Jorge H. Pinzón

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.

Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology

Stony corals in the genus Pocillopora are among the most common and widely distributed of Indo‐Pacific corals and, as such, are often the subject of physiological and ecological research. In the far Tropical Eastern Pacific (TEP), they are major constituents of shallow coral communities, exhibiting considerable variability in colony shape and branch morphology and marked differences in response to thermal stress. Numerous intermediates occur between morphospecies that may relate to extensive hybridization. The diversity of the Pocillopora genus in the TEP was analysed genetically using nuclear ribosomal (ITS2) and mitochondrial (ORF) sequences, and population genetic markers (seven microsatellite loci). The resident dinoflagellate endosymbiont (Symbiodinium sp.) in each sample was also characterized using sequences of the internal transcribed spacer 2 (ITS2) rDNA and the noncoding region of the chloroplast psbA minicircle. From these analyses, three symbiotically distinct, reproductively isolated, nonhybridizing, evolutionarily divergent animal lineages were identified. Designated types 1, 2 and 3, these groupings were incongruent with traditional morphospecies classification. Type 1 was abundant and widespread throughout the TEP; type 2 was restricted to the Clipperton Atoll; and type 3 was found only in Panama and the Galapagos Islands. Each type harboured a different Symbiodinium‘species lineage’ in Clade C, and only type 1 associated with the ‘stress‐tolerant’Symbiodinium glynni (D1). The accurate delineation of species and implementation of a proper taxonomy may profoundly improve our assessment of Pocillopora’s reproductive biology, biogeographic distributions, and resilience to climate warming, information that must be considered when planning for the conservation of reef corals.

Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral.

Climate change is negatively affecting the stability of natural ecosystems, especially coral reefs. The dissociation of the symbiosis between reef-building corals and their algal symbiont, or coral bleaching, has been linked to increased sea surface temperatures. Coral bleaching has significant impacts on corals, including an increase in disease outbreaks that can permanently change the entire reef ecosystem. Yet, little is known about the impacts of coral bleaching on the coral immune system. In this study, whole transcriptome analysis of the coral holobiont and each of the associate components (i.e. coral host, algal symbiont and other associated microorganisms) was used to determine changes in gene expression in corals affected by a natural bleaching event as well as during the recovery phase. The main findings include evidence that the coral holobiont and the coral host have different responses to bleaching, and the host immune system appears suppressed even a year after a bleaching event. These results support the hypothesis that coral bleaching changes the expression of innate immune genes of corals, and these effects can last even after recovery of symbiont populations. Research on the role of immunity on corals resistance to stressors can help make informed predictions on the future of corals and coral reefs.

Microsatellite loci for Symbiodinium A3 (S. fitti) a common algal symbiont among Caribbean Acropora (stony corals) and Indo-Pacific giant clams (Tridacna)

We developed ten polymorphic microsatellite loci for S. fitti (type A3), and tested their utility on a Caribbean population associated with the coral Acropora palmata and an Indo-Pacific population harbored by the giant clam Tridacna maxima. Our analyses identified from 3 to 8 alleles for each haploid locus. Diversity (R) indices were 0.48 for the Indo-Pacific and 0.81 for the Caribbean. Greater than 95% of the samples possessed a single, symbiont, multilocus genotype (MLG). Among their many uses for the study of coral-algal symbioses, population genetic markers provide insight on the potential for symbiont dispersal, can be used to assess symbiont population stability/longevity in hospite, and partition symbiont diversity into reproductively isolated operational taxonomic units (i.e. species).

Nine novel, polymorphic microsatellite markers for the study of threatened Caribbean acroporid corals.

Caribbean reef‐building corals in the genus Acropora have been declining dramatically since the 1980s and are now listed as threatened. The study of their complex reproductive system (mixed asexual and sexual) and their population structure requires highly polymorphic nuclear genetic markers. Of eight previously developed microsatellite loci for A. palmata, only five behaved in a Mendelian fashion and only four reliably amplified the sister species, A. cervicornis. Here, nine novel microsatellite markers are presented that dramatically increase the power to distinguish between asexual and sexual reproductive events and may help to refine population boundaries and gene flow across their ranges.

