Skip to main content
Log in

Phylogeny of the HO family in cyprinus carpio and the response of the HO-1 gene to adding Bacillus coagulans in feed under Cd2+ stress

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

Abstract

The heavy metal cadmium (Cd2+) is an environmental pollutant that poses serious health hazards. Due to the increasing contamination of aquatic systems with Cd2+, the increased accumulation of Cd2+ in fish has become a food safety and public health concern. Heme oxygenase (HO) is an important antioxidant enzyme that plays a key role in defending the body against oxidative damage, but little research has been done in common carp. In this study, 6 HO genes were identified in the common carp genome database. Comparative genomics analysis showed considerable expansion of the HO genes and verified the four-round whole genome duplication (WGD) event in common carp. Phylogenetic analysis revealed that all HO genes of common carp were clustered into orthologous groups, indicating high conservation during evolution. In addition, the tissue distribution results showed that most HO genes had extensive tissue distribution and showed tissue-specific expression patterns. Exposure to 0.5 mg/L Cd2+ significantly reduced the expression of TGF-β and IL-10 in common carp, which may indicate that Cd2+ exposure can destroy the physical barrier function of the intestine, inhibit intestinal immune defense and induce intestinal inflammation. To find a suitable concentration of Bacillus coagulans that could activate HO-1 genes and the immunity of the organism, we investigated the changes in HO-1 gene expression levels in the intestinal tract of common carp under Cd2+ stress at 30 days and 60 days by adding different concentrations of B. coagulans to the feed. Compared with the Cd2+ stress group without supplementation, the expression levels of the HO-1 gene in the gut of three different concentrations of B. coagulans were almost increased. And B. coagulans with L2 concentrations had better activation effect on the HO-1 gene. Similarly, compared to the Cd2+ stressed group, adding B. coagulans to the diet can almost cause the early upregulation of IL-10 and TGF-β genes. Therefore, the addition of appropriate concentrations of B. coagulans may be a good way to activate HO-1, IL-10, and TGF-β genes, reduce oxidative damage, and encourage the immune.

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
Fig. 5

Similar content being viewed by others

Data availability

All HO gene sequences were deposited in the NCBI database with the continuous accession numbers MZ286949-MZ286954.

References

  • Abdhula K, Ganesha M, Shanmughapriyaa S, Vanithamania S, Natarajaseenivasana K (2015) Bacteriocinogenic potential of a probiotic strain Bacillus coagulans [BDU3] from Ngari. Int J Biol Macromol 79:800–806

    Article  Google Scholar 

  • Adeshina I, Abubakar I, Ajala B (2020) Dietary supplementation with Lactobacillus acidophilus enhanced the growth, gut morphometry, antioxidant capacity, and the immune response in juveniles of the common carp, Cyprinus carpio. Fish Physiol Biochem 46:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • Aguilar-Toalá J, Hall F, Urbizo-Reyes U, Garcia H, Vallejo-Cordoba B, González-Córdova A, Hernández-Mendoza A, Liceaga A (2019) In silico prediction and in vitro assessment of multifunctional properties of postbiotics obtained from two probiotic bacteria. Probiotics Antimicrob Proteins 12:608–622

    Article  Google Scholar 

  • Basuroy S, Bhattacharya S, Tcheranova D, Qu Y, Parfenova H (2006) HO-2 provides endogenous protection against oxidative stress and apoptosis caused by TNF-α in cerebral vascular endothelial cells. Am J Physiol Cell Physiol 291:897–908

    Article  Google Scholar 

  • Bruneau A, Fortier M, Gagne F, Gagnon C, Turcotte P, Tayabali A, Davis T, Auffret M, Fournier M (2013) Size distribution effects of cadmium tellurium quantum dots (CdS/CdTe) immunotoxicity on aquatic organisms. Environ Sci Process Impacts 15:596–607

    Article  CAS  PubMed  Google Scholar 

  • Buddington R, Diamond J (1987) Pyloric ceca of fish: a “new” absorptive organ. Am J Physiol Gastrointest Liver Physiol 252:65–76

