Oxidative Stress, Gene Expression and Histopathology of Cultured Gilthead Sea Bream (Sparus Aurata) Naturally Co-infected with Ergasilus Sieboldi and Vibrio Alginolyticus

Overview

Journal BMC Vet Res

Publisher Biomed Central

Specialty Veterinary Medicine

Date 2023 Dec 16

PMID 38104092

Authors

Mahmoud Abou-Okada

Maha M Rashad

Ghada E Ali

Shimaa Abdel-Radi

Azza Hassan

Affiliations

Soon will be listed here.

Abstract

Background: Parasitic and bacterial co-infections have been associated with increasing fish mortalities and severe economic losses in aquaculture through the past three decades. The aim of this study was to evaluate the oxidative stress, histopathology, and immune gene expression profile of gilthead sea bream (Sparus aurata) co-infected with Ergasilus sieboldi and Vibrio alginolyticus.

Results: Vibrio alginolyticus and Ergasilus sieboldi were identified using 16 S rRNA and 28 S rRNA sequencing, respectively. The collagenase virulence gene was found in all Vibrio alginolyticus isolates, and the multiple antimicrobial resistance index ranged from 0.286 to 0.857. Oxidant-antioxidant parameters in the gills, skin, and muscles of naturally infected fish revealed increased lipid peroxidation levels and a decrease in catalase and glutathione antioxidant activities. Moreover, naturally co-infected gilthead sea bream exhibited substantial up-regulation of il-1β, tnf-α, and cyp1a1. Ergasilus sieboldi encircled gill lamellae with its second antennae, exhibited severe gill architectural deformation with extensive eosinophilic granular cell infiltration. Vibrio alginolyticus infection caused skin and muscle necrosis in gilthead sea bream.

Conclusion: This study described some details about the gill, skin and muscle tissue defense mechanisms of gilthead sea bream against Ergasilus sieboldi and Vibrio alginolyticus co-infections. The prevalence of co-infections was 100%, and no resistant fish were detected. These co-infections imbalance the health status of the fish by hampering the oxidant-antioxidant mechanisms and proinflammatory/inflammatory immune genes to a more detrimental side. Our results suggest that simultaneous screening for bacterial and parasitic pathogens should be considered.

References

Reynolds L, Finlay B, Maizels R . Cohabitation in the Intestine: Interactions among Helminth Parasites, Bacterial Microbiota, and Host Immunity. J Immunol. 2015; 195(9):4059-66. PMC: 4617609. DOI: 10.4049/jimmunol.1501432. View

Benhamed S, Guardiola F, Martinez S, Martinez-Sanchez M, Perez-Sirvent C, Mars M . Exposure of the gilthead seabream () to sediments contaminated with heavy metals down-regulates the gene expression of stress biomarkers. Toxicol Rep. 2017; 3:364-372. PMC: 5615830. DOI: 10.1016/j.toxrep.2016.02.006. View

Hosoya S, Kido S, Hirabayashi Y, Kai W, Kinami R, Yoshinaga T . Genomic regions of pufferfishes responsible for host specificity of a monogenean parasite, Heterobothrium okamotoi. Int J Parasitol. 2013; 43(11):909-15. DOI: 10.1016/j.ijpara.2013.06.006. View

Marchiori N, Goncalves E, Tancredo K, Pereira-Junior J, Garcia J, Martins M . Effect of water temperature and salinity in oviposition, hatching success and infestation of Aphanoblastella mastigatus (Monogenea, Dactylogyridae) on Rhamdia quelen. Braz J Biol. 2015; 75(4 Suppl 1):S245-52. DOI: 10.1590/1519-6984.14014. View

Lazado C, Caipang C . Mucosal immunity and probiotics in fish. Fish Shellfish Immunol. 2014; 39(1):78-89. DOI: 10.1016/j.fsi.2014.04.015. View

Smith N, Rise M, Christian S . A Comparison of the Innate and Adaptive Immune Systems in Cartilaginous Fish, Ray-Finned Fish, and Lobe-Finned Fish. Front Immunol. 2019; 10:2292. PMC: 6795676. DOI: 10.3389/fimmu.2019.02292. View

