2013) Aeromonas spp. whole genomes and virulence factors implicated in fish disease. J Fish Dis 36:371–388

    CAS  PubMed  Google Scholar 

  • Begam M, Sengupta M (2015) Immunomodulation of intestinal macrophages by mercury involves oxidative damage and rise of pro-inflammatory cytokine release in the fresh water fish Channa punctatus Bloch. Fish Shellfish Immunol 45:378–385

    CAS  PubMed  Google Scholar 

  • Belzile N, Wu GJ, Chen YW, Appanna VD (2006) Detoxifi-cation of selenite and mercury by reduction and mutual protec-tion in the assimilation of both elements by Pseudomonas fluo-rescens. Sci Total Environ 367:704–714

    CAS  PubMed  Google Scholar 

  • Bollrath J, Greten FR (2009) IKK/NF-kB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. Embo Rep 10(12):1314–1319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cai SJ, Wu CX, Gong LM, Song T, Wu H, Zhang LY (2012) Effects of nano-selenium on performance, meat quality, immune function, oxidation resistance, and tissue selenium content in broilers. Poult Sci 91:2532–2539

    CAS  PubMed  Google Scholar 

  • Chassaing B, Gewirtz AT (2014) Gut microbiota, low-grade inflammation, and metabolic syndrome. Toxicol Pathol 42:49–53

    PubMed  Google Scholar 

  • Chen QL, Sun YL, Liu ZH, Li YW (2017) Sex-dependent effects of subacute mercuric chloride exposure on histology, antioxidant status and immune-related gene expression in the liver of adult zebrafish (Danio rerio). Chemosphere 188:1–9

    PubMed  Google Scholar 

  • Dawood MA, Koshio S, Ishikawa M, El-Sabagh M, Esteban MA, Zaineldin AI (2016) Probiotics as an environment-friendly approach to enhance red sea bream, Pagrus major growth, immune response and oxidative status. Fish Shellfish Immunol 57:170–178

    CAS  PubMed  Google Scholar 

  • Dennis-Wall JC, Culpepper T Jr, C.N., Rowe, C.C., Burns, A.M., Rusch, C.T., (2017) Probiotics (Lactobacillus gasseri KS-13, Bifidobacterium bifidum G9–1, and Bifidobacterium longum MM-2) improve rhinoconjunctivitis-specific quality of life in individuals with seasonal allergies: a double-blind, placebo-controlled, randomized trial. Am J Clin Nutr 105:758–767

    CAS  PubMed  Google Scholar 

  • Doeschate, K. I. T., Coyne, V. E., (2008) Improved growth rate in farmed Haliotis midae through probiotic treatment. Aquaculture. 284, 0–179

  • El-Fawal HA, Waterman SJ, Feo AD, Shamy MY (1999) Neuroimmunotoxicology: humoral assessment of neurotoxicity and autoimmune mechanisms. Environ Health Perspect 107:767–775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eloe-Fadrosh EA, Brady A, Crabtree J, Drabek EF, Ma B, Mahurkar A (2015) Functional Dynamics of the gut microbiome in elderly people during probiotic consumption. Mbio 6:e00231-e315

    PubMed  PubMed Central  Google Scholar 

  • Elorza A, Rodríguez-Lago L, Martínez P, Hidalgo A, Aguirre U, Cabriada JL (2020) Gastrointestinal infection with Aeromonas: incidence and relationship to inflammatory bowel disease. Gastroenterol Hepatol 43:614–619

    PubMed  Google Scholar 

  • Gao XJ, Tang B, Liang HH, Yi L, Wei ZG (2019) Selenium deficiency induced an inflammatory response by the HSP60-TLR2-MAPKs signalling pathway in the liver of carp. Fish Shellfish Immunology 87:688–694

    CAS  PubMed  Google Scholar 

  • Harikrishnan R, Thamizharasan S, Devi G, Doan HV, Kumar T, Hoseinifar SH (2020) Dried lemon peel enriched diet improves antioxidant activity, immune response and modulates immuno-antioxidant genes in Labeo rohita against Aeromonas sorbia. Fish Shellfish Immunology 106:675–684

    CAS  PubMed  Google Scholar 

  • Harikrishnan R, Devi G, Balasundaram C, Doan HV, Jaturasitha S, Ringø E (2021) Effect of chrysophanic acid on immune response and immune genes transcriptomic profile in Catla catla against Aeromonas hydrophila. Sci Rep 11:612–662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499–503

    CAS  PubMed  Google Scholar 

  • Jobin C, Sartor RB (2000) NF-kB signaling proteins as therapeutic targets for inflammatory bowel diseases. Inflamm Bowel Dis 6:206–213

    CAS  PubMed  Google Scholar 

  • KhansariParraReyesFelipeTort AliRezaDavidLópezELluís (2017) Cytokine modulation by stress hormones and antagonist specific hormonal inhibition in rainbow trout (Oncorhynchus mykiss) and gilthead sea bream (Sparus aurata) head kidney primary cell culture. Gen Comp Endocrinol 250:122–135

