The Role of the Proteinase Inhibitor Ovorubin in Apple Snail Eggs Resembles Plant Embryo Defense against Predation

DREON, MARCOS SEBASTIÁN; ITUARTE, SANTIAGO; HERAS, HORACIO

PLOS ONE

PUBLIC LIBRARY SCIENCE

Año: 2010 vol. 5

1932-6203

BackgroundWork has thoroughly established that most eggs are intensely predated. Among the fewexceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which havevirtually no predators.Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuousreddish coloration, but the nature of the defense was unclear, except a screening for defenses thatidentified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinaseinhibitor (PI) whose role to protect against pathogens was taken for granted, according to theprevailing assumption. Through biochemical, biophysical and feeding experiments we studiedthe proteinase inhibitor function of ovorubin in egg defenses.Methodology/Principal findingsMass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinaseinhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering(SAXS) and cross-linking studies but, in contrast to the classical assumption, it does not preventbacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis.Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in ratsindicating that this highly stable PI is capable of surviving passage through the gastrointestinaltract in a biologically active form.ConclusionsTo our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestiveprotease of potential predators, limiting predator's ability to digest egg nutrients. This role hasnot been reported in the animal kingdom but it is similar to plant defenses against herbivory.Further, this would be the only defense model with no trade-offs between conspicuousness andnoxiousness by encoding into the same molecule both the aposematic warning signal and anantinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probablyunpalatable factors would explain the near absence of predators, opening new perspectives in thestudy of the evolution and ecology of egg defensive strategies.