Populations, not clones, are the unit of vibrio pathogenesis in naturally infected oysters

Abstract

Disease in oysters has been steadily rising over the past decade, threatening the long-term survival of commercial and natural stocks. Our understanding and management of such diseases are of critical importance as aquaculture is an important aspect of dealing with the approaching worldwide food shortage. Although some bacteria of the Vibrio genus isolated from diseased oysters have been demonstrated to be pathogenic by experimental infection, direct causality has not been established. Little is known about the dynamics of how the bacterial population hosted by oysters changes during disease progression. Combining experimental ecology, a high-throughput infection assay and genome sequencing, we show that the onset of disease in oysters is associated with progressive replacement of diverse benign colonizers by members of a phylogenetically coherent virulent population. Although the virulent population is genetically diverse, all members of that population can cause disease. Comparative genomics across virulent and nonvirulent populations identified candidate virulence factors that were clustered in population-specific genomic regions. Genetic analyses revealed that one gene for a candidate virulent factor, a putative outer membrane protein, is necessary for infection of oysters. Finally, analyses of oyster mortality following experimental infection suggest that disease onset can be facilitated by the presence of nonvirulent strains. This is a new form of polymicrobial disease, in which nonpathogenic strains contribute to increase mortality.

Salinity influences disease-induced mortality of the oyster Crassostrea gigas and infectivity of the ostreid herpesvirus 1 (OsHV-1)

“…A more likely hypothesis is that another microorganism killed these animals simultaneously weakened by a salinity shock. In our study, donors were infected in the field where the OsHV-1-induced mortality occurred, and they may have introduced a diversity of Vibrio species or other pathogens to the recipients (Lemire et al 2015, Petton et al 2015b). In addition, acute exposure to low salinity may have altered the defenses of oysters either directly by impairing their immunity (Matozzo & Marin 2011, Carregosa et al 2014, Knowles et al 2014 or indirectly by causing the oysters to allocate energy to regulate intracellular osmotic concentrations (Gilles 1972, Shumway 1977, Shumway et al 1977, Neufeld & Wright 1996, thus compromising the defense response.…”

“…Indeed, several non-pathogenic bacteria contribute to the mortality of oysters (Lemire et al 2015), and salinity is a major factor shaping the bacterial community in marine ecosystems (Herlemann et al 2011, Dupont et al 2014.…”

“…The SI was then (1) directed towards recipient oysters held at 4 salinities with or without prior acclimation or (2) brought to a salinity of 10 or 25 ‰ and directed towards recipient oysters maintained at 25 ‰. Overall, this method, which has been used in many previous studies (Petton et al 2013, 2015a,b, Tamayo et al 2014, Lassudrie et al 2015, Lemire et al 2015, Pernet et al 2015, reproduces the natural infection process and takes into account the fact that OsHV-1 triggers oyster mortality, although other microorganisms can also play a role (Saulnier et al 2010, Lemire et al 2015, Petton et al 2015b.…”

Antimicrobial peptides in marine invertebrate health and disease

“…Over the past few decades, abnormal mortalities of juvenile C. gigas oysters have affected the USA, Japan, Australia and Western Europe. Those mortalities of complex aetiology are due to a temperature-dependent polymicrobial disease that involves pathogenic Vibrio strains of the Splendidus clade and the ostreid herpes virus OsHV-1 mvar [9,17,22]. Vibrios also cause diseases at other oyster developmental stages.…”

What is killing Caribbean corals? Investigating a devastating coral disease.

“…The many disease-associated OTUs found among all sites became many putative WBD pathogen(s). Bacterial diseases can be caused by a few cells of a single pathogen invading the host tissues (low infectious dose) (Zwart, Daros and Elena 2011), a consortium of pathogens that may be sufficient but not necessary to cause disease signs (Lemire et al 2015) or normally commensal bacteria reaching a threshold, which initiates a switch to pathogenic behavior (Rutherford and Bassler 2012). Furthermore, commensal bacteria could become pathogenic due to an external environmental trigger (Lesser et al 2007).…”