(2009) Mieog, Jos Cornelis
Abstract
Scleractinian corals are ecosystem engineers and the growth and maintenance of coral reefs relies heavily on the success of these organisms. A key aspect of their success is the symbiotic relationship with single-cell algae of the genus Symbiodinium — also known as zooxanthellae. These algal (endo)symbionts provide the coral host with most of its nutrition and enhance the calcification process (skeletal growth), allowing it to thrive in oligotrophic waters. However, climate change is threatening this association, as seawater temperatures of only 1C above the long-term mean summer maximum can lead to a disruption of the symbiosis. When this happens, the zooxanthellae are expelled from the host tissues. If zooxanthella loss is severe, corals turn bright white as their calcium skeleton becomes visible through the now-transparent host tissue. This process is, therefore, referred to as coral bleaching. Severe and/or prolonged bleaching can result in colony mortality.
Zooxanthellae are, however, not all the same. A huge diversity of phylotypes has been identified within the genus Symbiodinium (presently eight “clades” are distinguished, with multiple “types” within each clade) and many of these symbiont types are strongly correlated with differences in holobiont (coral host plus algal symbionts) physiological performance — heat tolerance in particular. Thus, it has been hypothesized that association with different symbiont types provides physiological flexibility to corals and, therefore, a mechanism to respond to rising seawater temperatures. Bleaching — as stated in the Adaptive Bleaching Hypothesis (ABH) — provides an opportunity for corals to change their resident symbiont community from a heat-susceptible one into a more heat-tolerant one, and, as a result, become more thermo-tolerant themselves.
The central aim of this thesis was to assess the potential of the mechanisms described by the ABH to: (1) induce changes in the symbiotic communities of coral, and (2) mitigate the effects of global warming on coral reefs.
The first question that was asked was:
What is the source of the new, heat-tolerant symbiont type that becomes dominant while the coral is recovering from bleaching?
Two possible sources were identified: (1) the new symbiont is already present al low abundance in the coral host before bleaching, and increased in relative abundance (symbiont shuffling), or (2) the new symbiont is taken up from the environment (symbiont switching).
In Chapter 2 the potential for symbiont shuffling was assessed. At the beginning of the study (April 2004), it was generally believed that most corals only harbored one clade of symbionts, implying a low potential for symbiont shuffling because the mechanism requires a diverse in situ symbiotic community. However, we questioned this notion as a possible artifact of the limited detection abilities of the techniques commonly used in symbiont diversity studies. Electrophoretic techniques have a high resolution for discriminating different symbiont types, but a low sensitivity for detecting symbiont types that occur at (very) low, background levels symbiont types occurring in relative abundances below 5-10% of the total symbiont community would therefore have missed detection.
We developed a novel, real-time PCR assay that boosted the sensitivity for background clade detection over 100-fold. This assay was then used to re-screen a sample collection consisting of four common species of hard corals collected across the Great Barrier Reef (GBR) of Australia. These samples had been previously analyzed using standard electrophoretic techniques and only one symbiont clade per sample had been detected in all cases. Using our new real-time PCR assay, we were able to show that 78% of the corals sampled actually did harbor a background clade, indicating that the potential for symbiont shuffling was much larger than previously thought. Notably, most corals predominantly harbored Symbiodinium clade C, with the clade D occurring at background levels, and clade D zooxanthellae are generally considered to be more thermo-tolerant.
The real-time PCR assay was further developed in Chapters 3 and 4. The initial assay used the ITS1 region, which exists in the genome in many tandem-repeated copies. The number of copies can vary significantly between closely relate cells (e.g. within a type), which resulted in a loss of accuracy because of uncertainties in the translation of measured ITS1 copy numbers to symbiont cell numbers. In the optimized assay, introns of the actin genes were targeted (which were established to be single-to-low copy number loci in the symbiont genome), which increased the accuracy of the assay an estimated 10-fold. Another improvement was the introduction of a symbiont density measure the symbiont cell/ host cell ratio (S/H ratio) by determining the cell numbers of both the coral host and the algal symbionts within a DNA sample. The high variability of the intron region also allowed type-specific analyses within clade C.
