Abstract
Coral microbiomes are known to play important roles in organismal health, response to environmental stress, and resistance to disease. The coral microbiome contains 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 mechanism and controls of overall structure, stability, and function of the microbiome. We sought to test how coral microbiome dynamics were affected by interactions between two bacteria: Vibrio coralliilyticus, a known temperature-dependent pathogen of some corals, and Halobacteriovorax, a unique bacterial predator of Vibrio and other gram-negative bacteria. We challenged reef-building coral with V. coralliilyticus in the presence or absence of Halobacteriovorax predators, and monitored microbial community dynamics with 16S rRNA gene profiling time-series. Vibrio coralliilyticus inoculation increased the mean relative abundance of Vibrios by greater than 35% from the 4 to 8 hour time point, but not in the 24 & 32 hour time points. However, strong secondary effects of the Vibrio challenge were also observed for the rest of the microbiome such as increased richness (observed species), and reduced stability (increased beta-diversity). Moreover, after the transient increase in Vibrios, two lineages of bacteria (Rhodobacterales and Cytophagales) increased in coral tissues, suggesting that V. coralliilyticus challenge opens niche space for these known opportunists. Rhodobacterales increased from 6.99% (±0.05 SEM) to a maximum mean relative abundance of 48.75% (±0.14 SEM) in the final time point and Cytophagales from <0.001% to 3.656%. Halobacteriovorax predators are commonly present at low-abundance on coral surfaces. Based on the keystone role of predators in many ecosystems, we hypothesized that Halobacteriovorax predators might help protect corals by consuming foreign or “alien” gram negative bacteria. Halobacteriovorax inoculation also altered the microbiome but to a lesser degree than V. coralliilyticus, and Halobacteriovorax were never detected after inoculation. Simultaneous challenge with both V. coralliilyticus and predatory Halobacteriovorax eliminated the increase in V. coralliilyticus, ameliorated changes to the rest of the coral microbiome, and prevented the secondary blooms of opportunistic Rhodobacterales and Cytophagales seen in the V. coralliilyticus challenge. These data suggest that, under certain circumstances, host-associated bacterial predators may mitigate the ability of other bacteria to destabilize the microbiome.
Highlights
Coral reefs have experienced sharp declines in coral cover from environmental factors (De’ath et al, 2012), temperature induced bleaching (Fitt & Warner, 1995), and disease (Bourne et al, 2009; Burge et al, 2014), with some areas of the Caribbean experiencing as much as 80% coral loss over the past several decades (Gardner et al, 2003)
While many studies have identified microbial consortia that increase in diseased corals (e.g., GignouxWolfsohn & Vollmer, 2015), etiological agents are generally unknown for the majority of coral diseases (Mouchka, Hewson & Harvell, 2010) and others are defined in broad terms as polymicrobial disease (Cooney et al, 2002)
Never the less, determining how bacterial challenge can alter the normal flora of a host may provide insight into whether mutualists are lost and additional antagonisms arise during an infection cycle and contribute to secondary negative effects on animal hosts
Summary
Coral reefs have experienced sharp declines in coral cover from environmental factors (De’ath et al, 2012), temperature induced bleaching (Fitt & Warner, 1995), and disease (Bourne et al, 2009; Burge et al, 2014), with some areas of the Caribbean experiencing as much as 80% coral loss over the past several decades (Gardner et al, 2003). While many studies have identified microbial consortia that increase in diseased corals (e.g., GignouxWolfsohn & Vollmer, 2015), etiological agents are generally unknown for the majority of coral diseases (Mouchka, Hewson & Harvell, 2010) and others are defined in broad terms as polymicrobial disease (Cooney et al, 2002). Bacterial communities of diseased corals are known to have large numbers of opportunistic pathogens and secondary colonizers (Gignoux-Wolfsohn & Vollmer, 2015). It has been hypothesized that the majority of coral disease may be the result of normally-benign coral microbionts that become opportunistic pathogens during physiological stress to the host (Lesser et al, 2007a). The linkages between infection by a primary foreign agents and secondary opportunistic infections remain an area of active exploration
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