Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These “frontloaded” transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.

Classifying the biological traits of organisms can test conceptual frameworks of life-history strategies and allow for predictions of how different species may respond to environmental disturbances. We apply a trait-based classification approach to a complex and threatened group of species, scleractinian corals. Using hierarchical clustering and random forests analyses, we identify up to four life-history strategies that appear globally consistent across 143 species of reef corals: competitive, weedy, stress-tolerant and generalist taxa, which are primarily separated by colony morphology, growth rate and reproductive mode. Documented shifts towards stress-tolerant, generalist and weedy species in coral reef communities are consistent with the expected responses of these life-history strategies. Our quantitative trait-based approach to classifying life-history strategies is objective, applicable to any taxa and a powerful tool that can be used to evaluate theories of community ecology and predict the impact of environmental and anthropogenic stressors on species assemblages.

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The microbial cosmopolitan dispersion hypothesis often invoked to explain distribution patterns driven by high connectivity of oceanographic water masses and widespread dispersal ability has never been rigorously tested. By using a global marine bacterial dataset and iterative matrix randomization simulation, we show that marine bacteria exhibit a significantly greater dispersal limitation than predicted by our null model using the "everything is everywhere" tenet with no dispersal limitation scenario. Specifically, marine bacteria displayed bipolar distributions (i.e., species occurring exclusively at both poles and nowhere else) significantly less often than in the null model. Furthermore, we observed fewer taxa present in both hemispheres but more taxa present only in a single hemisphere than expected under the null model. Each of these trends diverged further from the null expectation as the compared habitats became more geographically distant but more environmentally similar. Our metaanalysis supported a latitudinal gradient in bacterial diversity with higher richness at lower latitudes, but decreased richness toward the poles. Bacteria in the tropics also demonstrated narrower latitudinal ranges at lower latitudes and relatively larger ranges in higher latitudes, conforming to the controversial macroecological pattern of the "Rapoport rule." Collectively, our findings suggest that bacteria follow biogeographic patterns more typical of macroscopic organisms, and that dispersal limitation, not just environmental selection, likely plays an important role. Distributions of microbes that deliver critical ecosystem services, particularly those in polar regions, may be vulnerable to the same impacts that environmental stressors, climate warming, and degradation in habitat quality are having on biodiversity in animal and plant species.ICoMM | MIRADA-LTERS | microbial biogeography | macroecology

Dinoflagellates of the genus Symbiodinium form an endosymbiosis with reef building corals, in which photosynthetically derived nutrients comprise the majority of the coral energy budget. An extraordinary amount of functional and genetic diversity is contained within the coral-associated Symbiodinium, with some phylotypes (i.e., genotypic groupings), conferring enhanced stress tolerance to host corals. Recent advances in DNA sequencing technologies have enabled transcriptome-wide profiling of the stress response of the cnidarian coral host; however, a comprehensive understanding of the molecular response to stress of coral-associated Symbiodinium, as well as differences among physiologically susceptible and tolerant types, remains largely unexplored. Here, we examine the transcriptome-wide response to heat stress via RNA-Seq of two types of Symbiodinium, the putatively thermotolerant type D2 and the more susceptible type C3K, resident within the same coral host species, Acropora hyacinthus. Contrary to previous findings with coral hosts, we find no detectable change in gene expression across the dinoflagellate transcriptome after 3 days of elevated thermal exposure, despite physical evidence of symbiosis breakdown. However, hundreds of genes identified as orthologs between the C and D types exhibited significant expression differences within treatments (i.e., attributable solely to type, not heat exposure). These include many genes related to known thermotolerance mechanisms including heat shock proteins and chloroplast membrane components. Additionally, both the between-treatment similarities and between-type differences remained pervasive after 12-18 months of common garden acclimation and in mixed Symbiodinium assemblages within the same coral host colony.

