The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins

The freshwater snails Pomacea Perry, 1810 lay conspicuous aerial egg clutches that are ignored by most predators. Egg biochemical defenses in the apple snail Pomacea canaliculata (Lamarck, 1822) are provided by multifunctional proteins. We analyzed the eggs of a sympatric species, Pomacea maculata Perry, 1810, studying the gross composition, toxicity, hemagglutinating activity, and its antinutritive and antidigestive properties. Eggs are mostly composed of polysaccharides (mainly galactogen) and proteins, followed by lipids and nonsoluble calcium. Two perivitellins account for ∼85% dry mass of the egg protein. The major lipids are phospholipids and sterols. A suite of potential defenses was determined, including strong lethal neurotoxicity on mice and moderate antidigestive and lectin activities. Remarkably, their polysaccharides were refractive to in vitro digestion by digestive glycosidases. This study characterized ∼99% of egg composition and identified multiple potential defenses, provided not only by proteins but also by polysaccharides. This is the first evidence to our knowledge that reserve sugars may be involved in defenses, giving further insight into the unusual reproductive strategy of these well-defended snail eggs.

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Pomacea maculata.

10.1079/cpc.116486.20210102246 ◽

2021 ◽

Author(s):

Rob Cowie ◽

Romi L. Burks ◽

Amy E. Miller ◽

Alexandria L. Hill

Keyword(s):

Invasive Species ◽

South America ◽

Species Identification ◽

Geographical Area ◽

Freshwater Snail ◽

Pomacea Canaliculata ◽

Apple Snail ◽

Pomacea Maculata ◽

Golden Apple Snail ◽

History Of

Abstract P. maculata is a freshwater snail native to a wide geographical area in South America from the Rio de la Plata in Argentina and Uruguay to the Amazon in Brazil. It is commonly confused with any number of similar large apple snails, including the well-known invasive golden apple snail Pomacea canaliculata (listed among '100 of the world's worst invasive species'). Both species have been introduced to South-East and East Asia, although for many years they were not distinguished and the Asian introductions were widely identified as "golden apple snails" and the name P. canaliculata was applied to them. Due to the confusion in species identification, the history of introduction of P. maculata remains somewhat uncertain as does its invasiveness and pest potential. Much of the literature is confounded, for example, the snails illustrated by Cowie (2002) as P. canaliculata are in fact P. maculata. The majority of invasive populations in Asia appear to be P. canaliculata, often not mixed with P. maculata (Hayes et al., 2008; Tran et al., 2008) and the pest potential of P. canaliculata in such cases is clear. However, much less has been written about the invasiveness and pest potential of 'P. maculata'.

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Non-digestible proteins and protease inhibitors: implications for defense of the colored eggs of the freshwater apple snailPomacea canaliculata

Canadian Journal of Zoology ◽

10.1139/cjz-2018-0210 ◽

2019 ◽

Vol 97 (6) ◽

pp. 558-566 ◽

Cited By ~ 5

Author(s):

Santiago Ituarte ◽

Tabata Romina Brola ◽

Marcos Sebastián Dreon ◽

Jin Sun ◽

Jian-Wen Qiu ◽

...

Keyword(s):

Quaternary Structure ◽

Economic Losses ◽

Pomacea Canaliculata ◽

Apple Snail ◽

Medical Issues ◽

Biological Potential ◽

Pomacea Maculata ◽

Biochemical Validation ◽

Rat Growth ◽

Ancient Gene Duplication

Apple snails (Pomacea Perry, 1810) are successful invaders that cause ecological perturbations, economic losses, and medical issues. A peculiar trait of this snail is a high biological potential, related to the absence of predators of their eggs. Eggs show protease inhibitor (PI) activity, originally ascribed to PcOvo perivitellin in the apple snail Pomacea canaliculata (Lamarck, 1822) but absent in PmPV1, the orthologoue of PcOvo, in eggs of the apple snail Pomacea maculata Perry, 1810. As egg fluid diminishes rat growth rate, an antidigestive effect, similar to plant defenses against herbivory, was hypothesized. However, PI activity has not been characterized in apple snail eggs. Here we identify and partially characterize P. canaliculata egg PI and improve our knowledge of the quaternary structure and evolution of PcOvo. Through N-terminal, transcriptomic or proteomic sequencing, and biochemical validation, we identified a Kunitz-type and a Kazal-type inhibitor that, though at low concentration in the egg, exhibit strong PI activity against trypsin, chymotrypsin, elastase, and subtilisin. Additionally, we report three new subunits for the non-digestible storage protein PcOvo. They are likely products of ancient gene duplication, as their sequences exhibit moderate similarity (30%). To our knowledge, this is the first report of Kazal-type inhibition among invertebrate eggs. Inhibiting varied proteases, PI seems an efficient adaptive trait that limits predator’s capacity to digest egg nutrients.

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The extraction of antioxidative compounds from rusks enriched with millet flour (Panicum miliaceum L.)

Journal of the Serbian Chemical Society ◽

10.2298/jsc171229028p ◽

2018 ◽

Vol 83 (6) ◽

pp. 723-732 ◽

Cited By ~ 1

Author(s):

Dajana Poleksic ◽

Milica Pavlicevic ◽

Jelena Rakovic-Simic ◽

Vladislav Rac ◽

Biljana Vucelic-Radovic ◽

...

Keyword(s):

Solvent Extraction ◽

Phenolic Compounds ◽

Formic Acid ◽

Wheat Flour ◽

Total Content ◽

In Vitro Digestion ◽

Dry Mass ◽

Antioxidative Capacity ◽

Panicum Miliaceum

Two different ways of extracting antioxidative compounds (including soluble polyphenols) from rusks made from wheat flour with added millet (Panicum miliaceum L.) were compared, i.e., solvent extraction and in vitro digestion. Wheat flour was replaced by millet flour in amounts of 10, 20 or 30 wt. % (per dry mass). Solvent extraction was realized using a mixture of ethanol and water in different percentages, with or without the addition of formic acid. The total content of phenolic compounds (TPC) was determined using Folin? ?Ciocalteu reagent, while the antioxidative capacity was measured by the DPPH (2,2-diphenyl-1-picrylhydrazyl) assay. The efficiency of solvent extraction was enhanced by the addition of formic acid. The addition of millet flour in amounts up to 20 % enhanced the antioxidative properties. It was shown that in vitro digestion was more efficient in the extraction of antioxidative compounds, in comparison with solvent extraction.

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