Daniel T. Pettay

Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance.

Mutualisms between reef-building corals and endosymbiotic dinoflagellates are particularly sensitive to environmental stress, yet the ecosystems they construct have endured major oscillations in global climate. During the winter of 2008, an extreme cold-water event occurred in the Gulf of California that bleached corals in the genus Pocillopora harbouring a thermally ‘sensitive’ symbiont, designated Symbiodinium C1b-c, while colonies possessing Symbiodinium D1 were mostly unaffected. Certain bleached colonies recovered quickly while others suffered partial or complete mortality. In most colonies, no appreciable change was observed in the identity of the original symbiont, indicating that these partnerships are stable. During the initial phases of recovery, a third species of symbiont B1Aiptasia, genetically identical to that harboured by the invasive anemone, Aiptasia sp., grew opportunistically and was visible as light-yellow patches on the branch tips of several colonies. However, this symbiont did not persist and was displaced in all cases by C1b-c several months later. Colonies with D1 were abundant at inshore habitats along the continental eastern Pacific, where seasonal turbidity is high relative to offshore islands. Environmental conditions of the central and southern coasts of Mexico were not sufficient to explain the exclusivity of D1 Pocillopora in these regions. It is possible that mass mortalities associated with major thermal disturbances during the 1997–1998 El Niño Southern Oscillation eliminated C1b-c holobionts from these locations. The differential loss of Pocillopora holobionts in response to thermal stress suggests that natural selection on existing variation can cause rapid and significant shifts in the frequency of particular coral–algal partnerships. However, coral populations may take decades to recover following episodes of severe selection, thereby raising considerable uncertainty about the long-term viability of these communities.

The Relative Significance of Host–Habitat, Depth, and Geography on the Ecology, Endemism, and Speciation of Coral Endosymbionts in the Genus Symbiodinium

Dinoflagellates in the genus Symbiodinium are among the most abundant and important group of eukaryotic microbes found in coral reef ecosystems. Recent analyses conducted on various host cnidarians indicated that Symbiodinium assemblages in the Caribbean Sea are genetically and ecologically diverse. In order to further characterize this diversity and identify processes important to its origins, samples from six orders of Cnidaria comprising 45 genera were collected from reef habitats around Barbados (eastern Caribbean) and from the Mesoamerican barrier reef off the coast of Belize (western Caribbean). Fingerprinting of the ribosomal internal transcribed spacer 2 identified 62 genetically different Symbiodinium. Additional analyses of clade B Symbiodinium using microsatellite flanker sequences unequivocally characterized divergent lineages, or “species,” within what was previously thought to be a single entity (B1 or B184). In contrast to the Indo-Pacific where host-generalist symbionts dominate many coral communities, partner specificity in the Caribbean is relatively high and is influenced little by the host’s apparent mode of symbiont acquisition. Habitat depth (ambient light) and geographic isolation appeared to influence the bathymetric zonation and regional distribution for most of the Symbiodinium spp. characterized. Approximately 80% of Symbiodinium types were endemic to either the eastern or western Caribbean and 40–50% were distributed to compatible hosts living in shallow, high-irradiance, or deep, low-irradiance environments. These ecologic, geographic, and phylogenetic patterns indicate that most of the present Symbiodinium diversity probably originated from adaptive radiations driven by ecological specialization in separate Caribbean regions during the Pliocene and Pleistocene periods.

Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in ‘stress‐tolerant’ clade D Symbiodinium

Reef corals harbouring clade D Symbiodinium spp. (endosymbiotic dinoflagellates) appear more tolerant of environmental stress. As sea surface temperatures rise, symbioses involving Symbiodinium D may increase in prevalence. For this reason, eight polymorphic microsatellite loci were developed for clade D Symbiodinium. From the analysis of 132 samples originating from cnidarian hosts in the Atlantic, Pacific and Indian Oceans, 4 to 35 alleles were found at each haploid locus and diversity indices ranged from 0.35 to 0.97. Population genetic analyses of these symbionts should reveal how environmental perturbations affect genetic diversity, geographical distributions, and possible host‐range expansions to new coral species.

Transcriptional Response of Two Core Photosystem Genes in Symbiodinium spp. Exposed to Thermal Stress