In Chapter 4, the real-time PCR assay was used to investigate the potential for symbiont switching. Nine colonies of the common reef-building coral Acropora millepora — which harbored predominantly Symbiodinium clade D with a type C1 background — were experimentally bleached using the herbicide DCMU (diuron). The corals were then allowed to recover in the presence of high levels of environmental zooxanthellae belonging to Symbiodinium type C2*. Real-time PCR analyses showed that the corals underwent a moderate to severe bleaching response, followed by significant recovery. However, unforeseen problems related to the used coral population and the environmentally administered atypical symbiont type led to inconclusive results; improvements to the experimental design are discussed to assist future studies evaluating this mechanism of symbiont change.
The next set of questions was:
To what extent does the symbiont type shape coral fitness, and what are the relative contributions of the coral host and the local environmental conditions?
Are there trade-offs between heat-tolerance and other favorable characteristics (such as high growth rate) and what defines them?
Previous studies convincingly showed how symbiont type shaped certain physiological parameters. However, it was still largely unknown how strong the influence of the symbiont type was on the holobiont’s fitness compared to coral host population and/or the local environmental conditions, and how these factors affected each other. In order to study all three factors simultaneously, custom holobionts were prepared, i.e., coral-Symbiodinium associations from which the genetic make-up of both the coral host and the algal symbiont were experimentally controlled (Chapter 5). A. millepora colonies were collected from two contrasting locations and allowed to spawn in the laboratory. Azooxanthellate juveniles were then exposed to six types of Symbiodinium spanning clades A, C and D. Once symbioses with the newly settled coral juveniles were established, the custom holobionts were (partially reciprocally) outplanted back to the two contrasting locations of the two original A. millepora populations. Over the next 7-8 months, their growth and survival were monitored, after which the custom holobionts were returned to the lab for the assessment of their thermo-tolerance. The results showed that symbiont type was the strongest predictor for holobiont fitness. In contrast, almost no host population effects were evident on growth, survival, or heat-tolerance. D holobionts were the most thermo-tolerant, whereas A holobionts were the most thermally sensitive.
The ABH predicts that trade-offs are likely to exist between thermo-tolerance and other favorable characteristics, explaining why thermo-tolerant symbionts are not dominant in the absence of heat-stress. We found a trade-off between growth (and, to a lesser extend, survival) and heat-tolerance. However, this trade-off was dependent on the environment, as growth (and survival), but not heat-tolerance, was secondarily shaped by the local environmental conditions.
The next question asked was:
What is the field evidence for the ABH?
In a collaborative project led by fellow PhD candidate Alison Jones (Central Queensland University, Australian Institute of Marine Science), seventy-nine corals of an A. millepora population situated on a southern inshore reef of the GBR were randomly tagged and followed through a natural bleaching event (Chapter 6). Prior to bleaching, the population harbored predominantly thermo-sensitive Symbiodinium C2 (93.5%), while the remaining corals harbored a more tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving colonies that harbored C2 changed to D or C1 predominance. Corals that were associated with C2 before bleaching had higher mortality rates (37%) than colonies that already were associated with D (8%). In total, only about 18% of the original A. millepora population survived unchanged, showing the magnitude of the effect of the bleaching event on the Symbiodinium community structure for this population. The change towards more thermally tolerant symbiont types, as predicted by the ABH, is likely to have substantially increased the thermal tolerance of this coral population. This study showed, for the very first time, that symbiont change after bleaching does happen at large scales under field conditions.
The last question investigated in this thesis was inspired by the results described in Chapter 5:
What is the cause of the large difference in growth between A. millepora juveniles harboring C1 or D at Magnetic Island?
