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Velansky, P. Lipidomics of Marine Invertebrates. Encyclopedia. Available online: https://encyclopedia.pub/entry/17315 (accessed on 27 July 2024).
Velansky P. Lipidomics of Marine Invertebrates. Encyclopedia. Available at: https://encyclopedia.pub/entry/17315. Accessed July 27, 2024.
Velansky, Peter. "Lipidomics of Marine Invertebrates" Encyclopedia, https://encyclopedia.pub/entry/17315 (accessed July 27, 2024).
Velansky, P. (2021, December 20). Lipidomics of Marine Invertebrates. In Encyclopedia. https://encyclopedia.pub/entry/17315
Velansky, Peter. "Lipidomics of Marine Invertebrates." Encyclopedia. Web. 20 December, 2021.
Lipidomics of Marine Invertebrates
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This entry is adapted from the peer-reviewed paper 10.3390/md19120660

Marine invertebrates are a paraphyletic group that comprises more than 90% of all marine animal species. Lipids form the structural basis of cell membranes, are utilized as an energy reserve by all marine invertebrates, and are, therefore, considered important indicators of their ecology and biochemistry. The nutritional value of commercial invertebrates directly depends on their lipid composition. The lipid classes and fatty acids of marine invertebrates have been studied in detail, but data on their lipidomes (the profiles of all lipid molecules) remain very limited. To date, lipidomes or their parts are known only for a few species of mollusks, coral polyps, ascidians, jellyfish, sea anemones, sponges, sea stars, sea urchins, sea cucumbers, crabs, copepods, shrimp, and squid.

fatty acids lipid molecular species mass spectrometry lipidomics Invertebrates

1. Introduction

Invertebrates have not been recognized as an actual taxon since this group includes all animals that do not have a spine and that were placed in it by the so-called residual principle. This is a classic example of a paraphyletic group. According to modern concepts, the animals attributed by Lamarck to invertebrates are divided into more than twenty equivalent groups of a higher rank, phyla. Furthermore, there are numerous departments of invertebrate zoology, and the term “invertebrates” currently indicates the professional specialization of zoologists. The group of marine invertebrates comprises more than 90% of all marine animal species [1].
Lipids are among the most important organic compounds found in all marine invertebrates. Lipids form the structural basis of cell membranes, are utilized as an energy reserve by these animals, and are, therefore, used as important indicators of their ecology and biochemistry. Lipids are relatively small hydrophobic molecules and are highly diverse in their structure. There are several definitions of “lipids”, but we focus mainly on fatty acids (FAs) and lipids with fatty acyl groups such as wax esters (WEs), triacylglycerols (TGs), monoalkyldiacylglycerols or diacylglycerol ethers (DAGEs), glycerophospholipids (GPLs), and sphingolipids.
Due to the rapid development of thin-layer chromatography, gas chromatography on capillary columns coupled with mass spectrometric detectors, high-resolution nuclear magnetic resonance, and preparative high-performance liquid chromatography, detailed information on the lipid class composition and FA composition of total lipids/lipid classes of marine invertebrates has become increasingly available, not only for the order/family level but also for the genus/species level. However, this classic lipidology deals with integral FA and lipid data because each lipid class consists of hundreds of lipid molecules, and total FAs are obtained through hydrolysis of thousands of lipid molecules.
Lipid molecules of certain types are often referred to as “lipid molecular species”; the term “lipidome” describes the complete lipid profile of an organism, and the studies in lipidomics consider the structure, function, interaction, and dynamics of lipid molecular species [2]. The field of lipidomics was first defined in 2003 [3] through integrating the defined chemical properties in individual lipid molecules with a comprehensive approach based on mass spectrometry.
The development of high-performance liquid chromatography and mass spectrometry has made it possible to analyze molecular species of lipids without any sample preparation. There are two main approaches to lipidome analysis: untargeted and targeted. Untargeted lipidomics implies the determination of the complete lipid profile using high-resolution mass spectrometers, including those without chromatographic separation (shotgun lipidomics). Targeted lipidomics focuses on the precise quantification of specific lipid molecules. In this case, sensitive high-speed mass spectrometers (triple quadrupole or quadrupole linear-ion trap) are usually used in the multiple-reaction monitoring mode.
During the period covered by this review, new equipment and methods have appeared that allow lipidomic studies to be carried out at a higher level. In 2005, mass spectrometers with a new type of high-resolution analyzer (Orbitrap) have become commercially available. Since 2006, ion-mobility mass spectrometers have become available, designed for better analysis of small molecules through separation based on the conformation of a molecule in addition to its mass. New methods that allow the determination of double-bond positions in specific FAs at a specific sn-position using MS with ozone-induced dissociation (OzID or O3-MS) [4][5] have appeared.
Compared to classical lipidology, the lipidomic approach provides more information about the lipid composition (distribution and sn-position in the glycerol backbone of acyl, alkyl, and alkenyl groups) and allows for more accurate quantitative analysis. Thus, the researcher receives a much larger amount of data that can be used to solve a wide range of problems in the study of invertebrates: lipid biosynthesis pathways determination, chemotaxonomy, determination of biotic and abiotic factors effects, investigation of embryogenesis, ontogenesis, and food chains.
In contrast to FAs and lipid classes, lipid molecular species profiles of marine invertebrates still remain very poorly understood. However, the number of publications on lipidomics of these marine animals showed an explosive increase over the past five years (Figure 1). This review highlights the progress in lipidomics of marine invertebrates for the period of 2004–2021.
Marinedrugs 19 00660 g001
Figure 1. Dynamics of publications on lipidomics of marine invertebrates.

