The idea that mass coal bleaching is caused by bacteria bleaching as opposed to temperature stress has been quite a contentious issue over the past decade. Despite the fact that massive amounts of evidence that have accumulated that support the idea that thermal stress has driven the mass episodes of coral bleaching (pigment loss associated with the dissociation of the symbiosis between coral and their dinoflagellates) over the past 30 years, some oxygen has been given to the alternative idea that mass coral bleaching is triggered by the presence of bacteria from the genus Vibrio.The idea that bacteria were involved in triggering coral bleaching originated from work done on the temperate coral Oculina patagonica from the Mediterranean sea (an invading species from the Atlantic coast of South America) seemed to suggest that the annual coral bleaching was due to a bacterial infection from a putative pathogen, Vibrio shiloi.
This discussion focuses on recent work done by my laboratory and which was published in the Nature journal ISME (download here) and which suggests that bacteria are not responsible for triggering mass coral bleaching (in O. patagonica or anything else). We are interested in your thoughts and hope that you will comment in the hope of resolving debate over this issue for once and for all.
The Bacterial Bleaching Hypothesis is based on a series of eloquent microbiological investigations conducted by Eugene Rosenberg and his group revealed the intra-cellular penetration, multiplication and subsequent cellular lysis of zooxanthellae by V.shiloi resulted in the annual bleaching of O.patagonica in temperatures above 28ºC. Since then, the bacterial bleaching hypothesis has been extrapolated as an explanation for global mass coral bleaching, and more recently, the coral ‘probiotic hypothesis’ (link). To some (including Eugene Rosenberg), the workplace emphasis onto bacteria rather than climate change as the cause for mass coral bleaching – the implications for the future of coral reefs would be highly significant if Rosenberg were correct.
This work has attracted considerable press. Here as an excerpt from the New Scientist magazine back in 2003:
“This much we know: coral bleaching is a modern epidemic that some biologists predict will kill up to half the world’s reefs this century as climate change raises sea temperatures. What we have missed is that some bleaching may actually be an infectious disease spread by a worm, a ‘malaria of the oceans’Corals depend on algae inside their bodies to provide carbohydrates and oxygen through photosynthesis. This partnership allows corals to thrive in infertile areas of ocean, and explains why reef communities are so rich.
But when water temperature rises, the algae either die or the corals eject them in response to the stress of the heat. Before too long the entire reef turns white. It is unclear how well reefs later recover, and the sharp rise in coral bleaching since the 1980s has sparked dire predictions for their future.
Most marine biologists agree that bleaching is caused by rising sea temperatures, and the best way to stop it is to cut carbon emissions. But that is an indirect, long-term strategy that may not save reefs in time. Now there may be a more immediate remedy.
In the late 1990s, Yossi Loya and Eugene Rosenberg led a team from Tel Aviv University that found a bacterium that causes coral bleaching. Crucially, it turns out to be more virulent at higher temperatures. “Coral biologists are not microbiologists,” says Rosenberg. “They saw the association of bleaching with temperature, but they did not see the bacterium.”
Rosenberg says his team is now developing a technology that could help prevent the disease’s spread, although he would not reveal details. He suspects much of the world’s coral bleaching is caused by similar pathogens, and some of them may have different vectors. This year, he showed that another new bacterial species, Vibrio coralliilyticus, causes bleaching in a Red Sea reef coral.
Ove Høegh-Guldberg, a coral bleaching expert and director of the Centre for Marine Studies at the University of Queensland, thinks mass bleaching events move too quickly to be caused by an infectious disease. “But it is possible that this microbe naturally inhabits corals, a bit like Escherichia coli in the human gut, and temperature increases cause it to trigger bleaching,” he says.
However, until recently, the V.shiloi / O.patagonica model of bacterial bleaching has remained a laboratory based experiment, with no field validation from samples collected in the wild. Having field validation is critical for this idea. After all, there are any number of examples where scientists have been fooled by laboratory artifacts. In terms of understanding climate change, I felt that it was very important to check these ideas out.
Consequently, in 2005, students and researchers from my lab spent 6 months in Israel exploring the microbial ecology of Oculina patagonica in the Mediterranean Sea, which has resulted in a recent publication in the Nature journal ISME (Download the .pdf here)
Our team made the surprising discovery that Occulina patagonica off the Medditeranean coast of Israel (the same place where the specimens were collected for the numerous studies by Rosenberg and colleagues) bleached without any Vibrio being present.
The team from my laboratory documented the natural microbial community of the Oculina patagonica during a survey of the annual bleaching event. Our research determined that the microbial community shifts are complex, and resulted in significant shifts in the endolithic population associated with the bleaching of the host tissue. In contrast to previous studies by Rosenberg et al, Vibrio could not be detected within the host tissues, despite continued active bleaching and degradation of the symbiosis. This was not consistent with Vibrio being the cause of coral bleaching in Oculina patagonica.
