Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus

Abstract

Coral bleaching is the disruption of symbioses between coral animals and their photosynthetic microalgal endosymbionts (zooxanthellae). It has been suggested that large-scale bleaching episodes are linked to global warming. The data presented here demonstrate that Vibrio coralliilyticus is an etiological agent of bleaching of the coral Pocillopora damicornis. This bacterium was present at high levels in bleached P. damicornis but absent from healthy corals. The bacterium was isolated in pure culture, characterized microbiologically, and shown to cause bleaching when it was inoculated onto healthy corals at 25 degrees C. The pathogen was reisolated from the diseased tissues of the infected corals. The zooxanthella concentration in the bacterium-bleached corals was less than 12% of the zooxanthella concentration in healthy corals. When P. damicornis was infected with V. coralliilyticus at higher temperatures (27 and 29 degrees C), the corals lysed within 2 weeks, indicating that the seawater temperature is a critical environmental parameter in determining the outcome of infection. A large increase in the level of the extracellular protease activity of V. coralliilyticus occurred at the same temperature range (24 to 28 degrees C) as the transition from bleaching to lysis of the corals. We suggest that bleaching of P. damicornis results from an attack on the algae, whereas bacterium-induced lysis and death are promoted by bacterial extracellular proteases. The data presented here support the bacterial hypothesis of coral bleaching.

FIG. 1.

Electron micrograph of negatively stained V. coralliilyticus YB1. Bar = 0.2 μm.

FIG. 2.

Healthy (a), bacterium-bleached (b), and bacterium-lysed (c) P. damicornis. The bleached coral (b) was estimated to be 90% bleached compared to the uninoculated control (a); the lysed coral (c) was estimated to be 50% lysed.

FIG. 3.

Electron micrograph of a thin section of a bleached P. damicornis coral, 13 days after infection with V. coralliilyticus at 24.5°C. Bar = 0.5 μm.

FIG. 4.

Extracellular protease activity of V. coralliilyticus YB1 as a function of growth temperature. Strain YB1 was grown with aeration in MBT medium at different temperatures. Values for culture turbidity (A₆₀₀) and extracellular protease activity (units) were determined during the exponential and stationary phases. The numbers above the bars indicate the time (in hours) when the assay was performed at each growth temperature.

FIG. 5.

Comparison of the N-terminal amino acid sequences of Vibrio proteases. The boxes enclose amino acids that are identical in all five proteases.