2. Lipidomic Data

Since the early 1950s, the contents of total lipids and lipid classes, as well as the FA composition of total, non-polar (storage), and polar (structural) lipids of marine invertebrates have been examined by a large number of laboratories across the world. In some cases, FA composition of certain lipid classes has been analyzed. As a result, a general concept of distribution of lipid classes and FA over these animals, from genera to phyla, has been formed. At the beginning of lipidomic studies, several intermediate investigations analyzed the FA composition of each lipid class but not their actual molecular species profiles [6][7][8]. Currently, many studies deal with the polar part of lipidomes (mainly GPL); however, some works have already presented total lipidomes [9][10][11][12]. In this part, we have attempted to characterize the major lipid molecular species and their chemotaxonomic distribution in the marine invertebrates studied.
In marine invertebrates, the major non-polar lipid classes are TG, WE, and DAGE. The major polar lipid classes are phospholipids: PC, PE, PS, and PI. Accordingly, these four GPL classes contain choline, ethanolamine, serine, and inositol groups in the polar head of their molecules. Depending on the groups at sn-1 and sn-2 positions of the glycerol backbone, each GPL class can contain three forms (or subclasses): 1,2-diacyl, 1-O-alkyl-2-acyl (plasmanyl), and 1-O-(alk-1′-enyl)-2-acyl (plasmenyl, PlsGPL). After the name of ether moiety (number of carbon atoms: number of double bonds) at sn-1 position, the letter “a” indicates 1-O-alkyl group, and the letter “p” indicates 1-O-(alk-1′-enyl) group. In addition to GPL, ceramide aminoethylphosphonate (CAEP), a sphingosine-based phosphonolipid, is one of the major structural lipids in marine invertebrates.

