The
“Extended” Coral Holobiont: Truth or Fiction?
The term “coral holobiont” refers to the mutualistic
relationship between coral animals and a diverse range of microorganisms (dinoflagellates,
bacteria, archaea, fungi and viruses). As discussed in lectures and many
previous blogs, there is a growing appreciation in science for the fundamental dependence
of all macroscopic organisms on microbes. In particular there is an increasing
opinion that a healthy coral reef has a certain signature of associated
microbial life, and in shifting into a diseased state, the associated microbial
consortium also changes. A major contribution to the growing appreciation of
microbial life is the rapid development of molecular and genetic tools to
assess diversity, population numbers and metabolic interactions within ecosystems.
As powerful molecular survey techniques have taken over the literature,
unfortunately the limitations, and potential contaminations, of such methods in
many cases have been forgotten. The reviewed paper does not use fashionable
molecular techniques, but instead aimed to visualise any adherent microbial
presence on the surface of normal, presumed healthy, Porites compressa using scanning electron microscopy (SEM).
Johnston & Rohwer (2007) collected coral
fragments from a reef around Coconut Island, Hawaii. Fragments were mounted
onto plastic splints and kept in aquaria for several days for observations
(polyps extended or contracted), before being fixed for electron microscopy.
The fixation technique used was particularly important as it was exceptionally
fast; the modified Parducz fixative was fast-acting enough to fix expanded
polyps in a state of only partial shortening of the tentacles. Other
traditional fixatives cause living corals to contract into their skeleton
before the coral’s structural and metabolic components are inactivated and
chemically preserved. In contrast to many previous reports, Johnston &
Rohwer found no evidence for microbial life living directly on coral epidermal
cells. Specifically the authors report that corals with extended polyps were clean
of directly adhering microbes and evidence of adhering material was limited to
clumps, or flocs, of detrital material on the occasional sample. Samples which
had permanently retracted polyps had developed a stable mucous sheet which
became heavily colonized by both prokaryotic and eukaryotic microbes. However,
the microbes did not penetrate the mucous sheet and the animal’s epidermal cell
surfaces remained sterile.
In 2003 Nancy Knowlton and Forest Rohwer published
a key paper proposing corals as a more extensive holobiont. In this important
publication the authors recognised microbial associates of reef corals are
largely unknown, but describe preliminary studies which indicate that
individual coral colonies host diverse assemblages of bacteria. Since 2003
there has been a huge explosion of coral-microbe investigations. The results
reported by Johnston & Rohwer (2007) in no way rule out the theory of coral-microbe
mutualisms, however they conceivably change the way we think of the overall
holobiont. Perhaps the more extensive holobiont consists of a dynamic community
of microorganisms hovering in the boundary layers of water immediately above
the epidermis rather than in the tissues or directly adhered to cell surfaces.
It is difficult to understand just how the reviewed work fits into the coral
holobiont literature, it is hard to imagine that hundreds of molecular surveys
are incorrect and merely an artefact of contamination or mucus associated
bacteria alone. In my opinion the most important conclusion of Johnston &
Rohwer’s work is that molecular techniques should not proceed in isolation,
methods such as SEM and FISH should be included as protocol to increase understanding
of the spatial distribution of microorganisms in the coral holobiont. I think
the study would have been more complete if accompanied by a molecular survey of
a subset of samples; this would have provided direct comparisons between
techniques and given the contradictory results more validity.
Johnston, I. S.,
& Rohwer, F. (2007). Microbial
landscapes on the outer tissue surfaces of the reef-building coral Porites
compressa. Coral Reefs, 26(2), 375–383.
Hi Vicky,
ReplyDeleteFirstly, great post! I totally agree that future studies would benefit from a more integrated approach including both optical analysis and culture independent techniques. The only study I have read which integrates both approaches is a key paper by Frias-Lopez et al. (2002).
The idea you propose regarding the extensive holobiont was particularly interesting and something which I was unaware of but as you say, it is hard to imagine that so many molecular surveys could be the product of contamination. The publication by Frias-Lopez et al. (2002) also studies coral associated bacteria on the tissue surfaces on three coral species (2 Monstastrea and 1 Diploria). Culture independent methods revealed distinct bacterial communities inhabiting healthy coral tissue which was confirmed by SEM analysis as occurring within a stringy exopolymer matrix on the tissue surface.
I think the absence of adhered cells on the coral used in the study you’ve reviewed could be an evolutionary adaptation of this coral, or possibly the family Proitidae. After reading some of the literature, they seem to be particularly robust, being less suspectible to a number of diseases when compared to other coral species/family. In the Frias-lopez et al. paper, the bacterial communities of healthy, BBD (black band disease) and dead corals are compared using the techniques stated above. The authors conclude that dead coral tissues are devoid of BBD bacteria as the microbial mat migrates across the coral. Perhaps, without an original matrix formed by bacteria and host, some diseases may find it particularly difficult to colonise these tissues?
Scott.
Here’s the reference for the Friaz-Lopez paper, if you’re interested.
Frias-Lopez, J., Zerkle, A.L., Bonheyo, G.T. and Fouke, B.W. (2002) Partintioning of Bacterial Communities between Seawater and Healthy, Block Band Diseased, and Dead Coral Surfaces. APPLIED AND ENVIRONMENTAL MICROBIOLOGY 68, 2214-2228.
Hi Scott,
ReplyDeleteThanks for your comment and for bringing up the interesting work by Frias-Lopez et al., I was surprised to hear you were unaware of the extended coral holobiont theory considering we’ve had lectures on it (from Emma) haha!
Frias-Lopez and colleagues work was certainly important in the lead up to the ‘coral as an extensive holobiont’ theory, by the sounds of it they had the right idea when it comes to methodology. I just don’t know why more studies don’t combine molecular techniques with SEM; it seems like everybody has forgotten that there are serious limitations to genomic methods and don’t even acknowledge them, never mind account for them.
I think disease pathogens are certainly opportunistic, and like you said exploit an already established relationship. In the future I think it’s going to be really important to consider disease as multifactorial and dynamic process, and like you say, differing susceptibilities are likely to be important too. Maybe it would be important to get a more mechanistic understanding of what is driving the resilience observed by certain taxa.
Thanks,
Vicky