Proceedings of the National Academy of Sciences (PNAS)

Abstract

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

Abstract

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 metabolomewide relationships between molecules and the putative chemical groups that differentiate them (e.g., H2, CH2, COCH2). 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 ofmolecular 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.

Assisted gene flow (AGF) is a conservation intervention to accelerate
species adaptation to climate change by importing genetic
diversity into at-risk populations. Corals exemplify both the need for
AGF and its technical challenges; corals have declined in abundance,
suffered pervasive reproductive failures, and struggled to adapt to
climate change, yet mature corals cannot be easily moved for breeding,
and coral gametes lose viability within hours. Here, we report
the successful demonstration of AGF in corals using cryopreserved
sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata
eggs from the western Caribbean (Curaçao) with cryopreserved
sperm from genetically distinct populations in the eastern and central
Caribbean (Florida and Puerto Rico, respectively). We then confirmed
interpopulation parentage in the Curaçao–Florida offspring
using 19,696 single-nucleotide polymorphism markers. Thus, we
provide evidence of reproductive compatibility of a Caribbean coral
across a recognized barrier to gene flow. The 6-mo survival of AGF
offspring was 42%, the highest ever achieved in this species, yielding
the largest wildlife population ever raised from cryopreserved
material. By breeding a critically endangered coral across its range
withoutmoving adults, we show that AGF using cryopreservation is
a viable conservation tool to increase genetic diversity in threatened
marine populations.

Coastal ecosystems and the services they provide are adversely affected by a wide variety of human activities. In particular, seagrass meadows are negatively affected by impacts accruing from the billion or more people who live within 50 km of them. Seagrass meadows provide important ecosystem services, includ- ing an estimated $1.9 trillion per year in the form of nutrient cycling; an order of magnitude enhancement of coral reef fish productivity; a habitat for thousands of fish, bird, and invertebrate species; and a major food source for endangered dugong, mana- tee, and green turtle. Although individual impacts from coastal development, degraded water quality, and climate change have been documented, there has been no quantitative global assess- ment of seagrass loss until now. Our comprehensive global assess- ment of 215 studies found that seagrasses have been disappearing at a rate of 110 km2 yr 1 since 1980 and that 29% of the known areal extent has disappeared since seagrass areas were initially recorded in 1879. Furthermore, rates of decline have accelerated from a median of 0.9% yr 1 before 1940 to 7% yr 1 since 1990. Seagrass loss rates are comparable to those reported for man- groves, coral reefs, and tropical rainforests and place seagrass meadows among the most threatened ecosystems on earth. 

Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measure- ment of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponen- tially with distance. The spatial scale of dispersal is an order of mag- nitude less than previous estimates—the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direc- tion is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered re- flects long-term patterns of gene flow. These results challenge as- sumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short- distance dispersers. 

Abstract:

Ecological studies have rarely been performed at the community level across a large biogeographic region. Sponges are now the primary habitat-forming organisms on Caribbean coral reefs. Recent species-level investigations have demonstrated that preda- tory fishes (angelfishes and some parrotfishes) differentially graze sponges that lack chemical defenses, while co-occurring, palatable species heal, grow, reproduce, or recruit at faster rates than defended species. Our prediction, based on resource allocation theory, was that predator removal would result in a greater proportion of palatable species in the sponge community on overfished reefs. We tested this prediction by performing surveys of sponge and fish community composition on reefs having different levels of fishing intensity across the Caribbean. A total of 109 sponge species was recorded from 69 sites, with the 10 most common species comprising 51.0% of sponge cover (3.6–7.7% per species). Nonmetric multidimensional scaling indicated that the species composition of sponge communities depended more on the abundance of sponge-eating fishes than geographic location. Across all sites, multiple-regression analyses revealed that spongivore abundance explained 32.8% of the variation in the proportion of palatable sponges, but when data were limited to geographically adjacent locations with strongly contrasting levels of fishing pressure (Cayman Islands and Jamaica; Curaçao, Bonaire, and Martinique), the adjusted R2 values were much higher (76.5% and 94.6%, respectively). Overfishing of Caribbean coral reefs, particularly by fish trapping, removes sponge predators and is likely to result in greater competition for space between faster-growing palatable sponges and endangered reef-building corals. 

Ocean acidification (OA) refers to the ongoing decline in oceanic pH resulting from the uptake of atmospheric CO2. Mounting experimental evidence suggests that OA will have negative consequences for a variety of marine organisms. Whereas the effect of OA on the calcification of adult reef corals is increasingly well documented, effects on early life history stages are largely unknown. Coral recruitment, which necessitates successful fertilization, larval settlement, and postsettlement growth and survivorship, is critical to the persistence and resilience of coral reefs. To determine whether OA threatens successful sexual recruitment of reef-building corals, we tested fertilization, settlement, and postsettlement growth of Acropora palmata at pCO2 levels that represent average ambient conditions during coral spawning (∼400 μatm) and the range of pCO2 increases that are expected to occur in this century [∼560 μatm (mid-CO2) and ∼800 μatm (high-CO2)]. Fertilization, settlement, and growth were all negatively impacted by increasing pCO2, and impairment of fertilization was exacerbated at lower sperm concentrations. The cumulative impact of OA on fertilization and settlement success is an estimated 52% and 73% reduction in the number of larval settlers on the reef under pCO2 conditions projected for the middle and the end of this century, respectively. Additional declines of 39% (mid-CO2) and 50% (high-CO2) were observed in postsettlement linear extension rates relative to controls. These results suggest that OA has the potential to impact multiple, sequential early life history stages, thereby severely compromising sexual recruitment and the ability of coral reefs to recover from disturbance