The loss of hemoglobin and myoglobin does not minimize oxidative stress in Antarctic icefishes

Abstract

The unusual pattern of expression of hemoglobin (Hb) and myoglobin (Mb) among Antarctic notothenioid fishes provides an exceptional model system for assessing the impact of these proteins on oxidative stress. We tested the hypothesis that the lack of oxygen-binding proteins may reduce oxidative stress. Levels and activity of pro-oxidants and small-molecule and enzymatic antioxidants, and levels of oxidized lipids and proteins in the liver, oxidative skeletal muscle and heart ventricle were quantified in five species of notothenioid fishes differing in the expression of Hb and Mb. Levels of ubiquitinated proteins and rates of protein degradation by the 20S proteasome were also quantified. Although levels of oxidized proteins and lipids, ubiquitinated proteins, and antioxidants were higher in red-blooded fishes than in Hb-less icefishes in some tissues, this pattern did not persist across all tissues. Expression of Mb was not associated with oxidative damage in the heart ventricle, whereas the activity of citrate synthase and the contents of heme were positively correlated with oxidative damage in most tissues. Despite some tissue differences in levels of protein carbonyls among species, rates of degradation by the 20S proteasome were not markedly different, suggesting either alternative pathways for eliminating oxidized proteins or that redox tone varies among species. Together, our data indicate that the loss of Hb and Mb does not correspond with a clear pattern of either reduced oxidative defense or oxidative damage.

The Relationship between Myoglobin, Aerobic Capacity, Nitric Oxide Synthase Activity and Mitochondrial Function in Fish Hearts

“…Thus, the loss of Mb in Hb + species was not associated with a reduced aerobic metabolic capacity, and this agrees with the literature [12,17,21]. Interestingly, the expression of Mb was associated with a greater CS activity in Hb − icefishes [50], a trait that does not appear to be shared with Hb + fishes. In our study, CS activity was negatively correlated with these species' RVM and P:O ratio (Supplementary Figure S3 and Figure 1D), and these data suggest that increased CS activity may be needed in fish with smaller hearts and/or that have a lower efficiency of oxidative phosphorylation.…”

“…This finding is consistent with the study of O'Brien et al (2019). These authors showed that variation in Mb expression in five species of notothenioid fishes was not associated with oxidative stress/damage in the ventricle [50]. This may be because inter-specific ROS scavenging by Mb + and Mb − fishes may only be relevant/observed under conditions of limited oxygen.…”

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

“…Evidence suggests the primary selective pressure for Antarctic bacteria is oxidative stress ( Russo et al 2010 ). Cryonotothenioids express high levels of antioxidants but still show evidence of high oxidation stress ( Todgham et al 2007 ; Chen et al 2008 ; Peck 2016 , O’Brien et al 2018 ). Several TRP channels are gated or modulated by ROS, including mammalian TRPV1, TRPA1, and TRPM7 ( Takahashi et al 2011 ; Inoue et al 2021 ; Pantke et al 2021 ).…”

Cardiac mitochondrial metabolism may contribute to differences in thermal tolerance of red- and white-blooded Antarctic notothenioid fishes

“…The greater activity of CS (and higher energy charge) in N. coriiceps hearts compared with C. aceratus hearts is supported by high levels of the intracellular oxygen-binding protein myoglobin (Mb), which is absent in C. aceratus hearts (Moylan and Sidell, 2000;O'Brien et al, 2018;Sidell et al, 1997). In vitro studies have shown that hearts of icefishes that express Mb are capable of maintaining cardiac output at higher afterload pressures compared with those lacking Mb (Acierno et al, 1997), and we have found that Chionodraco rastrospinosus, whose heart expresses Mb, achieves higher heart rates in situ compared with C. aceratus (S. E. Egginton, M. Axelsson, E. L. Crockett, K. M. O'Brien and A. P. Farrell, unpublished).…”