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Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny - PubMed

  • ️Mon Jan 01 2018

Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

F Joseph Pollock et al. Nat Commun. 2018.

Abstract

Scleractinian corals' microbial symbionts influence host health, yet how coral microbiomes assembled over evolution is not well understood. We survey bacterial and archaeal communities in phylogenetically diverse Australian corals representing more than 425 million years of diversification. We show that coral microbiomes are anatomically compartmentalized in both modern microbial ecology and evolutionary assembly. Coral mucus, tissue, and skeleton microbiomes differ in microbial community composition, richness, and response to host vs. environmental drivers. We also find evidence of coral-microbe phylosymbiosis, in which coral microbiome composition and richness reflect coral phylogeny. Surprisingly, the coral skeleton represents the most biodiverse coral microbiome, and also shows the strongest evidence of phylosymbiosis. Interactions between bacterial and coral phylogeny significantly influence the abundance of four groups of bacteria-including Endozoicomonas-like bacteria, which divide into host-generalist and host-specific subclades. Together these results trace microbial symbiosis across anatomy during the evolution of a basal animal lineage.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1

Anatomical differences in coral microbiomes. Coral mucus, tissue, and skeleton microbiomes differ in richness, composition, and response to host vs. environmental factors based on 16S rRNA gene sequence data. a Microbial community richness (observed OTUs) in coral mucus (teal), tissue (orange) and skeleton (purple), assessed at an even depth of 1000 reads per sample. P-values reflect Tukey’s HSD. b Principal coordinates plot of coral-associated microbial communities (Unweighted UniFrac; n = 614). Reads were rarefied to 1000 reads per sample. Coral compartments show significant differences in community composition (Adonis R2 = 0.028; permutational p < 0.001). The percent variation explained by the principal coordinates is indicated at the axes. Boxplots of the second PC elucidate differences among compartments. P-values reflect Tukey’s HSD. c Relative influence of host and environmental factors on microbiome composition (Weighted UniFrac, Adonis adjusted R2) in each compartment. Darker cells for a compartment indicate that it is more strongly influenced by that trait than the other compartments (Adonis adjusted R2 values z-score normalized within columns). Cell values reflect adjusted R2, which penalizes R2 for each factor downward to allow for fair comparison among factors with varying degrees of freedom. Asterisks indicate a significant effect of that factor (Adonis permutational p < 0.05) on the microbiome in that compartment, following stringent Bonferroni correction across all traits and compartments. While both host and environmental factors influenced all compartments, host factors tended to influence coral tissue and skeleton more strongly than mucus, whereas host environment more influenced mucus microbiomes. All values in the table, plus other combinations of rarefaction depth and multivariate dissimilarity measure are presented in Supplementary Data 4

Fig. 2
Fig. 2

Effects of latitude and coral relative colony size on coral microbiomes. In all panels, we rely on phylogenetic Generalized Linear Mixed Models (pGLMMs; Methods), which account for potential confounding effects of coral phylogeny, for effect size and significance. a Microbial community richness (observed OTUs) as a function of latitude and coral anatomy (teal, coral mucus; orange, tissue; purple, skeleton). For visualization of latitudinal effects on richness, linear correlations are shown with colored lines, and their 95% confidence intervals are shown by shaded areas. Associations between latitude and microbiome richness were significant in coral mucus and tissue, but not skeleton (pMCMC: mucus, 0.0018; tissue, 0.0004; skeleton 0.468; pGLMM effect sizes: mucus, 0.026; tissue, 0.035; skeleton, 0.007). b Microbiome richness as a function of coral colony size relative to the maximum recorded size for each species and coral anatomy. Relative colony size vs. microbiome richness was visualized with linear regression. A negative association between coral relative size and microbiome richness was significant in tissue and skeleton, but a positive association in mucus was not significant (pMCMC: mucus, 0.86; tissue, 0.0008; skeleton, 0.02; pGLMM effect sizes: mucus, 0.028; tissue, −0.591; skeleton, −0.392). c Percent of tested microbial genera significantly associated with latitude and colony size in phylogenetically-controlled pGLMMs (Supplementary Data 6)

Fig. 3
Fig. 3

Effects of host identity, phylogeny, and cophylogeny on bacterial families. Results are derived from co-phylogenetic GLMM analysis within prevalent bacterial families, and incorporate geographic area, bacterial and coral host identity, and bacterial and coral host phylogeny (see Methods and workflow in Fig. 1). Each block of rows corresponds to a factor in the model (main effects are not shown). Each row within a block corresponds to a tissue compartment (teal = mucus, orange = tissue, and purple = skeleton; see coral polyp illustration), while each column corresponds to an independent model fit for the specified microbial group. Dots were plotted only for ‘significant’ factors (ICC lower bound > 0.01). The size of each dot represents the intra-class correlation coefficient (ICC) 95% credible lower bounds from co-phylogenetic linear model analysis. While coral host identity is associated with bacterial phylogeny for most prevalent bacterial families (top block of rows), only 4 bacterial families show co-phylogeny with corals (middle block of rows)

Fig. 4
Fig. 4

Distribution of Endozoicomonas-like bacteria across coral hosts. The heatmap illustrates patterns of association between Endozoicomonas-like bacteria and coral hosts. Colored cells represent the relative abundance of Endozoicomonas-like bacterial sequences (out of the total abundance of Endozoicomonas-like bacteria) in each coral host, plotted on a scale from 0% (white) to 100% (dark blue). The x-axis is arranged by coral host phylogeny, which is shown at the top. The y-axis is arranged by the phylogeny of the most abundant Endozoicomonas-like bacterial sequences observed in host tissues, which is shown to the left (Bayesian posterior support values are shown for clades of interest). Clade HG (Host Generalist; green box) is prevalent in diverse species spanning both the Complex and Robust clades. Clades HS-R (Host-specific: Robust; pink box) and HS-C (Host-specific: Complex; yellow box) are composed of host-specific Endozoicomonas-like lineages. On the right, the host organisms of each sequence variant’s perfect matches in NCBI’s nr database are shown. Cultured and named strains are identified with abbreviations (EE: Endozoicomonas elysicola, EM: Endozoicomonas montiporae, EG: Endozoicomonas gorgoniicola, EN: Endonucleobacter bathymodioli). Sequences in clades HS-R and HS-C are consistently associated with Robust and Complex clade corals, respectively (see Supplementary Fig. 5 for more detail)

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