In Focus

Zooxanthellae (, ) symbioses on reefs

Madeleine JH van Oppen Australian Institute of Marine Science Ingo Burghardt PMB No.3, Townsville QLD 4810 Tel (07) 4753 4370 Australian Institute of Fax (07) 4772 5852 Marine Science Email [email protected] PMB No.3, Townsville QLD 4810

The large three-dimensional structures that make up disruption of the occurs. Disruption of the symbiosis is coral reefs (Figure 1) are primarily the product of calcium usually expressed as the loss of the single-celled photosymbionts carbonate deposition by zooxanthellate scleractinian and/or their photosynthetic pigments, and is a common stress , i.e., stony corals living in symbiosis with response of corals. of the genus Symbiodinium (a.k.a. ) (Figure 2). This photosymbiosis permits fast nutrient cycling in the generally oligotrophic tropical waters 1.

The zooxanthellae live inside the gastrodermal cells of the coral, translocate photosynthate to their coral and increase rates of skeletal growth. In this way, a large part of the coral’s energy requirements are met through zooxanthellae 2. The zooxanthellae receive several essential nutrients from the host and in some cases also protection from external conditions such as damaging light intensities. The coral-Symbiodinium symbiosis is obligate; corals will starve and may die if prolonged

Figure 2: Zooxanthellae type C1 70 isolated from a coral colony of tenuis, viewed through an Axioskop mot plus microscope using Differential Interference Contrast Figure 1. The colourful and healthy of Tydeman reef microscopy. Cells are 7-9 µm in diameter. Culture established in the northern . Photo credit: Eric Matson. by Walt Dunlap. Photo credit: Cathy Liptrot.

