Diverse coral reef invertebrates exhibit patterns of phylosymbiosis

Abstract

Microbiome assemblages of plants and animals often show a degree of correlation with host phylogeny; an eco-evolutionary pattern known as phylosymbiosis. Using 16S rRNA gene sequencing to profile the microbiome, paired with COI, 18S rRNA and ITS1 host phylogenies, phylosymbiosis was investigated in four groups of coral reef invertebrates (scleractinian corals, octocorals, sponges and ascidians). We tested three commonly used metrics to evaluate the extent of phylosymbiosis: (a) intraspecific versus interspecific microbiome variation, (b) topological comparisons between host phylogeny and hierarchical clustering (dendrogram) of host-associated microbial communities, and (c) correlation of host phylogenetic distance with microbial community dissimilarity. In all instances, intraspecific variation in microbiome composition was significantly lower than interspecific variation. Similarly, topological congruency between host phylogeny and the associated microbial dendrogram was more significant than would be expected by chance across all groups, except when using unweighted UniFrac distance (compared with weighted UniFrac and Bray–Curtis dissimilarity). Interestingly, all but the ascidians showed a significant positive correlation between host phylogenetic distance and associated microbial dissimilarity. Our findings provide new perspectives on the diverse nature of marine phylosymbioses and the complex roles of the microbiome in the evolution of marine invertebrates.

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Fig. 1: ASV richness (top panel) and Shannon–Wiener diversity index (bottom panel) for each invertebrate group and seawater.
Fig. 2: Relative abundance of the top 25 prokaryotic families found across each invertebrate group as well as seawater and blank extractions.
Fig. 3: Bray–Curtis dissimilarity based on microbial composition visualised using NMDS.
Fig. 4: Intraspecific and interspecific Bray–Curtis dissimilarity scores for each invertebrate group.
Fig. 5: Host phylogeny and microbial dendrogram comparisons for each invertebrate group.

Data availability

All microbial data have been made available at the NCBI Sequence Read Archive under the BioProject accession number PRJNA577361 and host sequence data are available at the CNGB Sequence Archive under the accession numbers N_000000252.1–N_000000348.1.

Code availability

Code used for the analysis is available at https://github.com/paobrien.

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Acknowledgements

The authors would like to thank Katharina Fabricius, Georgina Torras and Bettina Glasl for their assistance in the field. We also thank Orpheus Island Research Station and the Molecular Ecology and Evolution Laboratory for facilitating field and laboratory work. We thank Zhenyu Peng, Guohai Hu, Bo Wang, Xudan Li, Wei Zhou, Sha Liao and Junqiang Xu for providing SE400 sequencing. Guohai Hu and Bo Wang are affiliated with Guangdong Provincial Key Laboratory of Genome Read and Write (No. 2017B030301011). We also thank Long Zhou and Qiye Li for coordinating the project. This work was funded by the Beijing Genome Institute, Earthwatch Institute and Mitsubishi Corporation. PAO is supported by an AIMS@JCU postgraduate research scholarship.

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PAO, DGB, NSW, DJM and GZ conceived and developed the study. PAO, DGB, NSW, PRF and HAS contributed to field work. PAO, ST, CY and HAS contributed to molecular lab work. PAO analysed the microbial data and generated figures and HAS finalised the figures. PAO, ST, CY and NA analysed the phylogenetic data. PAO drafted the paper and all authors revised the paper and approved the final version.

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Correspondence to Guojie Zhang or David G. Bourne.

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O’Brien, P.A., Tan, S., Yang, C. et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J (2020). https://doi.org/10.1038/s41396-020-0671-x

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