Thursday, 10 January 2013

Ciliates- the true instigators of White Syndrome in corals?



Although coral diseases have a major impact on coral communities, the highly complex host-pathogen interactions, influenced by bacterial community composition and environmental variables, complicate the identification of causative agents. For instance, the proposed pathogens Vibrio coralliilyticus, V. shiloi and V. harveyi are not only associated with diseased coral, but have also been detected in apparently healthy corals with increasing abundance during disease or stress. So it has been proposed that all infectious agents are opportunistic and that immunocompetent organisms can host many pathogens without any symptoms. 


Sweet and Bythell (2012) focused on one of the most ecologically important coral diseases, namely white diseases/syndromes, collectively known as White Syndrome (WS), including White Plague and White Band Disease. In fact, previous studies had failed to provide evidence for any bacterial populations associated with the pathogenesis or bacterial-induced necrosis. Moreover increasing evidence suggests that ciliates and other protozoans can also act as pathogens in coral diseases such as skeletal eroding band and Brown Band Disease (BrB). That’s why the presented study aimed to provide a comprehensive, culture-independent molecular analysis of both ciliate and bacterial communities associated with WS with Brown Band Disease as reference of known ciliate-associated syndromes as first step towards understanding the causal agents of WS. 


In order to make a clear difference between agents that are directly involved in pathogenesis and microbes that colonise dead and decaying tissues only after the disease has started spreading, the progression of the disease was monitored to ensure samples only represented actively progressing disease lesions. 


DGGE revealed significant differences of bacterial 16S rRNA between non-diseased colonies, the apparently healthy tissues adjacent to the disease lesion and the disease lesion. However, to the surprise of the authors, no significant difference was detected between samples from WS- and BrB- diseased corals. 


Arcobacter sp. was the only bacterium that showed a marked increase in abundance in the disease lesion, whereas it was only apparent in the healthy tissues and absent from non-diseased tissues. Other bacteria, such as V. harveyi and Glyomyces sp., were present in low abundance in non-diseased corals and increased both in apparently healthy tissue and at the disease lesion itself. 


However, no ciliates were observed or detected by molecular screening in samples of non-diseased and apparently healthy coral samples. Moreover, time-lapse videography was used to follow pathogenesis and a number of ciliate morphotypes were observed to actively engulf coral tissues at the site of lesion progression. In fact, the two dominant ciliates (Morph1 and Morph2), detected in both WS and BrB samples, actively burrowed into and beneath the live, intact coral tissues. 


These observations (also see link for videos) led to the conclusion that ciliates are largely responsible for the macroscopic signs of both WS and BrB. Furthermore because of the strong similarities in both bacterial and ciliate communities associated with WS and BrB, Sweet and Bythell suggest that they are actually the same disease and should be synonymised in future! 


The study did not allow identifying the causative agents for WS, but two different hypotheses are proposed and offer perspective for future research: (i) Bacteria e.g. Arcobacter sp. as primary causal agents, with ciliated invading already weakened tissue (ii) ciliates cause WS with bacteria infecting the host only after ciliate pathogenesis (supported by the observations of this study).


While the major spotlight was on bacterial pathogens, is it possible that the involvement of ciliates in coral diseases has just been overlooked? This study illustrates the extreme complexity of studying coral diseases and how difficult it is to distinguish between who runs riot and who just follows the trend. 


Here are two time-lapse videos showing the progression of WS and BrB:


Sweet, M. & Bythell, J., 2012. Ciliate and bacterial communities associated with White Syndrome and Brown Band Disease in reef-building corals. Environmental microbiology, 14(8), pp.2184–99.

5 comments:

  1. Hi Anna, really interesting post. I think it is quite likely that organisms such as the ciliates have been overlooked when it comes to coral disease. I've had a look at the videos, I wish they were a bit slower as I can't really see any of the detail of what is happening. In your opinion, how convincing is Sweet and Bythell's evidence to support the ciliates cause WS hypothesis?

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  2. Hi Vicky
    I agree, it would have been interesting if they had recorded the burrowing into the coral tissue. The legend for the video says: Time-lapse microvideography of lesion progression in White Syndrome. A diverse ciliate community can been seen massing at the edge and underneath the tissues at the lesion edge. Polychaete worms can also be seen predating on the ciliates. Individual ciliate cells of the smaller morphotype, Morph1 cannot be seen at this magnification and appear as yellowish masses. Video sequence is 300 frames at a sampling rate of 3 min per frame.

    The fact that ciliates were only found in diseased samples and that they actively burrowed into apparently healthy tissue seems to provide strong evidence that ciliates are involved in WS. However, what factor(s) allows the colonisation of the healthy coral in the first place is still unknown. The authors make clear that their paper should be considered as first step towards understanding WS causation and don't exclude the possibility that bacteria could be the primary causal agents. The paper provides a list with descriptions of the main ciliates found in this study for future reference.

    So overall I think ciliates should not be omitted in future coral disease studies. The next step would be to isolate the ciliates (above all Morph1 and Morph2) and to test whether they cause WS in healthy coral samples under different environmental conditions. Could it be possible that stress induced (high temperature?) microbial community change in the coral allows the colonisation by ciliates in the first place? Are there any antagonistic interactions between ciliates and bacteria, or do some bacteria favour ciliate colonization?

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  3. Out of interest mainly in the method, was this videoed in the field or lab? Or were the diseased corals collected from the field and videoed in the lab?

    I would certainly be interested to see how this topic progresses! Like you've said the priority here is to isolate the ciliates and see if they can cause disease on their own in healthy samples.

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  4. In order to make sure that the samples for the category "diseased" were actually showing actively progessing lesions, the corals were tagged and photographed over four days, before diseased samples were taken. They say that additional samples were collected for the microscopy work, so the videos were recorded in the lab. I guess it's easier to manipulate in the lab, e.g. right illumination. Also the microscope and cameras used do not seem to be resistent to water. Whether the progression of lesions shown in the video is a true representation about what is happening in the environment remains unknown.

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  5. Hi Anna and Vicky. There's some great dialogue here and insight to the paper. You may like to check this earlier paper that reveals how the ciliates harvest the zooxanthellae. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1828814/

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