UV-B exposure reduces locomotor performance by impairing muscle function but not mitochondrial ATP production

Abstract

Ultraviolet B radiation (UV-B) can reduce swimming performance by increasing reactive oxygen species (ROS) formation. High concentrations of ROS can damage mitochondria, resulting in reduced ATP production. ROS can also damage muscle proteins, thereby leading to impaired muscle contractile function. We have shown previously that UV-B exposure reduces locomotor performance in mosquitofish (Gambusia holbrooki) without affecting metabolic scope. Our aim was therefore to test whether UV-B influences swimming performance of mosquitofish by ROS-induced damage to muscle proteins without affecting mitochondrial function. In a fully factorial design, we exposed mosquitofish to UV-B and no-UV-B controls in combination with exposure to N-acetylcysteine (NAC) plus no-NAC controls. We used NAC, a precursor of glutathione, as an antioxidant to test whether any effects of UV-B on swimming performance were at least partly due to UV-B-induced ROS. UV-B significantly reduced critical sustained swimming performance and tail beat frequencies, and it increased ROS-induced damage (protein carbonyl concentrations and lipid peroxidation) in muscle. However, UV-B did not affect the activity of sarco-endoplasmic reticulum ATPase (SERCA), an enzyme associated with muscle calcium cycling and muscle relaxation. UV-B did not affect ADP phosphorylation (state 3) rates of mitochondrial respiration, and it did not alter the amount of ATP produced per atom of oxygen consumed (P:O ratio). However, UV-B reduced the mitochondrial respiratory control ratio. Under UV-B exposure, fish treated with NAC showed greater swimming performance and tail beat frequencies, higher glutathione concentrations, and lower protein carbonyl concentrations and lipid peroxidation than untreated fish. Tail beat amplitude was not affected by any treatment. Our results showed, firstly, that the effects of UV-B on locomotor performance were mediated by ROS and, secondly, that reduced swimming performance was not caused by impaired mitochondrial ATP production. Instead, reduced tail beat frequencies indicate that muscle of UV-B exposed fish were slower, which was likely to have been caused by slower contraction rates, because SERCA activities remained unaffected.

Living in flowing water increases resistance to ultraviolet B radiation

“…ROS can interfere with calcium release dynamics from the sarcoplasmic reticulum and the calcium sensitivity of troponin (Cheng et al, 2016). Hence, UV-B-induced ROS may reduce swimming performance by interfering with calcium cycling dynamics, although we have shown previously that UV-B did not affect SERCA activity in mosquitofish (Ghanizadeh Kazerouni et al, 2015).…”

“…Oxidative damage to membranes and proteins occurs when ROS production outpaces the capacity of cellular antioxidant defences (Constantini, 2014;Lesser, 2006). UV-B-induced ROS damage to muscle proteins results in impaired locomotor performance (Ghanizadeh Kazerouni et al, 2015. Physical activity increases ROS production by contracting muscle acutely (Powers and Jackson, 2008).…”

Cost of transport is a repeatable trait but is not determined by mitochondrial efficiency in zebrafish (Danio rerio)

“…We dissected the skeletal tail muscle and divided it along the longitudinal axis of the fish in two equal halves, and tissue was used immediately for measurements of mitochondrial bioenergetics. Mitochondrial bioenergetics were measured according to published protocols (Ghanizadeh Kazerouni et al, 2015;Dos Santos et al, 2013) except where noted otherwise below. Skeletal muscle tissue (0.13-0.26 g) was homogenised on ice in a Potter-Elvehjem glass tissue homogeniser in nine volumes (w/v) of isolation buffer (140 mmol l −1 KCl, 20 mmol l −1 HEPES, 5 mmol l −1 MgCl 2 , 2 mmol l −1 EGTA, 1 mmol l −1 ATP, pH 7.0).…”

Parental exposure modulates the effects of UV‐B on offspring in guppies

“…; Wilhelm Filho ; Murphy ), and may thereby affect locomotor performance. However, exposure to UV‐B did not affect metabolic scope in mosquitofish even though locomotor performance was curtailed (Ghanizadeh Kazerouni, Franklin & Seebacher ). Our data here show that metabolism is resilient to UV‐B even across generations and that antioxidant defences were effective in preventing ROS damage to mitochondria at least at the UV‐B doses we used.…”

“…; Debecker et al . ; Ghanizadeh Kazerouni, Franklin & Seebacher ). Hence, while UV‐B is an essential component in vision and signalling of many species (Paul & Gwynn‐Jones ), its damaging effects on organism function can have far reaching ecological consequences by altering survival, life histories and trophic interactions within populations (Bancroft, Baker & Blaustein ; Alton, Wilson & Franklin ; Alton et al .…”