SYMBIODINIUM (DINOPHYTA) DIVERSITY AND STABILITY IN AQUARIUM CORALS

Indo‐Pacific reef corals growing for years in closed‐system aquaria provide an alternate means to investigate host–symbiont specificity and stability. The diversity of dinoflagellate endosymbionts (Symbiodinium spp.) from coral communities in private and public aquaria was investigated using molecular‐genetic analyses. Of the 29 symbiont types (i.e., species) identified, 90% belonged to the most prevalent group of Symbiodinium harbored by Indo‐Pacific reef corals, Clade C, while the rest belonged to Clade D. Sixty‐five percent of all types were known from field surveys conducted throughout the Pacific and Indian oceans. Because specific coral–dinoflagellate partnerships appear to have defined geographic distributions, correspondence of the same symbionts in aquarium and field‐collected specimens identifies regions where particular colonies must have been collected in the wild. Symbiodinium spp. in clade D, believed to be “stress‐tolerant” and/or “opportunistic,” occurred in a limited number of individual colonies. The absence of a prevalent, or “weedy,” symbiont suggests that conditions under which aquarium corals are grown do not favor competitive replacements of their native symbiont populations. The finding of typical and diverse assemblages of Symbiodinium spp. among aquarium corals living many years under variable chemical/physical conditions, artificial and natural light, while undergoing fragmentation periodically, indicates that individual colonies maintain stable, long‐term symbiotic associations.

Cnidarian Immunity: From Genomes to Phenomes

Cnidarians rely on the innate immune defenses based on self/non-self recognition, signaling and effector responses to kill pathogens and heal wounds. Like other invertebrates, the immune system of cnidarians can be classified into several functional components and many of these elements have now been described in various cnidarian model systems. These include recognition receptors, toll-like receptors and peptidoglycan binding proteins, prophenoloxidase and melanin synthesis for an impermeable melanin barrier, anti-microbial proteins and molecules, reactive oxygen-producing and scavenging systems and wound repair and cellular systems. This chapter will summarize the current state of knowledge of cnidarian immune pathways and mechanisms. We will summarize the available data, guiding the reader through the steps of initiating and executing an immune response: recognition, signaling, effector and repair mechanisms. We will also explore the current research of constitutive immunity observed in healthy organisms and elicited immune responses seen in naturally infected organisms or organisms exposed to live pathogens or pathogen associated molecular patterns. We will connect these known immune pathways with how they are expressed and regulated and how this may influence the wide variation in disease resistance observed in the field, both within and between species. The overarching goal of this chapter is to take the reader from a genomic to phenotypic perspective, while keeping pathways and mechanisms in a whole organism and ecological context, whenever possible.

General Ecological Aspects of Anthozoan-Symbiodinium Interactions in the Mediterranean Sea

The aim of this chapter is to provide a general overview of the main ecological aspects of Anthozoan-Symbiodinium mutualisms in the Mediterranean Sea. There are reports of at least twelve species of symbiotic anthozans in the basin. These anthozoans establish symbiotic relations with Symbiodinium Temperate A and B2 (Symbiodinium psygmophilum), corresponding to the only two species of Symbiodinium described in the region. A synthesis of the trophic and biochemical aspects of the interaction between Symbiodinum and their cnidarian hosts is given to contribute to the understanding of the mechanisms that maintain this special association. Finally, current knowledge about the ecological importance of this interaction in engineering species is examined. This review is framed to highlight the ecological importance of this symbiotic relationship in ecosystem construction and maintenance on an enclosed, temperate marine basin.

Ancient origin of the CARD-coiled coil/Bcl10/MALT1-like paracaspase signaling complex indicates unknown critical functions

The CARD–coiled coil (CC)/Bcl10/MALT1-like paracaspase (CBM) signaling complexes composed of a CARD–CC family member (CARD-9, -10, -11, or -14), Bcl10, and the type 1 paracaspase MALT1 (PCASP1) play a pivotal role in immunity, inflammation, and cancer. Targeting MALT1 proteolytic activity is of potential therapeutic interest. However, little is known about the evolutionary origin and the original functions of the CBM complex. Type 1 paracaspases originated before the last common ancestor of planulozoa (bilaterians and cnidarians). Notably in bilaterians, Ecdysozoa (e.g., nematodes and insects) lacks Bcl10, whereas other lineages have a Bcl10 homolog. A survey of invertebrate CARD–CC homologs revealed such homologs only in species with Bcl10, indicating an ancient common origin of the entire CBM complex. Furthermore, vertebrate-like Syk/Zap70 tyrosine kinase homologs with the ITAM-binding SH2 domain were only found in invertebrate organisms with CARD–CC/Bcl10, indicating that this pathway might be related to the original function of the CBM complex. Moreover, the type 1 paracaspase sequences from invertebrate organisms that have CARD–CC/Bcl10 are more similar to vertebrate paracaspases. Functional analysis of protein–protein interactions, NF-κB signaling, and CYLD cleavage for selected invertebrate type 1 paracaspase and Bcl10 homologs supports this scenario and indicates an ancient origin of the CARD–CC/Bcl10/paracaspase signaling complex. By contrast, many of the known MALT1-associated activities evolved fairly recently, indicating that unknown functions are at the basis of the protein conservation. As a proof-of-concept, we provide initial evidence for a CBM- and NF-κB-independent neuronal function of the Caenorhabditis elegans type 1 paracaspase malt-1. In conclusion, this study shows how evolutionary insights may point at alternative functions of MALT1.