Coral microbiomes are known to play important roles in organismal health, response to environmental stress, and resistance to disease. Pathogens invading the coral microbiome encounter diverse assemblages of resident bacteria, ranging from defensive and metabolic symbionts to opportunistic bacteria that may turn harmful in compromised hosts. However, little is known about how these bacterial interactions influence the overall structure, stability, and function of the microbiome during the course of pathogen challenge. We sought to test how coral microbiome dynamics were affected by interactions between two of its members: Vibrio coralliilyticus, a known temperature-dependent coral pathogen, and Halobacteriovorax, a unique bacterial predator of Vibrio and other gram-negative bacteria. We challenged specimens of the important reef-building coral Montastraea cavernosa with Vibrio coralliilyticus pathogens in the presence or absence of Halobacteriovorax predators, and monitored microbial community dynamics with 16S rRNA gene time-series. In addition to its direct effects on corals, pathogen challenge reshaped coral microbiomes in ways that allowed for secondary blooms of opportunistic bacteria. As expected, Vibrio coralliilyticus addition increased the infiltration of Vibrio into coral tissues. This increase of Vibrios in coral tissue was accompanied by increased richness, and reduced stability (increased beta-diversity) of the rest of the microbiome, suggesting strong secondary effects of pathogen invasion on commensal and mutualistic coral bacteria. Moreover, after an initial increase in Vibrios, two opportunistic lineages (Rhodobacterales and Cytophagales) increased in coral tissues, suggesting that this pathogen opens niche space for opportunists. Based on the keystone role of predators in many ecosystems, we hypothesized that Halobacteriovorax predators might help protect corals by consuming gram-negative pathogens. In keeping with a protective role, Halobacteriovorax addition alone had only minor effects on the microbiome, and no infiltration of Halobacteriovorax into coral tissues was detected in amplicon libraries. Simultaneous challenge with both pathogen and predator eliminated detectable V. corallyticus infiltration into coral tissue samples, ameliorated changes to the rest of the coral microbiome, and prevented secondary blooms of opportunistic Rhodobacterales and Cytophagales. Thus, we show that primary infection by a coral pathogen is sufficient to cause increases in opportunists, as seen in correlational studies. These data further provide a proof-of-principle demonstration that, under certain circumstances, host-associated bacterial predators can mitigate the ability of pathogens to infiltrate host tissue, and stabilize the microbiome against complex secondary changes that favor growth of opportunistic lineages.
NMR analysis of metabolic responses to extreme conditions of the temperature-dependent coral pathogen Vibrio coralliilyticus
