Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection

This article describes the clinical manifestation of natural <i>Vibrio anguillarum</i> infection in rainbow trout (Oncorhynchus mykiss) during an outbreak on a fish farm. (i) Using an integrated approach, we characterized the pathogenesis of vibriosis from the morphological, hematologica...

Full description

Bibliographic Details
Main Authors: Stanislav Rimaso Kurpe, Irina Viktorovna Sukhovskaya, Ekaterina Vitalyevna Borvinskaya, Alexey Anatolievich Morozov, Aleksey Nikolaevich Parshukov, Irina Evgenyevna Malysheva, Alina Valeryevna Vasileva, Natalia Alexandrovna Chechkova, Tamara Yurevna Kuchko
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/12/19/2642
_version_ 1827655506745884672
author Stanislav Rimaso Kurpe
Irina Viktorovna Sukhovskaya
Ekaterina Vitalyevna Borvinskaya
Alexey Anatolievich Morozov
Aleksey Nikolaevich Parshukov
Irina Evgenyevna Malysheva
Alina Valeryevna Vasileva
Natalia Alexandrovna Chechkova
Tamara Yurevna Kuchko
author_facet Stanislav Rimaso Kurpe
Irina Viktorovna Sukhovskaya
Ekaterina Vitalyevna Borvinskaya
Alexey Anatolievich Morozov
Aleksey Nikolaevich Parshukov
Irina Evgenyevna Malysheva
Alina Valeryevna Vasileva
Natalia Alexandrovna Chechkova
Tamara Yurevna Kuchko
author_sort Stanislav Rimaso Kurpe
collection DOAJ
description This article describes the clinical manifestation of natural <i>Vibrio anguillarum</i> infection in rainbow trout (Oncorhynchus mykiss) during an outbreak on a fish farm. (i) Using an integrated approach, we characterized the pathogenesis of vibriosis from the morphological, hematological, and biochemical points of view. The molecular mechanisms associated with the host immune response were investigated using mass spectrometric analysis of trout plasma proteins. (ii) According to the severity of infection (the extent of tissue damage, the level of expression of pro-inflammatory genes, and changes in the leukocyte profile) three fish populations were identified among infected trout: fish with severe lesions (SL), fish with the moderate infectious process (IP) and asymptomatic fish (AS). (iii) Lymphopenia, granulocytosis, and splenomegaly were strong trends during the progression of infection and informative indicators of severe manifestation of disease, associated with hemorrhagic shock, metabolic acidosis, and massive tissue damage. (iv) As expected, pro-inflammatory interleukins, complement components, acute phase proteins, and antimicrobial peptides were implicated in the acute pathogenesis. Systemic coagulopathy was accompanied by increased antithrombotic reactions. (v) Reconstruction of metabolic pathways also revealed a high energy requirement for the immune response in severely affected fish. (vi) An unexpected result was a small difference between fish with moderate symptoms and fish with no or minor external signs of pathology (putatively resistant to infection). Increased production of antiproteases and enhanced blood coagulation cascade were observed in healthier fish, which may underlie the mechanisms of a controlled, non-self-damaging immune response to infection. (vii) Depending on the progression of the disease and the presence of the pathogen, a stepwise or linear change in the abundance of some plasma proteins was revealed. These proteins could be proposed as molecular markers for diagnosing the health and immune status of trout when cultured in fish farms.
first_indexed 2024-03-09T22:08:39Z
format Article
id doaj.art-a1aee897ff0541fbb294211a8b93c311
institution Directory Open Access Journal
issn 2076-2615
language English
last_indexed 2024-03-09T22:08:39Z
publishDate 2022-10-01
publisher MDPI AG
record_format Article
series Animals
spelling doaj.art-a1aee897ff0541fbb294211a8b93c3112023-11-23T19:37:17ZengMDPI AGAnimals2076-26152022-10-011219264210.3390/ani12192642Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> InfectionStanislav Rimaso Kurpe0Irina Viktorovna Sukhovskaya1Ekaterina Vitalyevna Borvinskaya2Alexey Anatolievich Morozov3Aleksey Nikolaevich Parshukov4Irina Evgenyevna Malysheva5Alina Valeryevna Vasileva6Natalia Alexandrovna Chechkova7Tamara Yurevna Kuchko8Institute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaInstitute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaInstitute of Biology, Irkutsk State University, 664003 Irkutsk, RussiaLimnological Institute of the Siberian Branch of the Russian Academy of Sciences (LIN SB RAS), 3 Ulan-Batorskaya Street, 664033 Irkutsk, RussiaInstitute of Biology of the Karelian Research Centre of the Russian Academy of Sciences (IB KarRC RAS), 