The perivitelline fluid 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.[1]

During embryonic development the perivitelline fluid is ingested macropinocytotically by the embryos and the resulting phagosomes fuse with β-granules containing hydrolytic enzymes, which digest the perivitelline fluid components.[1][2][3][4][5]

Origin

The perivitelline fluid is synthesized by the albumen gland of female snails (also known as albumen gland-capsule gland complex or uterine gland), an accessory gland from the reproductive tract. Fertilized oocytes enter the albumen gland and, on their way out, are coated with the perivitelline fluid.[1][6][7] The amount of perivitelline fluid per egg vary considerably among species.[1] However, the amount of perivitelline fluid per egg is constant within a given species.[8] In this regard, it has been shown in Pomacea apple snails that during the reproductive season, when the nutrient precursors decrease in the albumen gland due to successive ovipositions, females tend to reduce the number of eggs per clutch but not the amount allocated to each egg.[9]

Composition

The perivitelline fluid contains predominantly galactogen, proteins, and calcium.[8][10][11][12]

Carbohydrate is invariably the most abundant component of the perivitelline fluid. Specifically, the eggs of most gastropod accumulate the polysaccharide galactogen,[8][10][11][12][13] which would provide the main energy source for the developing embryo. A small amount of soluble glucose was also detected in some species.[11][12]

Proteins, called perivitellins, are the second most abundant component of the perivitelline fluid. Perivitellins are also a source of nutrients for snail embryos [11][14] and play a role in protection against pathogens[12][14][15][16] and predators, and include non-digestible perivitellins, toxins and protease inhibitors.[12][17][18][19][20][21][22][23][24][25] These proteins were thoroughly studied in apple snails from the genus Pomacea, where they were originally grouped in two most abundant protein fractions perivitellin-1 or PV1, perivitellin-2 or PV2 (comprising approximately 70% of total protein), and a heterogeneous fraction dubbed perivitellin-3 or PV3 fraction.[26][27] Recent proteomic analyses, however, showed that the perivitelline fluid from Pomacea snails has between 34-38 different proteins with a wide variety of functions.[28][29][30]

Lipids are a minor component, mostly represented by membrane lipids, indicating that snails do not use lipids as a major energy reserve during reproduction.[11][12] Apart from structural lipids, some eggs also contain carotenoid pigments, notably astaxanthin.[12][17][27] These lipidic pigments have been associated with antioxidant and photoprotective functions,[27][31][32] and also provide Pomacea eggs with the typical bright color that would function as a warning signal (i.e. aposematism) to deter predators.[27][33][34][35]

Among the inorganic components, calcium ion is the most abundant in the perivitelline fluid. As these snails have direct development, calcium needs to be stored to allow the snail to develop the shell during organogenesis. Besides, calcium is the main component of the eggshell of those snails with aerial oviposition.[36]

