A rapid phenotype change in the pathogen Perkinsus marinus was associated with a historically significant marine disease emergence in the eastern oyster

Ryan B Carnegie,Susan E Ford,Lúcia S L Safi,Laura A Whitefleet-Smith,Rita K Crockett,Eugene M Burreson,Lydia M Bienlien,Peter R Kingsley-Smith

doi:10.1038/s41598-021-92379-6

Abstract

The protozoan parasite Perkinsus marinus, which causes dermo disease in Crassostrea virginica, is one of the most ecologically important and economically destructive marine pathogens. The rapid and persistent intensification of dermo in the USA in the 1980s has long been enigmatic. Attributed originally to the effects of multi-year drought, climatic factors fail to fully explain the geographic extent of dermo’s intensification or the persistence of its intensified activity. Here we show that emergence of a unique, hypervirulent P. marinus phenotype was associated with the increase in prevalence and intensity of this disease and associated mortality. Retrospective histopathology of 8355 archival oysters from 1960 to 2018 spanning Chesapeake Bay, South Carolina, and New Jersey revealed that a new parasite phenotype emerged between 1983 and 1990, concurrent with major historical dermo disease outbreaks. Phenotypic changes included a shortening of the parasite’s life cycle and a tropism shift from deeper connective tissues to digestive epithelia. The changes are likely adaptive with regard to the reduced oyster abundance and longevity faced by P. marinus after rapid establishment of exotic pathogen Haplosporidium nelsoni in 1959. Our findings, we hypothesize, illustrate a novel ecosystem response to a marine parasite invasion: an increase in virulence in a native parasite.

Highlights

The protozoan parasite Perkinsus marinus, which causes dermo disease in Crassostrea virginica, is one of the most ecologically important and economically destructive marine pathogens
Numerous emerging diseases have been produced by introduced exotic pathogens, such as “multinucleate sphere X” (MSX) disease caused by Haplosporidium nelsoni in eastern oysters, Crassostrea virginica, from the United States of America (USA), and bonamiasis caused by Bonamia ostreae in flat oysters, Ostrea edulis, from E urope[3,4]; infectious hematopoietic necrosis in rainbow trout, Oncorhynchus mykiss, in Europe[5]; and infectious hypodermal and haemopoietic necrosis, Taura syndrome, and white spot syndrome in penaeid shrimp world-wide[6]
P. marinus began a progressive range expansion northward to the northern Atlantic coast of the USA at that time, producing major disease outbreaks along the way: in Delaware Bay in 1990, where it had previously been scarcely detectable and primarily in association with oysters transplanted from the Chesapeake Bay; and in Long Island Sound and southern New England, USA, between 1991 and 1 99415

Summary

Introduction

The protozoan parasite Perkinsus marinus, which causes dermo disease in Crassostrea virginica, is one of the most ecologically important and economically destructive marine pathogens. Dermo represents the unusual case of an established disease that was long present in a host population but which intensified sharply in the mid-1980s This development was first apparent in the Chesapeake Bay region of the Mid-Atlantic coast of the USA. While warming seawater temperatures may explain the range expansion of P. marinus and dermo disease to the north since 1990, they fail to fully explain the sudden and persistent intensification of P. marinus activity in Chesapeake Bay in the mid-1980s14 Nor do they explain an intensification of dermo disease around the same time as far south as South Carolina in the South Atlantic Bight[19], which, in contrast with northern waters such as Delaware Bay and Long Island Sound, had not warmed significantly[20]. Environmental factors do not completely explain a lasting increase in P. marinus infections and associated mortality along the USA Atlantic Coast from the mid-1980s

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