    Article  Google Scholar 

  • Chang X, Li H, Feng J, Chen Y, Nie G, Zhang J (2018) Effects of cadmium exposure on the composition and diversity of the intestinal microbial community of common carp (Cyprinus carpio L.). Ecotoxicol Environ Saf 171:92–98

    Article  PubMed  Google Scholar 

  • Chen J, Xu Y, Han Q, Yao Y, Xiong H, Teng X (2018) Immunosuppression, oxidative stress, and glycometabolism disorder caused by cadmium in common carp (Cyprinus carpio L.): Application of transcriptome analysis in risk assessment of environmental contaminant cadmium. J Hazard Mater 366:386–394

    Article  PubMed  Google Scholar 

  • Chen J, Zhang S, Tong J, Teng X, Zhang Z, Li S, Teng X (2020) Whole transcriptome-based miRNA-mRNA network analysis revealed the mechanism of inflammation-immunosuppressive damage caused by cadmium in common carp spleens. Sci Total Environ 717: 137081.1-137081.10

  • Chen J, Chen D, Li J, Liu Y, Gu X, Teng X (2021) Cadmium-induced oxidative stress and immunosuppression mediated mitochondrial apoptosis via JNK-FoxO3a-PUMA pathway in common carp (Cyprinus carpio L.) Gills. Aquat Toxicol 233:105775

    Article  CAS  PubMed  Google Scholar 

  • Cheng C, Noordeloos A, Jeney V, Soares M, Moll F, Pasterkamp G, Serruys P, Duckers H (2009) Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque. Circulation 119:3017–3027

    Article  CAS  PubMed  Google Scholar 

  • Dong H, Jiang J, Zheng L, Pang J (2010) Research advances of novel microecologic probiotics Bacillus coagulans. Food Sci 31:292–294

    CAS  Google Scholar 

  • Dong C, Jiang L, Peng W, Xu J, Shahid M, Al-Ghanim K, Sun X, Xu P, Cui Z (2015) Phylogenetic and evolutionary analyses of the frizzled gene family in common carp (Cyprinus carpio) provide insights into gene expansion from whole-genome duplications. Plos One 10:e0144037

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong C, Lin C, Feng J, Jian X, Peng X (2016) Genome wide identification, phylogeny, and expression of aquaporin genes in common carp (Cyprinus carpio). Plos One 11:e0166160

    Article  PubMed  PubMed Central  Google Scholar 

  • Giri S, Sukumaran V, Park S (2019) Effects of bioactive substance from turmeric on growth, skin mucosal immunity and antioxidant factors in common carp, Cyprinus carpio. Fish Shellfish Immunol 92:612–620

    Article  CAS  PubMed  Google Scholar 

  • Guo S, Zheng J, Yuan S, Zhu Q, Wu W (2017) Immunosuppressive effects and associated compensatory responses in zebrafish after full life-cycle exposure to environmentally relevant concentrations of cadmium. Aquat Toxicol 188:64–71

    Article  CAS  PubMed  Google Scholar 

  • Han Q, Tong J, Sun Q, Teng X, Zhang H, Teng X (2020) The involvement of miR-6615-5p/Smad7 axis and immune imbalance in ammonia-caused inflammatory injury via NF-κB pathway in broiler kidneys. Poult Sci 99(11):5378–5388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M (2004) Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 336:241–250

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Liu Y (1988) Preliminary study on intestinal hepatopancreas protease activity in grass carp. Acta Hydrobiol Sin 12:328–334

    Google Scholar 

  • Huo H, Chen S, Li L, Nie P (2019) Functional characterization of IL-10 and its receptor subunits in a perciform fish, the mandarin fish, Siniperca chuatsi. Dev Comp Immunol 97:64–75

    Article  CAS  PubMed  Google Scholar 

  • Isani G, Andreani G, Cocchioni F, Fedeli D, Carpene E, Falcioni G (2009) Cadmium accumulation and biochemical responses in Sparus aurata following sub-lethal Cd exposure. Ecotoxicol Environ Saf 72:224–230

