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

Harter, Till S.; Sackville, Michael A.; Wilson, Jonathan M.; Metzger, David C. H.; Egginton, Stuart; Esbaugh, Andrew J.; Farrell, Anthony P.; Brauner, Colin J.

doi:10.1242/jeb.190918

Cited by 15 publications

(7 citation statements)

References 75 publications

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“…Among Antarctic notothenioids, further specialization is observed in the family of the white-blooded icefishes (Channichthyidae). Characterized by a complete loss of both hemoglobin and red blood cells ( Sidell and O’Brien 2006 ), icefish have evolved various mechanisms to compensate for this lack of active oxygen transport including larger hearts and thus greater cardiac stroke volume ( Sidell and O’Brien 2006 ), changes in the morphology and density of mitochondria ( Johnston et al 1998 ; O’Brien and Mueller 2010 ), a novel molecular method to increase CO 2 excretion ( Harter et al 2018 ), and increased cellular lipids ( Palmerini et al 2009 ). Even after the evolution of these phenotypes, icefish still exhibit limited cardiac performance, with <10% of the oxygen carrying capacity of red-blooded notothenioids ( Holeton 1970 ) and far larger cardiac energy expenditures ( Tota et al 1991 ; Tota and Gattuso 1996 ).…”

Section: Introductionmentioning

confidence: 99%

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Rivera‐Colón

Rayamajhi

Minhas

et al. 2023

Molecular Biology and Evolution

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White-blooded Antarctic icefishes, a family within the adaptive radiation of Antarctic notothenioid fishes, are an example of extreme biological specialization to both the chronic cold of the Southern Ocean and life without hemoglobin. As a result, icefishes display derived physiology that limits them to the cold and highly oxygenated Antarctic waters. Against these constraints, remarkably one species, the pike icefish Champsocephalus esox, successfully colonized temperate South American waters. To study the genetic mechanisms underlying secondarily temperate adaptation in icefishes, we generated chromosome-level genome assemblies of both C. esox and its Antarctic sister species, Champsocephalus gunnari. The C. esox genome is similar in structure and organization to that of its Antarctic congener; however, we observe evidence of chromosomal rearrangements coinciding with regions of elevated genetic divergence in pike icefish populations. We also find several key biological pathways under selection, including genes related to mitochondria and vision, highlighting candidates behind temperate adaptation in C. esox. Substantial antifreeze glycoprotein (AFGP) pseudogenization has occurred in the pike icefish, likely due to relaxed selection following ancestral escape from Antarctica. The canonical AFGP locus organization is conserved in C. esox and C. gunnari, but both show a translocation of two AFGP copies to a separate locus, previously unobserved in cryonotothenioids. Altogether, the study of this secondarily temperate species provides an insight into the mechanisms underlying adaptation to ecologically disparate environments in this otherwise highly specialized group.

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Section: Introductionmentioning

confidence: 99%

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Rivera‐Colón

Rayamajhi

Minhas

et al. 2023

Molecular Biology and Evolution

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“…CA4 isotypes are particularly relevant in the context of the gill tissue, since mammalian CA4 is typically expressed at high levels in lung epithelium, where its protein product is anchored to the luminal side of the pulmonary membrane. Other authors have previously described the expression of a membrane-bound CA isoform, accessible to the blood plasma, in the gills of the icefish Champsocephalus gunnari , hypothesizing its participation in CO 2 excretion [ 63 ]. However, the partial sequence reported by Harter and colleagues belongs to the CA4B group, most likely covering just a minor role in the global CA activity in the gills of Cryonotothenioidea ( Figure 4 C).…”

Section: Resultsmentioning

confidence: 99%

Cold Adaptation in Antarctic Notothenioids: Comparative Transcriptomics Reveals Novel Insights in the Peculiar Role of Gills and Highlights Signatures of Cobalamin Deficiency

