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

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral-CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs

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