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Gut microbiome composition associates with corticosteroid treatment, morbidity, and senescence in Chinook salmon (Oncorhynchus tshawytscha)

  • Jerez-Cepa, I., Gorissen, M., Mancera, J. M. & Ruiz-Jarabo, I. What can we learn from glucocorticoid administration in fish? Effects of cortisol and dexamethasone on intermediary metabolism of gilthead seabream (Sparus aurata L.). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 231, 1–10 (2019).

    Article 
    CAS 

    Google Scholar 

  • Brown, C. L., Urbinati, E. C., Zhang, W., Brown, S. B. & McComb-Kobza, M. Maternal thyroid and glucocorticoid hormone interactions in larval fish development, and their applications in aquaculture. Rev. fish. Sci. Aquac. 22, 207–220 (2014).

    Article 

    Google Scholar 

  • Tort, L. Stress and immune modulation in fish. Dev. Comp. Immunol. 35, 1366–1375 (2011).

    Article 
    CAS 

    Google Scholar 

  • Schreck, C. B. & Tort, L. In Fish Physiology (eds Schreck, C. B. et al.) vol. 35, 1–34 (Elsevier, 2016).

  • Sternberg, E. M., Chrousos, G. P., Wilder, R. L. & Gold, P. W. The stress response and the regulation of inflammatory disease. Ann. Intern. Med. 117, 854–866 (1992).

    Article 
    CAS 

    Google Scholar 

  • Staufenbiel, S. M., Penninx, B. W. J. H., Spijker, A. T., Elzinga, B. M. & van Rossum, E. F. C. Hair cortisol, stress exposure, and mental health in humans: A systematic review. Psychoneuroendocrinology 38, 1220–1235 (2013).

    Article 
    CAS 

    Google Scholar 

  • Pickering, A. D. & Pottinger, T. G. Cortisol can increase the susceptibility of brown trout, Salmo trutta L., to disease without reducing the white blood cell count. J. Fish Biol. 27, 611–619 (1985).

    Article 
    CAS 

    Google Scholar 

  • McCormick, S. D. et al. Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth factor I and cortisol. Aquaculture 168, 221–235 (1998).

    Article 
    CAS 

    Google Scholar 

  • McConnachie, S. H. et al. Consequences of acute stress and cortisol manipulation on the physiology, behavior, and reproductive outcome of female Pacific salmon on spawning grounds. Horm. Behav. 62, 67–76 (2012).

    Article 
    CAS 

    Google Scholar 

  • Moffat, S. D., An, Y., Resnick, S. M., Diamond, M. P. & Ferrucci, L. Longitudinal change in cortisol levels across the adult life span. J. Gerontol. A Biol. Sci. Med. Sci. 75, 394–400 (2020).

    Article 
    CAS 

    Google Scholar 

  • Oh, H.-J. et al. Age-related decrease in stress responsiveness and proactive coping in male mice. Front. Aging Neurosci. 10, 128 (2018).

    Article 
    PubMed Central 

    Google Scholar 

  • Woods, H. A. 2nd. & Hellgren, E. C. Seasonal changes in the physiology of male Virginia opossums (Didelphis virginiana): Signs of the Dasyurid semelparity syndrome?. Physiol. Biochem. Zool. 76, 406–417 (2003).

    Article 

    Google Scholar 

  • Barry, T. P., Unwin, M. J., Malison, J. A. & Quinn, T. P. Free and total cortisol levels in semelparous and iteroparous Chinook salmon. J. Fish Biol. 59, 1673–1676 (2001).

    Article 
    CAS 

    Google Scholar 

  • Petrosus, E., Silva, E. B., Lay, D. Jr. & Eicher, S. D. Effects of orally administered cortisol and norepinephrine on weanling piglet gut microbial populations and Salmonella passage. J. Anim. Sci. 96, 4543–4551 (2018).

    PubMed Central 

    Google Scholar 

  • Shi, D. et al. Impact of gut microbiota structure in heat-stressed broilers. Poult. Sci. 98, 2405–2413 (2019).

    Article 

    Google Scholar 

  • Uren Webster, T. M., Rodriguez-Barreto, D., Consuegra, S. & Garcia de Leaniz, C. Cortisol-related signatures of stress in the fish microbiome. Front. Microbiol. 11, 1621 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • Ridlon, J. M. et al. Clostridium scindens: A human gut microbe with a high potential to convert glucocorticoids into androgens. J. Lipid Res. 54, 2437–2449 (2013).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • UrenWebster, T. M., Consuegra, S. & Garcia de Leaniz, C. Early life stress causes persistent impacts on the microbiome of Atlantic salmon. Comp. Biochem. Physiol. Part D Genomics Proteomics 40, 100888 (2021).

