Gruber-Vodicka, Harald R.

Abstract Microbes perform critical functions in corals, yet most knowledge is derived from the photic zone. Here, we discover two mollicutes that dominate the microbiome of the deep-sea octocoral, Callogorgia delta, and likely reside in the mesoglea. These symbionts are abundant across the host’s range, absent in the water, and appear to be rare in sediments. Unlike other mollicutes, they lack all known fermentative capabilities, including glycolysis, and can only generate energy from arginine provided by the coral host. Their genomes feature several mechanisms to interact with foreign DNA, including extensive CRISPR arrays and restriction-modification systems, which may indicate their role in symbiosis. We propose the novel family Oceanoplasmataceae which includes these symbionts and others associated with five marine invertebrate phyla. Its exceptionally broad host range suggests that the diversity of this enigmatic family remains largely undiscovered. Oceanoplasmataceae genomes are the most highly reduced among mollicutes, providing new insight into their reductive evolution and the roles of coral symbionts.

AbstractMicrobes perform critical functions in corals yet most knowledge is derived from the photic zone. Here, we discovered two mollicutes that dominate the microbiome of the deep-sea octocoral,Callogorgia delta,and reside in the mesoglea. These symbionts were abundant across the host’s range, absent in the water, and rare in sediments. The symbionts lack all known fermentative capabilities including glycolysis and can only generate energy from arginine provided by the coral host. Their genomes feature extensive mechanisms to interact with foreign DNA which may be indicative of their role in symbiosis. We erect the novel family Oceanoplasmataceae which includes these symbionts and others associated with four marine invertebrate phyla. Its exceptionally broad host range suggests that the diversity of this enigmatic family remains largely undiscovered. Oceanoplasmataceae genomes are the most highly reduced among mollicutes providing new insight into their reductive evolution and the roles of coral symbionts.

AbstractPlacozoa is an enigmatic phylum of simple, microscopic, marine metazoans1,2. Although intracellular bacteria have been found in all members of this phylum, almost nothing is known about their identity, location and interactions with their host3–6. We used metagenomic and metatranscriptomic sequencing of single host individuals, plus metaproteomic and imaging analyses, to show that the placozoan Trichoplax sp. H2 lives in symbiosis with two intracellular bacteria. One symbiont forms an undescribed genus in the Midichloriaceae (Rickettsiales)7,8 and has a genomic repertoire similar to that of rickettsial parasites9,10, but does not seem to express key genes for energy parasitism. Correlative image analyses and three-dimensional electron tomography revealed that this symbiont resides in the rough endoplasmic reticulum of its host’s internal fibre cells. The second symbiont belongs to the Margulisbacteria, a phylum without cultured representatives and not known to form intracellular associations11–13. This symbiont lives in the ventral epithelial cells of Trichoplax, probably metabolizes algal lipids digested by its host and has the capacity to supplement the placozoan’s nutrition. Our study shows that one of the simplest animals has evolved highly specific and intimate associations with symbiotic, intracellular bacteria and highlights that symbioses can provide access to otherwise elusive microbial dark matter.

Symbioses between eukaryotes and sulfur-oxidizing (thiotrophic) bacteria have convergently evolved multiple times. Although well described in at least eight classes of metazoan animals, almost nothing is known about the evolution of thiotrophic symbioses in microbial eukaryotes (protists). In this study, we characterized the symbioses between mouthless marine ciliates of the genusKentrophoros, and their thiotrophic bacteria, using comparative sequence analysis and fluorescencein situhybridization. Ciliate small-subunit rRNA sequences were obtained from 17 morphospecies collected in the Mediterranean and Caribbean, and symbiont sequences from 13 of these morphospecies. We discovered a newKentrophorosmorphotype where the symbiont-bearing surface is folded into pouch-like compartments, illustrating the variability of the basic body plan. Phylogenetic analyses revealed that all investigatedKentrophorosbelonged to a single clade, despite the remarkable morphological diversity of these hosts. The symbionts were also monophyletic and belonged to a new clade within the Gammaproteobacteria, with no known cultured representatives. Each host morphospecies had a distinct symbiont phylotype, and statistical analyses revealed significant support for host–symbiont codiversification. Given that these symbioses were collected from two widely separated oceans, our results indicate that symbiotic associations in unicellular hosts can be highly specific and stable over long periods of evolutionary time.