Oculina patagonica; evidence in support of the coral holobiont and probiotic hypotheses

Vibrio shiloi is known as a causative agent in the bleaching of the coral Oculina patagonica in the Eastern Mediterranean. Bleaching events are correlated with high water temperatures in the summer of ~30°C with up to 80% of O. patagonica colonies bleaching. However, since 2002 widespread resistance to V. shiloi has been observed for O. patagonica although the species has continued to bleach on a seasonal pattern since. Mills et al., 2013 conducted a study to ascertain firstly, the current bleaching cause for O. patagonica, and secondly, the mechanism that O. patagonica became resistant to V. shiloi. Corals as all invertebrates lack as adaptive immune system with the ability to produce antibodies, so what was the mechanism for this resistance?

Several prevalent bacterial strains were isolated (culture dependent methods) from healthy O. patagonica colonies in order to test for the presence of causative bleaching and V. shiloi protective bacteria. DNA was extracted from pure colonies and 16S rRNA sequences identified using GenBank. Isolated bacterium EM1 was found to be a strain of Vibrio coralliiyticus (99.8 % identity), whilst bacterium EM3 was found to be a new candidate species/genus with only 94.8 % similarity to Vibrio hepatarius. Cross-streaking and liquid culture experiments identified that bacterium EM3 produced an extracellular diffuse inhibitor that prevented growth of V. shiloi specifically, but had no effect upon bacterium EM1.

O. patagonica fragments collected from reefs in the Eastern Mediterranean were subject to three experimental laboratory treatments. Treatment 1 (colonies n=28) induced bleaching through gradual temperature increase to mimic summer environmental conditions. The temperature was raised to 31 °C causing 86 % visual coral bleaching. The second treatment (n=34) mimiced the first, gradually increasing water temperatures, but at 28 °C a 24hr antibiotic treatment (nalidixic acid, chosen for its effectiveness against coral associated bacteria) was administered. The water temperature was subsequently raised to 31 °C. Only 29 % visual bleaching was observed, whilst zooxanthellae counts were 5.3 fold higher than temperature induced bleaching without antibiotic treatment. In the third treatment independent addition of V. shiloi (coral colonies n=12) and bacterium EM1 (coral colonies n=6) to antibiotic treated O. patagonica coral fragments at 31 °C increased visual bleaching to 83 % and reduced zooxanthellae counts by 50 and 75 % respectively.

This study demonstrated that antibiotics can be protective against heat-induced bleaching for Oculina patagonica. Traditionally bleaching has been thought to be mediated by reactive oxygen species ‘leakage’ from the decoupling of photosynthesis in the zooxanthellae host. Since antibiotics would have little effect upon the rate of photosynthesis and ROS production, alternative causes for bleaching must be sought. The coral holobiont and probiotic hypothesis fits well with the results from this study.

The coral probiotic hypothesis is a recent advent of the holobiont hypothesis and postulates that beneficial bacteria acquired by the coral host help defend against infection, disease and bleaching. In this way corals can rapidly ‘adapt’ to changing environmental conditions. It is likely that excessively high temperatures act as a structuring mechanism upon the associated microbial community of the coral leading to an increase in expression of virulence genes and bleaching. Vibrio species are known coral pathogens, whilst in this study inoculation of O. patagonica with V. coralliiyticus induced bleaching in 5 out of 6 antibiotic treated corals. Antibiotic treatment in this study reduced water Vibrio spp. counts 670-fold, correlating with a significant reduction in bleaching, implicating vibrio species such as V. coralliiyticus as important bleaching mediators under stressed conditions.

Interestingly, the diffuse antimicrobial produced by bacteria EM3 seems to explain the ability of O. patagonica to resist V. shiloi infection as observed in the Eastern Mediterranean since ~2002. The incorporation of this strain into the coral holobiont with its antimicrobial action may confer a fitness advantage to O. patagonica in the Eastern Mediterranean sea. However the exact nature of this proposed antimicrobial is unknown and deserves further investigation. It is also unknown how the coral acquired strain EM3, presumably from the water column. Due to the specific nature of host/microbial association and temporal and spatial variation in microbial water column communities it would be informative to discover how ubiquitous strain EM3 is.

This study and its discovery of causative bleaching bacteria and protective bleaching bacteria is an effective step forward in the illumination of coral health, increasingly important in the 21^st centuary as we try to understand and conserve our ocean’s rainforests. I would like to see further study look at the comparative actions and interactions between the traditional ROS mediated bleaching hypothesis and the more recent hypothesis of microbial mediation. Likely their action is not independent, but synergistic. 

Reference:

Mills, E., Shechtman, K., Loya, Y., & Rosenberg, E. (2013). Bacteria appear to play important roles both causing and preventing the bleaching of the coral Oculina patagonica. MEPS, 489, 155-162.