References

  1. ^ a b c d De Jong-Brink M, Boer HH, Joose J (1983). "Mollusca". In Adiyodi KG, Adiyodi RG (eds.). Reproductive Biology of Invertebrates. Vol. I: Oogenesis, oviposition and oosorption. John Wiley and Sons. pp. 297–355.
  2. ^ Bluemink JG (1967). The subcellular structure of the blastula of Limnaea stagnalis L. (Mollusca) and the metabolization of the nutrient reserve (Ph.D. thesis). Utrecht.
  3. ^ Favard P, Carasso N (1958). "Origine et ultrastructure des plaquettes vitelline de la planorbe". Arch. Anat. Mier. Morph. Exptl. 47: 211–229.
  4. ^ Bottke W (1977). Ferritin-Dotter bei der Schnecke Planorbarius corneus L. Verh. Dtsch. Zool. Ges.. Stuttgart: Gustav Fischer Verlag. p. 301.
  5. ^ Koch E, Winik BC, Castro-Vazquez A (April 2009). "Development beyond the gastrula stage and digestive organogenesis in the apple-snail Pomacea canaliculata (Architaenioglossa, Ampullariidae)". Biocell. 33 (1): 49–65. doi:10.32604/biocell.2009.33.049. PMID 19499886.
  6. ^ Hayes KA, Cowie RH, Thiengo SC, Strong EE (2012). "Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda)". Zoological Journal of the Linnean Society. 166 (4): 723–753. doi:10.1111/j.1096-3642.2012.00867.x. ISSN 1096-3642.
  7. ^ Catalán M, Dreon MS, Heras H, Pollero RJ, Fernández SN, Winik B (June 2006). "Pallial oviduct of Pomacea canaliculata (Gastropoda): ultrastructural studies of the parenchymal cellular types involved in the metabolism of perivitellins". Cell and Tissue Research. 324 (3): 523–33. doi:10.1007/s00441-005-0132-x. PMID 16453107. S2CID 30906846.
  8. ^ a b c Horstmann HG (1956). "Der galaktogengehalt der Eier von Lymnaea stagnalis während der embryonalentwicklung". Biochem. Z. 328: 342–347.
  9. ^ Cadierno MP, Saveanu L, Dreon MS, Martín PR, Heras H (August 2018). "Biosynthesis in the Albumen Gland-Capsule Gland Complex Limits Reproductive Effort in the Invasive Apple Snail Pomacea canaliculata". The Biological Bulletin. 235 (1): 1–11. doi:10.1086/699200. PMID 30160995. S2CID 52135669.
  10. ^ a b Morrill JB, Norris E, Smith SD (1964). "Electro- and immunoelectrophoretic patterns of egg albumen of the pond snail Limnea palustris". Acta Embryol. Morph. Exp. 7: 155–166.
  11. ^ a b c d e Heras H, Garin CF, Pollero RJ (1998). "Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata (Mollusca: Gastropoda)". Journal of Experimental Zoology. 280 (6): 375–383. doi:10.1002/(SICI)1097-010X(19980415)280:6<375::AID-JEZ1>3.0.CO;2-K.
  12. ^ a b c d e f g Giglio ML, Ituarte S, Pasquevich MY, Heras H (2016-09-12). "The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins". Canadian Journal of Zoology. 94 (11): 777–785. doi:10.1139/cjz-2016-0049. hdl:1807/74381.
  13. ^ Raven CP (1972). "Chemical embriology of Mollusca". In Florkin M, Scheer BT (eds.). Chemical Zoology. New York: Academic Press. pp. 155–185.
  14. ^ a b Kamiya H, Sakai R, Jimbo M (2006). "Bioactive Molecules from Sea Hares". In Gavagnin G, Cimino M (eds.). Molluscs. Progress in Molecular and Subcellular Biology. Vol. 43. Berlin, Heidelberg: Springer. pp. 215–39. doi:10.1007/978-3-540-30880-5_10. ISBN 978-3-540-30880-5. PMID 17153345.
  15. ^ Ituarte S, Dreon MS, Ceolin M, Heras H (2012-11-20). "Agglutinating activity and structural characterization of scalarin, the major egg protein of the snail Pomacea scalaris (d'Orbigny, 1832)". PLOS ONE. 7 (11): e50115. Bibcode:2012PLoSO...750115I. doi:10.1371/journal.pone.0050115. PMC 3502340. PMID 23185551.
  16. ^ Hathaway JJ, Adema CM, Stout BA, Mobarak CD, Loker ES (April 2010). "Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (gastropoda, mollusca)". Developmental and Comparative Immunology. 34 (4): 425–35. doi:10.1016/j.dci.2009.12.001. PMC 2813990. PMID 19995576.
  17. ^ a b Dreon MS, Heras H, Pollero RJ (July 2004). "Characterization of the major egg glycolipoproteins from the perivitellin fluid of the apple snail Pomacea canaliculata". Molecular Reproduction and Development. 68 (3): 359–64. doi:10.1002/mrd.20078. PMID 15112330. S2CID 22032382.
  18. ^ Dreon MS, Frassa MV, Ceolín M, Ituarte S, Qiu JW, Sun J, et al. (2013-05-30). "Novel animal defenses against predation: a snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins". PLOS ONE. 8 (5): e63782. Bibcode:2013PLoSO...863782D. doi:10.1371/journal.pone.0063782. PMC 3667788. PMID 23737950.
  19. ^ Dreon MS, Fernández PE, Gimeno EJ, Heras H (June 2014). "Insights into embryo defenses of the invasive apple snail Pomacea canaliculata: egg mass ingestion affects rat intestine morphology and growth". PLOS Neglected Tropical Diseases. 8 (6): e2961. doi:10.1371/journal.pntd.0002961. PMC 4063725. PMID 24945629.
