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Population differentiation of Rhodobacteraceae along with coral compartments

Abstract

Coral mucus, tissue, and skeleton harbor compositionally different microbiota, but how these coral compartments shape the microbial evolution remains unexplored. Here, we sampled bacteria inhabiting a prevalent coral species Platygyra acuta and sequenced genomes of 234 isolates comprising two populations in Rhodobacteraceae, an alphaproteobacterial lineage representing a significant but variable proportion (5–50%) of the coral microbiota. The Ruegeria population (20 genomes) contains three clades represented by eight, six, and six isolates predominantly sampled from the skeleton (outgroup), mucus (clade-M), and skeleton (clade-S), respectively. The clade-M possesses functions involved in the utilization of coral osmolytes abundant in the mucus (e.g., methylamines, DMSP, taurine, and L-proline), whereas the clade-S uniquely harbors traits that may promote adaptation to the low-energy and diurnally anoxic skeleton (e.g., sulfur oxidation and swimming motility). These between-clade genetic differences were largely supported by physiological assays. Expanded analyses by including genomes of 24 related isolates (including seven new genomes) from other marine environments suggest that clade-M and clade-S may have diversified in non-coral habitats, but they also consolidated a key role of distinct coral compartments in diversifying many of the above-mentioned traits. The unassigned Rhodobacteraceae population (214 genomes) varies only at a few dozen nucleotide sites across the whole genomes, but the number of between-compartment migration events predicted by the Slatkin–Maddison test supported that dispersal limitation between coral compartments is another key mechanism diversifying microbial populations. Collectively, our results suggest that different coral compartments represent ecologically distinct and microgeographically separate habitats that drive the evolution of the coral microbiota.

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Fig. 1: The phylogeny and population differentiation of the Ruegeria population.
Fig. 2: The genomic differentiation of the Ruegeria population.
Fig. 3: The catabolic pathways of methylamine-related coral osmolytes in the Ruegeria population.
Fig. 4: Growth experiments of three clade-M strains and three clade-S strains.
Fig. 5: The phylogenetic distribution and pseudogene characterization of the flagellar gene cluster fla1 across the expanded Ruegeria population composed of isolates from both coral and non-coral marine habitats, along with the motility assays of select isolates.
Fig. 6: Compartmentalization of two subpopulations of the Rhodobacteraceae population each from a distinct coral individual.

Data availability

The assembled genomic sequences and raw reads of the coral-associated Ruegeria population, the seven Ruegeria isolates from non-coral marine habitats, and the coral-associated unassigned Rhodobacteraceae population are made publicly available at NCBI under GenBank assembly accession number PRJNA596594, PRJNA682389, and PRJNA596592, respectively.

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Acknowledgements

We thank Ryan Ho-Leung Tsang for the coral sample collection, Tsz-Yan Ng for guiding coral sample processing, Xiao Chu and Shuangfei Zhang for their help on bacteria cultivation, Hao Zhang and Minglei Ren for their help in data analysis, and Xinqin Lin for her advice in experimental design. We thank Xiao Chu, Minglei Ren, and Zhichao Zhou for providing isolates from the brown algae ecosystem, sediments, and mangrove ecosystem. This work was supported by the Shenzhen Science and Technology Committee (JCYJ20180508161811899), the National Natural Science Foundation of China (41776129), the Hong Kong Environment and Conservation Fund (15/2016), the Hong Kong Research Grants Council General Research Fund (14163917), and the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16).

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Luo, D., Wang, X., Feng, X. et al. Population differentiation of Rhodobacteraceae along with coral compartments. ISME J (2021). https://doi.org/10.1038/s41396-021-01009-6

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