Discovery of deep-sea coral symbionts from a novel family of marine bacteria, Oceanoplasmataceae, with severely reduced genomes

Abstract

In addition to abundant animal communities, corals from all ocean depths support diverse microbial associates that are important to coral health. While some of these microbes have been classified taxonomically, understanding the metabolic potential of coral-associated bacteria and how they interact with their coral hosts is limited by a lack of genomic data. One example is Mycoplasma and other members of the class Mollicutes which are widespread coral associates. Here we investigated the association between two novel members of the class Mollicutes and the deep-sea octocoral Callogorgia delta. We screened C. delta, a closely related species C. americana, sediment, and water for mollicutes using 16S metabarcoding. One ASV was found in most colonies screened (99/108) and often dominated the microbiome (up to 99%). Another ASV was detected at lower abundance and prevalence in these corals. Both were absent in all water and were absent or rare in the sediment. We sequenced metagenomes and metatranscriptomes to assemble and annotate genomes and propose the names Ca. Oceanoplasma callogorgiae and Ca. Thalassoplasma callogorgiae. The genomes were small, revealed a reliance on the arginine dihydrolase pathway for ATP production, and contained CRISPR-Cas systems with extensive arrays. CARD-FISH microscopy unveiled an abundant bacterium in the mesoglea which is likely to be Ca. O. callogorgiae. These novel mollicutes cluster with others from diverse invertebrate hosts. Altogether, this work describes the association of these novel mollicutes in C. delta, provides insight into widespread coral associates, and identifies a novel clade of marine mollicutes whose diversity remains largely undiscovered.

Capacity of deep‐sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization

“…The alternative explanation, that C. delta was supplemented with chemosynthetically fixed carbon from a bacterial symbiont living within its tissue, was less likely for three reasons. (i) The assembled whole genome of Mollicutes (i.e., the dominant bacterial phylotype, see Figure 3 ) collected from some of the C. delta colonies used in the current study showed lack of chemosynthetic pathways (Vohsen et al, 2022 ). (ii) The relative abundances of C. delta dominant symbiotic bacteria (i.e., Mollicutes—Figure 3 ) were not significantly different between seep and non‐seep samples and did not correlate with stable isotope values (Figure S6 ).…”

Octocoral microbiomes vary substantially across environmental gradients in deep waters

“…Both C. delta and P. biscaya hosted three dominant ASVs. All three dominant ASVs in C. delta were recently described [29] as novel members of the class Mollicutes: two Ca. Oceanoplasma and one Ca.…”

“…and possess capabilities relevant to the coral host such as producing vitamins [25, 26], degrading dimethylsulfoniopropionate [27], and cycling phosphorus [28]. Similarly, corallicolid apicomplexans and Mycoplasma are commonly found in many coral species and reside within or on coral tissue [10, 18, 29]. Most apicomplexans [30] and Mycoplasma spp.…”

“…Endozoicomonas responds to coral tissue extracts by activating genes involved in initiating symbiosis 33 . Similarly, corallicolid apicomplexans and Mycoplasma are commonly found in many coral species and reside within or on coral tissue 16,24,36 . Most apicomplexans 37 and Mycoplasma spp.…”