A solution to Nature's haemoglobin knockout: a plasma-accessible carbonic anhydrase catalyses CO₂ excretion in Antarctic icefish gills

In all vertebrates studied to date, CO₂ excretion depends on the enzyme carbonic anhydrase (CA) that catalyses the rapid conversion of HCO₃− to CO₂ at the gas-exchange organs. The largest pool of CA is present within red blood cells (RBC) and, in some vertebrates, plasma-accessible CA (paCA) isoform...

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Bibliographic Details
Main Authors: Harter, TS, Sackville, M, Wilson, JM, Metzger, DCH, Egginton, S, Esbaugh, AJ, Farrell, AP, Brauner, CJ
Format: Article in Journal/Newspaper
Language:English
Published: The Company of Biologists 2018
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Online Access:https://eprints.whiterose.ac.uk/136503/
https://eprints.whiterose.ac.uk/136503/1/JEXBIO-2018-190918v1-Harter%20%28002%29.pdf
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Summary:In all vertebrates studied to date, CO₂ excretion depends on the enzyme carbonic anhydrase (CA) that catalyses the rapid conversion of HCO₃− to CO₂ at the gas-exchange organs. The largest pool of CA is present within red blood cells (RBC) and, in some vertebrates, plasma-accessible CA (paCA) isoforms participate in CO₂ excretion. However, teleost fishes typically do not have paCA at the gills and CO₂ excretion is reliant entirely on RBC CA; a strategy that is not possible in icefishes. As the result of a natural knockout, Antarctic icefishes (Channichthyidae) are the only known vertebrates that do not express haemoglobin (Hb) as adults, and largely lack RBC in the circulation (haematocrit<1%). Previous work has indicated the presence of high levels of membrane-bound CA activity in the gills of icefishes, but without determining its cellular orientation. Thus, we hypothesised that icefishes express a membrane-bound CA isoform at the gill that is accessible to the blood plasma. The CA distribution was compared in the gills of two closely-related notothenioid species, one with Hb and RBCs (Notothenia rossii) and one without (Champsocephalus gunnari). Molecular, biochemical and immunohistochemical markers indicate high levels of a Ca4 isoform in the gills of the icefish (but not the red-blooded N. rossii), in a plasma-accessible location that is consistent with a role in CO₂ excretion. Thus, in the absence of RBC CA, the icefish gill could exclusively provide the catalytic activity necessary for CO₂ excretion; a pathway that is unlike that of any other vertebrate.