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      Specific regulations of gill membrane fatty acids in response to environmental variability reveal fitness differences between two suspension-feeding bivalves ( Nodipecten subnodosus and Spondylus crassisquama)

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          Abstract

          Lay summary

          Gill membrane lipids of two bivalves presented specific regulations in response to both environmental and dietary resource variabilities. This highlights the importance of considering both trophic and physiological processes when studying responses to environmental stressors; an approach that can be defined as ‘trophic ecophysiology’.

          Abstract

          Bivalves’ physiological functions (i.e. growth, reproduction) are influenced by environmental variability that can be concomitant with trophic resource variations in terms of quality and quantity. Among the essential molecules that bivalves need to acquire from their diet to maintain physiological functions, fatty acids (FAs) such as polyunsaturated fatty acids (e.g. 20:4n-6 (arachidonic acid), 20:5n-3 (eicosapentaenoic acid) and 22:6n-3 (docosahexaenoic acid)) have been described to play a critical role. The present study examined the FA composition of gill membrane lipids of two bivalve species, Nodipecten subnodosus and Spondylus crassisquama, sampled in a coastal lagoon of the Northeastern Pacific (Ojo de Liebre, Mexico), at two contrasting locations (inner versus outer part of the lagoon) and at two different periods (February and August 2016). Spatiotemporal variations showed that FA composition of gill membrane lipids was highly correlated to FA composition of reserve lipids from digestive gland. This highlights the marked impact of the diet on FA composition of gill membranes. Interestingly, both species presented differences in the seasonal accumulations of plasmalogens and of particular FA that are not found in their diet (e.g. non-methylene interrupted FA, 22:4n-9 trans, 20:1n-11), suggesting specific regulations of FA incorporation and lipid class composition in gill membranes to maintain optimal membrane function in their specific and changing environment. This study highlights the importance to characterize the spatial and temporal variability of food resources in order to apprehend the physiological consequences of environmental variability, as well as species differential regulation capacities in a changing world.

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          Most cited references47

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          Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?

          J R Hazel (1995)
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            Plasmalogens: biosynthesis and functions.

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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2020
                25 August 2020
                25 August 2020
                : 8
                : 1
                : coaa079
                Affiliations
                [1 ] Univ Brest, CNRS, IRD, Ifremer, LEMAR, IUEM , F-29280, Plouzane, France
                [2 ] WasserCluster Lunz—Inter-University Centre for Aquatic Ecosystem Research , Dr. Carl Kupelwieser Promenade 5, A-3293, Lunz am See, Austria
                [3 ] Centro de Investigaciones Biológicas del Noroeste (CIBNOR) , La Paz, BCS, Mexico
                Author notes
                Corresponding author: WasserCluster Lunz—Inter-University Centre for Aquatic Ecosystem Research, Dr. Carl Kupelwieser Promenade 5, A-3293, Lunz am See, Austria. Email: m.mathieuresuge@ 123456gmail.com
                Article
                coaa079
                10.1093/conphys/coaa079
                7447844
                32864137
                00da417c-d267-4072-b88a-60c063bdf108
                © The Author(s) 2020. Published by Oxford University Press and the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 November 2019
                : 15 May 2020
                : 11 August 2020
                : 31 July 2020
                Page count
                Pages: 14
                Funding
                Funded by: funder-nameFrench government under the program ‘Investissements d’Avenir’, and two ‘Mission Longue Durée’ received by Edouard Kraffe in CIBNOR from the Institut de Recherche pour le Développement;
                Funded by: funder-name296397;
                Funded by: funder-nameConacyt-Foins;
                Funded by: funder-nameLaboratoire d’Excellence’ LabexMER;
                Award ID: ANR-10-LABX-19
                Funded by: funder-nameEvaluation orientation de la Coopération Scientifique–Asociación Nacional de Universidades e Instituciones de Educación Superior (ECOS-ANUIES) program;
                Award ID: 262983
                Categories
                AcademicSubjects/SCI00840
                Research Article

                bivalves,coastal lagoon,gill membrane fatty acids,diet influence,physiological regulation,trophic ecophysiology

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