    Article  CAS  PubMed  Google Scholar 

  • Islam M, Ahmed M, Raknuzzaman M, Habibullah-Al-Mamun M, Islam M (2015) Heavy metal pollution in surface water and sediment: a preliminary assessment of an urban river in a developing country. Ecol Ind 48:282–291

    Article  CAS  Google Scholar 

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    Article  PubMed  Google Scholar 

  • Jiang W, Liu Y, Jiang J, Wu P, Feng L, Zhou X (2015) Copper exposure induces toxicity to the antioxidant system via the destruction of Nrf2/ARE signaling and caspase-3-regulated DNA damage in fish muscle: amelioration by myo-inositol. Aquat Toxicol 159:245–255

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Li P, Shi Z (2014) Molecular responses in digestive tract of juvenile common carp after chronic exposure to sublethal tributyltin. Ecotoxicol Environ Saf 109:10–14

    Article  CAS  PubMed  Google Scholar 

  • Lindenstrm T, Secombes C, Buchmann K (2004) Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Vet Immunol Immunopathol 97:137–148

    Article  Google Scholar 

  • Ling S, Luo Z, Chen G, Zhang D, Liu X (2017) Waterborne Zn influenced Zn uptake and lipid metabolism in two intestinal regions of juvenile goby Synechogobius hasta. Ecotoxicol Environ Saf 148:578–584

    Article  PubMed  Google Scholar 

  • Liu L, Dumbrepatil A, Fleischhacker A, Marsh E, Ragsdale S (2020) Heme oxygenase-2 is post-translationally regulated by heme occupancy in the catalytic site. J Biol Chem 295:17227–17240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mcrae N, Gaw S, Glover C (2017) Effects of waterborne cadmium on metabolic rate, oxidative stress, and ion regulation in the freshwater fish, inanga (Galaxias maculatus). Aquat Toxicol 194:1–9

    Article  PubMed  Google Scholar 

  • Ojo A, Wood C (2007) In vitro analysis of the bioavailability of six metals via the gastro-intestinal tract of the rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 83:10–23

    Article  CAS  PubMed  Google Scholar 

  • Press C, Evensen Ø (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9:309–318

    Article  Google Scholar 

  • Rubiolo J, Mithieux G, Vega F (2008) Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur J Pharmacol 591:66–72

    Article  CAS  PubMed  Google Scholar 

  • RytkNen K, Prokkola J, Salonen V, Nikinmaa M (2014) Transcriptional divergence of the duplicated hypoxia-inducible factor alpha genes in zebrafish. Gene 541:60–66

    Article  Google Scholar 

  • Sandhu N, Liang L, Mcgeer J, Dores R, Vijayan M (2019) Cadmium disrupts melanocortin 2 receptor signaling in rainbow trout. Aquat Toxicol 209:26–33

    Article  CAS  PubMed  Google Scholar 

  • Shibahara S, Yoshizawa M, Suzuki H, Takeda K, Meguro K (1993) Functional analysis of cDNAs for two types of human heme oxygenase and evidence for their separate regulation. J Biochem 113:214–218

    Article  CAS  PubMed  Google Scholar 

  • Sigbjørn L, Ben F, Simen R, Jason R, Matthew P, Torfinn N, Torgeir R (2016) The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–205

    Article  Google Scholar 

  • Thévenod F (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxicol Appl Pharmacol 238:221–239

    Article  PubMed  Google Scholar 

  • Trakshel G, Kutty R, Maines M (1986) Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J Biol Chem 261:11131–11137

    Article  CAS  PubMed  Google Scholar 

  • Valko M, Morris H, Cronin M (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • Wallace K, Akhter S, Smith E, Lorent K, Pack M (2005) Intestinal growth and differentiation in zebrafish. Mech Dev 122:157–173

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Chau L (2010) Heme oxygenase-1 in cardiovascular diseases: molecular mechanisms and clinical perspectives. Chang Gung Med J 33:13–24