Ansaloni

Gerdol

Torboli

et al. 2021

IJMS

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Far from being devoid of life, Antarctic waters are home to Cryonotothenioidea, which represent one of the fascinating cases of evolutionary adaptation to extreme environmental conditions in vertebrates. Thanks to a series of unique morphological and physiological peculiarities, which include the paradigmatic case of loss of hemoglobin in the family Channichthyidae, these fish survive and thrive at sub-zero temperatures. While some of the distinctive features of such adaptations have been known for decades, our knowledge of their genetic and molecular bases is still limited. We generated a reference de novo assembly of the icefish Chionodraco hamatus transcriptome and used this resource for a large-scale comparative analysis among five red-blooded Cryonotothenioidea, the sub-Antarctic notothenioid Eleginops maclovinus and seven temperate teleost species. Our investigation targeted the gills, a tissue of primary importance for gaseous exchange, osmoregulation, ammonia excretion, and its role in fish immunity. One hundred and twenty genes were identified as significantly up-regulated in Antarctic species and surprisingly shared by red- and white-blooded notothenioids, unveiling several previously unreported molecular players that might have contributed to the evolutionary success of Cryonotothenioidea in Antarctica. In particular, we detected cobalamin deficiency signatures and discussed the possible biological implications of this condition concerning hematological alterations and the heavy parasitic loads typically observed in all Cryonotothenioidea.

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“…Finally, the response of icefishes to environmental stressors such as temperature continues to be an active area of research (Table 3) (Beers and Sidell, 2011;Mueller et al, 2012;Joyce et al, 2018;O'Brien et al, 2018). Icefishes are also genetically and physiologically studied for being 'evolutionary mutant models' in regard to the absence of hemoglobin in their blood and the lack of cardiac myoglobin in some species (Near et al, 2006;Albertson et al, 2009;Desvignes et al, 2016;Harter et al, 2018;Bargelloni et al, 2019;Kim et al, 2019).…”

Section: Icefishesmentioning

confidence: 99%

Productivity and Change in Fish and Squid in the Southern Ocean

et al. 2021

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Southern Ocean ecosystems are globally important and vulnerable to global drivers of change, yet they remain challenging to study. Fish and squid make up a significant portion of the biomass within the Southern Ocean, filling key roles in food webs from forage to mid-trophic species and top predators. They comprise a diverse array of species uniquely adapted to the extreme habitats of the region. Adaptations such as antifreeze glycoproteins, lipid-retention, extended larval phases, delayed senescence, and energy-conserving life strategies equip Antarctic fish and squid to withstand the dark winters and yearlong subzero temperatures experienced in much of the Southern Ocean. In addition to krill exploitation, the comparatively high commercial value of Antarctic fish, particularly the lucrative toothfish, drives fisheries interests, which has included illegal fishing. Uncertainty about the population dynamics of target species and ecosystem structure and function more broadly has necessitated a precautionary, ecosystem approach to managing these stocks and enabling the recovery of depleted species. Fisheries currently remain the major local driver of change in Southern Ocean fish productivity, but global climate change presents an even greater challenge to assessing future changes. Parts of the Southern Ocean are experiencing ocean-warming, such as the West Antarctic Peninsula, while other areas, such as the Ross Sea shelf, have undergone cooling in recent years. These trends are expected to result in a redistribution of species based on their tolerances to different temperature regimes. Climate variability may impair the migratory response of these species to environmental change, while imposing increased pressures on recruitment. Fisheries and climate change, coupled with related local and global drivers such as pollution and sea ice change, have the potential to produce synergistic impacts that compound the risks to Antarctic fish and squid species. The uncertainty surrounding how different species will respond to these challenges, given their varying life histories, environmental dependencies, and resiliencies, necessitates regular assessment to inform conservation and management decisions. Urgent attention is needed to determine whether the current management strategies are suitably precautionary to achieve conservation objectives in light of the impending changes to the ecosystem.

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

Cited by 15 publications

References 75 publications

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Cold Adaptation in Antarctic Notothenioids: Comparative Transcriptomics Reveals Novel Insights in the Peculiar Role of Gills and Highlights Signatures of Cobalamin Deficiency

Productivity and Change in Fish and Squid in the Southern Ocean

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