2.1. Mollusca

In mollusks, PC is the most abundant GPL class, followed by PE. Up to 290 molecular species of polar lipids (PL) and up to 1200 molecular species of total lipids (TL) can be found in oysters Crassostrea and Ostrea [13][14][15][16][17][18][19]. The most abundant molecular species of oyster GPL have the diacyl form and contain saturated FAs (mainly 16:0 and 18:0) at the sn-1 position and polyunsaturated FAs (mainly, 20:5n-3 and 22:6n-3) at the sn-2 position of the glycerol backbone. For example, PC 16:0/20:5, PC 16:0/22:6, PE 16:0/20:5, PE 18:0/20:5, PS 18:0/20:5, and PI 18:0/22:6 are the most abundant species of diacyl GPL in C. plicatula [14]. Among alkylacyl-GPL, PC 16:0a/22:6, PE 18:0a/20:5, and PS 18:0a/22:2 are the dominant molecular species. The molecules with 18:0p/22:6 and 18:0p/22:2 may dominate the alkenylacyl-GPL, PE, and PS, respectively. The molecules with non-methylene-interrupted (NMI) FAs such as PS 18:0p/22:2, PS 20:0p/20:2, and PS 16:0p/22:2 are also observed in C. gigas [18]. The non-polar part of the oyster lipidome has not been analyzed.
About 410 molecules in TL [20], 230 molecules of PL [21], and 40 molecules of TG [22] have been identified in mussels of the genus Mytilus. All major ethanolamine GPL recognized in mussel lipids are plasmalogens with the 18:0 chain dominating these ether PL [19][23]. Besides 20:5n-3 and 22:6n-3, an abundance of NMI acyl chains has been found in mussel alkenylacyl-PE [24][21]. Similar to oyster lipids, the PC of mussels is mainly composed of diacylic molecular species, with the 20:5n-3 and 22:6n-3 chains prevailing at the sn-2 position of glycerol [24]. However, Wang et al. [18] detected 33, 54, and 63% of the alkenylacyl form in the PC, PE, and PS of M. edulis, respectively. A high abundance of NMI fatty acids, like that of the 20:2 and 22:2 ones, is found in alkenylacyl-PS [18]. Polar lipidomes of adult and juvenile M. edulis are similar; cardiolipin (CL) and their tetradocosahexaenoic molecular species (CL 88:24) have additionally been recorded from juveniles [22]. Acyl chains of TG molecules in juveniles of M. edulis contain up to 62 carbon atoms and up to 15 double bonds [22].
The lipidome of the blue mussel M. galloprovincialis has been intensively investigated. In a general analysis, 14 WE, 34 TG, 41 PC, 23 PE, 4 PS, 6 PI, and 10 CAEP molecular species were detected in the total lipids of this animal [23]. However, direct analyses of PL allowed a detailed description of 185 choline GPL, 131 ethanolamine GPL, 45 lysoPE, 57 lysoPC, 33 CAEP, 14 N-monomethylated CAEP, and 19 CPE (ceramide phosphoethanolamines) molecules [25][24][26]. Mussels of this species are well known to contain at least four classes of ceramide lipids (CAEP, N-Me-CAEP, N-diMe-CAEP, and CPE), but only a few studies describe the variety of bivalve ceramide molecular species [25]. Trace amounts of unusual diacyl choline and ethanolamine phosphonolipids have been found, which lack the oxygen atom between the phosphorus atom and choline or ethanolamine groups [23][24]. Another interesting acyl chain found at the sn-2 position of alkenylacyl-PE is 28:8 [24].

2.2. Cnidaria

Many cnidarian species contain symbiotic dinoflagellates (SD, microalgae of the family Symbiodiniaceae). It is obvious that the total lipidome of such cnidarians consists of both invertebrate animal lipids (WE, DAGE, GPL, and CAEP) and microalgae lipids (glycolipids and betaine lipids). Total TGs of symbiotic cnidarians are a mixture of TG molecules that originate from symbionts and the host. Up to 450 molecules have been identified in the TL of cnidarians.
WE is an abundant storage lipid class in cnidarians. A comparison between WE profiles of three coral groups (symbiotic reef-building corals, symbiotic alcyonarians, and asymbiotic gorgonians) has shown cetylpalmitate (16:0/16:0) to be a major component in all the corals [27]. Other saturated WEs contain 30, 34, and 36 carbon atoms. More than 80% of saturated molecular species are found in the WEs of the reef-building coral A. cerealis [28]. In general, the unsaturated WE content (16:0/16:1, 16:0/18:1, and 16:0/20:1) of alcyonarians is higher than that of reef-building corals [27]. In contrast to symbiotic coral species, asymbiotic gorgonians contain a noticeable amount of long-chain WE molecular species (C37–C41) with an odd number of carbon atoms [27]. Dienoic WEs (16:2/16:0, 16:0/16:2, 18:0/16:2, 16:0/18:2, 18:0/18:2, 16:2/20:0, and 18:0/18:2) are among the dominant WE molecular species in the alcyonarian Sinularia sp. [9]. As reported, dienoic molecules are absent from the WEs of the alcyonarian S. siaesensis [11]. Only 17% of WEs are comprised of mono- and dienoic molecules in the zoantharian Palythoa sp. [12].