Zhang C, Li D, Chi C, Ling F, Wang G . Dactylogyrus intermedius parasitism enhances Flavobacterium columnare invasion and alters immune-related gene expression in Carassius auratus. Dis Aquat Organ. 2015; 116(1):11-21. DOI: 10.3354/dao02902. View

Bush A, Lafferty K, Lotz J, Shostak A . Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 1997; 83(4):575-83. View

Sayyaf Dezfuli B, Giari L, Bosi G . Survival of metazoan parasites in fish: Putting into context the protective immune responses of teleost fish. Adv Parasitol. 2021; 112:77-132. DOI: 10.1016/bs.apar.2021.03.001. View

10.

Lindenstrom T, Secombes C, Buchmann K . Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Vet Immunol Immunopathol. 2004; 97(3-4):137-48. DOI: 10.1016/j.vetimm.2003.08.016. View

11.

Abdel-Radi S, Rashad M, Ali G, Eissa A, Abdelsalam M, Abou-Okada M . Molecular characterization and phylogenetic analysis of parasitic copepoda; isolated from cultured gilthead sea bream () in Egypt, associated with analysis of oxidative stress biomarkers. J Parasit Dis. 2022; 46(4):1080-1089. PMC: 9606149. DOI: 10.1007/s12639-022-01531-0. View

12.

Mozhdeganloo Z, Heidarpour M . Oxidative stress in the gill tissues of goldfishes (Carassius auratus) parasitized by Dactylogyrus spp. J Parasit Dis. 2014; 38(3):269-72. PMC: 4087321. DOI: 10.1007/s12639-013-0239-z. View

13.

Dezfuli B, Giari L, Lui A, Lorenzoni M, Noga E . Mast cell responses to Ergasilus (Copepoda), a gill ectoparasite of sea bream. Fish Shellfish Immunol. 2011; 30(4-5):1087-94. DOI: 10.1016/j.fsi.2011.02.005. View

14.

Dezfuli B, Squerzanti S, Fabbri S, Castaldelli G, Giari L . Cellular response in semi-intensively cultured sea bream gills to Ergasilus sieboldi (Copepoda) with emphasis on the distribution, histochemistry and fine structure of mucous cells. Vet Parasitol. 2010; 174(3-4):359-65. DOI: 10.1016/j.vetpar.2010.08.024. View

15.

Huang Z, Yu K, Fang Y, Dai H, Cai H, Li Z . Comparative Genomics and Transcriptomics Analyses Reveal a Unique Environmental Adaptability of . Microorganisms. 2020; 8(4). PMC: 7232310. DOI: 10.3390/microorganisms8040555. View

16.

Yuniar A, Palm H, Walter T . Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Parasitol Res. 2007; 100(6):1193-204. DOI: 10.1007/s00436-006-0391-9. View

17.

Chu P, He L, Zhu D, Huang R, Liao L, Li Y . Identification, expression and functional characterisation of CYP1A in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2019; 95:35-43. DOI: 10.1016/j.fsi.2019.10.022. View

18.

Song Y, Wang G, Yao W, Gao Q, Nie P . Phylogeny of freshwater parasitic copepods in the Ergasilidae (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA sequences. Parasitol Res. 2007; 102(2):299-306. DOI: 10.1007/s00436-007-0764-8. View

19.

Liu X, Chen N, Gao X, Zhang Y, Li X, Zhang Y . The infection of red seabream iridovirus in mandarin fish (Siniperca chuatsi) and the host immune related gene expression profiles. Fish Shellfish Immunol. 2018; 74:474-484. DOI: 10.1016/j.fsi.2018.01.020. View

20.

Srikanth K, Pereira E, Duarte A, Ahmad I . Glutathione and its dependent enzymes' modulatory responses to toxic metals and metalloids in fish--a review. Environ Sci Pollut Res Int. 2013; 20(4):2133-49. DOI: 10.1007/s11356-012-1459-y. View