Microbiomes of gall-inducing copepod crustaceans from the corals Stylophora pistillata (Scleractinia) and Gorgonia ventalina (Alcyonacea)

Abstract

Corals harbor complex and diverse microbial communities that strongly impact host fitness and resistance to diseases, but these microbes themselves can be influenced by stresses, like those caused by the presence of macroscopic symbionts. In addition to directly influencing the host, symbionts may transmit pathogenic microbial communities. We analyzed two coral gall-forming copepod systems by using 16S rRNA gene metagenomic sequencing: (1) the sea fan Gorgonia ventalina with copepods of the genus Sphaerippe from the Caribbean and (2) the scleractinian coral Stylophora pistillata with copepods of the genus Spaniomolgus from the Saudi Arabian part of the Red Sea. We show that bacterial communities in these two systems were substantially different with Actinobacteria, Alphaproteobacteria, and Betaproteobacteria more prevalent in samples from Gorgonia ventalina, and Gammaproteobacteria in Stylophora pistillata. In Stylophora pistillata, normal coral microbiomes were enriched with the common coral symbiont Endozoicomonas and some unclassified bacteria, while copepod and gall-tissue microbiomes were highly enriched with the family ME2 (Oceanospirillales) or Rhodobacteraceae. In Gorgonia ventalina, no bacterial group had significantly different prevalence in the normal coral tissues, copepods, and injured tissues. The total microbiome composition of polyps injured by copepods was different. Contrary to our expectations, the microbial community composition of the injured gall tissues was not directly affected by the microbiome of the gall-forming symbiont copepods.

Figure 1

(a) The Caribbean sea fan Gorgonia ventalina (Alcyonacea) with pink galls (b, arrowed) induced by a copepod of Sphaerippe sp. (Lamippidae); (c) female of Sphaerippe sp., ventral view, SEM photo; (d) the Red Sea stony coral Stylophora pistillata (Scleractinia) with modified corallites (e, arrowed) induced by copepods of the genus Spaniomolgus (Rhynchomolgidae); (f) female copepod Spaniomolgus sp., ventro-lateral view, SEM photo^,. Scale bars: a–10, b–5, c–0.01, d–8, e–2, f–0.01 cm.

Figure 2

Hierarchical clustering based on relative genus-level taxon abundance. We merge OTUs based on their genus-level taxonomy, if the genus was not identified for an OTU, then the lowest of identified taxonomic category was used. The clustering was based on the Hellinger distances between samples. Only highly abundant taxa are shown. Healthy coral samples are in green, gall samples pink, and copepod samples blue. Abbreviations: Gv_g1, Gv_g2 — gall tissue of the Caribbean sea fan Gorgonia ventalina (Alcyonacea); Gv_h1, Gv_h2 — healthy polyp of G. ventalin; Gv_c1, Gv_c2 and Gv_c3 — female specimens of Sphaerippe sp. (Copepoda: Poecilostomatoida: Lamippidae) from galls of G. ventalina; Sp_h1, Sp_h2 and Sp_h3 — healthy polyp of the Red Sea stony coral Stylophora pistillata (Scleractinia); Sp_g1, Sp_g2 — gall tissue (modified polyp) of S. pistillata from the Red Sea; Sp_c1, Sp_c2 and Sp_c3 — female specimens of Spaniomolgus sp. (Copepoda: Poecilostomatoida: Rhynchomolgidae) from gall of S. pistillata.

Figure 3

Relative phylum/class abundance in different samples. Abbreviations as in Table 1 and Fig. 2.

Figure 4

Principal component analysis (PCA) based on the Hellinger distance for all samples. PC1 explains 31% of the variance, and PC2 explains 20% of the variance. Taxa with the largest impact on PC1 and PC2 are shown as arrows. Abbreviations as in Table 1 and Fig. 2.