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

Cruz‐Flores, Roberto; Cáceres-Martı́nez, Jorge; Muñoz-Flores, M.; Vásquez‐Yeomans, Rebeca; Rodríguez, Mónica Hernández; Río-Portilla, Miguel A. Del; Rocha‐Olivares, Axayácatl; Castro-Longoria, Ernestina

doi:10.1016/j.jip.2016.09.001

Cited by 14 publications

(14 citation statements)

References 14 publications

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“…However, it is difficult to assess and isolate the impact of temperature and species on our observations because we were only able to compare the red, elevated temperature group with the white, ambient group. While this study did not confirm phage particles by TEM, the highly-recognizable granular, pleomorphic inclusions have consistently revealed observable phage (Cruz-Flores & Cáceres-Martínez, 2016; Cruz-Flores et al, 2016; Friedman et al, 2014a). The mottled, complex morphology of the phage-containing inclusions has been interpreted as evidence of active phage-induced lysis (Friedman & Crosson, 2012).…”

Section: Discussioncontrasting

confidence: 75%

“…However, currently this is not believed possible because classical inclusions are consistently accompanied by phage-containing ones. This has been recorded in recent histology assessments from abalone populations in Baja Mexico and Cayucos, San Nicolas Island, and Carmel California (Cruz-Flores et al, 2016; Friedman et al, 2014a) and has been observed in abalone from Bodega Head (J Moore, pers. obs., 2015).…”

Section: Discussionsupporting

confidence: 58%

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Differing responses of red abalone (Haliotis rufescens) and white abalone (H. sorenseni) to infection with phage-associated Candidatus Xenohaliotis californiensis

Vater

Byrne

Marshman

et al. 2018

PeerJ

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The Rickettsiales-like prokaryote and causative agent of Withering Syndrome (WS)—Candidatus Xenohaliotis californiensis (Ca. Xc)—decimated black abalone populations along the Pacific coast of North America. White abalone—Haliotis sorenseni—are also susceptible to WS and have become nearly extinct in the wild due to overfishing in the 1970s. Candidatus Xenohaliotis californiensis proliferates within epithelial cells of the abalone gastrointestinal tract and causes clinical signs of starvation. In 2012, evidence of a putative bacteriophage associated with Ca. Xc in red abalone—Haliotis rufescens—was described. Recently, histologic examination of animals with Ca. Xc infection in California abalone populations universally appear to have the phage-containing inclusions. In this study, we investigated the current virulence of Ca. Xc in red abalone and white abalone at different environmental temperatures. Using a comparative experimental design, we observed differences over time between the two abalone species in mortality, body condition, and bacterial load by quantitative real time PCR (qPCR). By day 251, all white abalone exposed to the current variant of Ca. Xc held in the warm water (18.5 °C) treatment died, while red abalone exposed to the same conditions had a mortality rate of only 10%, despite a relatively heavy bacterial burden as determined by qPCR of posterior esophagus tissue and histological assessment at the termination of the experiment. These data support the current status of Ca. Xc as less virulent in red abalone, and may provide correlative evidence of a protective phage interaction. However, white abalone appear to remain highly susceptible to this disease. These findings have important implications for implementation of a white abalone recovery program, particularly with respect to the thermal regimes of locations where captively-reared individuals will be outplanted.

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Section: Discussioncontrasting

confidence: 75%

Section: Discussionsupporting

confidence: 58%

Differing responses of red abalone (Haliotis rufescens) and white abalone (H. sorenseni) to infection with phage-associated Candidatus Xenohaliotis californiensis

Vater

Byrne

Marshman

et al. 2018

PeerJ

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“…Rickettsiales‐like organisms are reported to form IVs in diverse types of host cells (Morrison & Shum, 1983; Elston & Peacock, 1984; Mialhe et al, 1987; Norton et al, 1993a; Wen et al, 1994; Renault & Cochennec, 1994; Friedman et al, 2000; Cruz‐Flores et al, 2016). In histological sections, the majority of the IVs reported in molluscs stain basophilic with H&E (Table 2).…”

Section: Histologymentioning

confidence: 99%

“…Morphologically, RLOs have been described as rod‐shaped, spherical and coccoid to pleomorphic (Harshbarger & Chang, 1977; Buchanan, 1978; Comps & Raimbault, 1978; Comps, 1980; Meyers, 1981; Gulka et al, 1983; Morrison & Shum, 1983; Elston & Peacock, 1984; Elston, 1986a; Norton et al, 1993a; Renault & Cochennec, 1994; Wen et al, 1994; Friedman et al, 2000; Wu & Pan, 2000; Molloy et al, 2001; Li & Wu, 2004; Lohrmann, 2009; Zhu et al, 2012; Carvalho et al, 2013; Cruz‐Flores et al, 2016) Figure 4a. Some atypical shapes that have been described include banana (Norton et al, 1992, 1993a)‐ and spaghetti (Norton et al, 1993b)‐like shapes.…”

Section: Ultrastructurementioning

confidence: 99%

“…Distinct cell wall types have been observed, with a double‐membrane‐type cell wall most commonly being reported (Harshbarger & Chang, 1977; Buchanan, 1978; Comps, 1980; Goggin & Lester 1990; Norton et al, 1993b; Lohrmann, 2009), followed by a double trilaminar cell wall (Morrison & Shum, 1983; Elston & Peacock, 1984; Comps & Tigé, 1999; Wu & Pan, 1999a; Li & Wu, 2004), while the least common type is a trilaminar cell wall (Meyers, 1981; Adam et al, 1994; Sun & Wu, 2004; Cruz‐Flores et al, 2016; Fig. 4a).…”

Section: Ultrastructurementioning

confidence: 99%

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Rickettsiales‐like organisms in bivalves and marine gastropods: a review

Cruz‐Flores

Cáceres-Martı́nez

2020

Reviews in Aquaculture

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Rickettsiales‐like organisms (RLOs) are intracellular bacteria that have been reported to be symbionts of over 60 species of bivalves and marine gastropod molluscs of aquaculture importance around the world. Morphologically, some of these prokaryotes are similar to bacteria from the order Rickettsiales, and in most cases, they form intracytoplasmic inclusions similar to those observed in bacteria of the family Anaplasmataceae. Genetically, only Candidatus Xenohaliotis californiensis (CXc), a parasite of several abalone species, has been classified as a member of the order Rickettsiales. The other two characterized RLOs are distantly related; one belongs to the same class (α‐proteobacteria), and the other belongs to the γ‐proteobacteria. Hyperparasitism of RLOs by bacteriophages has been reported in several species of mollusc and appears to have a negative effect on RLOs. The intracellular lifestyle of RLOs has been associated with cell alterations including hypertrophy and compression of the cytoplasmic organelles, and in most cases, no host reaction is observed by histology. In some cases, a high infection intensity of RLOs has been related to dysfunction of the affected organs that can result in disease, and in other cases, high burdens of RLOs have been associated with mortality, but most of these cases have yet to be confirmed. To date, only CXc has been confirmed as the aetiological agent of a chronic and potentially lethal disease of several abalone species known as withering syndrome. This disease is listed by the World Organization of Animal Health. With the ever‐increasing interest in preserving fisheries and expanding the aquaculture production of mollusc species, more efforts should be focused on the characterization and study of RLOs to elucidate the type of symbiosis they maintain with their host and determine when they are acting as true pathogens that should be subjected to control in aquaculture. This review provides an overview of the literature on RLOs that infect bivalves and gastropods of aquaculture importance, and we discuss the most important aspects of these unique prokaryotes.

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