Population differentiation of Rhodobacteraceae along with coral compartments

• Published in: The ISME Journal Vol. 15; no. 11; pp. 3286 - 3302
• Main Authors: Luo, Danli, Wang, Xiaojun, Feng, Xiaoyuan, Tian, Mengdan, Wang, Sishuo, Tang, Sen-Lin, Ang, Put, Yan, Aixin, Luo, Haiwei
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-11-2021; Nature Publishing Group
• Subjects: 45/22; 45/23; 631/158/855; 631/326/41/2530; Animals; Anthozoa; Biomedical and Life Sciences; Compartments; Dispersal; Ecological effects; Ecology; Evolution; Evolutionary Biology; Genomes; Harbors; Life Sciences; Marine environment; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microbiota; Microorganisms; Mucus; Nucleotides; Oxidation; Population differentiation; Populations; Proline; Rhodobacteraceae; Sulfur; Sulfur oxidation; Swimming; Taurine
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-021-01009-6

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.