Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors

Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes

Janzen-Connell effects in a broadcast-spawning Caribbean coral: Distance-dependent survival of larvae and settlers.

The Janzen-Connell hypothesis states that host-specific biotic enemies (pathogens and predators) promote the coexistence of tree species in tropical forests by causing distance- or density-dependent mortality of seeds and seedlings. Although coral reefs are the aquatic analogues of tropical forests, the Janzen-Connell model has never been proposed as an explanation for high diversity in these ecosystems. We tested the central predictions of the Janzen-Connell model in a coral reef, using swimming larvae and settled polyps of the common Caribbean coral Montastraea faveolata. In a field experiment to test for distance- or density-dependent mortality, coral settler mortality was higher and more strongly density dependent in locations down-current from adult corals. Survival did not increase monotonically with distance, however, revealing the influence of fluid dynamics around adult corals in structuring spatial patterns of mortality. Complementary microbial profiles around adult coral heads revealed that one potential cause of settler mortality, marine microbial communities, are structured at the same spatial scale. In a field experiment to test whether factors causing juvenile mortality are host specific, settler mortality was 2.3-3.0 times higher near conspecific adults vs. near adult corals of other genera or in open reef areas. In four laboratory experiments to test for distance-dependent, host-specific mortality, swimming coral larvae were exposed to water collected near conspecific adult corals, near other coral genera, and in open areas of the reef. Microbial abundance in these water samples was manipulated with filters and antibiotics to test whether the cause of mortality was biotic (i.e., microbial). Juvenile survivorship was lowest in unfiltered water collected near conspecifics, and survivorship increased when this water was filter sterilized, collected farther away, or collected near other adult coral genera. Together these results demonstrate for the first time that the diversity-promoting mechanisms embodied in the Janzen-Connell model can operate in a marine ecosystem and in an animal. The distribution of adult corals across a reef will thus influence the spatial pattern of juvenile survival. When rare coral species have a survival advantage, coral species diversity per se becomes increasingly important for the persistence and recovery of coral cover on tropical reefs

Janzen-Connell effects in a broadcast-spawning Caribbean coral: Distance-dependent survival of larvae and settlers.

The Janzen-Connell hypothesis states that host-specific biotic enemies (pathogens and predators) promote the coexistence of tree species in tropical forests by causing distance- or density-dependent mortality of seeds and seedlings. Although coral reefs are the aquatic analogues of tropical forests, the Janzen-Connell model has never been proposed as an explanation for high diversity in these ecosystems. We tested the central predictions of the Janzen-Connell model in a coral reef, using swimming larvae and settled polyps of the common Caribbean coral Montastraea faveolata. In a field experiment to test for distance- or density-dependent mortality, coral settler mortality was higher and more strongly density dependent in locations down-current from adult corals. Survival did not increase monotonically with distance, however, revealing the influence of fluid dynamics around adult corals in structuring spatial patterns of mortality. Complementary microbial profiles around adult coral heads revealed that one potential cause of settler mortality, marine microbial communities, are structured at the same spatial scale. In a field experiment to test whether factors causing juvenile mortality are host specific, settler mortality was 2.3-3.0 times higher near conspecific adults vs. near adult corals of other genera or in open reef areas. In four laboratory experiments to test for distance-dependent, host-specific mortality, swimming coral larvae were exposed to water collected near conspecific adult corals, near other coral genera, and in open areas of the reef. Microbial abundance in these water samples was manipulated with filters and antibiotics to test whether the cause of mortality was biotic (i.e., microbial). Juvenile survivorship was lowest in unfiltered water collected near conspecifics, and survivorship increased when this water was filter sterilized, collected farther away, or collected near other adult coral genera. Together these results demonstrate for the first time that the diversity-promoting mechanisms embodied in the Janzen-Connell model can operate in a marine ecosystem and in an animal. The distribution of adult corals across a reef will thus influence the spatial pattern of juvenile survival. When rare coral species have a survival advantage, coral species diversity per se becomes increasingly important for the persistence and recovery of coral cover on tropical reefs

Characterisation of atmospheric semi-volatile organic compounds.

Atmospheric semi-volatile organic compounds (SVOCs), including polycyclic aromatic hydrocarbons (PAHs), are ubiquitous environmental pollutants, which may be present in the gaseous phase and adsorbed onto the surface of aerosol particles. A novel portable miniature denuder consisting of two multi-channel silicone rubber traps separated by a quartz fibre filter has been developed for such applications. It allows for the concentration of SVOCs in each phase to be determined, which is important for human health risk assessments. The overall particle transmission efficiency through the denuder was found to be 92 ± 4% for particles between 16 and 320 nm. SVOCs in the traps (gas phase) or on the filter (particle phase) are analysed by GC-MS, or by GCxGC-MS for enhanced separation capability. This enhances detection limits and allows for lower sampling flow rates and shorter sampling times. These denuders have been applied in studies involving the monitoring of emissions from domestic fires, vehicles and underground mine diesel engines

Appendix A. Parameter estimations and maximum-likelihood values for experiments depicted in Figs. 2–7.

Parameter estimations and maximum-likelihood values for experiments depicted in Figs. 2–7

Natural history of coral-algae competition across a gradient of human activity in the Line Islands

Competition between corals and benthic algae is prevalent on coral reefs worldwide and has the potential to influence the structure of the reef benthos. Human activities may influence the outcome of these interactions by favoring algae to become the superior competitor, and this type of change in competitive dynamics is a potential mechanism driving coral−algal phase shifts. Here we surveyed the types and outcomes of coral interactions with benthic algae in the Line Islands of the Central Pacific. Islands ranged from nearly pristine to heavily fished. We observed major differences in the dominant groups of algae interacting with corals between sites, and the outcomes of coral−algal interactions varied across reefs on the different islands. Corals were generally better competitors against crustose coralline algae regardless of location, and were superior competitors against turf algae on reefs surrounding uninhabited islands. On reefs surrounding inhabited islands, however, turf algae were generally the superior competitors. When corals were broken down by size class, we found that the smallest and the largest coral colonies were the best competitors against algae; the former successfully fought off algae while being completely surrounded, and the latter generally avoided algal overgrowth by growing up above the benthos. Our data suggest that human disruption of the reef ecosystem may lead to a building pattern of competitive disadvantage for corals against encroaching algae, particularly turf algae, potentially initiating a transition towards algal dominance