{rfName}
Co

Indexed in

License and use

Icono OpenAccess

Altmetrics

Grant support

We would like to thank the staff at the Tromso Aquaculture Research Station, Karvika, Norway for daily maintenance of the fish. E.M. Breines and E. Hareide, Research Group for Arctic Infection Biology, UiT - The Arctic University of Norway, are thanked for excellent laboratory assistance. The work was financed by the German Federal Institute for Risk Assessment, Berlin, Germany (grant 1329-520 and 1322-578). The publication charges for this article have been funded by a grant from the publication fund of UiT - The Arctic University of Norway.

Analysis of institutional authors

Jimenez De Bagues, Maria PilerAuthor

Share

October 24, 2019
Publications
>
Article

Concomitant Temperature Stress and Immune Activation may Increase Mortality Despite Efficient Clearance of an Intracellular Bacterial Infection in Atlantic Cod

Publicated to:Frontiers In Microbiology. 9 (2963): 2963- - 2018-12-04 9(2963), DOI: 10.3389/fmicb.2018.02963

Authors: Larsen, Anett K; Nymo, Ingebjorg H; Sorensen, Karen K; Seppola, Marit; Rodven, Rolf; Jimenez de Bagues, Maria Piler; Al Dahouk, Sascha; Godfroid, Jacques

Affiliations

AMAP, Tromso, Norway - Author
German Fed Inst Risk Assessment, Berlin, Germany - Author
Norwegian Vet Inst, Tromso, Norway - Author
UiT Arctic Univ Norway, Arctic Infect Biol, Dept Arctic & Marine Biol, Tromso, Norway - Author
UiT Arctic Univ Norway, Dept Med Biol, Tromso, Norway - Author
UiT Arctic Univ Norway, Dept Res & Dev, Tromso, Norway - Author
Univ Zaragoza, Unidad Tecnol Prod & Sanidad Anim, Ctr Invest & Tecnol Agroalimentaria, Inst Agroalimentario Aragon, Zaragoza, Spain - Author
See more

Abstract

The environmental temperature has profound effects on biological systems of marine aquatic organisms and plays a critical role in species distribution and abundance. Particularly during the warmer seasons, variations in habitat temperature may introduce episodes of stressful temperatures which the organisms must adapt to and compensate for to maintain physiological homeostasis. The marine environment is changing and predicted raises in water temperatures will affect numerous marine species. Translocation of pathogens follow migration of species and alternations in physical environmental parameters may have influence upon the virulence of pathogens, as well as the hosts immune responses. While pathogenicity of many true pathogens is expected to increase following climate induced temperature stress, the impact from environmental stressors on the occurrence and severity of opportunistic infections is unknown. Here we describe how thermal stress in the cold-water species Atlantic cod influenced the fish immune responses against an opportunistic intracellular bacterium. Following experimental infection with Brucella pinnipedialis at normal water temperature (6 degrees C) and sub-optimal temperature (15 degrees C), cod cleared the intracellular bacteria more rapidly at the highest temperature. The overall immune response was faster and of higher amplitude at 15 degrees C, however, a significant number of cod died at this temperature despite efficient clearance of infection. An increased growth rate not affected by infection was observed at 15 degrees C, confirming multiple energy demanding processes taking place. Serum chemistry suggested that general homeostasis was influenced by both infection and increased water temperature, highlighting the cumulative stress responses (allostatic load) generated by simultaneous stressors. Our results suggest a trade-off between resistance and tolerance to survive infection at sub-optimal temperatures and raise questions concerning the impact of increased water temperatures on the energetic costs of immune system activation in aquatic ectotherms.

Keywords

brucellaclimate changedisease resistancegadus morhuaimmunologyopportunistic infectionstressBehavioral feverBrucellaBrucella-pinnipedialisClimate changeClimate-changeDisease resistanceExpression analysisGadus morhuaGadus-morhua l.ImmunologyNoatunensisOpportunistic infectionResponsesSeals cystophora-cristataStressSystemTemperatureTolerance

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Frontiers In Microbiology due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2018, it was in position 32/133, thus managing to position itself as a Q1 (Primer Cuartil), in the category Microbiology.

From a relative perspective, and based on the normalized impact indicator calculated from the Field Citation Ratio (FCR) of the Dimensions source, it yields a value of: 4.84, which indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-09, the following number of citations:

  • WoS: 27
  • Scopus: 30
  • Europe PMC: 6

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-09:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 52.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 54 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 2.
  • The number of mentions on the social network X (formerly Twitter): 3 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Germany; Norway.