Molecular ontogeny of larval immunity in European eel at increasing temperatures

Abstract

Temperature is a major factor that modulates the development and reactivity of the immune system. Only limited knowledge exists regarding the immune system of the catadromous European eel, Anguilla anguilla, especially during the oceanic early life history stages. Thus, a new molecular toolbox was developed, involving tissue specific characterisation of 3 housekeeping genes, 9 genes from the innate and 3 genes from the adaptive immune system of this species. The spatial pattern of immune genes reflected their function, e.g. complement component c3 was mainly produced in liver and il10 in the head kidney. Subsequently, the ontogeny of the immune system was studied in larvae reared from hatch to first-feeding at four temperatures, spanning their thermal tolerance range (16, 18, 20, and 22°C). Expression of some genes (c3 and igm) declined post hatch, whilst expression of most other genes (mhc2, tlr2, il1β, irf3, irf7) increased with larval age. At the optimal temperature, 18°C, this pattern of immune-gene expression revealed an immunocompromised phase between hatch (0 dph) and teeth-development (8 dph). The expression of two of the studied genes (mhc2, lysc) was temperature dependent, leading to increased mRNA levels at 22°C. Additionally, at the lower end of the thermal spectrum (16°C) immune competency appeared reduced, whilst close to the upper thermal limit (22°C) larvae showed signs of thermal stress. Thus, protection against pathogens is probably impaired at temperatures close to the critical thermal maximum (CTmax), impacting survival and productivity in hatcheries and natural recruitment.

‘Aerobic scope protection’ reduces ectotherm growth under warming

“…The immune system is tailored to the risk of infection and cell damage (e.g. through oxidative stress or thermal increase in turnover), but these functions may become restrictive at higher temperatures (Dittmar et al, 2014;Miest et al, 2019;Wegner et al, 2008).…”

“…The immune system is tailored to the risk of infection and cell damage (e.g. through oxidative stress or thermal increase in turnover), but these functions may become restrictive at higher temperatures (Dittmar et al., 2014; Miest et al., 2019; Wegner et al., 2008). Nerve function is optimised for a certain thermal range through ion channel function and membrane fluidity (Cossins et al., 1977; Jutfelt et al., 2019).…”

Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

“…Maternal antibody transfer improved the protection against pathogenic attacks for developing embryos of zebrafish [109]. In European eel, the molecular ontogeny of the immune system has been studied for larval stages from hatch until first-feeding at different temperatures [74], with an array of candidate genes being involved in early immune response. Several of these genes were also investigated in this study, and indicate the maternal transfer of igm mRNA in European eel via the ovary to the eggs.…”

What Goes Wrong during Early Development of Artificially Reproduced European Eel Anguilla anguilla? Clues from the Larval Transcriptome and Gene Expression Patterns

“…In teleost fish, early larvae mostly rely on a complex network of innate defense mechanisms (physical barriers, cellular defenses, and inflammatory cytokines) to orchestrate a rapid immune response against the hostile environment (reviewed by [13]). For European eels, it has been recently hypothesized that early larvae are immunocompromised and highly sensitive to pathogens [15]. Besides defense against antigens, early larvae need to cope with seawater salinities and thus face ion invasion and dehydration.…”

“…Although much effort has been devoted to understanding larval mortality (European eels: [6,15,35,36]; Japanese eels: [37][38][39][40][41]), it remains unclear what goes wrong during early ontogeny of artificially reproduced eels. With recent advances in sequencing technology, transcriptomic approaches have been widely used to understand marine fish larvae development [23].…”