First report of a xenoma-forming parasitic ciliate in a gastropod: The case of the invasive snail Pomacea canaliculata

Abstract

The apple snail Pomacea canaliculata is native to South America and has been introduced into many regions outside its natural range. Despite being one of the world’s 100 worst invasive species, little is known about the pathologies caused by parasites other than digeneans. Here, we identify and characterize a xenoma-forming ciliate in P. canaliculata from three waterbodies in the province of Buenos Aires, Argentina, using histology, transmission electron microscopy (TEM), and molecular analyses. Under a stereomicroscope, the xenomas appeared individually as white nodules measuring up to 2 mm in diameter. Of the 133 snails examined by histology, 23 were infected with xenomas (17 %) that occupied the connective tissue of most organs, with 74 % of these were located in the kidney. Snails from the three water bodies were infected. The highest prevalence was observed in the Mar del Plata Port Reserve Pond (25 %), followed by Los Padres Lake (16.4 %) and Pigüé-Venado Channel (14.4 %). Of the infected snails, 70 % had a low infection intensity (fewer than 10 xenomas per slide). No significant inflammatory response was observed in host tissues. However, in specimens with xenoma accumulations, significant tissue changes were observed, including organ enlargement in the gill lamellae, mantle border, and lung, as well as tubule compression and connective tissue replacement in the digestive gland. The host cell becomes hypertrophied, and its nucleus disintegrates. Although no cilia were observed in histological sections, TEM analysis revealed that the organisms had cilia near the cytostome and around the body, a large food vacuole, a macronucleus, and a micronucleus. Phylogenetic analysis of the SSU rDNA sequence placed the ciliate in the class Phyllopharyngea, showing the closest relationship to an uncultured eukaryote identified by BLAST. This is the fifth record of xenoma-inducing ciliates in mollusks and the first report in a gastropod.