MICROBIOLOGY AUSTRALIA • MAY 2009 67 In Focus

Over the past few decades, this phenomenon – called coral It is well established that widespread or mass bleaching is caused bleaching – has been more prominent than before, a pattern by higher than usual temperatures in combination with high which is strongly correlated to increasing sea surface temperatures irradiance 13, and that bleaching is a response to elevated levels (SSTs) as a consequence of climate change 3. These mass of reactive oxygen species (ROS) in the tissues 14. There are three bleaching events have caused the loss of a significant portion of ways in which heat and light stress can result in a net production the world’s coral reefs 4, 5. Further, a recent study suggests that of ROS – (1) through damage to the reaction centre protein 15 caused by high atmospheric CO2 levels leads D1 of photosystem II (PSII) of the zooxanthellae , (2) through to under high irradiance conditions, and acts the impairment of CO2 fixation mechanisms in the Calvin cycle synergistically with high temperature to lower thermal bleaching downstream of PSII 16, and (3) through the thermal instability and thresholds 6. Ocean acidification also reduces coral growth, at disruption of the thylakoid membranes on which PSII (and PSI) least in massive corals 7. Hence, the increased greenhouse gas is located 17. Some of the ROS produced in the photosymbiont levels in our atmosphere stemming from growth in human diffuse into the host cell. High levels of ROS are also produced population size and per capita consumption impact negatively on in the host mitochondria as a consequence of temperature/light coral-zooxanthellae symbioses through both reduced growth and –induced damage to the mitochondrial membrane (reviewed increased risk of bleaching. in 18). It has recently been proposed that ROS activate the host transcription factor NF-κB, which in turn induces apoptosis of the A wide range of other cnidarian animals such as many Symbiodinium-containing host cell, either directly or indirectly corallimorpharians, zoanthids, soft corals, sea fans, anemones via the induction of nitric oxide synthase 18, 19. Nitric oxide can and some also host zooxanthellae 8, 9. In addition, also be produced by the photosymbiont and diffuse into the host non-cnidarian coral reef invertebrates and a few form cell, thereby inducing the apoptetic pathway 18. symbioses with members of the genus Symbiodinium. However, these symbioses have received far less attention and their In addition to apoptosis, a range of other mechanisms have been observed to lead to loss of photosymbionts in cnidarians 20, and sensitivity to increased CO2 and temperature are not as well understood. it is not yet clear which of these are the most prevalent during natural bleaching events, whether different mechanisms occur Symbiodinium diversity with different stressors or extent of stress, or whether these occur sequentially or simultaneously and vary between taxa. Initially, it was believed that the genus Symbiodinium is These include in situ degradation of zooxanthellae, exocytosis, represented by a single species, Symbiodinium microadriaticum detachment of zooxanthellae-containing host cells, and host cell Freudenthal 10. With the advent of molecular tools, however, it has necrosis (reviewed in 18, 20). become evident that the genus is unusually diverse and comprises at least eight divergent lineages (i.e. phylogenetic clades A-H Bleaching susceptibility and the role of the identified by DNA sequences) and many putative species, usually zooxanthellae referred to as types, e.g. C1, B3, etc. 11. Members of four of the Corals vary in their bleaching susceptibility; differences exist eight clades (A-D) commonly associate with scleractinian corals, between species 21, but also among 22 and within 23 conspecific while members of clades F and G are rare and those of clades populations. In the case of the former, a range of host animal E and H have never been observed in these reef-builders. Indo- factors, such as tissue thickness and growth form 24, skeletal light Pacific scleractinians mainly associate with Symbiodinium types scattering 25, anti-oxidant levels 26 and photoprotective pigments belonging to clades C and D. In West Atlantic scleractinian corals, 27, 28 may be responsible for the differences. In addition to host however, members of Symbiodinium B are most common, factors, exposure to high irradiance 29 or high temperature 30 prior followed by C, A and D 12. It is becoming clear that much of the to the heat stress during the summer season as well as the type genetic diversity encompassed within the genus is matched of zooxanthellae harboured 22 have been shown to play important by physiological diversity, and that the type of zooxanthellae roles in some coral-algal associations. For example, the coral harboured can shape the physiological performance of the coral associates with a range of zooxanthellae colony, including its bleaching susceptibility (reviewed in 12). types on the Great Barrier Reef 31, but those with types D and C1 Climate change and coral bleaching are most bleaching tolerant, both in the laboratory and in the field 22, 23. Corals derive their deep brown colour from the zooxanthellae living within their tissues. Coral bleaching is a term used Further, individual colonies that changed from dominance by to describe the loss of the photosymbionts and/or their type C2 (while harbouring type D at extremely low densities) photosynthetic pigments, leading to a blanched and eventually to D increased their thermal tolerance limit 22, a process called white appearance of the coral as the calcium carbonate skeleton symbiont shuffling 32. Sympatric colonies of the coral Stylophora becomes visible through its now translucent tissues. pistillata hosting distinct clade C zooxanthellae types also show

