Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection

Ichthyophthirius multifiliis, a ciliated parasite causing ichthyophthiriasis (white spot disease) in freshwater fishes, results in significant economic loss to the aquaculture sector. One of the important predisposing factors for ichthyophthiriasis is low water temperature (i.e., below 20°C), which...

Full description

Bibliographic Details
Main Authors: V. Kumar, B. K. Das, H. S. Swain, H. Chowdhury, S. Roy, A. K. Bera, R. Das, S. N. Parida, S. Dhar, A. K. Jana, B. K. Behera
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.956478/full
_version_ 1817997173712748544
author V. Kumar
B. K. Das
H. S. Swain
H. Chowdhury
S. Roy
A. K. Bera
R. Das
S. N. Parida
S. Dhar
A. K. Jana
B. K. Behera
author_facet V. Kumar
B. K. Das
H. S. Swain
H. Chowdhury
S. Roy
A. K. Bera
R. Das
S. N. Parida
S. Dhar
A. K. Jana
B. K. Behera
author_sort V. Kumar
collection DOAJ
description Ichthyophthirius multifiliis, a ciliated parasite causing ichthyophthiriasis (white spot disease) in freshwater fishes, results in significant economic loss to the aquaculture sector. One of the important predisposing factors for ichthyophthiriasis is low water temperature (i.e., below 20°C), which affects the health and makes freshwater fishes more susceptible to parasitic infections. During ichthyophthiriasis, fishes are stressed and acute immune reactions are compromised, which enables the aquatic bacterial pathogens to simultaneously infect the host and increase the severity of disease. In the present work, we aimed to understand the parasite–bacteria co-infection mechanism in fish. Later, Curcuma longa (turmeric) essential oil was used as a promising management strategy to improve immunity and control co-infections in fish. A natural outbreak of I. multifiliis was reported (validated by 16S rRNA PCR and sequencing method) in Pangasianodon hypophthalmus from a culture facility of ICAR-CIFRI, India. The fish showed clinical signs including hemorrhage, ulcer, discoloration, and redness in the body surface. Further microbiological analysis revealed that Aeromonas hydrophila was associated (validated by 16S rRNA PCR and sequencing method) with the infection and mortality of P. hypophthalmus, confirmed by hemolysin and survival assay. This created a scenario of co-infections, where both infectious agents are active together, causing ichthyophthiriasis and motile Aeromonas septicemia (MAS) in P. hypophthalmus. Interestingly, turmeric oil supplementation induced protective immunity in P. hypophthalmus against the co-infection condition. The study showed that P. hypophthalmus fingerlings supplemented with turmeric oil, at an optimum concentration (10 ppm), exhibited significantly increased survival against co-infection. The optimum concentration induced anti-stress and antioxidative response in fingerlings, marked by a significant decrease in cortisol and elevated levels of superoxide dismutase (SOD) and catalase (CAT) in treated animals as compared with the controls. Furthermore, the study indicated that supplementation of turmeric oil increases both non-specific and specific immune response, and significantly higher values of immune genes (interleukin-1β, transferrin, and C3), HSP70, HSP90, and IgM were observed in P. hypophthalmus treatment groups. Our findings suggest that C. longa (turmeric) oil modulates stress, antioxidant, and immunological responses, probably contributing to enhanced protection in P. hypophthalmus. Hence, the application of turmeric oil treatment in aquaculture might become a management strategy to control co-infections in fishes. However, this hypothesis needs further validation.
first_indexed 2024-04-14T02:34:17Z
format Article
id doaj.art-5d204f85f72b4a74a4ba6b7e28ede973
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-04-14T02:34:17Z
publishDate 2022-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-5d204f85f72b4a74a4ba6b7e28ede9732022-12-22T02:17:34ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-09-011310.3389/fimmu.2022.956478956478Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infectionV. Kumar0B. K. Das1H. S. Swain2H. Chowdhury3S. Roy4A. K. Bera5R. Das6S. N. Parida7S. Dhar8A. K. Jana9B. K. Behera10Aquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaIndian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaFisheries Enhancement and Management (FEM) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaReservoir and Wetland Fisheries (RWF) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaAquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaFisheries Resource Assessment and Informatics (FRAI) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaFisheries Enhancement and Management (FEM) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaAquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaAquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaAquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaAquatic Environmental Biotechnology and Nanotechnology (AEBN) Division, Indian