    Article 
    CAS 

    Google Scholar 

  • Bozzi, D. et al. Salmon gut microbiota correlates with disease infection status: Potential for monitoring health in farmed animals. Anim. Microbiome 3, 30 (2021).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Xiong, J.-B., Nie, L. & Chen, J. Current understanding on the roles of gut microbiota in fish disease and immunity. Zool. Res. 40, 70–76 (2019).

    Google Scholar 

  • Williams, C. L., Garcia-Reyero, N., Martyniuk, C. J., Tubbs, C. W. & Bisesi, J. H. Jr. Regulation of endocrine systems by the microbiome: Perspectives from comparative animal models. Gen. Comp. Endocrinol. 292, 113437 (2020).

    Article 
    CAS 

    Google Scholar 

  • Schmidt, K. et al. Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232, 1793–1801 (2015).

    Article 
    CAS 

    Google Scholar 

  • Crumeyrolle-Arias, M. et al. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 42, 207–217 (2014).

    Article 
    CAS 

    Google Scholar 

  • Bell, E. A., Ball, A. G., Deprey, K. L. & Uno, J. K. The impact of antibiotics on the intestinal microbiome and the gut-brain axis in zebrafish. FASEB J. 32, 765–771 (2018).

    Article 

    Google Scholar 

  • Björnsson, B. T., Stefansson, S. O. & McCormick, S. D. Environmental endocrinology of salmon smoltification. Gen. Comp. Endocrinol. 170, 290–298 (2011).

    Article 

    Google Scholar 

  • Carruth, L. L., Jones, R. E. & Norris, D. O. Cortisol and Pacific Salmon: A new look at the role of stress hormones in olfaction and home-stream migration. Integr. Comp. Biol. 42, 574–581 (2002).

    Article 
    CAS 

    Google Scholar 

  • Donaldson, E. M. & Fagerlund, U. H. M. Effect of sexual maturation and gonadectomy at sexual maturity on cortisol secretion rate in sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Board Can. 27, 2287–2296 (1970).

    Article 

    Google Scholar 

  • Dickhoff, W. W. Development, Maturation, and Senescence of Neuroendocrine Systems 253–266 (Elsevier, 1989).

    Book 

    Google Scholar 

  • Maule, A. G., Schreck, C. B. & Kaattari, S. L. Changes in the immune system of coho salmon (Oncorhynchus kisutch) during the parr-to-smolt transformation and after implantation of cortisol. Can. J. Fish. Aquat. Sci. 44, 161–166 (1987).

    Article 
    CAS 

    Google Scholar 

  • Llewellyn, M. S. et al. Parasitism perturbs the mucosal microbiome of Atlantic Salmon. Sci. Rep. 7, 1–10 (2017).

    Article 

    Google Scholar 

  • Vasemägi, A., Visse, M. & Kisand, V. Effect of environmental factors and an emerging parasitic disease on gut microbiome of wild Salmonid fish. mSphere 2, e00418-17 (2017).

    Article 
    PubMed Central 

    Google Scholar 

  • Kelly, C. & Salinas, I. Under pressure: Interactions between commensal microbiota and the teleost immune system. Front. Immunol. 8, 559 (2017).

    Article 
    PubMed Central 

    Google Scholar 

  • Fast, M. D., Hosoya, S., Johnson, S. C. & Afonso, L. O. B. Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol. 24, 194–204 (2008).

    Article 
    CAS 

    Google Scholar 

  • Carrizo, V. et al. Effect of cortisol on the immune-like response of rainbow trout (Oncorhynchus mykiss) myotubes challenged with Piscirickettsia salmonis. Vet. Immunol. Immunopathol. 237, 110240 (2021).

    Article 
    CAS 

    Google Scholar 

  • Nervino, S. Intestinal lesions and parasites associated with prespawn mortality in Chinook salmon (Oncorhynchus tshawytscha). (2022).

  • Couch, C. E. et al. Enterocytozoon schreckii n. sp. infects the enterocytes of adult chinook salmon (Oncorhynchus tshawytscha) and may be a sentinel of immunosenescence. mSphere 7, e0090821 (2022).

    Article 

    Google Scholar 

  • Redding, J. M., Schreck, C. B., Birks, E. K. & Ewing, R. D. Cortisol and its effects on plasma thyroid hormone and electrolyte concentrations in fresh water and during seawater acclimation in yearling coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 56, 146–155 (1984).

