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First published online May 1, 2006
Journal of Experimental Biology 209, 1791-1802 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02091
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When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes

Bruce D. Sidell1,* and Kristin M. O'Brien2

1 School of Marine Sciences, University of Maine, 5751 Murray Hall, Orono, ME 04469-5751, USA
2 Institute of Arctic Biology, University of Alaska, Fairbanks, PO Box 757000, Fairbanks, AK 99775, USA


Figure 1
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Fig. 1. Lack of circulating hemoglobin and red cells is the signature characteristic of Antarctic icefishes. These two tubes contain freshly drawn blood from a hemoglobin-expressing notothenioid fish (Notothenia coriiceps) on the left and a hemoglobinless Antarctic icefish (Chaenocephalus aceratus) on the right.

 

Figure 2
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Fig. 2. Hearts from three species of notothenioid fishes. The channichthyid icefish Chaenocephalus aceratus has a pale yellow ventricle (far left) and lacks myoglobin (Mb) protein expression. The channichthyid icefish Chionodraco rastrospinosus expresses myoglobin protein and displays a rose-colored ventricle (middle). The related notothenioid species Notothenia coriiceps has a characteristically red ventricle (far right) associated with the presence of myoglobin protein. Note that both channichthyid hearts are considerably larger than that from the red blooded species despite all having been dissected from animals of equivalent body mass. (Figure is from Moylan and Sidell, 2000Go.)

 

Figure 3
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Fig. 3. Several independent mutational events have led to loss of myoglobin (Mb) expression during evolution of the icefish family. Expression of Mb is mapped on the consensus phylogeny of the Family Channichthyidae. Vertical red bars indicate points of independent mutational events leading to loss of Mb expression. The figure is modeled after that from Grove et al. (Grove et al., 2004Go) and based upon a cladogram originally presented by Near et al. (Near et al., 2003Go).

 

Figure 4
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Fig. 4. Myoglobin enhances the performance of icefish hearts. Cardiac output was measured in hearts from Mb-containing Chionodraco rastrospinosus and Mb-lacking Chaenocephalus aceratus at their inherent rhythms. The afterload against which the heart pumped perfusate was incrementally increased to describe the decay in heart performance as a function of pressure challenge. (A) When pumping oxygenated Ringers solution, Mb-containing hearts (Mb+, filled circles) were able to maintain cardiac output to greater afterload challenges than could Mb-lacking hearts (Mb–, open circles). (B) When 5 mmol l–1 NaNO2, which selectively poisons Mb function, was incorporated into the perfusate, mechanical performance of Mb-containing hearts was decremented so dramatically that they were outperformed by Mb-lacking hearts, which were refractory to the treatment. (Adapted from Acierno et al., 1997Go.)

 

Figure 5
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Fig. 5. Retinal vasculature of: (A) Pagothenia borchgrevinki, an Hb-expressing nototheniid (reproduced with permission from Eastman and Lannoo, 2004Go). (B) Chaenocephalus aceratus, a Hb-lacking icefish (J. Eastman and B. D. Sidell, unpublished). Lenses and vitreous bodies have been removed from the eyes to allow a clear view of the blood vessels. Yellow coloration is from perfusion and filling of the vasculature with MicrofilTM silicone rubber compound.

 

Figure 6
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Fig. 6. Nitric oxide (NO) regulates many of the physiological processes that are characteristic traits of icefish. NO stimulates angiogenesis through the activation of vascular endothelial growth factor (VEGF). Mitochondrial biogenesis is induced by NO via peroxisome proliferator-activated receptor {gamma} coactivator 1{alpha} (PGC-1). NO has also been shown to induce muscle hypertrophy, although this molecular pathway has yet to be defined. The authors acknowledge the use of Scienceslides (Visiscience Corp.) in creating this figure.

 





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