    CAS  PubMed  Google Scholar 

  • Wang S, Wang W, Guo Y, Guo Y, Wei J, Zhang Y (2007) Aeute and chronic toxieity of chromium and cadmium on grass carp fries (ctenopharyngodon idellus). J Lanzhou Univ (Nat Sci) 43:60–64

    Google Scholar 

  • Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, Stuhlmeier K, Kolbe T, Stulnig T, Horl W, Hengstschlager M (2008) The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29:565–577

    Article  CAS  PubMed  Google Scholar 

  • William K, Huang T, Maines M (1997) Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247:725–732

    Article  Google Scholar 

  • Wood C, Franklin N, Niyogi S (2006) The protective role of dietary calcium against cadmium uptake and toxicity in freshwater fish: an important role for the stomach. Environ Chem 3:389–394

    Article  CAS  Google Scholar 

  • Xie D, Li Y, Liu Z, Chen Q (2019) Inhibitory effect of cadmium exposure on digestive activity, antioxidant capacity and immune defense in the intestine of yellow catfish (Pelteobagrus fulvidraco). Comp Biochem Physiol C: Toxicol Pharmacol 222:65–73

    CAS  Google Scholar 

  • Xiong D, Xie C, Zhang H, Liu H (2011) Digestive enzymes along digestive tract of a carnivorous fish Glyptosternum maculatum (Sisoridae, Siluriformes). J Anim Physiol Anim Nutr 95:56–64

    Article  CAS  Google Scholar 

  • Xu P, Zhang X, Wang X, Li J, Liu J, Kuang Y, Xu J, Zheng X (2014) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219

    Article  CAS  PubMed  Google Scholar 

  • Yang A, Xing H, Yu Z, Jia P, Gu X, Teng X (2019) The evaluation of potential immunotoxicity induced by environmental pollutant ammonia in broilers. Poult Sci 98:3165–3175

    Article  Google Scholar 

  • Zheng J, Yuan S, Wu C, Lv Z (2016) Acute exposure to waterborne cadmium induced oxidative stress and immunotoxicity in the brain, ovary and liver of zebrafish (Danio rerio). Aquat Toxicol 180:36–44

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Xiang X, Ye Y, Lin S, Luo L (2003) Comparisons of Activities of the Digestive Enzymes among Spinibarbus sinensis Bleeker, Pelteobagrus fulvidraco Richardson and Sinilabeo rendahli Kimura. J Anhui Agric Univ 30:78–81

    CAS  Google Scholar 

  • Zhuo L, Syed W, Qin Z, Teng X (2021) The contributions of miR-25-3p, oxidative stress, and heat shock protein in a complex mechanism of autophagy caused by pollutant cadmium in common carp (Cyprinus carpio L.) hepatopancreas. Environ Pollut 287:117554

    Article  Google Scholar 

Download references

Acknowledgements

This study is financially supported by the National Natural Science Foundation of China (31801032).

Author information

Authors and Affiliations

Authors

Contributions

Chuanju Dong conceived the project and designed the scientific objectives. Zhou Jiang, Kaiyue Liu and Meng Zhang collected and prepared the fish samples. Zhou Jiang, Yaguo Xue and Chuanju Dong conducted the experiment and finished bioinformatics analysis. Chuanju Dong and Zhou Jiang prepared the manuscript. Chuanju Dong and Xuejun Li revised the manuscript.

Corresponding authors

Correspondence to Xuejun Li or Chuanju Dong.

Ethics declarations

Ethics statement

This study was conducted under the permission of the Animal Conservation and Utilization Committee of Fisheries College of Henan Normal University. Common carp were treated appropriately to minimize suffering.

Consent for publication

All authors have read and approved the final manuscript.

Conflict of interest

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

Jiang, Z., Zhang, M., Liu, K. et al. Phylogeny of the HO family in cyprinus carpio and the response of the HO-1 gene to adding Bacillus coagulans in feed under Cd2+ stress. Fish Physiol Biochem 48, 117–131 (2022). https://doi.org/10.1007/s10695-021-01041-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-021-01041-5

Keywords

Navigation