11 Pushkinskaya Street, 185910 Petrozavodsk, RussiaInstitute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaInstitute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaInstitute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaInstitute of Biology, Ecology and Agricultural Technologies of the Petrozavodsk State University (PetrSU), 185640 Petrozavodsk, RussiaThis article describes the clinical manifestation of natural <i>Vibrio anguillarum</i> infection in rainbow trout (Oncorhynchus mykiss) during an outbreak on a fish farm. (i) Using an integrated approach, we characterized the pathogenesis of vibriosis from the morphological, hematological, and biochemical points of view. The molecular mechanisms associated with the host immune response were investigated using mass spectrometric analysis of trout plasma proteins. (ii) According to the severity of infection (the extent of tissue damage, the level of expression of pro-inflammatory genes, and changes in the leukocyte profile) three fish populations were identified among infected trout: fish with severe lesions (SL), fish with the moderate infectious process (IP) and asymptomatic fish (AS). (iii) Lymphopenia, granulocytosis, and splenomegaly were strong trends during the progression of infection and informative indicators of severe manifestation of disease, associated with hemorrhagic shock, metabolic acidosis, and massive tissue damage. (iv) As expected, pro-inflammatory interleukins, complement components, acute phase proteins, and antimicrobial peptides were implicated in the acute pathogenesis. Systemic coagulopathy was accompanied by increased antithrombotic reactions. (v) Reconstruction of metabolic pathways also revealed a high energy requirement for the immune response in severely affected fish. (vi) An unexpected result was a small difference between fish with moderate symptoms and fish with no or minor external signs of pathology (putatively resistant to infection). Increased production of antiproteases and enhanced blood coagulation cascade were observed in healthier fish, which may underlie the mechanisms of a controlled, non-self-damaging immune response to infection. (vii) Depending on the progression of the disease and the presence of the pathogen, a stepwise or linear change in the abundance of some plasma proteins was revealed. These proteins could be proposed as molecular markers for diagnosing the health and immune status of trout when cultured in fish farms.https://www.mdpi.com/2076-2615/12/19/2642aquacultureinfectionplasma proteomicsrainbow troutstress response<i>Vibrio anguillarum</i>
spellingShingle Stanislav Rimaso Kurpe
Irina Viktorovna Sukhovskaya
Ekaterina Vitalyevna Borvinskaya
Alexey Anatolievich Morozov
Aleksey Nikolaevich Parshukov
Irina Evgenyevna Malysheva
Alina Valeryevna Vasileva
Natalia Alexandrovna Chechkova
Tamara Yurevna Kuchko
Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
Animals
aquaculture
infection
plasma proteomics
rainbow trout
stress response
<i>Vibrio anguillarum</i>
title Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
title_full Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
title_fullStr Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
title_full_unstemmed Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
title_short Physiological and Biochemical Characteristics of Rainbow Trout with Severe, Moderate and Asymptomatic Course of <i>Vibrio anguillarum</i> Infection
title_sort physiological and biochemical characteristics of rainbow trout with severe moderate and asymptomatic course of i vibrio anguillarum i infection
topic aquaculture
infection
plasma proteomics
rainbow trout
stress response
<i>Vibrio anguillarum</i>
url https://www.mdpi.com/2076-2615/12/19/2642
work_keys_str_mv AT stanislavrimasokurpe physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT irinaviktorovnasukhovskaya physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT ekaterinavitalyevnaborvinskaya physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT alexeyanatolievichmorozov physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT alekseynikolaevichparshukov physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT irinaevgenyevnamalysheva physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT alinavaleryevnavasileva physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT nataliaalexandrovnachechkova physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection
AT tamarayurevnakuchko physiologicalandbiochemicalcharacteristicsofrainbowtroutwithseveremoderateandasymptomaticcourseofivibrioanguillarumiinfection