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      Effect of elevated temperature on membrane lipid saturation in Antarctic notothenioid fish

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          Abstract

          Homeoviscous adaptation (HVA) is a key cellular response by which fish protect their membranes against thermal stress. We investigated evolutionary HVA (long time scale) in Antarctic and non-Antarctic fish. Membrane lipid composition was determined for four Perciformes fish: two closely related Antarctic notothenioid species ( Trematomus bernacchii and Pagothenia borchgrevinki); a diversified related notothenioid Antarctic icefish ( Chionodraco hamatus); and a New Zealand species ( Notolabrus celidotus). The membrane lipid compositions were consistent across the three Antarctic species and these were significantly different from that of the New Zealand species. Furthermore, acclimatory HVA (short time periods with seasonal changes) was investigated to determine whether stenothermal Antarctic fish, which evolved in the cold, stable environment of the Southern Ocean, have lost the acclimatory capacity to modulate their membrane saturation states, making them vulnerable to anthropogenic global warming. We compared liver membrane lipid composition in two closely related Antarctic fish species acclimated at 0 °C (control temperature), 4 °C for a period of 14 days in T. bernacchii and 28 days for P. borchgrevinki, and 6 °C for 7 days in both species. Thermal acclimation at 4 °C did not result in changed membrane saturation states in either Antarctic species. Despite this, membrane functions were not compromised, as indicated by declining serum osmolality, implying positive compensation by enhanced hypo-osmoregulation. Increasing the temperature to 6 °C did not change the membrane lipids of P. borchgrevinki. However, in T. bernacchii, thermal acclimation at 6 °C resulted in an increase of membrane saturated fatty acids and a decline in unsaturated fatty acids. This is the first study to show a homeoviscous response to higher temperatures in an Antarctic fish, although for only one of the two species examined.

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          The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment.

          It is clear from the literature reviewed that modifications in membrane lipid composition play a major role in the adaptation of diverse organisms to specific environments and physiological circumstances. Acyl chain and molecular species restructuring in phospholipids are the most ubiquitous adaptations to environmental insult, being implicated in membrane adjustments to temperature, pressure, water activity, pH and salinity. In contrast, other adaptations (e.g. modulation of anionic phospholipids (salinity adaptation), trehalose content (dehydration) and the PC/PE ratio (temperature acclimation] appear to be more context specific. Although the volume of correlative data relating membrane composition to environmental state is impressive, several questions must be explicitly addressed in future research if a mechanistic understanding of the role of lipids in fine tuning membrane function is to be achieved. These include: (1) Adaptation thresholds--How much environmental variation is required before an acclimatory response is initiated, and is the extent of membrane perturbation induced by such minimally effective stimuli similar for different stress vectors? Interspecific comparisons of the Na+/K(+)-ATPase of fish collected at different depths indicate that species must be separated in depth by a distance corresponding to a pressure difference of 20 MPa before pressure adaptation is evident. Assuming a dT/dP value of 0.23 (Table 1), a 20 MPa change in pressure corresponds to ca. a 5 degrees C change in temperature, which agrees well with the minimal temperature change required to elicit changes in the lipid composition of plasma membranes in kidney tissue of thermally-acclimating trout. A pressure of 20 MPa also corresponds approximately to the maximum depth from which deep sea animals survive being brought to the surface. Collectively, these observations suggest that the minimally effective stimuli for both temperature and pressure adaptation are similar. Comparable data are not available for other environmental variables. (2) Signal transduction--What signals are being sensed and how are they transduced into an adaptational response? In some cases, it is clear that the enzymes of lipid metabolism respond directly (either by a variation in catalytic rate or substrate preference) to variations in the physical environment in an apparently adaptive manner (e.g. refer Sections VI.A.1 and VI.B.2). It seems unlikely, however, that such direct effects can explain the totality of the adaptive capacity of organisms, especially given the evidence for the induction of desaturase synthesis in cold adaptation (refer to Section VI.A.2).(ABSTRACT TRUNCATED AT 400 WORDS)
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            Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view.