Council of Agricultural Research (ICAR)-Central Inland Fisheries Research Institute (CIFRI), Barrackpore, IndiaIchthyophthirius multifiliis, a ciliated parasite causing ichthyophthiriasis (white spot disease) in freshwater fishes, results in significant economic loss to the aquaculture sector. One of the important predisposing factors for ichthyophthiriasis is low water temperature (i.e., below 20°C), which affects the health and makes freshwater fishes more susceptible to parasitic infections. During ichthyophthiriasis, fishes are stressed and acute immune reactions are compromised, which enables the aquatic bacterial pathogens to simultaneously infect the host and increase the severity of disease. In the present work, we aimed to understand the parasite–bacteria co-infection mechanism in fish. Later, Curcuma longa (turmeric) essential oil was used as a promising management strategy to improve immunity and control co-infections in fish. A natural outbreak of I. multifiliis was reported (validated by 16S rRNA PCR and sequencing method) in Pangasianodon hypophthalmus from a culture facility of ICAR-CIFRI, India. The fish showed clinical signs including hemorrhage, ulcer, discoloration, and redness in the body surface. Further microbiological analysis revealed that Aeromonas hydrophila was associated (validated by 16S rRNA PCR and sequencing method) with the infection and mortality of P. hypophthalmus, confirmed by hemolysin and survival assay. This created a scenario of co-infections, where both infectious agents are active together, causing ichthyophthiriasis and motile Aeromonas septicemia (MAS) in P. hypophthalmus. Interestingly, turmeric oil supplementation induced protective immunity in P. hypophthalmus against the co-infection condition. The study showed that P. hypophthalmus fingerlings supplemented with turmeric oil, at an optimum concentration (10 ppm), exhibited significantly increased survival against co-infection. The optimum concentration induced anti-stress and antioxidative response in fingerlings, marked by a significant decrease in cortisol and elevated levels of superoxide dismutase (SOD) and catalase (CAT) in treated animals as compared with the controls. Furthermore, the study indicated that supplementation of turmeric oil increases both non-specific and specific immune response, and significantly higher values of immune genes (interleukin-1β, transferrin, and C3), HSP70, HSP90, and IgM were observed in P. hypophthalmus treatment groups. Our findings suggest that C. longa (turmeric) oil modulates stress, antioxidant, and immunological responses, probably contributing to enhanced protection in P. hypophthalmus. Hence, the application of turmeric oil treatment in aquaculture might become a management strategy to control co-infections in fishes. However, this hypothesis needs further validation.https://www.frontiersin.org/articles/10.3389/fimmu.2022.956478/fullI. multifiliisA. hydrophilaP. hypophthalmusturmeric oilanti-stressantioxidative response
spellingShingle V. Kumar
B. K. Das
H. S. Swain
H. Chowdhury
S. Roy
A. K. Bera
R. Das
S. N. Parida
S. Dhar
A. K. Jana
B. K. Behera
Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
Frontiers in Immunology
I. multifiliis
A. hydrophila
P. hypophthalmus
turmeric oil
anti-stress
antioxidative response
title Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
title_full Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
title_fullStr Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
title_full_unstemmed Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
title_short Outbreak of Ichthyophthirius multifiliis associated with Aeromonas hydrophila in Pangasianodon hypophthalmus: The role of turmeric oil in enhancing immunity and inducing resistance against co-infection
title_sort outbreak of ichthyophthirius multifiliis associated with aeromonas hydrophila in pangasianodon hypophthalmus the role of turmeric oil in enhancing immunity and inducing resistance against co infection
topic I. multifiliis
A. hydrophila
P. hypophthalmus
turmeric oil
anti-stress
antioxidative response
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.956478/full
work_keys_str_mv AT vkumar outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT bkdas outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT hsswain outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT hchowdhury outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT sroy outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT akbera outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT rdas outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT snparida outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT sdhar outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT akjana outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection
AT bkbehera outbreakofichthyophthiriusmultifiliisassociatedwithaeromonashydrophilainpangasianodonhypophthalmustheroleofturmericoilinenhancingimmunityandinducingresistanceagainstcoinfection