  20. ^ Heras H, Frassa MV, Fernández PE, Galosi CM, Gimeno EJ, Dreon MS (September 2008). "First egg protein with a neurotoxic effect on mice". Toxicon. 52 (3): 481–8. doi:10.1016/j.toxicon.2008.06.022. PMID 18640143.
  21. ^ Ituarte S, Brola TR, Fernández PE, Mu H, Qiu JW, Heras H, Dreon MS (2018-06-01). "A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology". PLOS ONE. 13 (6): e0198361. Bibcode:2018PLoSO..1398361I. doi:10.1371/journal.pone.0198361. PMC 5983499. PMID 29856808.
  22. ^ tuarte S, Brola TR, Dreon MS, Sun J, Qiu JW, Heras H (2019-02-01). "Non-digestible proteins and protease inhibitors: implications for defense of the colored eggs of the freshwater apple snail Pomacea canaliculata". Canadian Journal of Zoology. 97 (6): 558–566. doi:10.1139/cjz-2018-0210. hdl:1807/95364. S2CID 92566772.
  23. ^ Pasquevich MY, Dreon MS, Qiu JW, Mu H, Heras H (November 2017). "Convergent evolution of plant and animal embryo defences by hyperstable non-digestible storage proteins". Scientific Reports. 7 (1): 15848. Bibcode:2017NatSR...715848P. doi:10.1038/s41598-017-16185-9. PMC 5696525. PMID 29158565. S2CID 8393065.
  24. ^ Giglio ML, Ituarte S, Ibañez AE, Dreon MS, Prieto E, Fernández PE, Heras H (2020). "Novel Role for Animal Innate Immune Molecules: Enterotoxic Activity of a Snail Egg MACPF-Toxin". Frontiers in Immunology. 11: 428. doi:10.3389/fimmu.2020.00428. PMC 7082926. PMID 32231667. S2CID 212676110.
  25. ^ Giglio ML, Ituarte S, Milesi V, Dreon MS, Brola TR, Caramelo J, et al. (August 2020). "Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails". Journal of Structural Biology. 211 (2): 107531. doi:10.1016/j.jsb.2020.107531. hdl:11336/143650. PMID 32446810. S2CID 218873723.
  26. ^ Garin CF, Heras H, Pollero RJ (December 1996). "Lipoproteins of the egg perivitelline fluid of Pomacea canaliculata snails (Mollusca: Gastropoda)". The Journal of Experimental Zoology. 276 (5): 307–14. doi:10.1002/(SICI)1097-010X(19961201)276:5<307::AID-JEZ1>3.0.CO;2-S. PMID 8972583.
  27. ^ a b c d Pasquevich MY, Dreon MS, Heras H (March 2014). "The major egg reserve protein from the invasive apple snail Pomacea maculata is a complex carotenoprotein related to those of Pomacea canaliculata and Pomacea scalaris". Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology. 169: 63–71. doi:10.1016/j.cbpb.2013.11.008. hdl:11336/100510. PMID 24291422.
  28. ^ Sun J, Zhang H, Wang H, Heras H, Dreon MS, Ituarte S, et al. (August 2012). "First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition". Journal of Proteome Research. 11 (8): 4240–8. doi:10.1021/pr3003613. hdl:11336/94414. PMID 22738194.
  29. ^ Mu H, Sun J, Cheung SG, Fang L, Zhou H, Luan T, et al. (February 2018). "Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails". Journal of Proteomics. 172: 36–48. doi:10.1016/j.jprot.2017.11.002. hdl:10754/626132. PMID 29122728.
  30. ^ Ip JC, Mu H, Zhang Y, Heras H, Qiu JW (April 2020). "Egg perivitelline fluid proteome of a freshwater snail: Insight into the transition from aquatic to terrestrial egg deposition". Rapid Communications in Mass Spectrometry. 34 (7): e8605. doi:10.1002/rcm.8605. hdl:11336/128840. PMID 31657488. S2CID 204947433.
  31. ^ Dreon MS, Heras H, Pollero RJ (January 2003). "Metabolism of ovorubin, the major egg lipoprotein from the apple snail". Molecular and Cellular Biochemistry. 243 (1–2): 9–14. doi:10.1023/a:1021616610241. PMID 12619883. S2CID 6345962.
  32. ^ Dreon MS, Ceolín M, Heras H (April 2007). "Astaxanthin binding and structural stability of the apple snail carotenoprotein ovorubin". Archives of Biochemistry and Biophysics. 460 (1): 107–12. doi:10.1016/j.abb.2006.12.033. PMID 17324373.
  33. ^ Heras H, Dreon MS, Ituarte S, Pollero RJ (2007-07-01). "Egg carotenoproteins in neotropical Ampullariidae (Gastropoda: Arquitaenioglossa)". Comparative Biochemistry and Physiology. Toxicology & Pharmacology. 146 (1–2): 158–67. doi:10.1016/j.cbpc.2006.10.013. PMID 17320485.
  34. ^ Ituarte S, Dreon MS, Ceolín M, Heras H (September 2008). "Isolation and characterization of a novel perivitellin from the eggs of Pomacea scalaris (Mollusca, Ampullariidae)". Molecular Reproduction and Development. 75 (9): 1441–8. doi:10.1002/mrd.20880. PMID 18213678. S2CID 24352602.
  35. ^ Dreon MS, Schinella G, Heras H, Pollero RJ (February 2004). "Antioxidant defense system in the apple snail eggs, the role of ovorubin". Archives of Biochemistry and Biophysics. 422 (1): 1–8. doi:10.1016/j.abb.2003.11.018. PMID 14725852.
  36. ^ Tompa AS (1980). "Studies on the reproductive biology of gastropods: Part III. Calcium provision and the evolution of terrestrial eggs among gastropods". Journal of Conchology. 30: 145–154.
Categories