Increasing the illumination slowly over several weeks protects against light damage in the eyes of the crustacean Mysis relicta

Abstract

The eyes of two glacial-relict populations of opossum shrimp Mysis relicta inhabiting the different photic environments of a deep, darkbrown freshwater lake and a variably lit bay of the Baltic Sea differ in their susceptibility to functional depression from strong light exposures. The lake population is much more vulnerable than the sea population. We hypothesized that the difference reflects physiological adaptation mechanisms operating on long time scales rather than genetically fixed differences between the populations. To test this, we studied how acclimation to ultra-slowly increased illumination (on time scales of several weeks to months) affected the resilience of the eyes to bright-light exposures. Light responses of whole eyes were measured by electroretinography, the visualpigment content of single rhabdoms by microspectrophotometry and the structural integrity of photoreceptor cells by electron microscopy (EM). Slow acclimation mitigated and even abolished the depression of photoresponsiveness caused by strong light exposures, making a dramatic difference especially in the lake animals. Still, acclimation in the sea animals was faster and the EM studies suggested intrinsic differences in the dynamics of microvillar membrane cycling. In conclusion, we report a novel form of physiological adaptation to general light levels, effective on the time scale of seasonal changes. It explains part but not all of the differences in light tolerance between the lake and sea populations.

Dark-adaptation in the eyes of a lake and a sea population of opossum shrimp (Mysis relicta): retinoid isomer dynamics, rhodopsin regeneration, and recovery of light sensitivity

“…The light had a pseudo-white spectrum spanning approximately 400–700 nm (see Fig. 2 e in Viljanen et al 2017 ) and intensity ~ 10 12 photons m −2 s −1 nm −1 measured at the water surface. The percentage of native R remaining after this exposure cannot be very precisely estimated due to the unknown position of screening pigments, which, in their light-adapted position, may filter > 90% of incoming light (Jokela-Määttä et al 2005 ), the varying orientation and position of ommatidia, and the unknown degree of photoreconversion MII → R. Under the conservative assumption that the light intensity incident on the photoreceptive membranes is only 1% of that at the water surface, we estimate that more than 99.5% of all rhodopsins have at least initially been converted to MII during the 30 min exposure.…”

“…Absorption spectra from single rhabdoms were measured with a single-beam, fast wavelength-scanning microspectrophotometer as described by Govardovskii et al ( 2000 ), Donner et al ( 2016 ) and Viljanen et al ( 2017 ). All handling and preparation took place in darkness under IR viewing.…”

“…560 nm in L p and 535 nm in S p on average, a difference that can be explained by expression of two rhodopsins with λ max around 525 and 570 nm in unequal proportions (Zak et al 2013 ; Donner et al 2016 ). On the other hand, measurements of post-bleach absorbance in single rhabdoms indicate that MII peaks around 490–500 nm in both populations (Viljanen et al 2017 ), strengthening the conclusion that photoreconversion MII → R must be negligible in their long-wavelength-dominated, low-light habitats.…”

“…Even if both light-dependent and light-independent mechanisms may be present in all species, the relative weights of the two routes must differ depending on the amount of light typically available to the animal. Here, we study two populations of Mysis relicta from southern Finland, with a long history as a model pair for studies of evolutionary and epigenetic divergence in response to differing dim-light environments (Lindström and Nilsson 1988 ; Jokela-Määttä et al 2005 ; Donner et al 2016 ; Viljanen et al 2017 ). They have been postglacially isolated in what are now a very dark brown freshwater lake (population denoted L p ) and a somewhat less dark, greenish, oligohaline bay of the Baltic Sea (population denoted S p ).…”

“…The two populations differ in their capacity to recover from strong light exposures, which, in L p eyes, may cause long-term sensitivity suppression and disorganization of the photoreceptive membranes, often described as light damage (Lindström and Nilsson 1988 ; Lindström et al 1988 , 2001 ). On the other hand, Viljanen et al ( 2017 ) have argued that these effects represent extremes on a continuum of physiological responses to varying light levels, and showed that slow acclimation of L p to higher illumination levels over months mitigates or even abolishes the suppression of L p light sensitivity upon strong exposures.…”