Perivitellins

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Perivitellins are egg proteins found in the perivitelline fluid of many gastropods. They are multifunctional complexes providing the developing embryo with nutrition, protection from the environment, and defense against predators. [1]

Contents

Despite the central role perivitellins play in reproduction and development, there is little information about their role in gastropod Molluscs. Most studies of perivitellins have been performed in eggs of Ampullaridae, a family of freshwater snails (Caenogastropoda), notably the Pomacea genus, mostly those of Pomacea canaliculata , Pomacea scalaris and Pomacea maculata . [2] [3]

Synthesis

Perivitellins are almost exclusively synthesized in the albumen gland (also known as albumen gland-capsule gland complex or uterine gland), an accessory gland from the female reproductive system of gastropods. [4] [5] This has been experimentally confirmed for the perivitellins ovorubin (PcOvo) and PcPV2, which were only found in the albumen gland with no extra-gland synthesis, circulation or storage. [6] [7] [8] During the reproductive season, these perivitellins are transferred to eggs. After oviposition, they are rapidly restored in the albumen gland, decreasing their total amount in the gland only after repeated ovipositions. [4] [9] In Pomacea canaliculata snails, perivitellins would act, together with the polysaccharide galactogen, as a limiting factor of the reproductive effort during reproduction. [4]

Types of perivitellins

The first studies performed in Pomacea canaliculata identified two proteins named perivitellin-1, PV1 or ovorubin (now called PcOvo) and perivitellin-2 or PV2 massively accumulated in eggs, comprising 60-70% of total protein, respectively, and a heterogeneous fraction dubbed perivitellin-3 or PV3 fraction. [10] Recent proteomic analyses of perivitelline fluids, however, identified a total of 34 proteins from Pomacea canaliculata , 38 in Pomacea maculata, and 32 in Pomacea diffusa . [11] [12] [13] [14]

Perivitellin-1 or PcOvo (former ovorubin) and perivitellin-2 or PcPV2 are probably the best characterized from snails. [5] [8] [10] [15] [16] [17] [18] [19] Both perivitellins are multimeric and glycosylated proteins with remarkable thermal stability up to 100°C and 60°C, respectively, and over a wide range of pH. [20] [21] They are also highly resistant to the combined action of pepsin and trypsin proteases. [17] [18] [21]

The perivitelline fluid of Pomacea scalaris and Pomacea diffusa contain one major perivitellin, PsSC (also named scalarin) and PdPV1, respectively, which are structurally and phylogenetically related to PcOvo. [19] [22] [23] [24] The perivitelline fluid of P. maculata is also similar, with two major perivitellins, PmPV1 and PmPV2, structurally and functionally similar to PcOvo and PcPV2, respectively. [25] [26] [27]

The rest of Pomacea perivitellins (over 25) have been characterized at the transcriptomic and proteomic levels, but biochemical studies are still largely missing. [28]

Perivitellin functions

Perivitellins provide nutrition, energy storage, defense against predation, and protection from the environment to the developing embryo.

A functional classification of the perivitellin aminoacid sequences based on the Kyoto Encyclopedia of Genes and Genomes (KEGG), classified them in "environmental information processing", among which several immune proteins are included, "metabolism", "organismal systems", "cellular processes", "other", and a considerable number of "unknown" proteins.

The first functional studies performed in Pomacea canaliculata , considered them mostly as storage proteins that provided energetic and structural precursors for the embryos, since they are consumed during development. [16]

Later research on PV1s (PcOvo, PmPV1, and PsSC) reported that their carotenoid cofactor, notably astaxanthin, serves as a potent antioxidant and provides the reddish color to the eggs. [1] [20] [25] [29] These carotenoproteins are also highly resistant to gastrointestinal digestion, and withstand the passage through the digestive system without significant modifications; this characteristic was related to embryo defenses, deterring predators by lowering the nutritional value of the eggs. [8] [22] [26] PcOvo and PsSC also carry phosphate groups attached to serine residues that may serve as a phosphorus reserve for the embryo. [19] Unlike PcOvo and PmPV1, PsSC is also an active lectin that agglutinates bacteria and alters the gastrointestinal mucosa of rats, functions associated with embryo protection against both pathogens and predators. [19] [23]

