Abstract
The pathogenic enterobacterium, Serratia marcescens, is a potential fish pathogen having been isolated in fish culturing environments. However, information on its effects on the physiology of cultured fish species is scarce. This study therefore aimed at ascertaining the physiological status of African catfish (Clarias gariepinus) that has been experimentally challenged with S. marcescens. Healthy juvenile C. gariepinus were experimentally challenged with either 1 × 104 CFU/ml or 5 × 104 CFU/ml inoculums of S. marcescens via oral gavage and the hematological (percentage packed cell volume (PCV), red blood cells (RBC) counts, white blood cells (WBC), counts and differential leucocytes counts) and innate humoral (plasma levels of nitric oxide and respiratory burst) parameters were determined at 4 h, 24 h, 48 h, and 14 days post-challenge periods. The control fish were gavaged with distilled water. The bacterial-challenged fish had significantly higher WBC counts, and increased levels of plasma nitric oxide and respiratory burst while the RBC counts and the PCV decreased significantly in the bacterial-challenged fish compared to control. The response of the fish to bacterial challenge is both inoculum size- and duration-dependent. The incubation of C. gariepinus with 5 × 104 CFU/mL inoculums of S. marcescens elicited more effects in the fish compared to the control or 1 × 104 CFU/mL group. The results of this study showed that infection with S. marcescens has the potential to modulate the immune system of the fish with the inflammatory pathways playing an important role in the defense of the fish against bacterial infection.
Similar content being viewed by others
Data availability
All data sets, on which the conclusions of the manuscript rely on, are present in the results section in the manuscript.
References
Adeyemi JA (2014) Oxidative stress and antioxidant enzymes activities in the African catfish, Clarias gariepinus, experimentally challenged with Escherichia coli and Vibrio fischeri. Fish Physiol Biochem 40:347–354
Adeyemi JA, Atere TG, Oyedara OO, Olabiyi KO, Olaniyan OO (2014) Hematological assessment of health status of African catfish Clarias gariepinus (Burchell 1822) experimentally challenged with Escherichia coli and Vibrio fischeri. Comp Clin Pathol 23:1309–1313
Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programs. In Shariff M, Arthur JR, Subasinghe RP (eds.) Diseases in Asian aquaculture ii. Fish health section. Manila: Asian Fish Soc 85–202
Baya AM, Toranzo AE, Lupiani B, Santos Y, Hetrick FM (1992) Serratia marcescens: a potential pathogen for fish. J Fish Dis 15:15–26
Bernard LA, Sutton WC (2006) Infection due to chromobacteria. Report of a case of pneumonia due to Chromobacterium prodigiosum successfully treated with kanamycin. Arch Intern Med 105:311–315
Biller JD, Takahasi LS (2018) Oxidative stress and fish immune system: phagocytosis and leukocyte respiratory burst activity. An Acad Bras Cienc. https://doi.org/10.1590/0001-3765201820170730
Biller-Takahashi JD, Takahashi LS, Saita MV, Gimbo RY, Urbinati EC (2013) Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Braz J Biol 73:425–429
Brauner CJ, Harter TS (2017) Beyond just hemoglobin: red blood cell potentiation of hemoglobin-oxygen unloading in fish. J Appl Physiol 123:935–941
Caruso G, Maricchiolo G, Micale V, Genovese L, Caruso R, Denaro MG (2010) Physiological responses to starvation in the European eel (Anguilla anguilla): effects on haematological, biochemical, non-specific immune parameters and skin structures. Fish Physiol Biochem 36:71–83
Chakrabarti S, Poidevin M, Lemaitre B (2014) The drosophila MAPK p38c 354 regulates oxidative stress and lipid homeostasis in the intestine. PLoS Genet 10:355–1004659
Czeczuga B, Czeczuga-Semeniuk E, Semeniuk A, Semeniuk J (2013) Straminipiles (Oomycota) developing on the eggs of an African catfish, Clarias gariepinus Burchell in water bodies of Poland. Afr J Microbiol Res 7:2378–2384