    Google Scholar 

  • Kumar NR, Raman RP, Jadhao SB, Brahmchari RK, Kumar K, Dash G (2012) Effect of dietary supplementation of Bacillus licheniformison gut microbiota, growth and immune response in giant freshwater prawn, Macrobrachium rosenbergii(de Man, 1879). Aquacult Int 21:387–403

    Google Scholar 

  • Lian ZG, Bai J, Hu XC, Lü A, Sun J, F., Guo, Y.J., (2020) Detection and characterization of Aeromonas salmonicida subsp. salmonicida infection in crucian carp Carassius auratus. Vet Res Commun 44:61–72

    PubMed  Google Scholar 

  • Liu YR, Delgado-Baquerizo M, Bi L, Zhu J, He JZ (2018a) Consistent responses of soil microbial taxonomic and functional attributes to mercury pollution across China. Microbiome 6:183. https://doi.org/10.1186/s40168-018-0572-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YR, Johs A, B, i L., Lu, X., Hu, H.W., Sun, D., (2018b) Unraveling microbial communities associated with methylmer-cury production in paddy soils. Environ Sci Technol 52:13110–13118. https://doi.org/10.1021/acs.est.8b03052

    Article  CAS  PubMed  Google Scholar 

  • Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267

    CAS  PubMed  Google Scholar 

  • Organization WH (2001) Health and nutritional properties of probiotics in food including powdered milk with live lactic acid bacteria: a joint FAO/WHO expert consultation. WHO, Geneva

    Google Scholar 

  • Osuna CE, Grandjean P, Weihe P, El-Fawal HAN (2014) Autoantibodies associated with prenatal and childhood exposure to environmental chemicals in Faroese children. Toxicol Sci 142:158–166

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parízek J, Ostádalová I (1976) The protective effect of small amounts of selenite in sublimate intoxication. Experientia 23:142–143

    Google Scholar 

  • Queiroz ML, Perlingeiro RC, Dantas DC, Bizzacchi JM, Capitani EMD (1994) Immunoglobulin levels in workers exposed to inorganic mercury. Pharmacol Toxicol 74:72–75

    CAS  PubMed  Google Scholar 

  • Rice KM, Walker EM, Wu M, Gillette C, Blough ER (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47:74–83

    PubMed  PubMed Central  Google Scholar 

  • Sareila O, Kelkka T, Pizzolla A, Hultqvist M, Rikard H (2011) NOX2 complex–derived ROS as immune regulators. Antioxid Redox Signal 15:2197–2208

    CAS  PubMed  Google Scholar 

  • Savan, R., Sakai, M., (2006) Genomics of fish cytokines. Comparative Biochemistry & Physiology Part D Genomics & Proteomics. 1, 0–101.

  • Sfakianakis DG, Renieri E, Kentouri M, Tsatsakis AM (2015) Effect of heavy metals on fish larvae deformities: a review. Environ Res 137:246–255

    CAS  PubMed  Google Scholar 

  • Shang, X.C., Yu, Peng., Yin, Y.W., Zhang, Y., Lu, Y.T., Mao, Q.H., (2021) Effect of selenium-rich Bacillus subtilis against mercury-induced intestinal damage repair and oxidative stress in common carp. Comp Biochem Physiol C Toxicol Pharmacol. 239, 108851

  • Sommer F, Backhed F (2013) The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11:227–238

    CAS  PubMed  Google Scholar 

  • Taro K, Shizuo A (2007) Signaling to NF-κB by toll-like receptors. Trends Mol Med 13:460–469

    Google Scholar 

  • Teemu H, Seppo S, Jussi M, Raija T, Kalle L (2008) Reversible surface binding of cadmium and lead by lactic acid and bifidobacteria. Int J Food Microbiol 125:170–175

    CAS  PubMed  Google Scholar 

  • Tomalka J, Hise AG (2015) Inflammasomes in aspergillosis—it takes two to tango. Cell Host Microbe 17:290–292

    CAS  PubMed  Google Scholar 

  • Veena KB, Radhakrishnan CK, Chacko J (1997) Heavy metal induced biochemical effects in an estuarine teleost. Indian J Mar Sci 26:74–78

    CAS  Google Scholar 

  • Wang N, Gao C, Zhang P, Guan L, Wang Y, Qin Y (2019) Effect of Bacillus cereus against cadmium induced hematological disturbances and immunosuppression in Carassius auratus gibelio. Fish Shellfish Immunol 89:141–148

    CAS  PubMed  Google Scholar 

  • Won, S., Hamidoghli, A., Choi, W., Park, Y., Jang, W., Kong, I., (2020) Effects of Bacillus subtilis WB60 and Lactococcus lactis on growth, immune responses, histology and gene expression in Nile tilapia, Oreochromis niloticus. Microorganisms.8, 0–10.