PV2s are toxins only found in Pomacea canaliculata (PcPV2) and Pomacea maculata (PmPV2) perivitelline fluid. [25] [30] [31] They are potent neurotoxins when intraperitoneally injected to mice, while exerting enterotoxic functions when ingested. [27] [30] [32] Each of the two dimeric units of either PcPV2 or PmPV2 consists of a carbohydrate-binding protein of the tachylectin family (acting as a targeting module) disulfide-linked to a pore-forming subunit of the Membrane Attack Complex and Perforin (MACPF) subfamily (toxic module). [18] [27] These toxins bear a structural resemblance to botulinic and ricin heterodimeric toxins, the so-called "AB toxins" previously known only in bacteria and plants. Perivitellin-2 is also resistant to gastrointestinal digestion, which contributes to lowering the egg nutritional value. [18] [32]

Finally, a recent study of Pomacea canaliculata PV3 fraction identified and characterized two protease inhibitors from the Kunitz and Kazal families, a function also related to an antipredator defense since it would prevent predators to digest proteins from the eggs when ingested. [28]

Related Research Articles

<span class="mw-page-title-main">Ampullariidae</span> Family of gastropods

Ampullariidae, whose members are commonly known as apple snails, is a family of large freshwater snails that includes the mystery snail species. They are aquatic gastropod mollusks with a gill and an operculum. These snails simultaneously have a gill and a lung as functional respiratory structures, which are separated by a division of the mantle cavity. This adaptation allows these animals to be amphibious. Species in this family are considered gonochoristic, meaning that each individual organism is either male or female.

<span class="mw-page-title-main">Yolk</span> Part of an egg which feeds the developing embryo

Among animals which produce eggs, the yolk is the nutrient-bearing portion of the egg whose primary function is to supply food for the development of the embryo. Some types of egg contain no yolk, for example because they are laid in situations where the food supply is sufficient or because the embryo develops in the parent's body, which supplies the food, usually through a placenta. Reproductive systems in which the mother's body supplies the embryo directly are said to be matrotrophic; those in which the embryo is supplied by yolk are said to be lecithotrophic. In many species, such as all birds, and most reptiles and insects, the yolk takes the form of a special storage organ constructed in the reproductive tract of the mother. In many other animals, especially very small species such as some fish and invertebrates, the yolk material is not in a special organ, but inside the egg cell.

A trypsin inhibitor (TI) is a protein and a type of serine protease inhibitor (serpin) that reduces the biological activity of trypsin by controlling the activation and catalytic reactions of proteins. Trypsin is an enzyme involved in the breakdown of many different proteins, primarily as part of digestion in humans and other animals such as monogastrics and young ruminants. Serpins – including trypsin inhibitors – are irreversible and suicide substrate-like inhibitors.

The vitelline membrane or vitelline envelope is a structure surrounding the outer surface of the plasma membrane of an ovum or, in some animals, the extracellular yolk and the oolemma. It is composed mostly of protein fibers, with protein receptors needed for sperm binding which, in turn, are bound to sperm plasma membrane receptors. The species-specificity between these receptors contributes to prevention of breeding between different species. It is called zona pellucida in mammals. Between the vitelline membrane and zona pellucida is a fluid-filled perivitelline space.

<span class="mw-page-title-main">Pore-forming toxin</span> Protein-produced toxins that create pores in cell membrane

Pore-forming proteins are usually produced by bacteria, and include a number of protein exotoxins but may also be produced by other organisms such as apple snails that produce perivitellin-2 or earthworms, who produce lysenin. They are frequently cytotoxic, as they create unregulated pores in the membrane of targeted cells.

<i>Pila</i> (gastropod) Genus of gastropods

Pila is a genus of large freshwater snails with an operculum, African and Asian apple snails, aquatic gastropod mollusks in the family Ampullariidae, the apple snails.

<i>Pomacea</i> Genus of gastropods

Pomacea is a genus of freshwater snails with gills and an operculum, aquatic gastropod mollusks in the family Ampullariidae, the apple snails. The genus is native to the Americas; most species in this genus are restricted to South America.

