Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection

Front Immunol. 2023 Sep 4:14:1254677. doi: 10.3389/fimmu.2023.1254677. eCollection 2023.

Abstract

Introduction: The marine aquaculture industry has been witnessing a worldwide emergence of tenacibaculosis, a poorly understood bacterial disease caused by Tenacibaculum maritimum that affects commercially important fish. So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pathogen-host interaction operating in tenacibaculosis remain to be disclosed. This study aimed at contributing to a better understanding of this disease, by evaluating the early innate immune response triggered in European sea bass (Dicentrarchus labrax) by a bath-challenge with T. maritimum.

Methods: Groups of sea bass were bath-challenged with T. maritimum (challenged fish) or mock-challenged. Undisturbed fish were used as controls (time 0). Samples of blood, liver and mucosal organs (skin, gills and posterior-intestine) were collected at 0 h (control) and at 6, 24, 48 and 72 h post-challenge (n=12). Mucosal organs were used for analyzing the expression of immune-related genes by RT-qPCR, as well as blood samples for assessing haematological and innate humoral parameters and liver for oxidative stress assessment.

Results: An increased expression of il-1β, il8, mmp9 and hamp1 was detected in all mucosal organs of infected fish when compared with control and mock-challenged fish, suggesting a pro-inflammatory response against T. maritimum transversal to all organs. The faster induction of these pro-inflammatory genes was observed in the gills. Regarding the systemic response, challenged fish presented neutrophilia, monocytosis, signs of anemia, and a decrease of bactericidal and lysozyme activities in plasma. Almost no variations were observed regarding hepatic oxidative stress.

Discussion/conclusions: The present study suggests that T. maritimum induces a local innate immune response upon bath infection not only in the skin of European sea bass, but also in the gills and posterior-intestine, likely triggered by the T. maritimum's capacity to adhere, colonize and damage these organs that can function as entry ways to bacteria, leading ultimately to the seen host's systemic response.

Keywords: aquaculture; bacterial infection; innate immunity; mucosal immunity; tenacibaculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bass*
  • Immunity, Innate
  • Liver
  • Tenacibaculum*

Supplementary concepts

  • Tenacibaculum maritimum

Associated data

  • figshare/10.6084/m9.figshare.23998017

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work is supported by national funds through FCT - Foundation for Science and Technology - within the scope of UIDB/04423/2020 and UIDP/04423/2020. IF, DP, AdV, and BC benefited from grants by FCT (SFRH/BD/147750/2019, UI/BD/150900/2021, L57/2016/CP1355/CT0010 and 2020.00290.CEECIND). AdV was funded by Portuguese national funds through the FCT–Fundação para a Ciência e a Tecnologia, I.P., and, when eligible, by COMPETE 2020 FEDER funds, under the Scientific Employment Stimulus–Individual Call 2021.02251.CEECIND/CP1663/CT0016. This work also received funding from the European Union’s Horizon Europe research and innovation program under grant agreement No. 101084651 (project IGNITION).