            A cause and effect understanding of thermal limitation and adaptation at various levels of biological organization is crucial in the elaboration of how the Antarctic climate has shaped the functional properties of extant Antarctic fauna. At the same time, this understanding requires an integrative view of how the various levels of biological organization may be intertwined. At all levels analysed, the functional specialization to permanently low temperatures implies reduced tolerance of high temperatures, as a trade-off. Maintenance of membrane fluidity, enzyme kinetic properties (Km and k(cat)) and protein structural flexibility in the cold supports metabolic flux and regulation as well as cellular functioning overall. Gene expression patterns and, even more so, loss of genetic information, especially for myoglobin (Mb) and haemoglobin (Hb) in notothenioid fishes, reflect the specialization of Antarctic organisms to a narrow range of low temperatures. The loss of Mb and Hb in icefish, together with enhanced lipid membrane densities (e.g. higher concentrations of mitochondria), becomes explicable by the exploitation of high oxygen solubility at low metabolic rates in the cold, where an enhanced fraction of oxygen supply occurs through diffusive oxygen flux. Conversely, limited oxygen supply to tissues upon warming is an early cause of functional limitation. Low standard metabolic rates may be linked to extreme stenothermy. The evolutionary forces causing low metabolic rates as a uniform character of life in Antarctic ectothermal animals may be linked to the requirement for high energetic efficiency as required to support higher organismic functioning in the cold. This requirement may result from partial compensation for the thermal limitation of growth, while other functions like hatching, development, reproduction and ageing are largely delayed. As a perspective, the integrative approach suggests that the patterns of oxygen- and capacity-limited thermal tolerance are linked, on one hand, with the capacity and design of molecules and membranes, and, on the other hand, with life-history consequences and lifestyles typically seen in the permanent cold. Future research needs to address the detailed aspects of these interrelationships.
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              Anthropogenic impacts on marine ecosystems in Antarctica.

              Antarctica is the most isolated continent on Earth, but it has not escaped the negative impacts of human activity. The unique marine ecosystems of Antarctica and their endemic faunas are affected on local and regional scales by overharvesting, pollution, and the introduction of alien species. Global climate change is also having deleterious impacts: rising sea temperatures and ocean acidification already threaten benthic and pelagic food webs. The Antarctic Treaty System can address local- to regional-scale impacts, but it does not have purview over the global problems that impinge on Antarctica, such as emissions of greenhouse gases. Failure to address human impacts simultaneously at all scales will lead to the degradation of Antarctic marine ecosystems and the homogenization of their composition, structure, and processes with marine ecosystems elsewhere. © 2011 New York Academy of Sciences.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                18 May 2018
                2018
                : 6
                : e4765
                Affiliations
                [1 ] Department of Wine, Food and Molecular Biosciences, Faculty of Agriculture and Life Sciences, Lincoln University , Christchurch, New Zealand
                [2 ] Department of Ecology, Faculty of Agriculture and Life Sciences, Lincoln University , Christchurch, New Zealand
                [3 ] Department of Agricultural Sciences, Faculty of Agriculture and Life Sciences, Lincoln University , Christchurch, New Zealand
                [4 ] Office of the Prime Minister’s Chief Science Advisor, University of Auckland , Auckland, New Zealand
                Author information
                http://orcid.org/0000-0001-9645-5568
                http://orcid.org/0000-0001-6933-5253
                Article
                4765
                10.7717/peerj.4765
                5961637
                29796342
                cd37cdd9-aa4d-41b2-b727-6f0c950e0dd3
                © 2018 Malekar et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 30 January 2018
                : 23 April 2018
                Funding
                Funded by: Antarctica New Zealand
                Funded by: Lincoln University New Zealand
                The field study for this experiment was supported by Antarctica New Zealand. Funding for biochemical analysis and paper writing was supported by Lincoln University New Zealand. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Aquaculture, Fisheries and Fish Science
                Biochemistry
                Marine Biology
                Aquatic and Marine Chemistry
                Environmental Impacts

                membrane remodelling,climate change,homeoviscous adaptation,antarctic fish,notothenioids,phospholipids,membrane fluidity,temperature acclimation,thermal adaptation,lipid saturation

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