The complexity of coral holobiont structure and the variable coral reef environment can induce a high degree of variability in the bacterial community composition 25, 38, 39, and have together contributed to uncertainties with regard to the role and significance of bacterial symbionts in aiding ecological adaptation of corals. The microbiome associated with reef corals has been reported as one of the most complex and diverse studied to date 24. Corals depend on Symbiodiniaceae satisfying their energy requirements via the transfer of photosynthetically fixed carbon 30 and the assimilation of dissolved inorganic nitrogen and phosphorus 31, while the association with bacteria may serve a wide variety of functional roles, including nitrogen fixation, sulfur cycling, protection against pathogens, and stress tolerance 6, 32, 33, 34, 35, 36, 37. Accordingly, coral health is dependent on the structure and composition of the coral metaorganism primarily comprised of the coral animal host, its endosymbiotic dinoflagellate algae (Symbiodiniaceae family) 26, and a suite of other microbes (bacteria, archaea, fungi, viruses), collectively termed the coral holobiont 7, 27, 28, 29. Reef-building corals are a prime example for organisms that critically depend on their microbial communities with regard to both host physiology and ecosystem functioning 24, 25. However, such information is critical to assess how flexible microbial associations are and to what degree they contribute to the physiology of their host organisms 1, 5, 9, 23. Yet, empirical studies differentiating the relative contribution from the host genetic background and surrounding environment on microbiome structure in natural systems remain scarce and are largely limited to the biomedical field and human microbiome studies 20, 21, 22. Consistently, transplant experiments have revealed intraspecific variation of microbial community composition across disparate environments, which may serve as a potential source of adaptive variation 6, 17, 18, 19. Previous studies have demonstrated that host-associated microbial community compositions are not stochastic, but determined by host species and habitat 10, 11, 12, 13, 14, 15, 16. Consequently, changes in microbial community composition are increasingly hypothesized to contribute to acclimatization and holobiont adaptation 1, 8, 9. Microbial communities of eukaryotic organisms play a critical role in the ecological success and health of their hosts 1, 2 as they provide a broad set of functions related to host metabolism, immunity, and stress tolerance within the so-called metaorganism 3, 4, 5, 6, 7. Our study suggests microbiome flexibility as a mechanism of environmental adaptation with association of different bacterial taxa partially dependent on host genotype. In contrast, bacteria determined by host genotype seemed to be functionally redundant.
Predictions of genomic function based on taxonomic profiles suggest that environmentally determined taxa supported a functional restructuring of the microbial metabolic network. Similarly, but to a lesser extent, microbiomes varied across different genotypes in identical habitats, denoting the influence of host genotype.
Bacterial community composition of coral clones differed between reef habitats, highlighting the contribution of the environment. Resembling human identical twin studies, we examined bacterial community differences of naturally occurring fire coral clones within and between contrasting reef habitats to assess the relative contribution of host genotype and environment to microbiome structure. Coral microbiomes are critical to holobiont functioning, but much remains to be understood about how prevailing environment and host genotype affect microbial communities in ecosystems.
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