Abstract

Simple SummaryOur bodies run on an internal schedule or clock, telling us when to rest, sleep, or digest, and when to wake up, be active, or burn calories. That’s why we experience jetlag because we may well set our watches forward or backward, but our bodies haven’t yet. Imagine a seasonal clock that helps get us through the year, not just through the day. We set out to prove that such a clock exists in fish just like it does in humans. We exposed rainbow trout to bacteria to imitate natural encounters. We raised fish in the laboratory under the same light and temperature all year long. When we tested them in summer and winter, the fish consequently experienced days that were artificially longer/shorter or warmer/colder. Nonetheless, certain fish white blood cells didn’t react or see the bacteria as a threat in winter unlike in summer. They were probably behaving based on the time of year, or season and not on their immediate environment, just like how a jetlagged individual behaves based on an internal clock, not on what it’s like outside. Immunity and other processes are regulated differently between seasons, making animals less or more vulnerable in summer or winter.In poikilothermic vertebrates, seasonality influences different immunological parameters such as leukocyte numbers, phagocytic activity, and antibody titers. This phenomenon has been described in different teleost species, with immunological parameters peaking during warmer months and decreased levels during winter. In this study, the cellular immune responses of rainbow trout (Oncorhynchus mykiss) kept under constant photoperiod and water temperature against intraperitoneally injected Aeromonas salmonicida during the summer and winter were investigated. The kinetics of different leukocyte subpopulations from peritoneal cavity, spleen, and head kidney in response to the bacteria was measured by flow cytometry. Furthermore, the kinetics of induced A. salmonicida-specific antibodies was evaluated by ELISA. Despite maintaining the photoperiod and water temperature as constant, different cell baselines were detected in all organs analyzed. During the winter months, B- and T-cell responses were decreased, contrary to what was observed during summer months. However, the specific antibody titers were similar between the two seasons. Natural antibodies, however, were greatly increased 12 h post-injection only during the wintertime. Altogether, our results suggest a bias toward innate immune responses and potential lymphoid immunosuppression in the wintertime in trout. These seasonal differences, despite photoperiod and water temperature being kept constant, suggest an internal inter-seasonal or circannual clock controlling the immune system and physiology of this teleost fish.

Highlights

  • All species on our planet have co-evolved with their environment, responding to exogenous stimuli and rhythms, and have developed intrinsic clocks that allow them to anticipate periodic changes and respond [1]

  • Analyzing the number of leukocytes in the peritoneum (Figure 1c), significantly higher numbers of myeloid cells were detected in the wintertime, whereas no statistically significant difference was measured for the lymphoid population

  • Due to the significant changes in the B-cell compartment and the expected contribution of B cells to the response against the bacteria, we evaluated specific and non-specific antibody production by Enzyme-Linked Immunosorbent Assay (ELISA) across all the time points used

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Summary

Introduction

All species on our planet have co-evolved with their environment, responding to exogenous stimuli and rhythms, and have developed intrinsic clocks that allow them to anticipate periodic changes and respond [1]. Different species are influenced by several cycles, such as daily and circadian rhythms; tidal, lunar, and semi-lunar cycles; and seasonality (circannual rhythms) [2]. Circadian rhythms are well studied in mammals and have been characterized at transcriptomic levels [3,4]. This rhythmicity influences physiological parameters such as immune cell levels and composition in the bloodstream or in the organs throughout 24 h cycles [5]. Aeromonas salmonicida is the causative agent of furunculosis, an infectious disease affecting wild and farmed salmonids. This bacterium has been widely used as a stimulation and infection model in salmonids [6]. We hypothesize that the immune response against a pathogen could be influenced by the time of day but by the time of the year or seasons, as fish possess circannual rhythms

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