Dawn to Dusk: Diurnal Rhythm of the Immune Response in Rainbow Trout (Oncorhynchus Mykiss)

Abstract

The daily change of light and dark periods influences different physiological processes including feeding, resting and locomotor activity. Previously, several studies on mammalian models revealed a strong link between day-night rhythms and key immunological parameters. Since teleost fishes possess innate and adaptive immune responses like those observed in higher vertebrates, we aimed to elucidate how changes in light-dark cycles shape the immune system of fish. Using the rainbow trout laboratory model, we investigated the link between diurnal rhythms and immune competence of fish. Initially, the cell composition and phagocytic activity of leukocytes was analyzed in the circulation as well as in the head kidney, the functional ortholog of mammalian bone marrow. Once the baseline was established, we evaluated the ability of fish to respond to a bacterial stimulus, as well as the changes in antimicrobial activity of the serum. Our results suggest increased immune competence during the day, manifested by the higher presence of myeloid cells in the circulation; increased overall phagocytic activity; and higher capacity of the sera to inhibit the growth of Aeromonas salmonicida. Notably, our flow cytometric analysis identified the myeloid cells as the major population influenced by the time of day, whereas IgM + B cells and thrombocytes did not vary in a significant manner. Interestingly, the presence of myeloid cells in blood and head kidney followed complementary trends. Thus, while we observed the highest number of myeloid cells in the blood during early morning, we witnessed a reverse trend in the head kidney, suggesting a homing of myeloid cells to reservoir niches with the onset of the dark phase. Further, the presence of myeloid cells was mirrored in the expression of the proinflammatory marker tnfa as well as in the number of leukocytes recruited to the peritoneal cavity in the peritonitis model of inflammation. Overall, the data suggest a connection between diurnal rhythms and the immune response of rainbow trout and highlight the relevance of rhythmicity and its influence on experimental work in the field of fish chronoimmunology.

Antimicrobial Peptides of Salmonid Fish: From Form to Function

“…This suggests that not all leukocytes may respond to vitamin C and E. coli in the same manner as macrophages or monocytes. Furthermore, the composition of rainbow trout head kidney, in terms of leukocyte populations, has been shown to fluctuate over time [ 88 ].…”

Effects of different photoperiods and feeding regimes on immune response, oxidative status, and tissue damage in juvenile rainbow trout (Oncorhynchus mykiss)

“…For example, in zebrafish (Danio rerio), the inflammatory response is regulated by the core biological clock genes period1b and period 2 (Ren et al, 2018). In rainbow trout, significant circadian rhythms were also found for serum bactericidal activity and immune defense factors (Lazado et al, 2018) and in the number of leukocytes and myeloid cells (Montero et al, 2020). Further, the effect of feeding time on fish immune function was also reported in a zebrafish study where fish in the scheduled feeding group exhibited higher levels of lysozyme, b-defensin, and hepcidin transcripts (Lazado et al, 2019).…”

Blood Will Tell: What Hematological Analyses Can Reveal About Fish Welfare

“…Together with the bactericidal activity, these parameters provide valuable downstream information about the effects of stress hormone release on the immune performance under challenging conditions. Hormones are also likely to induce rather subtle changes in the activity of these immune parameters, either daily or seasonally, and between the sexes (203)(204)(205). Most of these analyses are carried out ex vivo within a limited time after the previous collection.…”