ALBERT

Description: Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only 5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.

Description: The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal–algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal–algal pair also with its prokaryotic microbiome.

Description: The structural framework provided by corals is crucial for reef ecosystem function and services, but high seawater temperatures can be detrimental to the calcification capacity of reef-building organisms. The Red Sea is very warm, but total alkalinity (TA) is naturally high and beneficial for reef accretion. To date, we know little about how such detrimental and beneficial abiotic factors affect each other and the balance between calcification and erosion on Red Sea coral reefs, i.e., overall reef growth, in this unique ocean basin. To provide estimates of present-day reef growth dynamics in the central Red Sea, we measured two metrics of reef growth, i.e., in situ net-accretion/-erosion rates (Gnet) determined by deployment of limestone blocks and ecosystem-scale carbonate budgets (Gbudget), along a cross-shelf gradient (25 km, encompassing nearshore, midshore, and offshore reefs). Along this gradient, we assessed multiple abiotic (i.e., temperature, salinity, diurnal pH fluctuation, inorganic nutrients, and TA) and biotic (i.e., calcifier and epilithic bioeroder communities) variables. Both reef growth metrics revealed similar patterns from nearshore to offshore: net-erosive, neutral, and net-accretion states. The average cross-shelf Gbudget was 0.66 kg CaCO3 m−2 yr−1, with the highest budget of 2.44 kg CaCO3 m−2 yr−1 measured in the offshore reef. These data are comparable to the contemporary Gbudgets from the western Atlantic and Indian oceans, but lie well below “optimal reef production” (5–10 kg CaCO3 m−2 yr−1) and below maxima recently recorded in remote high coral cover reef sites. However, the erosive forces observed in the Red Sea nearshore reef contributed less than observed elsewhere. A higher TA accompanied reef growth across the shelf gradient, whereas stronger diurnal pH fluctuations were associated with negative carbonate budgets. Noteworthy for this oligotrophic region was the positive effect of phosphate, which is a central micronutrient for reef building corals. While parrotfish contributed substantially to bioerosion, our dataset also highlights coralline algae as important local reef builders. Altogether, our study establishes a baseline for reef growth in the central Red Sea that should be useful in assessing trajectories of reef growth capacity under current and future ocean scenarios.

Description: Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may tune microbial communities and employed an integrated multiomics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is numerically rare but globally distributed in the world’s oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.

Description: The coral structural framework is crucial for maintaining reef ecosystem function and services. Rising seawater temperatures impair the calcification capacity of reef-building organisms on a global scale, but in the Red Sea total alkalinity is naturally high and beneficial to reef growth. It is currently unknown how beneficial and detrimental factors affect the balance between calcification and erosion, and thereby overall reef growth, in the Red Sea. To provide estimates of present-day carbonate budgets and reef growth dynamics in the central Red Sea, we measured in situ net-accretion and net-erosion rates (Gnet) by deployment of limestone blocks to estimate census-based carbonate budgets (Gbudget) in four reef sites along a cross-shelf gradient (25 km). In addition, we assessed abiotic (i.e., temperature, inorganic nutrients, and carbonate system variables) and biotic (i.e., calcifier and bioeroder abundances) variables. Our data show that aragonite saturation states (Ω = 3.65–4.20) were in the upper range compared to the chemistry of other tropical reef sites. Further, Gnet and Gbudget encompassed positive (offshore) and negative (midshore-lagoon and exposed nearshore site) carbonate budgets. Notably, Gbudget maxima were lower compared to reef growth from undisturbed Indian Ocean reefs, but erosive forces for Red Sea reefs were not as strong as observed elsewhere. In line with this, a comparison with recent historical data from the northern Red Sea suggests that overall reef growth in the Red Sea has remained similar since 1995. When assessing reef sites across the shelf gradient, AT correlated well and positive with reef growth (ρ = 0.9), while temperature (ρ = −0.7), pH variation (ρ = −0.8), and pCO2 (ρ = −0.8) were weaker negative correlates. Noteworthy for this oligotrophic sea was the positive effect of PO43− (ρ = 0.7) on reef growth. In the best-fitting distance-based linear model, AT explained about 64 % of Gbudget. Interestingly, parrotfish abundances added up to 78 % of the explained variation, further corroborating recent studies that highlight the importance of parrotfish to reef ecosystem functioning. Our study provides a baseline for reef growth in the central Red Sea that will be particularly useful in assessing future trajectories of reef growth capacities under current and future ocean warming and acidification scenarios.