Coral reefs are threatened by climate change as coral-algal symbioses are currently living close to their upper thermal limits. The resilience of the algal partner plays a key role in determining the thermal tolerance of the coral holobiont and therefore, understanding the acclimatory limits of present day coral-algal symbioses is fundamental to forecasting corals’ responses to climate change. This study characterised the symbiont community in a highly variable and thermally extreme (Max = 37.5 °C, Min = 16.8 °C) lagoon located in the southern Persian/Arabian Gulf using next generation sequencing of ITS2 amplicons. Despite experiencing extreme temperatures, severe bleaching and many factors that would be expected to promote the presence of, or transition to clade D dominance, the symbiont communities of the lagoon remain dominated by the C3 variant, Symbiodinium thermophilum. The stability of this symbiosis across multiple genera with different means of symbiont transmission highlights the importance of Symbiodinium thermophilum for corals living at the acclimatory limits of modern day corals. Corals in this extreme environment did not undergo adaptive bleaching, suggesting they are living at the edge of their acclimatory potential and that this valuable source of thermally tolerant genotypes may be lost in the near future under climate change.
The microbial assemblages of marine organisms play fundamental biological roles in their eukaryotic hosts. Studies aimed at characterizing this diversity have increased over the last decade and with the availability of high-throughput sequencing, we are now able to characterize bacteria that were non-culturable and, therefore, went undetected. With the number of marine microbiome studies growing rapidly, it is increasingly important to develop a set of "best practices" in order to accurately represent the bacterial communities present, and correct for biases. To address this, we sampled the gut communities of the pan-tropical echinoid Echinometra mathaei from two environmentally distinct populations along the Arabian Peninsula. We used three common DNA extraction procedures and compared inferred bacterial diversity from each method through 16S ribosomal RNA (rRNA) gene amplicon sequencing. Our results show that the addition of a bead-beating and lysozyme step more effectively capture traditionally difficult to lyse taxa, such as gram-positive bacteria. Further, DNA extraction method plays an important role in estimates of Shannon diversity, with diversity indices significantly higher in both sites combined when a lysozyme and bead beating step was used. Finally, we conducted a literature synthesis to highlight the current diversity of approaches used to characterize the microbiome of marine invertebrates and found that the inclusion of a lysozyme treatment is uncommon (2% of surveyed studies), despite the importance of this step in recovery of rare OTUs as shown in our study.
Climate change is affecting the trophic ecology of reef fishes through changes in reef-associated food availability and fish feeding behavior. The southern Arabian Gulf is a thermally extreme environment, providing an opportunity to study fish diets on reefs with summer temperatures representative of next-century conditions elsewhere. Using 18S metagenomic analyses of stomach contents, we provide the first description of the dietary composition of three abundant reef fishes (Pomacanthus maculosus, Pomacentrus aquilus, and Pomacentrus trichrourus) from the thermally extreme southern Arabian Gulf, with five sampling periods across 1 year used to assess seasonal variation in diet. In total, 146 stomach content samples were sequenced, resulting in 9.6 million filtered reads that aligned to 17 classes in 14 phyla. Corals (Cnidaria, Anthozoa) dominated stomach contents of all three fishes (overall mean: 74.6, 40.6, and 21.2% of stomach reads, respectively), suggesting coral consumption to be characteristic of reef fish diet in the region. Sanger sequencing validated the presence of corals in the stomach contents and identified two common genera in the region, Porites and Platygyra, as part of the diet. Other common phyla included sponges and annelid worms (P. maculosus: 14.9%, 4.1%; P. aquilus: 5.9%, 16.7%; P. trichrourus: 8.2%, 14.7%, respectively), with the remainder comprised of 11 other phyla. Algae were virtually absent in diets of all three species. The P. maculosus diet was consistently coral/sponge dominated across the year, but there was substantial seasonal variation in the damselfishes, with diets dominated by coral in the hottest month (August; P. aquilus: 89.4%, P. trichrourus: 51.5%) but broadest in spring (March, May) when corals became less common (<19.8% each) and bivalves, free living ascidians, and various arthropods increased; parasitic cestodes were also abundant in damselfish stomachs in spring (mean: >16.4%). These results suggest that these fishes have developed a feeding ecology responsive to the fluctuating and extreme environmental conditions of their region. These results broaden our understanding of the diets of these three species and document the nature, complexity and temporal dynamics of reef fish diets in the most thermally extreme coral reef environment on earth.
Sustained accretion of calcium carbonate (mostly by scleractinian corals) is fundamental for maintaining the structure and function of coral reef ecosystems, but may be greatly constrained by extreme and rapidly changing environmental conditions. Corals in the southern Persian Gulf already experience extreme temperature ranges (<20 to >34 • C), chronic hypersalinity (>43 psu) and frequent light limitation (<100 µmol photons m −2 s −1). We compared annual rates of calcification for two of the most common coral species in the region (Platygyra daedalea and Cyphastrea microphthalma) along marked gradients in environmental conditions in the southern Persian Gulf and into the Oman Sea. Overall calcification rates were 32% higher in P. daedalea colonies (x = 1.103 g cm −2 y −1 , n = 46) than in C. microphthalma (x = 0.835 g cm −2 y −1 , n = 37), probably reflecting inter-specific differences in energy allocation and skeletal density. There was also considerable variation in calcification rates among individual colonies from the same locations that was unrelated to depth or photosymbiont type. However, most interestingly, P. daedalea and C. microphthalma exhibited contrasting trends in mean annual calcification rates across locations. For P. daedalea, calcification rates were lowest at Delma, where the minimum temperatures were lowest and salinity was highest, and increased across the southern Persian Gulf with increases in minimum temperatures and decreases in salinity. These data suggest that calcification rates of P. daedalea are most constrained by minimum temperatures, which is consistent with the strong relationship between annual calcification rates and minimum local temperatures recorded across the Indo-Pacific. Conversely, linear extension and calcification of C. microphthalma in the southern Persian Gulf was lowest at Ras Ghanada, where there was lowest light and highest maximum temperatures. These data reveal striking taxonomic differences in the specific environmental constraints on coral calcification, which will further reinforce changes in the structure of coral assemblages with ongoing global climate change.
Extreme environmental gradients represent excellent study systems to better understand the variables that mediate patterns of genomic variation between populations. They also allow for more accurate predictions of how future environmental change might affect marine species. The Persian/Arabian Gulf is extreme in both temperature and salinity while the adjacent Gulf of Oman has conditions more typical of tropical oceans. The sea urchin Echinometra sp. EZ inhabits both of these seas and plays a critical role in coral reef health as a grazer and bioeroder, but, to date, there have been no population genomic studies on this or any urchin species in this unique region. E. sp. EZ’s life history traits (e.g., large population sizes, large reproductive clutches, and long life spans), in theory, should homogenize populations unless non-neutral processes are occurring. Here, we generated a draft genome and a restriction-site associated DNA sequencing dataset from seven populations along an environmental gradient across the Persian/Arabian Gulf and the Gulf of Oman. The estimated genome size of E. sp. EZ was 609 Mb and the heterozygosity was amongst the highest recorded for an echinoderm at 4.5%. We recovered 918 high quality SNPs from 85 individuals which we then used in downstream analyses. Population structure analyses revealed a high degree of admixture between all sites, although there was population differentiation and significant pairwise FST values between the two seas. Preliminary results suggest migration is bidirectional between the seas and nine candidate loci were identified as being under putative natural selection, including one collagen gene. This study is the first to investigate the population genomics of a sea urchin from this extreme environmental gradient and is an important contribution to our understanding of the complex spatial patterns that drive genomic divergence.
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