Good host - bad host: molecular and evolutionary basis for survival, its failure, and virulence factors of the zoonotic nematode Anisakis pegreffii

Abstract

AbstractParasitism is a highly successful life strategy and a driving force in genetic diversity that has evolved many times over. Consequently, parasitic organisms have adopted a rich display of traits associated with survival that guarantees an effective “communication” with the host immunity and a balance with surrounding microbiome. However, gain/loss of hosts along the evolutionary axis represents a complex scenario that as contemporary onlookers, we can observe only after a long time displacement. The zoonotic and monophyletic Anisakidae diverged from its terrestrial sister group Ascarididae 150-250 Ma, although a split from their common ancestral host, a terrestrial amniote, seemingly happened already in Early Carboniferous (360.47 Ma). Faced with the sea-level rise during the Permian-Triassic extinction (215 Ma), anisakids acquired a semiaquatic tetrapod host, and as a result of lateral host-switches in Cenozoic, colonised marine mammals, co-evolving with their “new hosts”. Although contemporary anisakids have lost the ability to propagate in terrestrial hosts, they can survive for a limited time in humans. To scrutinize anisakid versatility to infect evolutionary-distant host, we performed transcriptomic profiling of larvae infecting the accidental host (rat) and compared it to that of larvae infecting an evolutionary-familiar, paratenic host (fish). Identified differences and the modeling of handful of shared transcripts, provides the first insights into evolution of larval nematode virulence, warranting further investigation of shared transcript as potential drug therapy targets. Our findings have also revealed some key intrinsic cues that direct larval fate during infection.