Two species of antarctic icefishes (genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression

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SUMMARY The Antarctic icefishes (Family Channichthyidae) provide excellent examples of unique traits that can arise in a chronically cold and isolated environment. Their loss of hemoglobin (Hb) expression, and in some cases, loss of myoglobin (Mb) expression, has taught us much about the function of these proteins. Although absences of the proteins are fixed traits in icefishes, the losses do not appear to be of adaptive value. Contrary to some suggestions,loss of Hb has led to higher energetic costs for circulating blood, and losses of Mb have reduced cardiac performance. Moreover, losses of Hb and Mb have resulted in extensive modifications to the cardiovascular system to ensure adequate oxygen delivery to working muscles. Recent studies suggest that losses of Hb and Mb, and their associated nitric oxide (NO)-oxygenase activities, may have accelerated the development and evolution of these cardiovascular modifications. The high levels of NO that should occur in the absence of Hb and Mb have been shown in other animal groups to lead to an increase in tissue vascularization, an increase in the lumenal diameter of blood vessels, and an increase in mitochondrial densities. These characteristics are all hallmark traits of Antarctic icefishes. Homeostatic feedback mechanisms thus may have accelerated evolution of the pronounced cardiovascular traits of Antarctic icefishes.

Section: Patterns Of Oxygen-binding Protein Loss Among Thementioning

confidence: 99%

Section: Was Loss Of Hb And/or Mb Of Adaptive Value?mentioning

confidence: 99%

Section: Was Loss Of Hb And/or Mb Of Adaptive Value?mentioning

confidence: 99%

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When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes

Sidell

O’Brien

2006

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“…In addition to the loss of Hb, many species within the Channichthyid family lack Mb, an intracellular oxygen-binding protein found in muscle. In total, six out of 16 icefish species lack Mb expression in their heart ventricles, a loss that has occurred through four different mutational events Grove et al, 2004;Borley and Sidell, 2011). Lack of Mb expression has important functional effects (Acierno, et al, 1997), but overall significance in the long term may be less than that of Hb loss because the Mb deficit has evolved repeatedly in teleost fishes, whereas it appears that Hb deletion has been restricted to notothenioids alone (Macqueen et al, 2014).…”

Section: Loss Of Major Hemoproteinsmentioning

confidence: 99%

Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?

Beers

Jayasundara

2015

Antarctic notothenioids dominate the fish fauna of the Southern Ocean. Evolution for millions of years at cold and stable temperatures has led to the acquisition of numerous biochemical traits that allow these fishes to thrive in sub-zero waters. The gain of antifreeze glycoproteins has afforded notothenioids the ability to avert freezing and survive at temperatures often hovering near the freezing point of seawater. Additionally, possession of cold-adapted proteins and membranes permits them to sustain appropriate metabolic rates at exceptionally low body temperatures. The notothenioid genome is also distinguished by the disappearance of traits in some species, losses that might prove costly in a warmer environment. Perhaps the best-illustrated example is the lack of expression of hemoglobin in white-blooded icefishes from the family Channichthyidae. Loss of key elements of the cellular stress response, notably the heat shock response, has also been observed. Along with their attainment of cold tolerance, notothenioids have developed an extreme stenothermy and many species perish at temperatures only a few degrees above their habitat temperatures. Thus, in light of today's rapidly changing climate, it is critical to evaluate how these extreme stenotherms will respond to rising ocean temperatures. It is conceivable that the remarkable cold specialization of notothenioids may ultimately leave them vulnerable to future thermal increases and threaten their fitness and survival. Within this context, our review provides a current summary of the biochemical losses and gains that are known for notothenioids and examines these cold-adapted traits with a focus on processes underlying thermal tolerance and acclimation capacity.

“…Some 40 years later, close examination of heart ventricles from species within the channicthyiid family determined that six of the 16 members do not express the intracellular oxygen-binding protein myoglobin (Mb) (Grove et al, 2004;Moylan and Sidell, 2000;Sidell et al, 1997). Since then, many studies have revealed how these unique animals thrive despite the loss of, what were once thought to be, essential oxygen-binding proteins.…”

Section: Introductionmentioning

confidence: 99%

High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis

Urschel

O’Brien

2008

SUMMARYWe investigated the molecular mechanisms regulating differences in mitochondrial volume density between heart ventricles of Antarctic notothenioids that vary in the expression of hemoglobin (Hb) and myoglobin (Mb). In mammals, peroxisome proliferatoractivated receptor γ coactivator-1α (PGC-1α) and nuclear respiratory factor 1 (NRF-1) stimulate mitochondrial biogenesis and maintain mitochondrial density in muscle tissues. We hypothesized that these factors would also maintain mitochondrial density in the hearts of Antarctic notothenioids. The percent cell volume occupied by mitochondria is significantly lower in hearts of the red-blooded notothenioid Notothenia coriiceps (18.18±0.69%) in comparison with those of the icefish Chaenocephalus aceratus (36.53±2.07%), which lacks both Hb and cardiac Mb. Mitochondrial densities are not different between hearts of N. coriiceps and Chionodraco rastrospinosus, which lacks Hb, but whose heart expresses Mb. Despite differences in mitochondrial volume density between hearts of N. coriiceps and C. aceratus, the levels of transcripts of the genes encoding PGC-1α, NRF-1 and citrate synthase, and the copy number of mitochondrial DNA do not differ. Our results indicate that the high mitochondrial densities in hearts of C. aceratus may result from an increase in organelle size. The surface-to-volume ratio of mitochondria from N. coriiceps is 1.9-fold greater than that of mitochondria from C. aceratus. In addition, the levels of PGC-1α correlate with mitochondrial density in muscle tissues of notothenioids possessing mitochondria of similar size and morphology. Finally, the levels of PGC-1α are 4.6-fold higher in the aerobic pectoral adductor muscle in comparison with the glycolytic skeletal muscle of N. coriiceps. The potential physiological significance of an increase in mitochondrial size in hearts of Antarctic icefishes is discussed.