<i>Pomacea canaliculata</i> Species of gastropod

Pomacea canaliculata, commonly known as the golden apple snail or the channeled apple snail, is a species of large freshwater snail with gills and an operculum, an aquatic gastropod mollusc in the family Ampullariidae, the apple snails. South American in origin, this species is considered to be in the top 100 of the "World's Worst Invasive Alien Species". It is also ranked as the 40th worst alien species in Europe and the worst alien species of gastropod in Europe.

<i>Pomacea haustrum</i> Species of gastropod

Pomacea haustrum, common name the titan applesnail, is a species of large freshwater snail with an operculum, an aquatic gastropod mollusk in the family Ampullariidae, the applesnails.

<i>Pomacea paludosa</i> Species of gastropod

Pomacea paludosa, common name the Florida applesnail, is a species of freshwater snail with an operculum, an aquatic gastropod mollusk in the family Ampullariidae, the apple snails.

<span class="mw-page-title-main">AB toxin</span>

The AB toxins are two-component protein complexes secreted by a number of pathogenic bacteria, though there is a pore-forming AB toxin found in the eggs of a snail. They can be classified as Type III toxins because they interfere with internal cell function. They are named AB toxins due to their components: the "A" component is usually the "active" portion, and the "B" component is usually the "binding" portion. The "A" subunit possesses enzyme activity, and is transferred to the host cell following a conformational change in the membrane-bound transport "B" subunit. These proteins consist of two independent polypeptides, which correspond to the A/B subunit moieties. The enzyme component (A) enters the cell through endosomes produced by the oligomeric binding/translocation protein (B), and prevents actin polymerisation through ADP-ribosylation of monomeric G-actin.

<i>Pomacea maculata</i> Species of gastropod

Pomacea maculata is a species of large freshwater snail with an operculum, an aquatic gastropod mollusk in the family Ampullariidae, the apple snails.

<span class="mw-page-title-main">Galactogen</span> Chemical compound

Galactogen is a polysaccharide of galactose that functions as energy storage in pulmonate snails and some Caenogastropoda. This polysaccharide is exclusive of the reproduction and is only found in the albumen gland from the female snail reproductive system and in the perivitelline fluid of eggs.

The perivitellinefluid is an extracellular fluid found in the eggs of most gastropods and constitutes the main source of nutrition and defense for their embryos. It replaces the egg yolk of other animals, which in snail eggs is reduced to non-nutritive proteinaceous granules with putative enzymatic function.

Ovorubin is the most abundant perivitellin of the perivitelline fluid from Pomacea canaliculata snail eggs. This glyco-lipo-caroteno protein complex is a approx. 300 kDa multimer of a combination of multiple copies of six different ~30 kDa subunits.

Pomacea maculata perivitellin-1 (PmPV1) is the most abundant perivitellin found in the perivitelline fluid from Pomacea maculata snail eggs. This glyco-lipo-caroteno protein is an approx. 294 kDa multimer of a combination of multiple copies of six different ~30 kDa subunits. PmPV1 account >60% of the total proteins found in the Pomacea maculata eggs.

Scalarin (PsSC) is the most abundant perivitellin of the perivitelline fluid from Pomacea scalaris eggs. This glyco-lipo-caroteno protein is an approx. 380 kDa multimer combining multiple copies of six different 24-35 kDa subunits.

Perivitellin-2 (PV2) is a pore-forming toxin present in the egg perivitelline fluid of the apple snails Pomacea maculata (PmPV2) and Pomacea canaliculata (PcPV2). This protein, called perivitellin, is massively accumulated in the eggs. As a toxin PV2 protects eggs from predators, but it also nourishes the developing snail embryos.

<span class="mw-page-title-main">Pomacea columellaris</span> Species of snail

Pomacea columellaris is a South American species of freshwater snail in the apple snail family, Ampullariidae.

Temptin is a protein that acts as a water-borne pheromone in the marine gastropod mollusk Aplysia californica. It is an abundant protein that is synthesized in the albumen gland, and is released in the egg cords during oviposition, along with other proteins called attractin, seductin and enticin. Together, they make up a complex of water-soluble proteins that act together to attract mates for reproduction and induce spawning.

References

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