2.4. Echinodermata

Different animal tissues and extraction methods have been applied by different researchers in their studies of echinoderm lipidomes. Kostetsky et al. [29] used the classic Folch’s method [30] of extraction from fresh whole starfish, the intestinal tracts of sea urchins, and the muscular sacs of sea cucumbers collected by divers. Omran et al. [31] extracted the body walls of sea cucumbers with ethanol. Wang et al. [32] purchased dried sea cucumbers from a free market and carried out extraction according to Bligh and Dyer [33]. Therefore, these lipidomic data are quite heterogeneous.
Kostetsky et al. [29] described the composition of PE and PC molecular species in echinoderms from the Sea of Japan and showed that alkylacyl-PC and alkenylacyl-PE are the dominant forms, except for the sea urchin S. intermedius that contains 63% diacyl-PE, 7% alkylacyl-PE, and 30% alkenylacyl-PE. In the muscle tissues of echinoderms, the major PC molecular species are 18:1a/20:5, 16:0a/20:5, 18:0a/20:5, 18:1/20:5, 18:0/20:5, 20:1/20:5, and 16:0/20:5. The positional distribution of acyl groups (at sn-1/sn-2) in the PC molecules of starfish is characterized by the highest SFA/PUFA content, while sea cucumbers have the highest MUFA/PUFA content. The major PE molecules are 18:0p/20:4, 18:0p/20:5, 18:0a/20:5, 18:0/20:4, 18:0/20:5, 18:1/20:5, and 20:1/20:5. The molecular species of PE contain 63.4–84.3% SFA/PUFA and 11.9–33.4% MUFA/PUFA.

2.5. Porifera

The study of the sea sponge A. queenslandica (= Reniera sp.) [34] is considered “lipidomic” but deals with total FA and sterol profile and does not analyze lipid molecular species. However, the general approach to achieving the objectives of this study is consistent with the goal and principles of lipidomics, since an attempt is made to establish a link between the profile of lipid molecules and the presence of genes encoding enzymes for the synthesis of these lipids. Sponges are animals, but they host dense communities of microbial symbionts. Therefore, it is unclear which FAs can be synthesized by the animal de novo, and which require input from the microbial community. Similar to ghd FA profiles of other demosponges, that of A. queenslandica is dominated by SFAs and “demospongic” Δ5,9 VLCFA [29]. The genetic and FA repertoires of A. queenslandica are compared to identify which FA could be potentially synthesized and/or modified by the sponge. As regards SFA, no evidence has been found for the required fatty acid synthase-type enzyme in A. queenslandica, either the animal homolog (FASN) or the equivalent enzymes in fungi (Fas1/Fas2) or bacteria (fas). This sponge also appears to lack the enzyme necessary to synthesize the branched-chain FAs. However, A. queenslandica does contain some enzymes necessary for the downstream FA elongation. Additionally, Δ4-, Δ5-, Δ6-, and Δ9-like desaturases are present, while the sponge lacks Δ12 and Δ15 desaturases. It has been supposed that A. queenslandica cannot produce basic SFA de novo, but it should be able to modify certain FAs into the more complex Δ5,9 VLCFA [34].

3. Conclusions

Over the past six years, the number of publications with lipidomics applied in the study of marine invertebrates has increased dramatically, thus indicating a surge of interest in this research area. The rapid development of lipidomic techniques allows reliable identification and quantification of all lipid molecular species in marine invertebrates. The fundamental characteristics of lipidomes in some of the taxonomic groups of marine invertebrate animals are now beginning to be understood, but the number of the species studied still remains very small. Most studies were carried out on commercially exploited species. Today, lipidomic studies are based mainly on traditional lipid techniques applied to address traditional research issues such as the description of lipid composition, chemotaxonomy of marine invertebrates, seasonal variations in FAs and lipids, FA trophic markers in marine food webs, effects of environmental factors, etc. It is advisable to carry out analyses of FAs, lipid class, and the lipidome simultaneously. Close attention should be paid to the relationship between the lipidome/FAs and lipid biosynthesis pathways. It is necessary to extend the range of applications of lipidomics and develop a new robust lipidomic methodology that will not only complement traditional methods, but also bring lipidomics to a qualitatively higher level in the traditional areas of marine invertebrate research.

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