The cutaneous lipid composition of bat wing and tail membranes: a case of convergent evolution with birds (original) (raw)
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Cutaneous water loss and lipids of the stratum corneum in two syntopic species of bats
The lipid matrix of the stratum corneum (SC), the outer layer of the epidermis of mammals and birds, constitutes the barrier to diffusion of water vapor through the skin. The lipids of the SC are structured in the intercellular spaces of the mammalian epidermis in ordered layers, called lamellae, which have been postulated to prevent water loss. Lipids in the mammalian SC are mainly cholesterol, free fatty acids and ceramides, the latter forming the structural support for the lamellae. However, knowledge on how the lipid composition of the SC alters cutaneous water loss (CWL) in mammals is rudimentary, and is largely derived from studies on laboratory animals and humans. We measured CWL of individuals of two species of syntopic bats, Tadarida brasiliensis and Myotis velifer. In the first study of its kind on wild mammals, we correlated CWL with the lipid composition of the SC, measured using thin layer chromatography and high performance liquid chromatography coupled with atmospheric pressure photoionization mass spectrometry. Surface-specific CWL was 20.6% higher in M. velifer than in T. brasiliensis, although differences were not significant. Compared with individuals of M. velifer, individuals of T. brasiliensis had more classes, and a higher proportion, of polar ceramides in the SC, a feature associated with lower CWL. Individuals of T. brasiliensis also had a class of nonpolar ceramides that presumably spans the lamellae and gives more cohesiveness to the lipid matrix of the SC. We conclude that qualitative and quantitative modifications of the lipid composition of the SC contribute to regulate CWL of these two species of bats.
Organization of lipids in avian stratum corneum: Changes with temperature and hydration
Chemistry and Physics of Lipids, 2016
In response to increases in ambient temperature (T a), many animals increase total evaporative water loss (TEWL) through their skin and respiratory passages to maintain a constant body temperature, a response that compromises water balance. In birds, cutaneous water loss (CWL) accounts for approximately 65% of TEWL at thermoneutral temperatures. Although the proportion of TEWL accounted for by CWL decreases to only 25% at high T a , the magnitude of CWL still increases, suggesting changes in the barrier function of the skin. The stratum corneum (SC) is composed of flat, dead cells called corneocytes embedded in a matrix of lipids, many of which arrange in layers called lamellae. The classes of lipids that comprise these lamellae, and their attendant physical properties, determine the rate of CWL. We measured CWL at 25, 30, 35, and 40 C in House Sparrows (Passer domesticus) caught in the winter and summer, and in sparrows acclimated to warm and cold lab environments. We then used Fourier transform infrared spectroscopy to measure lipid-lipid and lipid-water interactions in the SC under different conditions of temperature and hydration, and correlated these results with lipid classes in the SC. As CWL increased at higher temperatures, the amount of gauche defects in lipid alkyl chains increased, indicating that lipid disorder is partially responsible for higher CWL at high temperatures. However, variation in CWL between groups could not be explained by the amount of gauche defects, and this remaining variation may be attributed to greater amounts of cerebrosides in birds with low CWL, as the sugar moieties of cerebrosides lie outside lipid lamellae and form strong hydrogen bonds with water molecules. 2015 Elsevier Ireland Ltd. All rights reserved.
Lipid composition of the stratum corneum and cutaneous water loss in birds along an aridity gradient
The Journal of experimental biology, 2012
Intercellular and covalently bound lipids within the stratum corneum (SC), the outermost layer of the epidermis, are the primary barrier to cutaneous water loss (CWL) in birds. We compared CWL and intercellular SC lipid composition in 20 species of birds from desert and mesic environments. Furthermore, we compared covalently bound lipids with CWL and intercellular lipids in the lark family (Alaudidae). We found that CWL increases in birds from more mesic environments, and this increase was related to changes in intercellular SC lipid composition. The most consistent pattern that emerged was a decrease in the relative amount of cerebrosides as CWL increased, a pattern that is counterintuitive based on studies of mammals with Gaucher disease. Although covalently bound lipids in larks did not correlate with CWL, we found that covalently bound cerebrosides correlated positively with intercellular cerebrosides and intercellular cholesterol ester, and intercellular cerebrosides correlated...
The Journal of experimental biology, 2015
The outermost 10-20 µm of the epidermis, the stratum corneum (SC), consists of flat, dead cells embedded in a matrix of intercellular lipids. These lipids regulate cutaneous water loss (CWL), which accounts for over half of total water loss in birds. However, the mechanisms by which lipids are able to regulate CWL and how these mechanisms change with depth in the SC are poorly understood. We used attenuated total reflectance Fourier transform infrared spectroscopy (ATR-FTIR) to measure lipid-lipid and lipid-water interactions as a function of depth in the SC of house sparrows (Passer domesticus Linnaeus) in the winter and summer. We then compared these molecular interactions at each depth with lipid composition at the same depth. We found that in both groups, water content increased with depth in the SC, and likely contributed to greater numbers of gauche defects in lipids in deeper levels of the SC. In winter-caught birds, which had lower rates of CWL than summer-caught birds, wate...
Presence and persistence of a highly ordered lipid phase state in the avian stratum corneum
The Journal of experimental biology, 2018
To survive high temperatures in a terrestrial environment, animals must effectively balance evaporative heat loss and water conservation. In passerine birds, cutaneous water loss (CWL) is the primary avenue of water loss at thermoneutral temperatures, and increases slightly as ambient temperature increases, indicating a change in the permeability of the skin. In the stratum corneum (SC), the outermost layer of skin, lipids arranged in layers called lamellae serve as the primary barrier to CWL in birds. The permeability of these lamellae depends in large part on the ability of lipid molecules to pack closely together in an ordered orthorhombic phase state. However, as temperature increases, lipids of the SC become more disordered, and may pack in more permeable hexagonal or liquid crystalline phase states. In this study, we used Fourier transform infrared spectroscopy to monitor the phase state of lipids in the SC of house sparrows () at skin temperatures ranging from 25 to 50°C. As ...