Dhasarathan P, Pugazhenthi M, Valivittan K (2014) Analysis of humoral immune response of animals exposed to bacterial antigens. Cent Eur J Immunol 39:323–326
Dryden M (2018) Reactive oxygen species: a novel antimicrobial. Int J Antimicrob Agents 51:299–303
Eissa AE, Attia MM, Elgendy MY, Ismail GA, Sabry NM, Prince A, Mahmoud MA, El-Demerdash GO, Abdelsalam M, Derwa HIM (2021) Streptococcus, Centrocestus formosanus and Myxobolus tilapiae concurrent infections in farmed Nile tilapia (Oreochromis niloticus). Microb Pathog 158:105084
Garza M, Mohan CV, Rahman M, Wieland B, Häsler B (2019) The role of infectious disease impact in informing decision-making for animal health management in aquaculture systems in Bangladesh. Prev Vet Med 167:202–213
Gong Q, Yang D, Jiang M, Zheng J, Peng B (2020) L-aspartic acid promotes fish survival against Vibrio alginolyticus infection through nitric oxide-induced phagocytosis. Fish Shellfish Immunol 97:359–366
Guardiola FA, Cuesta A, Abellán E, Meseguer J, Esteban MA (2014) Comparative analysis of the humoral immunity of skin mucus from several marine teleost fish. Fish Shellfish Immunol 40:24–31
Guevara-Guzman R, Emson PC, Kendrick KM (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J Neurochem 62:807–810
Gurevitch J, Weber D (2010) A strain of Serratia isolated from urine. Am J Clin Pathol 20:48–49
Heydari M, Firouzbakhsha F, Paknejad H (2020) Effects of Mentha longifolia extract on some blood and immune parameters, and disease resistance against yersiniosis in rainbow trout. Aquaculture 515:734586
Hitzfeld B (2005) Fish immune system. In: Vohr HW (eds) Encyclopedic reference of immunotoxicology. Springer, Berlin. https://doi.org/10.1007/3-540-27806-0_574
Jan K, Ahmed I, Dar NA (2021) Haematological and serum biochemical reference values of snow trout, Schizothorax labiatus habiting in river Sindh of Indian Himalayan region. J Fish Biol 98:1289–1302
Kordon AO, Karsi A, Pinchuk L (2018) Innate immune responses in fish: antigen presenting cells and professional phagocytes. Turk J Fish Aquat Sci 18:1123–1139
Kumar NP, Fukutani KF, Shruthi BS, Alves T, Silveira-Mattos PS, Rocha MS, West K, Natarajan M, Viswanathan V, Babu S, Andrade BB, Kornfeld H (2019) Persistent inflammation during anti-tuberculosis treatment with diabetes comorbidity. Elife 8:e46477. https://doi.org/10.7554/eLife.46477
Laibu PK, Maingi J, Kebira A (2018) Determination of bacterial composition, heavy metal pollution and physicochemical parameters of fish pond water in Abothuguchi Central, Meru County, Kenya. Bioteknologi 15:66–79
Langer SL, Vargas VMF, Flores-Lopes F, Malabarba LR (2009) Effects of bacterial infestation caused by human wastes on the skin structures of Mugil platanus Günther, 1880 (Mugilidae). Braz J Biol 69:333–338
Machado M, Azeredo R, Fontinha F, Fernández-Boo S, Conceição L, Dias J, Costas B (2018) Dietary methionine improves the European seabass (Dicentrarchus labrax) immune Status, inflammatory response, and disease resistance. Front Immunol 9:2672. https://doi.org/10.3389/fimmu.2018.02672
Martins ML, Mouriño JL, Amaral GV, Vieira FN, Dotta G, Jatobá AM, Pedrotti FS, Jerônimo GT, Buglione-Neto CC, Pereira G Jr (2008) Haematological changes in Nile tilapia experimentally infected with Enterococcus sp. Braz J Biol 68:657–661
Mikheev VN, Pasternak AF, Taskinen J, Valtonen ET (2010) Parasite-induced aggression and impaired contest ability in a fish host. Parasit Vectors 3:17. https://doi.org/10.1186/1756-3305-3-17
Nicholson LB (2016) The immune system. Essays Biochem 60:275–301
Olutiola PO, Famurewa O, Sonntag HG (2000) Introduction to general microbiology a practical approach. Bolaby Publication, Lagos, p 267
Owolabi OD (2011) Haematological and serum biochemical profile of the upside downcatfish, Synodontis membranacea Geoffroy Saint Hilaire from Jebba Lake, Nigeria. Comp Clin Pathol 20:163–172
