Dual RNAseq highlights the kinetics of skin microbiome and fish host responsiveness to bacterial infection
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Abstract
Background: Tenacibaculum maritimum is a fish pathogen known for causing serious damage to a broad range of wild and farmed marine fish populations worldwide. The recently sequenced genome of T. maritimum strain NCIMB 2154 T provided unprecedented information on the possible molecular mechanisms involved in the virulence of this species. However, little is known about the dynamic of infection in vivo, and information is lacking on both the intrinsic host response (gene expression) and its associated microbiota. Here, we applied complementary omic approaches, including dual RNAseq and 16S rRNA gene metabarcoding sequencing using Nanopore and short-read Illumina technologies to unravel the host–pathogen interplay in an experimental infection system using the tropical fish Platax orbicularis as model. Results: We showed that the infection of the host is characterised by an enhancement of functions associated with antibiotic and glucans catabolism functions but a reduction of sulfate assimilation process in T. maritimum . The fish host concurrently displays a large panel of immune effectors, notably involving innate response and triggering acute inflammatory response. In addition, our results suggest that fish activate an adaptive immune response visible through the stimulation of T-helper cells, Th17, with congruent reduction of Th2 and T-regulatory cells. Fish were, however, largely sensitive to infection, and less than 25% survived after 96 hpi. These surviving fish showed no evidence of stress (cortisol levels) or significant difference in microbiome diversity compared with controls at the same sampling time. The presence of T. maritimum in resistant fish skin and the total absence of any skin lesions suggest that these fish did not escape contact with the pathogen, but rather that some mechanisms prevented pathogens entry. In resistant individuals, we detected up-regulation of specific immune-related genes differentiating resistant individuals from controls at 96 hpi, which suggests a possible genomic basis of resistance, although no genetic variation in coding regions was found. Conclusion: Here we focus in detail on the interplay between common fish pathogens and host immune response during experimental infection. We further highlight key actors of defence response, pathogenicity and possible genomic bases of fish resistance to T. maritimum .
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Rahman, T., Suga, K., Kanai, K., & Sugihara, Y. (2015) · Fish Pathology · doi:10.3147/jsfp.50.44 · Cited by 12 · see citing works
GLe Luyer, J., & Deschamps, M. (2015) · Journal of Next Generation Sequencing & Applications · doi:10.4172/2469-9853.1000112 · Cited by 6 · see citing works
RUNX2 Transcriptional Regulation in Development and Disease
Brusgard, J. L., & Passaniti, A. (2013) · Cancer drug discovery and develogment/Cancer drug discovery and development · doi:10.1007/978-1-4614-8039-6_3 · Cited by 4 · see citing works
Targeting the bacterial-host interaction
Mosher, D. F. (2012) · Virulence · doi:10.4161/viru.21269 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Physiological biomarkers and fisheries management
Brosset, P., Cooke, S. J., Schull, Q., Trenkel, V. M., Soudant, P., & Lebigre, C. (2021) · Reviews in Fish Biology and Fisheries · doi:10.1007/s11160-021-09677-5 · Cited by 54 · see citing works
Self-citationBiomarkers in aquatic systems: Advancements, applications and future directions
Sikaily, A. E., & Shabaka, S. H. (2024) · The Egyptian Journal of Aquatic Research · doi:10.1016/j.ejar.2024.05.002 · Cited by 54 · see citing works
Bell, A. G., McMurtrie, J., Bolaños, L. M., Cable, J., Temperton, B., & Tyler, C. R. (2024) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiae021 · Cited by 27 · see citing works
Rosado, D., Canada, P., Silva, S. M., Ribeiro, N. A., Diniz, P., & Xavier, R. (2023) · FEMS Microbes · doi:10.1093/femsmc/xtad011 · Cited by 22 · see citing works
Interwoven processes in fish development: microbial community succession and immune maturation
Auclert, L. Z., Chhanda, M. S., & Derôme, N. (2024) · PeerJ · doi:10.7717/peerj.17051 · Cited by 17 · see citing works
Rosado, D., Pérez‐Losada, M., Severino, R., & Xavier, R. (2021) · Microbial Ecology · doi:10.1007/s00248-021-01795-8 · Cited by 16 · see citing works
Venegas, L., Ramayo‐Caldas, Y., Bohannan, B. J. M., Derôme, N., & Yañez, J. M. (2026) · Frontiers in Animal Science · doi:10.3389/fanim.2025.1678538 · Cited by 5 · see citing works
Pavić, D., Geček, S., Miljanović, A., Grbin, D., & Bielen, A. (2024) · Microorganisms · doi:10.3390/microorganisms12081733 · Cited by 3 · see citing works
The importance of gut microbes for nutrition and health
Piazzon, M. C., Ghosh, K., Ringø, E., & Kokou, F. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-21556-8.00013-2 · Cited by 2 · see citing works
Vásquez, I., Soto‐Dávila, M., Hossain, A., Gnanagobal, H., Hall, J. R., & Santander, J. (2025) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2025.110359 · Cited by 1 · see citing works
Valenzuela‐Muñoz, V., Gallardo‐Escárate, C., Morales, M. F., Valenzuela‐Miranda, D., & Gallardo-Cortes, C. (2025) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2025.110592
Fajei, E., Whyte, S. K., Soto‐Dávila, M., Eslamloo, K., Groves, L., Storey, K. B., Ghanei-Motlagh, R., Groman, D. B., Purcell, S. L., & Fast, M. D. (2025) · Aquaculture · doi:10.1016/j.aquaculture.2025.743530
Vijayan, N., Briseño, J., Simakov, O., & Nyholm, S. V. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2512903122
Epidémiologie de Tenacibaculum, agents responsables de la ténacibaculose du Platax orbicularis
Lopez, P. (2022) · doi:10.70675/52325561z35adz4cdfza24az523e95681e1a
Self-citationWu, S.-T., & Hsieh, C. (2026) · Journal of Fish Diseases · doi:10.1111/jfd.70308
- Authors
- Le Luyer, J., Schull, Q., Auffret, P., Lopez, P., Crusot, M., Belliard, C., Basset, C., Carradec, Q., Poulain, J., Planes, S., & Saulnier, D.
- Affiliations
- Ifremer (FR)
- Centre National de la Recherche Scientifique (FR)
- ORCID
- Venue
- Animal Microbiome
- Published
- 2021-05-07
- Volume
- 3
- Issue
- 1
- Pages
- 35-35
- ISSN
- 2524-4671 (ISSN-L)
- PMC
- PMC8106148
- OpenAlex
- W3158104908
- Cited by
- 16
- References
- 102
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 4 · 2023: 1 · 2022: 2 · 2021: 2
- FWCI
- 0.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Animal Microbiome (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ifremer (Capamax)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
- Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- Platax orbicularis, host-pathogen interaction, fish innate immunity, adaptive immune response, Th17 cells, Th2 cells, regulatory T cells, host resistance, immune gene expression, pathogenicity, sulfate assimilation, cortisol, experimental infection
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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