Reduced disease in black abalone following mass mortality: phage therapy and natural selection

Abstract

Black abalone, Haliotis cracherodii, populations along the NE Pacific ocean have declined due to the rickettsial disease withering syndrome (WS). Natural recovery on San Nicolas Island (SNI) of Southern California suggested the development of resistance in island populations. Experimental challenges in one treatment demonstrated that progeny of disease-selected black abalone from SNI survived better than did those from naïve black abalone from Carmel Point in mainland coastal central California. Unexpectedly, the presence of a newly observed bacteriophage infecting the WS rickettsia (WS-RLO) had strong effects on the survival of infected abalone. Specifically, presence of phage-infected RLO (RLOv) reduced the host response to infection, RLO infection loads, and associated mortality. These data suggest that the black abalone: WS-RLO relationship is evolving through dual host mechanisms of resistance to RLO infection in the digestive gland via tolerance to infection in the primary target tissue (the post-esophagus) coupled with reduced pathogenicity of the WS-RLO by phage infection, which effectively reduces the infection load in the primary target tissue by half. Sea surface temperature patterns off southern California, associated with a recent hiatus in global-scale ocean warming, do not appear to be a sufficient explanation for survival patterns in SNI black abalone. These data highlight the potential for natural recovery of abalone populations over time and that further understanding of mechanisms governing host–parasite relationships will better enable us to manage declining populations.

Hyperparasitism by the bacteriophage ( Caudovirales ) infecting Candidatus Xenohaliotis californiensis (Rickettsiales-like prokaryote) parasite of wild abalone Haliotis fulgens and Haliotis corrugata from the Peninsula of Baja California, Mexico

“…To determine if CXc was infected by the bacteriophage the appearance and staining characteristics of the MBVs that contained the bacteria were considered, uninfected MBVs of CXc stain pink to purple and have a uniform smooth appearance, while the iMBVs of CXc stain deep purple to navy blue and have a rough appearance and individual bacteria can be observed by light microscopy. Additionally, all histological slides were analyzed for the presence of a third type inclusion form by a rickettsiales-like marine bacteria tentatively described as stippled RLP which is not related to CXc Friedman et al, 2014;Cruz-Flores and Cáceres-Martínez unpublished data), these inclusions stain light blue and have a dotted appearance.…”

Complementary approaches to diagnosing marine diseases: a union of the modern and the classic

“…Sequencing paved the way for development of PCR [51], ISH [50] and qPCR [52] methods to help better understand field dynamics. These modern methods have allowed us to better understand the transmission and field dynamics of WS [41,[53][54][55].…”

“…The disease withering syndrome (WS) results from a complex relationship among its abalone hosts, the bacterial pathogen (a rickettsia-like organism 'Candidatus Xenohaliotis californiensis' (WS-RLO, [38]), and the environment (temperature anomalies) [39][40][41][42][43]. A recently discovered bacteriophage hyperparasite further complicates the disease dynamics in this system [44].…”

The ecology, evolution, impacts and management of host–parasite interactions of marine molluscs

“…Analyses reveal a potential 7-year cycle in disease, with peaks associated with strong positive anomalies of the North Atlantic Oscillation (NAO), which brings warmer temperatures, heavy rainfall and lower salinities. Similarly, a 10-year study along the coast of California, U.S.A., revealed that significant population declines in the black abalone, Haliotis cracherodii, from a Rickettsiales-like prokaryote causing Withering Syndrome, was accelerated during El Niño events as compared to non-El Niño periods (e.g., Moore et al, 2000a;Raimondi et al, 2002;Friedman et al, 2014).…”