This study is the first to determine microbial communities associated with the bleaching of O.patagonica under field conditions, which are in sharp contrast to previous laboratory “infections” of this temperate coral. The complete absence of intra-cellular bacteria (including V.shiloi) from corals collected in the wild is a surprising finding, and raises considerable doubt as to the generality and basis of the bacterial bleaching hypothesis.
In order to clarify this important work, I asked Dr Tracy Ainsworth (the lead author of the paper and former PhD student from my lab) to respond to a few questions associated with this study:
1. What is the basis for the idea that bacteria cause bleaching?
The hypothesis that bacteria cause bleaching in reef building corals comes from research on the annual bleaching of the temperature coral Oculina patagonica along the Mediterranean coastline. This bleaching event has been recorded annually for the past 14yrs. Laboratory based studies on the microbiology of this bleaching event has provided evidence that an intracellular pathogen causes lysis of the symbiotic dinoflagellate and ultimately bleaching of the coral host. These studies have focused on experimentally inducing bacterial-like signs in laboratory captive animals in order to understand the mechanisms by which the pathogen could illicit bleaching in the coral host in nature.
2. What was your original intention in undertaking the study?
Originally our research here aimed to apply a particular technique combining fluorescence in situ hybridization (FISH) and spectral imaging, which allows us to image and microscopically analyze particular types of bacteria that are associated with coral tissues, to a system described as a close intracellular association between a coral and a bacterial pathogen. This association had not previously been followed within a field or ecological situation over an entire bleaching event using an in situ technique. Here we aimed to use this technique to watch when and how the specific bacterial-coral association progressed and developed from healthy coral prior to the onset of summer, during the several month long bleaching of the host, until the loss of the coral tissue prior to the coral recovery and re-growth at the onset of winter. This involved sampling coral colonies along the coastline prior to, and throughout, the bleaching event and conduct microscopic studies of the coral tissues throughout a 6-month long sampling program.
3. What was new about your approach (question, field, technology) to this issue?
The technique we used combines FISH (a widely used technique in microbiology) and spectral imaging of the extremely fluorescent coral host tissue, and was found in other corals we studied to be a very effective, reliable, and rapid method to study coral-bacterial interactions. It is also very sensitive and can detect a few cells if they are present. Many studies have previously used bacterial culture techniques and bacterial sequencing, however these techniques give us the bigger picture of the microbial communities associated with the entire coral, but they are not able to let us see the finer, small-scale detail of coral-bacterial associations. For instance, by using the imaging technique we can see the bacteria that are closely associated within the coral tissue layers and cells, the disease lesion, and the other components of the coral holobiont such as the endolithic community within the coral skeleton. Techniques using bacterial culture and sequencing techniques combine all these finer scale regions into a single sample for analysis. Using a fine-scale approach can be important in studying the intra or extra cellular nature of the coral-bacterial association, and the location of the bacteria that are associated with the coral, and can give us insights into the role of the bacterial populations. For example the endolithic population maybe mistaken for being within the coral tissues, when they are in fact within the coral skeleton and clearly separated for the coral tissues.
4. Do you think there are any holes in this new idea that bacteria are not involved in coral bleaching?
We conducted positive controls (actually applying Vibrio to samples to show we could detect them if they were present) to ensure that our techniques and hence conclusions were reliable within this situation. We were able to successfully visualize the bacterial community within the host tissues from the experimentally, bacterial bleaching laboratory scenarios. We have also successfully used this technique to investigate bacterial populations associated with many other diseased corals. This evidence strongly suggests that there is currently no intracellular bacterial proliferation associated with the bleaching of the temperature coral Oculina patagonica in the field.
While not detracting from the previous work (except in terms of its relevance to the field and to bleaching in general), these results raise some other interesting questions on coral microbial ecology. Importantly, secondary bacterial colonization after a primary environmental stress to coral colonies may have very important implications to the future outcomes to the coral colonies. For instance, the organism does not only have to overcome the loss or breakdown of its valuable symbiosis, it also has to illict immune responses to overcome changing microbial communities and bacterial/microbial colonization and overgrowth. We suggest that understanding the timeline of changes associated with coral bleaching and the finer scale of coral-microbe interactions is important in understanding the long-term impacts of environmental stress to coral reefs.
Although there has been considerable debate within the literature, the future of the “bacterial bleaching hypothesis” seems somewhat limited. There are many questions yet to be resolved in the field of coral disease, and we are only beginning to understand the importance and diversity of coral – microbial interactions. A key question stemming from this research: do microbial populations play an important secondary, rather than primary, role in coral bleaching? How do impacts such as thermal stress influence our interpretation of coral-microbe interactions and the role of the coral host?
One question that has been resolved to my satisfaction is whether or not mass coral bleaching is caused by a bacterial pathogen or not . In my view, there is no longer any evidence to support the bacterial bleaching hypothesis. What do you think? I look forward to hearing from you.