coral-reef-arks-an-situ-mesocosm-toolkit-for-assembling-reef

Coral Reef Arks: An <em>In Situ</em> Mesocosm and Toolkit for Assembling Reef Communities

Coral reefs thrive and provide maximal ecosystem services when they support a multi-level trophic structure and grow in favorable water quality conditions ...

Harvard University

Untargeted metabolomics of environmental samples routinely detects thousands of small molecules, the vast majority of which cannot be identified. Meta-mass shift chemical (MeMSChem) profiling was developed to identify mass differences between related molecules using molecular networks. This approach illuminates metabolome-wide relationships between molecules and the putative chemical groups that differentiate them (e.g., H, CH, COCH). MeMSChem profiling was used to analyze a publicly available metabolomic dataset of coral, algal, and fungal mat holobionts (i.e., the host and its associated microbes and viruses) sampled from some of Earth's most remote and pristine coral reefs. Each type of holobiont had distinct mass shift profiles, even when the analysis was restricted to molecules found in all samples. This result suggests that holobionts modify the same molecules in different ways and offers insights into the generation of molecular diversity. Three genera of stony corals had distinct patterns of molecular relatedness despite their high degree of taxonomic relatedness. MeMSChem profiles also partially differentiated between individuals, suggesting that every coral reef holobiont is a potential source of novel chemical diversity.

Meta-mass shift chemical profiling of metabolomes from coral reefs.

Mutually beneficial interactions between species (mutualisms) shaped the evolution of eukaryotes and remain critical to the survival of species globally [1, 2]. Theory predicts that hosts should pass mutualist symbionts to their offspring (vertical transmission) [3-8]. However, offspring acquire symbionts from the environment in a surprising number of species (horizontal acquisition) [9-12]. A classic example of this paradox is the reef-building corals, in which 71% of species horizontally acquire algal endosymbionts [9]. An untested hypothesis explaining this paradox suggests that horizontal acquisition allows offspring to avoid symbiont-induced harm early in life. We reconstructed the evolution of symbiont transmission across 252 coral species and detected evolutionary transitions consistent with costs of vertical transmission among broadcast spawners, whose eggs tend to be positively buoyant and aggregate at the sea surface. Broadcasters with vertical transmission produce eggs with traits that favor reduced buoyancy (less wax ester lipid) and rapid development to the swimming stage (small egg size), both of which decrease the amount of time offspring spend at the sea surface. Wax ester provisioning decreased after vertically transmitting species evolved brooding from broadcasting, indicating that reduced buoyancy evolves only when offspring bear symbionts. We conclude that horizontal acquisition protects offspring from damage caused by high light and temperatures near the sea surface while providing benefits from enhanced fertilization and outcrossing. These findings help explain why modes of symbiont transmission and reproduction are strongly associated in corals and highlight benefits of delaying mutualist partnerships, offering an additional hypothesis for the pervasiveness of this theoretically paradoxical strategy.

The Paradox of Environmental Symbiont Acquisition in Obligate Mutualisms.

Corals and humans represent two extremely disparate metazoan lineages and are therefore useful for comparative evolutionary studies. Two lipid-based molecules that are central to human immunity, platelet-activating factor (PAF) and Lyso-PAF were recently identified in scleractinian corals. To identify processes in corals that involve these molecules, PAF and Lyso-PAF biosynthesis was quantified in conditions known to stimulate PAF production in mammals (tissue growth and exposure to elevated levels of ultraviolet light) and in conditions unique to corals (competing with neighbouring colonies over benthic space). Similar to observations in mammals, PAF production was higher in regions of active tissue growth and increased when corals were exposed to elevated levels of ultraviolet light. PAF production also increased when corals were attacked by the stinging cells of a neighbouring colony, though only the attacked coral exhibited an increase in PAF. This reaction was observed in adjacent areas of the colony, indicating that this response is coordinated across multiple polyps including those not directly subject to the stress. PAF and Lyso-PAF are involved in coral stress responses that are both shared with mammals and unique to the ecology of cnidarians.

Before platelets: the production of platelet-activating factor during growth and stress in a basal marine organism.

Disability inclusion enhances science.

Reef-building corals are ecosystem engineers that compete with other benthic organisms for space and resources. Corals harvest energy through their surface by photosynthesis and heterotrophic feeding, and they divert part of this energy to defend their outer colony perimeter against competitors. Here, we hypothesized that corals with a larger space-filling surface and smaller perimeters increase energy gain while reducing the exposure to competitors. This predicted an association between these two geometric properties of corals and the competitive outcome against other benthic organisms. To test the prediction, fifty coral colonies from the Caribbean island of Curaçao were rendered using digital 3D and 2D reconstructions. The surface areas, perimeters, box-counting dimensions (as a proxy of surface and perimeter space-filling), and other geometric properties were extracted and analyzed with respect to the percentage of the perimeter losing or winning against competitors based on the coral tissue apparent growth or damage. The increase in surface space-filling dimension was the only significant single indicator of coral winning outcomes, but the combination of surface space-filling dimension with perimeter length increased the statistical prediction of coral competition outcomes. Corals with larger surface space-filling dimensions (D > 2) and smaller perimeters displayed more winning outcomes, confirming the initial hypothesis. We propose that the space-filling property of coral surfaces complemented with other proxies of coral competitiveness, such as life history traits, will provide a more accurate quantitative characterization of coral competition outcomes on coral reefs. This framework also applies to other organisms or ecological systems that rely on complex surfaces to obtain energy for competition.

Article	Year
Meta-mass shift chemical profiling of metabolomes from coral reefs. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 29078340	2017
The Paradox of Environmental Symbiont Acquisition in Obligate Mutualisms. Current biology : CB\| PubMed ID: 29153324	2017
Before platelets: the production of platelet-activating factor during growth and stress in a basal marine organism. Proceedings. Biological sciences\| PubMed ID: 30111600	2018
Disability inclusion enhances science. Science (New York, N.Y.)\| PubMed ID: 31699927	2019
Space-filling and benthic competition on coral reefs. PeerJ\| PubMed ID: 34249480	2021

Aaron C. Hartmann

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