Journal of …, 2008
Because cutaneous water loss (CWL) represents half of total water loss in birds, selection to reduce CWL may be strong in desert birds. We previously found that CWL of house sparrows from a desert population was about 25% lower than that of individuals from a mesic environment. The stratum corneum (SC), the outer layer of the epidermis, serves as the primary barrier to water vapor diffusion through the skin. The avian SC is formed by layers of corneocytes embedded in a lipid matrix consisting of cholesterol, free fatty acids and two classes of sphingolipids, ceramides and cerebrosides. The SC of birds also serves a thermoregulatory function; high rates of CWL keep body temperatures under lethal limits in episodes of heat stress.
Journal of Experimental …, 2008
Because cutaneous water loss (CWL) represents half of total water loss in birds, selection to reduce CWL may be strong in desert birds. We previously found that CWL of house sparrows from a desert population was about 25% lower than that of individuals from a mesic environment. The stratum corneum (SC), the outer layer of the epidermis, serves as the primary barrier to water vapor diffusion through the skin. The avian SC is formed by layers of corneocytes embedded in a lipid matrix consisting of cholesterol, free fatty acids and two classes of sphingolipids, ceramides and cerebrosides. The SC of birds also serves a thermoregulatory function; high rates of CWL keep body temperatures under lethal limits in episodes of heat stress.
Avian Epidermal Lipids: Functional Considerations and Relationship to Feathering1
American Zoologist, 2000
The avian epidermis is composed of unique sebokeratinocytes that elaborate and secrete sebum-like lipids as they cornify. In addition to the lipid droplets, the avian epidermis elaborates, but rarely secretes, lipid-enriched organelles, the multigranular bodies. The multigranular bodies are analogous to the lamellar bodies of mammals (Menon et al., 1991), the secretion of which results in formation of occlusive lipid bilayers characteristic of mammalian stratum corneum and providing the permeability barrier. However, in contrast to mammals, the avian multigranular bodies form the reserve barrier mechanism. In the basal state, when multigranular bodies are not secreted, the avian cutaneous barrier is deficient, but allows evaporative cooling for thermoregulation. However, under conditions of water deficit, multigranular body secretion allows for rapid facultative waterproofing, as shown in zebra finches (Taenyopygia guttata). In certain glabrous regions of the skin, such as the maxillary rictus, interdigital web, and combs and wattles in the domestic fowl, there is a high degree of epidermal lipid secretion. Also specialized feathers such as powder downs elaborate lipid rich material, which can be classified as secretion. Additionally, an inverse relation between epidermal lipogenesis and the degree of feathering has been demonstrated, as in temporarily bare areas (e.g., brood patches) and following permanent feather loss from the head accompanying attainment of maturity in certain ibises and storks. In the latter, the neo-apteria often hold large reserves of carotenoids dissolved in the lipid droplets, possibly related to an altered gradient of retinoids influencing feather morphogenesis. Unusual secondary functions of epidermal lipids include cosmetic coloration (e.g., in the Japanese Crested Ibis) and chemical defense (e.g., in the Pitohui).
Fatty Acid Methyl Ester Profiles of Bat Wing Surface Lipids
Lipids, 2014
Sebocytes are specialized epithelial cells that rupture to secrete sebaceous lipids (sebum) across the mammalian integument. Sebum protects the integument from UV radiation, and maintains host microbial communities among other functions. Native glandular sebum is composed primarily of triacylglycerides (TAG) and wax esters (WE). Upon secretion (mature sebum), these lipids combine with minor cellular membrane components comprising total surface lipids. TAG and WE are further cleaved to smaller molecules through oxidation or host enzymatic digestion, resulting in a complex mixture of glycerolipids (e.g., TAG), sterols, unesterified fatty acids (FFA), WE, cholesteryl esters, and squalene comprising surface lipid. We are interested if fatty acid methyl ester (FAME) profiling of bat surface lipid could predict species specificity to the cutaneous fungal disease, white nose syndrome (WNS). We collected sebaceous secretions from 13 bat spp. using Sebutape Ò and converted them to FAME with an acid catalyzed transesterification. We found that Sebutape Ò adhesive patches removed *69 more total lipid than Sebutape Ò indicator strips. Juvenile eastern red bats (Lasiurus borealis) had significantly higher 18:1 than adults, but 14:0, 16:1, and 20:0 were higher in adults. FAME profiles among several bat species were similar. We concluded that bat surface lipid FAME profiling does not provide a robust model predicting species susceptibility to WNS. However, these results provide baseline data that can be used for lipid roles in future ecological studies, such as life history, diet, or migration.
Chemistry and physics of lipids, 2017
The outermost layer of skin, the stratum corneum (SC), contains a complex mixture of lipids, which controls the rate of cutaneous water loss (CWL) in reptiles, mammals, and birds. However, the molecular structure of SC lipids and how molecular configurations influence CWL is poorly understood. Here, the organization and structure of SC lipids extracted from birds were investigated by means of Langmuir films. Properties of lipids from the SC of arid and semi-arid adapted larks, known to have a low CWL, were compared with lipids extracted from the SC of mesic lark species with higher CWL to gain insight into how structure impacts CWL. Film properties were probed with surface pressure-area isotherms, Brewster angle microscopy (BAM), and vibrational sum frequency generation (VSFG). Results indicate organization and ordering of SC lipids in the arid-adapted hoopoe lark was vastly different from all other species, forming a miscible, rigid monolayer, whereas monolayers from semi-arid and ...