    Article 
    CAS 

    Google Scholar 

  • Marotz, C. et al. DNA extraction for streamlined metagenomics of diverse environmental samples. Biotechniques 62, 290–293 (2017).

    Article 
    CAS 

    Google Scholar 

  • Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA. 108(Suppl 1), 4516–4522 (2011).

    Article 
    CAS 

    Google Scholar 

  • Minich, J. J. et al. High-throughput miniaturized 16S rRNA amplicon library preparation reduces costs while preserving microbiome integrity. mSystems 3, e00166-18 (2018).

    Article 
    PubMed Central 

    Google Scholar 

  • Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Escalas, A. et al. Ecological specialization within a carnivorous fish family is supported by a herbivorous microbiome shaped by a combination of gut traits and specific diet. Front. Mar. Sci. 8, 622883 (2021).

    Article 

    Google Scholar 

  • Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    Article 
    CAS 

    Google Scholar 

  • Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).

    Article 

    Google Scholar 

  • R Core Team. R: A Language and Environment for Statistical Computing. (2020). https://www.R-project.org/.

  • Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).

    Article 
    CAS 

    Google Scholar 

  • Wright, E. Using DECIPHER v2.0 to analyze big biological sequence data in R. R. J. 8, 352 (2016).

    Article 

    Google Scholar 

  • Schliep, K., Potts, A. J., Morrison, D. A. & Grimm, G. W. Intertwining phylogenetic trees and networks. Methods Ecol. Evol. 8, 1212–1220 (2017).

    Article 

    Google Scholar 

  • Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 623–656 (1948).

    Article 
    MathSciNet 
    MATH 

    Google Scholar 

  • Shepard, R. N. The analysis of proximities: Multidimensional scaling with an unknown distance function. II. Psychometrika 27, 219–246 (1962).

    Article 
    MathSciNet 
    MATH 

    Google Scholar 

  • Oksanen, J. et al. The vegan package. Community Ecol. Packag. 10, 631–637 (2007).

    Google Scholar 

  • Martinez Arbizu, P. pairwiseAdonis: Pairwise Multilevel Comparison using Adonis. Preprint at (2017)

  • Zhang, Y. Likelihood-based and Bayesian methods for Tweedie compound Poisson linear mixed models. Stat. Comput. 23, 743–757 (2013).

    Article 
    MathSciNet 
    CAS 
    MATH 

    Google Scholar 

  • Hassenrück, C., Reinwald, H., Kunzmann, A., Tiedemann, I. & Gärdes, A. Effects of thermal stress on the gut microbiome of juvenile milkfish (Chanos chanos). Microorganisms 9, 5 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • Liu, Y. et al. Response mechanism of gut microbiome and metabolism of European seabass (Dicentrarchus labrax) to temperature stress. Sci. Total Environ. 813, 151786 (2022).

    Article 
    CAS 

    Google Scholar 

  • Du, F. et al. Response of the gut microbiome of Megalobrama amblycephala to crowding stress. Aquaculture 500, 586–596 (2019).

    Article 
    CAS 

    Google Scholar 

  • Stothart, M. R., Palme, R. & Newman, A. E. M. It’s what’s on the inside that counts: Stress physiology and the bacterial microbiome of a wild urban mammal. Proc. Biol. Sci. 286, 20192111 (2019).

    PubMed Central 

    Google Scholar 

  • Michels, N. et al. Gut microbiome patterns depending on children’s psychosocial stress: Reports versus biomarkers. Brain Behav. Immun. 80, 751–762 (2019).

    Article 

    Google Scholar 

  • Zhao, H., Jiang, X. & Chu, W. Shifts in the gut microbiota of mice in response to dexamethasone administration. Int. Microbiol. 23, 565–573 (2020).

    Article 
    CAS 

    Google Scholar 

  • Zanuzzo, F. S., Sabioni, R. E., Marzocchi-Machado, C. M. & Urbinati, E. C. Modulation of stress and innate immune response by corticosteroids in pacu (Piaractus mesopotamicus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 231, 39–48 (2019).

    Article 
    CAS 

    Google Scholar 

  • Timmermans, S., Souffriau, J. & Libert, C. A general introduction to glucocorticoid biology. Front. Immunol. 10, 1545 (2019).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Kugathas, S. & Sumpter, J. P. Synthetic glucocorticoids in the environment: First results on their potential impacts on fish. Environ. Sci. Technol. 45, 2377–2383 (2011).