Patil PK, Geetha R, Ravisankar T, Avunje S, Solanki HG, Abraham TJ, Vinoth SP, Jithendran KP, Alavandi SV, Vijayan KK (2021) Economic loss due to diseases in Indian shrimp farming with special reference to Enterocytozoon hepatopenaei (EHP) and white spot syndrome virus (WSSV). Aquaculture 533:736231
Pękala-Safińska A (2018) Contemporary threats of bacterial infections in freshwater fish. J Vet Res 62:261–267
Penttilä IM, Mahlamäki E, Mononen I, Kärkkäinen P (1985) Adaptation of the May-Grünwald-Giemsa staining method for automated differential counting of blood leukocytes by a Hematrak Analyzer. Scand J Haematol 34:274–280
Pridgeon JW, Klesius PH (2012) Major bacterial diseases in aquaculture and their vaccine development. Perspect Agric Vet Sci Nutr Nat Resour 7:1–16
Rombout JH, Huttenhuis HBT, Picchietti S, Scapigliati S (2005) Phylogeny and ontogeny of fish leucocytes. Fish Shellfish Immunol 19:441–455
Rusia V, Sood SK (1992) Routine haematological tests. In: Mukerjee KL (ed) Medical Laboratory Technology. McGraw Hill Publishing Co. Ltd, pp 252–258
Seibel H, Baßmann B, Rebl A (2021) Blood will tell: what hematological analyses can reveal about fish welfare. Front Vet Sci 8:616955. https://doi.org/10.3389/fvets.2021.616955
Sharma JN, Al-Omran A, Parvathy SS (2007) Role of nitric oxide in inflammatory diseases. Inflammopharmacology 15:252–259
Shinn AP, Pratoomyot J, Bron JE, Paladini G, Brooker EE, Brooker AJ (2015) Economic costs of protistan and metazoan parasites to global mariculture. Parasitology 142:196–270
Snieszko SF (1960) Microhematocrit as a tool in fishery research and management. U.S. Fish & Wildlife Service, Spec Sci Report Fisheries no. 341
Stosik MP, Tokarz-Deptuła B, Deptuła W (2018) Specific humoral immunity in Osteichthyes. Cent Eur J Immunol 43:335–340
Sugita H, Miyajma C, Kobayashi H, Deguchi Y (1996) Distribution of microflora in the intestinal tract of crap Cyprinus caprio. Nippon Suisan Gakkaishi 56:113–138
Uribe C, Folch H, Enriquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med 56:486–503
Wamala SP, Mugimba KK, Mutoloki S, Evensen O, Mdegela R, Byarugaba DK, Sorum H (2018) Occurrence and antibiotic susceptibility of fish isolated from Oreochromis niloticus (Nile tilapia) and Clarias gariepinus (African catfish) in Uganda. Fish Aquatic Sci 21:6. https://doi.org/10.1186/s41240-017-0080-x
Yanuhar U, Raharjo DKWP, Caesar NR, Junirahma, (2021) Hematology response of catfish (Clarias sp.) as an indicator of fish Health in Tuban Regency. IOP Conf Ser Earth Environ Sci 718:012059
Yao J, Li C, Zhang J, Liu S, Feng J, Wang R, Li Y, Jiang C, Song L, Chen A, Liu Z (2014) Expression of nitric oxide synthase (NOS) genes in channel catfish is highly regulated and time dependent after bacterial challenges. Dev Comp Immunol 45:74–86
Acknowledgements
The authors are grateful to Mrs. E. T. Ojo for assistance with the isolation and identification of Serratia marcescens
Author information
Authors and Affiliations
Contributions
JAA and COA were involved in the design of the experiment. JAA and JN were involved in data acquisition and analyses. JAA and JN were involved in writing the draft of the manuscript. JAA and COA were involved in writing the final draft of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
The experimental procedures conformed to national and international standards on the use of laboratory animals. Also, the study was approved by the institutional committee on the care and use of animals for experiments.
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
About this article
Cite this article
Adeyemi, J.A., Nwanze, J. & Adedire, C.O. Evaluation of hemato-immune parameters in African catfish, Clarias gariepinus (Burchell 1822) experimentally challenged with Serratia marcescens. Comp Clin Pathol 31, 475–481 (2022). https://doi.org/10.1007/s00580-022-03346-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00580-022-03346-0