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Coral stress tolerance is intricately tied to the animal's association with microbial symbionts. The most well-known of these symbioses is that between corals and their dinoflagellate photobionts (Symbiodinium spp.), whose genotype indirectly affects whether a coral can survive cyclical and anthropogenic warming events. Fungi comprise a lesser-known coral symbiotic community whose taxonomy, stability and function is largely un-examined. To assess how fungal communities inside a coral host correlate with water temperature and the genotype of co-occurring Symbiodinium, we sampled Acropora hyacinthus coral colonies from adjacent natural pools with different water temperatures and Symbiodinium identities. Phylogenetic analysis of coral-associated fungal ribosomal DNA amplicons showed a high diversity of Basidiomycetes and Ascomycetes, including several clades separated from known fungal taxa by long and well-supported branches. Community similarity did not correlate with any measured variables, and total fungal community composition was highly variable among A. hyacinthus coral colonies. Colonies in the warmer pool contained more phylogenetically diverse fungal communities than the colder pool and contained statistically significant 'indicator' species. Four taxa were present in all coral colonies sampled, and may represent obligate associates. Messenger RNA sequenced from a subset of these same colonies contained an abundance of transcripts involved in metabolism of complex biological molecules. Coincidence between the taxonomic diversity found in the DNA and RNA analysis indicates a metabolically active and diverse resident marine fungal community.

Distribution patterns of stress-tolerant coral symbionts suggest that maximum habitat temperatures can drive local scale adaptation of symbiont populations, but at regional scales other processes can dominate. We assayed clade membership for symbionts of 2 closely related corals from American Samoa, Fiji, the Philippines and Palmyra Atoll. Temperature stress-tolerant Clade D symbionts occur more frequently in American Samoa (83%) than in Palmyra, Fiji or the Philippines (<1%). In American Samoa, Clade D symbionts dominate habitats with higher maximum temperatures, while Clades C and D are both common under lower maximum temperatures. While corals in American Samoa show more stress-tolerant symbionts, this region does not exhibit higher sea surface temperatures, a greater record of heating anomalies or more bleaching than the other 3 regions. That these local patterns do not hold regionally suggests the importance of other factors, including host responses, other environmental correlates, within-clade physiological diversity and dispersal limitation, in driving the distribution of coral symbionts.KEY WORDS: Coral reefs · Climate change · Adaptation · Acropora · Symbiodinium · Cytochrome b · High temperature stress Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 378: [93][94][95][96][97][98][99][100][101][102][103] 2009 control (28.5°C) or elevated temperatures (31.3 or 32.0°C). Colonies hosting Clade C Symbiodinium in the 32.0°C treatment showed evidence of heatinduced damage to the light reactions of photosynthesis, while those hosting Clade D Symbiodinium did not. Rowan (2004) concluded that Clades C and D are adapted to different thermal regimes, and Clade D appears to be a high temperature specialist.The increased thermal robustness provided by hosting Clade D may incur some cost to the coral. Little et al. (2004) documented that juvenile Acropora tenuis and A. millepora hosting Clade D Symbiodinium grew at half the rate of those hosting Clade C at the same site. This is the only published example of a trade-off for Clade D thermal resistance, and it remains unknown if the growth limitations apply to A. tenuis and A. millepora adults and/or other species.Although some coral species host multiple symbiont types, others appear to host only a single type. Species in the genus Porites primarily associate with a single symbiont type (LaJeunesse et al. 2004, Thornhill et al. 2006a, while many species in the genera Acropora and Pocillopora commonly host multiple clades of Symbiodinium (van Oppen et al. 2001, Baker 2003, LaJeunesse et al. 2004). The proportion of scleractinian corals that can host multiple symbionts has been recently debated (Goulet 2006, Baker & Romanski 2007, but estimates using adequate sample sizes (n > 5 samples per species) suggest that at least 58% (72/124) of the species examined hosted more than one clade of symbiont (Baker & Romanski 2007). Even among those capable of hosting multiple symbionts, long-term monitoring studies have s...