    Article 
    CAS 

    Google Scholar 

  • Schaal, P. et al. Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon. Anim. Microbiome 4, 53 (2022).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Birlanga, V. B. et al. Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon. Sci. Rep. 12, 16719 (2022).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Cipriano, R. C., Ford, L. A., Smith, D. R., Schachte, J. H. & Petrie, C. J. Differences in detection of Aeromonas salmonicida in covertly infected Salmonid fishes by the stress-inducible furunculosis test and culture-based assays. J. Aquat. Anim. Health 9, 108–113 (1997).

    <a data-track="click" rel="nofollow noopener" data-track-label="10.1577/1548-8667(1997)0092.3.CO;2″ data-track-action=”article reference” href=”https://doi.org/10.1577%2F1548-8667%281997%29009%3C0108%3ADIDOAS%3E2.3.CO%3B2″ aria-label=”Article reference 66″ data-doi=”10.1577/1548-8667(1997)0092.3.CO;2″>Article 

    Google Scholar 

  • Lovy, J., Speare, D. J., Stryhn, H. & Wright, G. M. Effects of dexamethasone on host innate and adaptive immune responses and parasite development in rainbow trout Oncorhynchus mykiss infected with Loma salmonae. Fish Shellfish Immunol. 24, 649–658 (2008).

    Article 
    CAS 

    Google Scholar 

  • Bakhtiyar, Y., Yousuf, T. & Arafat, M. Y. Bacterial Fish Diseases 269–278 (Elsevier, 2022).

    Book 

    Google Scholar 

  • Benda, S. E., Naughton, G. P., Caudill, C. C., Kent, M. L. & Schreck, C. B. Cool, pathogen-free refuge lowers pathogen-associated prespawn mortality of Willamette River Chinook salmon. Trans. Am. Fish. Soc. 144, 1159–1172 (2015).

    Article 

    Google Scholar 

  • Barton, B. A. & Iwama, G. K. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu. Rev. Fish Dis. 1, 3–26 (1991).

    Article 

    Google Scholar 

  • Dolan, B. P. et al. Innate and adaptive immune responses in migrating spring-run adult chinook salmon, Oncorhynchus tshawytscha. Fish Shellfish Immunol. 48, 136–144 (2016).

    Article 
    CAS 

    Google Scholar 

  • Wedemeyer, G. A. Physiological response of juvenile coho salmon (Oncorhynchus kisutch) and rainbow trout (Salmo gairdneri) to handling and crowding stress in intensive fish culture. J. Fish. Res. Board Can. 33, 2699–2702 (1976).

    Article 

    Google Scholar 

  • Suomalainen, L.-R., Tiirola, M. A. & Valtonen, E. T. Influence of rearing conditions on Flavobacterium columnare infection of rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 28, 271–277 (2005).

    Article 

    Google Scholar 

  • Schmidt-Posthaus, H., Bernet, D., Wahli, T. & Burkhardt-Holm, P. Morphological organ alterations and infectious diseases in brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss exposed to polluted river water. Dis. Aquat. Organ. 44, 161–170 (2001).

    Article 
    CAS 

    Google Scholar 

  • Shi, N., Li, N., Duan, X. & Niu, H. Interaction between the gut microbiome and mucosal immune system. Mil. Med. Res. 4, 1–7 (2017).

    CAS 

    Google Scholar 

  • Mitchell, S. O. et al. “Candidatus Branchiomonas cysticola” is a common agent of epitheliocysts in seawater-farmed Atlantic salmon Salmo salar in Norway and Ireland. Dis. Aquat. Organ. 103, 35–43 (2013).

    Article 
    CAS 

    Google Scholar 

  • Kormas, K. A., Meziti, A., Mente, E. & Frentzos, A. Dietary differences are reflected on the gut prokaryotic community structure of wild and commercially reared sea bream (Sparus aurata). Microbiologyopen 3, 718–728 (2014).

    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Engel, M. et al. Influence of lung CT changes in chronic obstructive pulmonary disease (COPD) on the human lung microbiome. PLoS ONE 12, e0180859 (2017).

    Article 
    PubMed Central 

    Google Scholar 

  • Lucasson, A. et al. A core of functionally complementary bacteria colonizes oysters in Pacific Oyster Mortality Syndrome. bioRxiv https://doi.org/10.1101/2020.11.16.384644 (2020).

    Article 

    Google Scholar 


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    Adjusting time-of-day and depth of fishing provides an economically viable solution to seabird bycatch in an albacore tuna longline fishery