Mutualistic symbioses between scleractinian corals and endosymbiotic dinoflagellates (Symbiodinium spp.) are the foundation of coral reef ecosystems. For many coral-algal symbioses, prolonged episodes of thermal stress damage the symbionts photosynthetic capability, resulting in its expulsion from the host. Despite the link between photosynthetic competency and symbiont expulsion, little is known about the effect of thermal stress on the expression of photosystem genes in Symbiodinium. This study used real-time PCR to monitor the transcript abundance of two important photosynthetic reaction center genes, psbA (encoding the D1 protein of photosystem II) and psaA (encoding the P700 protein of photosystem I), in four cultured isolates (representing ITS2-types A13, A20, B1, and F2) and two in hospite Symbiodinium spp. within the coral Pocillopora spp. (ITS2-types C1b-c and D1). Both cultured and in hospite Symbiodinium samples were exposed to elevated temperatures (32°C) over a 7-day period and examined for changes in photochemistry and transcript abundance. Symbiodinium A13 and C1b-c (both thermally sensitive) demonstrated significant declines in both psbA and psaA during the thermal stress treatment, whereas the transcript levels of the other Symbiodinium types remained stable. The downregulation of both core photosystem genes could be the result of several different physiological mechanisms, but may ultimately limit repair rates of photosynthetic proteins, rendering some Symbiodinium spp. especially susceptible to thermal stress.

Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis

ABSTRACT The association between cnidarians and photosynthetic dinoflagellates within the genus Symbiodinium is a prevalent relationship in tropical and subtropical marine environments. Although the diversity of Symbiodinium provides a possible axis for niche diversification, increased functional range and resilience to physical stressors such as elevated temperature, how such diversity relates to the physiological balance between autotrophy and heterotrophy of the host animal remains unknown. Here, we experimentally show interspecific and intraspecific variability of photosynthetic carbon fixation and subsequent translocation by Symbiodinium to the model cnidarian host Aiptasia pallida. By using a clonal anemone line harboring different species of Symbiodinium, we determined that symbiont identity influences trophic plasticity through its density, capacity to fix carbon, quantity of translocated carbon and ultimately the hosts capacity to ingest and digest prey. Symbiont carbon translocation and host prey ingestion were positively correlated across symbiont combinations that consisted of different isoclonal lines of Symbiodinium minutum, while a combination with type D4-5 Symbiodinium displayed lower carbon translocation, and prey capture and digestion more similar to Aiptasia lacking symbionts. The absence of a shift toward greater heterotrophy when carbon translocation is low suggests that the metabolic demand of feeding and digestion may overwhelm nutritional stores when photosynthesis is reduced, and amends the possible role of animal feeding in resistance to or recovery from the effects of climate change in more obligate symbioses such as reef-building corals. Summary: Not all cnidarian–dinoflagellate symbioses are equally nutritionally advantageous to the animal as the genetic identity of the symbiont affects the hosts feeding capacity.

Microsatellite loci for the host-generalist “zooxanthella” Symbiodinium trenchi and other Clade D Symbiodinium

Nine new polymorphic microsatellites were developed for Symbiodinium trenchi (sensu type D1a). These loci were tested on populations of S. trenchi from corals in Palau and 3–19 alleles were observed at each haploid locus with an average of 7 alleles. Many of the primer sets successfully amplified loci within other members of Symbiodinium clade D, demonstrating their utility across the group. Clade D Symbiodinium spp. are generally regarded as thermally tolerant and are common in coral reef habitats with warm, turbid, and/or variable environmental conditions. These population genetic markers are therefore useful for investigating how stress-tolerant symbionts may respond to climate warming through range expansion and/or by developing new associations with various host cnidarians. Additionally, the cross-lineage utility of these markers should help delineate the evolutionary relationships among members of this clade.

Contrasting physiological plasticity in response to environmental stress within different cnidarians and their respective symbionts

Given concerns surrounding coral bleaching and ocean acidification, there is renewed interest in characterizing the physiological differences across the multiple host–algal symbiont combinations commonly found on coral reefs. Elevated temperature and CO2 were used to compare physiological responses within the scleractinian corals Montipora hirsuta (Symbiodinium C15) and Pocillopora damicornis (Symbiodinium D1), as well as the corallimorph (a non-calcifying anthozoan closely related to scleractinians) Discosoma nummiforme (Symbiodinium C3). Several physiological proxies were affected more by temperature than CO2, including photochemistry, algal number and cellular chlorophyll a. Marked differences in symbiont number, chlorophyll and volume contributed to distinctive patterns of chlorophyll absorption among these animals. In contrast, carbon fixation either did not change or increased under elevated temperature. Also, the rate of photosynthetically fixed carbon translocated to each host did not change, and the percent of carbon translocated to the host increased in the corallimorph. Comparing all data revealed a significant negative correlation between photosynthetic rate and symbiont density that corroborates previous hypotheses about carbon limitation in these symbioses. The ratio of symbiont-normalized photosynthetic rate relative to the rate of symbiont-normalized carbon translocation (P:T) was compared in these organisms as well as the anemone, Exaiptasia pallida hosting Symbiodinium minutum, and revealed a P:T close to unity (D. nummiforme) to a range of 2.0–4.5, with the lowest carbon translocation in the sea anemone. Major differences in the thermal responses across these organisms provide further evidence of a range of acclimation potential and physiological plasticity that highlights the need for continued study of these symbioses across a larger group of host taxa.