Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance

ArticleinProceedings of the National Academy of Sciences 103(27):10491-6 · August 2006with21 Reads
DOI: 10.1073/pnas.0603796103 · Source: PubMed
Abstract
Phylogenetically diverse polar and subpolar marine teleost fishes have evolved antifreeze proteins (AFPs) or antifreeze glycoproteins (AFGPs) to avoid inoculative freezing by internalized ice. For over three decades since the first fish antifreeze (AF) protein was discovered, many studies of teleost freezing avoidance showed hepatic AF synthesis and distribution within the circulation as pivotal in preventing the blood, and therefore the fish, from freezing. We have uncovered an important twist to this long-held paradigm: the complete absence of liver synthesis of AFGPs in any life stage of the Antarctic notothenioids, indicating that the liver plays no role in the freezing avoidance in these fishes. Instead, we found the exocrine pancreas to be the major site of AFGP synthesis and secretion in all life stages, and that pancreatic AFGPs enter the intestinal lumen via the pancreatic duct to prevent ingested ice from nucleating the hyposmotic intestinal fluids. AFGPs appear to remain undegraded in the intestinal milieu, and the composition and relative abundance of intestinal AFGP isoforms are nearly identical to serum AFGPs. Thus, the reabsorption of intact pancreas-derived intestinal AFGPs, and not the liver, is the likely source of circulatory AFGPs in notothenioid fishes. We examined diverse northern fish taxa and Antarctic eelpouts with hepatic synthesis of bloodborne AF and found that they also express secreted pancreatic AF of their respective types. The evolutionary convergence of this functional physiology underscores the hitherto largely unrecognized importance of intestinal freezing prevention in polar teleost freezing avoidance, especially in the chronically icy Antarctic waters.
    • "The migration and eventual establishment of these derived species in non-Antarctic coastal waters may have been facilitated by northward oscillations of the Antarctic Polar Front (APF) (Hüne et al., 2015; Kemp et al., 2010 ), an oceanographic feature that may have limited the northern extent of Antarctic species (Cristini et al., 2012; Eastman, 1993). Several " Antarctic escapees " that have established niches in sub- Antarctic regions still retain at least some of the cold-adapted physiological traits characteristic of Antarctic notothenioids such as functional AFGP genes (Cheng et al., 2003Cheng et al., , 2006 see Table 1 in Matschiner et al., 2015), as well as multiple haemoglobins (D'Avino and di Prisco, 1997) and altered oxygen transport (Egginton et al., 2002). In contrast, the early-diverged notothenioids have never established on the Antarctic shelf, either because of the lack of crucial biochemical and physiological cold adaptations (e.g. "
    [Show abstract] [Hide abstract] ABSTRACT: The non-Antarctic Notothenioidei families, Bovichtidae, Pseudaphritidae and Eleginopsidae, diverged early from the main notothenioid lineage. They are important in clarifying the early evolutionary processes that triggered notothenioid evolution in the Antarctic. The early-diverged group represents 8% of all notothenioid species and never established themselves on the Antarctic shelf. Most attention has been paid to the Antarctic notothenioids and their limited physiological tolerance to climate change and increased temperatures. In this review, we discuss key life history traits that are characteristic of the non-Antarctic early-diverged notothenioid taxa as well as the genetic resources and population differentiation information available for this group. We emphasise the population fitness and dynamics of these species and indicate how resource management and conservation of the group can be strengthened through an integrative approach. Both Antarctic waters and the non-Antarctic regions face rapid temperature rises combined with strong anthropogenic exploitation. While it is expected that early-diverged notothenioid species may have physiological advantages over high Antarctic species, it is difficult to predict how climate changes might alter the geographic range, behaviour, phenology and ultimately genetic variability of these species. It is possible, however, that their high degree of endemism and dependence on local environmental specificities to complete their life cycles might enhance their vulnerability.
    Full-text · Article · Nov 2015
    • "Убедительно говорят об этом примеры гетеротопного параллелизма как на видовом (фии логенетическом) уровне организации (независии мое сходство молекул у тресковых в Арктике и ноо тотениевидных в Антарктике и, возможно, в разз ных филогенетических ветвях Notothenioidei (Chen et al., 1997; Matschiner et al., 2011)), так и на организменном (онтогенетическом) уровне (синн тез молекул у тресковых и в желудочноокишечч ном тракте, и в печени). Хотя в последнем аспекте нототениевидные рыбы кажутся исключением, поскольку у них синтез гликопротеинов в печени не подтверждён (Cheng et al., 2006), но обнаружее ние гликопротеинов в их кожной слизи свидее тельствует о наличии у этих рыб гетеротопного синтеза AFGP. В геноме нототениевидных могут быть разные копии генов AFGP, подобно тому, что, например, имеет место с генами AFP типа I у американской, или зимней, камбалы Pseudopleuu ronectes americanus. "
    [Show abstract] [Hide abstract] ABSTRACT: Описан новый вид жабовидной бородатки Pogonophryne favosa sp. n. с мезобентали моря Космонавтов, Антарктика. Новый вид принадлежит к группе видов “mentella”, отличаясь от других видов группы наличием пятен на брюшной стороне тела и уникальным строением подбородочного усика. Проведено анатомо�гистологическое изучение надпазушных вздутий – необычных кожных образований, впервые обнаруженных у бородатковых рыб (Artedidraconidae). Обсуждается их возможная функция в системе холодоустойчивости антарктических нототениевидных рыб (Notothenioidei) и возможные исторические сроки их появления в семействе Artedidraconidae.
    Full-text · Dataset · Oct 2015 · Journal of Experimental Biology
    • "Notothenioid AFGPs are produced in pancreatic tissue and the anterior portion of the stomach, where they enter the gut cavity to exert their cryoprotective effects upon ingested ice. However, the pathway and mechanism of entry into the gut remain unknown (Cheng et al., 2006). Interestingly, a recent study revealed that AFGPs also inhibit the melting of ice crystals (Cziko et al., 2014). "
    [Show abstract] [Hide abstract] ABSTRACT: 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. © 2015. Published by The Company of Biologists Ltd.
    Full-text · Article · Jun 2015
Show more