  • WrobelPowerToborek JagodaKRonanMichal (2016) Biological activity of selenium: revisited. IUBMB Life 68:97–105

    Google Scholar 

  • Xu CJ, Shen GX, Chen C, Gélinas C, Kong AT (2005) Suppression of NF-kB and NF-kB regulated gene expression by sulforaphane and PEITC through IKBa, IKK pathway in human prostate cancer PC-3 cells. Oncogene 24:4486–4495

    CAS  PubMed  Google Scholar 

  • Xu F, Liu S, Li S (2015) Effects of selenium and cadmium on changes in the gene expression of immune cytokines in chicken splenic lymphocytes. Biol Trace Elem Res 165:214–221

    CAS  PubMed  Google Scholar 

  • Yan L, Liu G, Zhao B, Pang B, Wu W, Ai C (2020) Novel Biomedical functions of surfactin A from Bacillus subtilis in wound healing promotion and scar inhibition. J Agric Food Chem 68:6987–6997

    CAS  PubMed  Google Scholar 

  • Yang YX, Zhou HD, Yang YB, Li WS, Zhou M, Zeng ZY (2007) Lipopolysaccharide (LPS) regulates TLR4 signal transduction in nasopharynx epithelial cellline5–8F via NF-kB and MAPKs signaling pathways. Mol Immunol 44:984–992

    CAS  PubMed  Google Scholar 

  • Yin Y, Zhang P, Yue X, Du X, Li W, Yin Y, Yi C, Li Y (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: Bioaccumulation, antioxidant responses and immune responses. Ecotoxicol Environ Saf 161:755–762

    CAS  PubMed  Google Scholar 

  • Zaineldin AI, Hegazi S, Koshio S, Ishikawa M, Bakr A, El-Keredy AMS et al (2018) Bacillus subtilis as probiotic candidate for red sea bream: growth performance, oxidative status, and immune response traits. Fish Shellfish Immunol 79:303–312

    CAS  PubMed  Google Scholar 

  • Zhang ZH, Wu HZ, Xiao JF, Wang QY, Liu Q, Zhang YX (2012) Immune responses of zebrafish (Danio rerio) induced by bath-vaccination with a live attenuated Vibrio anguillarum vaccine candidate. Fish Shellfish Immunol 33(1):36–41

    PubMed  Google Scholar 

  • Zhang QF, Li YW, Liu ZH, Chen QL (2016a) Reproductive toxicity of inorganic mercury exposure in adult zebrafish: histological damage, oxidative stress, and alterations of sex hormone and gene expression in the hypothalamic-pituitary- gonadal axis. Aquat Toxicol 177:417–424

    CAS  PubMed  Google Scholar 

  • Zhang QF, Li YW, Liu ZH, Chen QL (2016b) Exposure to mercuric chloride induces developmental damage, oxidative stress and immunotoxicity in zebrafish embryos-larvae. Aquat Toxicol 181:76–85

    CAS  PubMed  Google Scholar 

  • Zhao, J., Shi, B., Jiang, Q.R., Ke, C.H., (2012) Changes in gut-associated flora and bacterial digestive enzymes during the development stages of abalone (Haliotis diversicolor). 338–341, 0–153.

  • Zheng L, Feng L, Jiang WD, Wu P, Tang L, Kuang SY (2018) Selenium deficiency impaired immune function of the immune organs in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 77:53–70

    CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by the National Key R&D program of China (no.2020YFD0900400); Ministry of Agriculture Special Project: Investigation of Fishery Resources and Environment in Key Waters in Northeast China; Jilin Province Science and Technology Development Plan Project (20190201179JC); and Jilin Province Industrial Technology Research and Development Special Project (2019C059-5).

Author information

Authors and Affiliations

Authors

Contributions

The specific work of each author in this study was as follows: Xinchi Shang, perception and design; surgical operation; final approval of the version to be published; Bo Wang, participation in the whole work; drafting of the article; data analysis; Qingsong Sun: methodology. Yue Zhang, methodology, investigation, writing-original draft. Yuting Lu, investigation. Shaojun Liu, methodology. Yuehong Li, investigation, writing-original draft. Thank you and best regards.

Corresponding author

Correspondence to Yuehong Li.

Ethics declarations

Ethics approval

All experimental and animal handling procedures were conducted according to the research protocols approved by the Institutional Animal Care and Use Committee, Jilin Agricultural University, Jilin Province, China.

Consent to participate

The author of the article is approved by everyone.

Consent for publication

All authors agree to publish this article to Fish Physiol Biochem.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shang, X., Wang, B., Sun, Q. et al. Selenium-enriched Bacillus subtilis reduces the effects of mercury-induced on inflammation and intestinal microbes in carp (Cyprinus carpio var. specularis). Fish Physiol Biochem 48, 215–226 (2022). https://doi.org/10.1007/s10695-022-01046-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-022-01046-8

Keywords

Navigation