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Title:Effect of environmental temperature on Antarctic fish antifreeze protein activity and concentration
Author(s):Fields, Lauren Ganister
Director of Research:DeVries, Arthur L.
Doctoral Committee Chair(s):DeVries, Arthur L.
Doctoral Committee Member(s):Cheng, Christina; Fuller, Rebecca; Suski, Cory
Department / Program:School of Integrative Biology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):Antarctic fish
antifreeze proteins
Abstract:The Southern Ocean is an extreme cold environment with regions that can be variable in their temperature profiles. The low latitudes of the western Antarctic Peninsula (WAP) experience freezing sea surface water temperatures and ice formation only during the austral winter but the water below 100 m is warmer due to the effects of the Circumpolar Deep Water (CDW) that flows onto the shelf. During the winter the temperature gradient can range from -1.9°C at the surface to +2.0°C at depth. In contrast, the high latitude regions of the southwestern Ross Sea and McMurdo Sound can be at the freezing point of seawater (-1.9°C) nearly year-round. McMurdo Sound is bordered to the south by the Ross Ice Shelf which is a source of upwelling of supercooled water. In the WAP environmental ice crystals are found only in the surface water from surface ice formation during the winter while the southwestern Ross Sea is ice covered for much of the year. The presence of environmental ice crystals poses a challenge for marine ectotherms. Despite this, marine life is abundant in this region. The largest group of fishes in this region is the suborder Notothenioidei. For notothenioid fishes blood serum osmolytes only depress the freezing point of their blood to about -1.0°C, almost a full degree warmer than the environmental freezing point. The success of this group in the Southern Ocean is attributable in part to the evolution of blood antifreeze proteins (AFPs) that adsorb to the surface of internalized ice crystals and inhibit their growth. The non-colligative depression of the blood serum freezing point can contribute enough protection to prevent freezing down to or below the freezing point of seawater. The evolution of AFPs is what allowed the notothenioid fishes to dominate the ichthyofaunal biomass of the Southern Ocean after freezing water temperatures caused most of the late Eocene fish fauna to go extinct. Notothenioids have two types of AFPs: antifreeze glycoproteins (AFGPs) that are comprised of glycosylated tripeptide repeats of various sizes from large size isoforms with numerous repeats to small size isoforms with relatively few tripeptide repeat sequences, and an antifreeze potentiating protein (AFPP) that potentiates the activity of the AFGPs. The largest family within Notothenioidei is the Nototheniidae, comprised of 49 species in 13 genera. Members of this family are found in both the WAP and Ross Sea regions of the Southern Ocean. Some species are confined to the WAP while others can be found circum-Antarctic. Fishes inhabiting the shallow and deep water environments in these regions have different temperature and ice conditions to contend with. Populations that are in the high latitude regions have increased threat of freezing due to the high prevalence of exogenous ice and have increased need for freeze protection than populations inhabiting the warm +2.0°C CDW. Because of this, populations inhabiting different thermal environments are hypothesized to have different AFP activities and different concentrations of circulating AFPs. To investigate whether populations of species within a genus differed in their AFPs and freezing points I sampled ten species from the genus Trematomus (family Nototheniidae) from both the high latitude southwestern Ross Sea and the WAP. This genus is often considered a high latitude radiation due to its abundance in both the shallow and deep water in this region. Surface temperature and environmental ice was similar in both locations but deep water temperatures differed with the southwestern Ross Sea having bottom temperatures of -1.9°C and the WAP as warm as +0.3°C. For both populations I investigated the contributions of the AFGP and AFPP activity to the blood serum freezing point depression in order to determine how they varied with depth, water temperature, and the presence of ice. Trematomids from the southwestern Ross Sea had lower blood serum freezing points than those inhabiting the WAP due to increased AFP activity from both the AFGPs and the AFPP. Populations from two species (Trematomus hansoni and Trematomus bernacchii) were collected from both shallow and deep waters within the Ross Sea where shallow and deep temperatures are the same (-1.9°C) but environmental ice crystals are found only in the shallow water. The populations from shallow depths had lower blood serum freezing points than populations inhabiting deep, ice-free water. I expanded this study to include more species from multiple genera from the WAP. Fishes were sampled during the austral winter 2014 when bottom water was between +0.5°C and -0.5°C. Five species from two of the four genera sampled are found circum-Antarctic, including three species from the genus Trematomus, the remaining three species from two genera are only found in the WAP. Given the variability I observed in trematomids from the WAP I hypothesized that species and whole genera of species would differ from one another in their blood freezing points, antifreeze activity, and AFGP concentration with regard to whether populations of the species were confined to the WAP or if they could be found circum-Antarctic. Species differed from one another in their AFP activity and AFGP concentration regardless of whether they were found solely in the WAP or if they could be found circum-Antarctic. Fish that are found only in deep water had lower AFGP concentrations and higher blood freezing points than fish that can be found in both shallow and deep water habitats. As I previously observed with the trematomids, species within a genus differed significantly from one another for Trematomus but did not differ from one another for Notothenia likely due to those species’ similar habitats and circum-Antarctic distributions. Despite the warm CDW temperature, all species had blood freezing points at or below the freezing point of seawater. I also focused on the southwestern Ross Sea where there is very little thermal variation for much of the year. I was interested in following one species with shallow water populations during the transition from freezing water temperatures through the onset of summer warming when water temperatures increased from -1.90°C to -0.31°C. I collected blood samples from T. bernacchii at three locations within McMurdo Sound. One site was sampled three times: once before the onset of summer warming, and twice after summer warming had already occurred. High resolution long deployment temperature loggers and conductivity, temperature, and depth measurements provided the temperatures for each site at the time of sampling and for the course of the year. Despite the comparatively small seasonal temperature increase, populations of T. bernacchii differed based on sampling. High concentrations of AFGP were observed from locations where water temperatures were still at -1.9°C but concentration decreased in the late season location corresponding to the increased temperature at that sampling time. Overall, I found that antifreeze protein concentration and activity was dependent on sampling location and temperature with populations from the southwestern Ross Sea having higher AFP activity and concentration than populations from the WAP. The same trend was seen when comparing sampling depth. Shallow water populations had higher AFP levels due to increased contact with environmental ice and deep water populations had lower AFP levels due to rarely coming into contact with environmental ice or by inhabiting deep water that could be 4°C warmer than the surface water. Species found at these warm depths but that also have circum-Antarctic distributions had higher AFP levels than species confined to warmer regions and warmer depths. At an even smaller temperature scale, the levels of AFP for T. bernacchii differed in direct response to seasonal temperature change, showing decreased AFP concentration in the austral summer as the McMurdo Sound waters began to warm. The freezing temperatures of some regions of the Southern Ocean require fishes to maintain high levels of circulating AFPs year-round. Relaxed selective pressure by inhabiting ice-free water or warm CDW may cause fishes to maintain less AFP or decreased AFP activity in the absence of the threat of freezing. 
Issue Date:2015-04-21
Rights Information:Copyright 2015 Lauren Fields
Date Available in IDEALS:2015-07-22
Date Deposited:May 2015

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