In Chapter 7, a second collaborative project was conducted with fellow PhD candidate Neal Cantin (James Cook University, Australian Institute of Marine Science). This study investigated the link between the photosynthetic and photosynthate incorporation in 9-month old C1 and D corals (A. millepora). The results showed that C1 corals had an 87% greater PSII photosynthetic capacity than D corals, and that this was correlated with a 121% higher translocation of photosynthate to the coral host. Exposure to diuron (DCMU, a herbicide that inhibits electron transport) resulted in a loss of the difference between C1 and D holobionts for both photosynthetic capacity and photosynthate translocation, further supporting the link between these two processes. We concluded that the greater carbon delivery from Symbiodinium C1 allowed faster growth, which most likely provided the C1-holobionts with a competitive advantage since rapid early development typically limits mortality (see Chapter 5).
CONCLUSIONS
The severe damage to coral reefs caused by climate change over the last decades has raised major concerns about the future of these ecosystems (Hoegh-Guldberg 1999; Hoegh-Guldberg et al. 2007). The research described in this thesis has found significant support for the ABH (Buddemeier & Fautin 1993; Buddemeier et al. 2004) as a mechanism — available to at least certain corals — for responding to the threat of rising seawater temperatures. Our evidence includes: (1) the high incidence of (thermally tolerant) clade D backgrounds, that may allow corals to shuffle their symbionts after bleaching, in four of the most common scleractinian species on the GBR, (2) the realization that symbiont type (at least in A. millepora) is the most important predictor of holobiont fitness, and (3) a Symbiodinium community change in an A. millepora population following a natural bleaching event, resulting in an increased thermo-tolerance for that population. These results showed that changing algal symbionts is an important mechanism for reef acclimatization in an era of climate change.
Many aspects of the ABH are still unknown, limiting our ability to predict the acclimatization potential, and further studies are urgently needed. First, the analyses of symbiont backgrounds have to be expanded to include other coral species and locations. We must also move to the subcladal level with these surveys, as physiological differences between Symbiodinium types within a clade can be as important as differences between types from different clades (Tchernov et al. 2004). Second, the generality of symbiont shuffling has to be determined, i.e., how many coral species can actually do it and do the same symbiont changes have similar effects in different coral species (e.g. Abrego et al. 2008)? Third, symbiont switching needs to be further examined; if it can happen on a similar (or larger) scale as shuffling, reef resilience would be significantly affected. Fourth, the influence of more symbiont types on the holobiont physiology needs to be examined, which can be accomplished by raising custom holobionts. Finally, the possibility of symbiont change over generations, rather than during the coral colony’s life, should be investigated (Baird et al. 2007).
The capacity of the ABH to mitigate the effects of global warming must not be overestimated for several important reasons. First, coral colonies may have to bleach first before symbiont change can take place (Buddemeier & Fautin 1993; Baker 2001; Berkelmans & van Oppen 2006), possibly causing high mortality in the process. Second, newly shuffled (or switched) corals that have successfully recovered from bleaching are still likely to be impaired in growth and reproduction (Baird & Marshall 2002). Third, if the stressor disappears for a prolonged period of time, the corals may change back to the original symbiont (Thornhill et al. 2006), leaving them again vulnerable to the next round of bleaching events. Last, the maximum extra heat-resistance that corals may gain by changing their symbionts may only be 1-1.5°C (Berkelmans & van Oppen 2006), which will be insufficient within the coming century if the most recent predictions of the Intergovernmental Panel for Climate Change are accurate (1.5-4C increase in the tropics by the end of this century; IPCC 2007).
On a more optimistic note, symbiont change is likely to play a positive role in the way some corals cope with global warming conditions, leading to new competitive hierarchies and, ultimately, helping to shape the coral community assemblages of the future. Most importantly, an increase in reef thermo-tolerance of 1-1.5C buys time — approximately 50 years (Donner et al. 2005) — in which measures for the reduction of greenhouse gas emissions can be implemented so that, hopefully, a catastrophic effect of climate change on coral reefs is avoided.
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