68 MICROBIOLOGY AUSTRALIA • MAY 2009 In Focus

different bleaching tolerances at a field site in the southern Great growth, and sexual reproduction 57. The high diversity of the Barrier Reef, but shuffling did not occur in these symbioses 33. zooxanthellae populations may be important in allowing the Differences in growth rates of juvenile corals have been attributed associations to acclimatise to changing environmental to zooxanthellae type in both A. millepora and A. tenuis 34, and conditions, including variations in solar radiation, temperature, this is linked to the different amounts of carbon translocated and nutrients. Thus there might be some potential for changing from the zooxanthellae to the host in the two symbioses 35. A symbionts under bleaching conditions by switching (i.e. uptake of link between symbiont type and the amount of algal-derived novel zooxanthellae types from the environment 32) or shuffling. photosynthetic carbon incorporated into host tissues has also been described for an anemone 36. Similarly, certain symbiont A less known group of solar-powered animals is that of the types release lower amounts of photosynthetically fixed carbon nudibranchs. Most solar-powered nudibranch species obtain in the presence of synthetic host factor 37. A suite of other Symbiodinium by feeding on corals (Figure 3); instead of physiological traits and thresholds have been correlated to digesting the zooxanthellae, the hosts keep the algae intact Symbiodinium type (reviewed in 12), hence the picture that is and photosynthetically active 40, 58, 59. Whether both hosts (coral emerging is that dinoflagellate of reef corals are and nudibranch) share the same symbiont diversity is still drivers of their physiological limits. under investigation [Burghardt et al., unpublished data]. Using chlorophyll fluorescence data and histological analyses, it has Symbiodinium associations with non-cnidarians been demonstrated that various species of A range of non-cnidarian invertebrates and protists living on coral represent different stages in the evolution of zooxanthellae- reefs host symbionts of the genus Symbiodinium. Within the nudibranch association. Within the genus there are species molluscs there are the giant clams (e.g. or Hippopus without symbionts, others with a short-term symbiotic spp. 38) as well as some nudibranch species (e.g. Phyllodesmium relationship and a small number of species with a highly efficient spp. 39, 40) that house zooxanthellae. Symbiodinium can also symbiosis 58, 60. The efficiency of the symbiosis is correlated with be found in a small number of species (Porifera 41), certain morphological adaptations. A preliminary phylogeny turbellarians (Plathelminthes 42) and 43, 44. Within of Phyllodesmium confirms this hypothesis [Wägele et al., these reef organisms the symbiosis is either facultative or obligate unpublished data]. and symbionts are normally living intracellularly. In nudibranchs they are located in digestive glandular cells 45, in Foraminifera in The way forward 46 the ecto- as well as in the endoplasm . In contrast, in bivalves The recent release of cnidarian genome and partial cnidarian and like Tridacna, Symbiodinium is located in the lumen of digestive Symbiodinium transcriptome sequences (reviewed in 61, 62) has 38 glandular ducts , whereas within the Turbellaria they can be allowed coral reef microbial symbiosis research to venture into 42 found inside parenchymal cells as well as extracellularly . As with new avenues. This includes the identification of cellular processes reef-building corals, the symbionts photosynthesise in hospite, underlying the establishment and disruption of the symbiosis exchange nutrients and gases with the host and reproduce through gene expression research 63-66 and comparative genome asexually 46-51.

Bleaching has been described from Tridacna 52, 53, 54 and foraminiferans 55. However, these studies are of a limited nature and investigate very few species, with comparative studies investigating the impact of environmental stressors on these almost completely lacking. Arguably the best studied non-cnidarian invertebrate-algal symbiosis on coral reefs is that of clams (e.g. 56). Infection of larvae of Hippopus and Tridacna clams with homologous (from the same host species) or heterologous (from different host species) clonal Symbiodinium types followed by a grow-out period in the field, showed that growth and survival differed based on the zooxanthellae type offered 57. However, the symbiont populations were no longer clonal and had become genetically diverse at the end of the grow- out period, making these results somewhat difficult to interpret. Figure 3. The solar-powered nudibranch Phyllodesmium The potential sources of this symbiont genetic diversity in rudmani (left), next to its xeniid coral food (right). The clam hosts include acquisition of new genotypes from the nudibranch mimics its coral host perfectly; the brownish colour water column during filter feeding, mutation during clonal in both organisms is due to the presence of zooxanthellae.

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analyses 67. Further, the close interaction between hosts and their 22. Berkelmans, R. & van Oppen, M.J.H. (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of endosymbionts is evident from two recent studies where lateral climate change. Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 273, 2305–2312. gene transfer occurred between microbial symbionts (both 23. Jones, A.M, et al. (2008) A community change in the algal endosymbionts bacterial and eukaryotic) and their eukaryotic hosts 68, 69. The next of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 275, 1359-1365. few years of genomic research are likely to provide a leap forward 24. Loya, Y. et al. (2001) Coral bleaching: the winners and the losers. Ecol. 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Dr Madeleine van Oppen is a principal research scientist at the Australian Institute of Marine Science (AIMS), Townsville QLD. She is a member of the ARC Centre of Excellence for Coral Reef Studies, and director of the Centre Contact [email protected] for Marine Microbiology and Genetics. Freecall: 1800 686 990 Dr Ingo Burghardt studies the ecophysiology, evolution and diversity of solarpowered nudibranchs and their symbiosis with zooxanthellae. He is currently on a German Science Foundation funded research visit at the Innovation Convenience Performance Australian Institute of Marine Science.

MICROBIOLOGY AUSTRALIA • MAY 2009 71 Micro Media ad 3.indd 1 9/2/09 3:08:15 PM