Microorganisms live in tight ecological associations with corals, but microbial community composition, functions and behaviours within coral reef ecosystems are not yet fully understood. To examine the community structure, metabolic capacity and the potential role of chemotaxis in the ecology of coral reef bacterial communities, we performed a suite of laboratory, in-situ and thermal stress experiments on Heron Island, the Great Barrier Reef (GBR). To characterise patterns in microbial composition and metabolic capacity across different niches on a coral reef, metagenomes were sequenced from seawater samples associated with the surfaces of corals, the sandy substrate and in open water, outside of the reef. Within these environments we also examined the potential ecological role of chemotaxis among coral associated bacteria, by using laboratory and in situ chemotaxis assays to test for levels of chemotaxis towards several chemoattractants known to be released by corals and their symbiotic dinoflagelletes including amino acids, carbohydrates, ammonium chloride, and dimethylsulfonopropionate (DMSP). Finally, to determine how environmental variability, specifically thermal stress, influences bacterial community composition, behaviour and metabolic capacity, manipulation experiments were conducted using Pocillopora damicornis in flow-through aquatic systems on Heron Island.
We found that the composition and metabolic potential of coral reef bacteria is highly heterogeneous across a coral reef ecosystem, with a shift from an oligotroph-dominated community (e.g. SAR11, Prochlorococcus, Synechococcus) in the open water and sandy substrate niches, to a community characterised by an increased frequency of copiotrophic bacteria (e.g. Vibrio, Pseudoalteromonas, Alteromonas) in the coral seawater niches. Among the major functional patterns observed were significant increases in genes associated with bacterial motility and chemotaxis in samples associated with the surfaces of coral colonies. These patterns were directly confirmed by chemotaxis experiments, which demonstrated that bacteria associated with the surfaces of the corals exhibited high levels of chemotaxis, particularly towards DMSP and several amino acids. Levels of chemotaxis by coral-associated bacteria were consistently higher than those demonstrated by non-coral associated bacteria. The phylogenetic composition of the chemotactic microbes, determined using 16S rRNA amplicon pyrosequencing, differed to the background community in the surrounding seawater, and incorporated several known coral-associated bacteria, Rhodobacteraceae, Flavobacteriaceae, Pseudomonadaceae and included potentially pathogenic Vibrios. Notably many of these bacteria, specifically Rhodobacterales, Flavobacterales and Vibrionales also became the dominant coral associated organisms under conditions of thermal stress experiments, indicating that these copiotrophic and chemotactic bacteria become key colonisers of thermally stressed corals.
Taken together our data demonstrate that coral reef bacterial communities are highly dynamic and that key groups of copiotrophic bacteria have the capacity to use sensitive chemotaxis to exploit nutrient gradients and potentially locate their coral hosts. Under conditions of heat stress, these behaviours may allow pathogenic organisms to locate and infect compromised hosts.