The Cyanobacteria-Dominated Sponge Dactylospongia elegans in the South China Sea: Prokaryotic Community and Metagenomic Insights

Abstract

The South China Sea is a special reservoir of sponges of which prokaryotic communities are less studied. Here, a new record of the sponge Dactylospongia elegans is reported near the coast of Jinqing Island in the South China Sea, and its prokaryotic community is comprehensively investigated. Sponge specimens displayed lower microbial diversity compared with surrounding seawater. At the phylum level, prokaryotic communities were consistently dominated by Proteobacteria, followed by Cyanobacteria, Chloroflexi, Acidobacteria, Actinobacteria, Gemmatimonadetes, Thaumarchaeota, and Poribacteria. Operational taxonomic unit (OTU) analysis alternatively showed that the most abundant symbiont was the sponge-specific cyanobacterial species “Candidatus Synechococcus spongiarum,” followed by OTUs belonging to the unidentified Chloroflexi and Acidobacteria. Phylogenetic tree based on 16S-23S internal transcribed spacer regions indicated that the dominated cyanobacterial OTU represented a new clade of “Ca. Synechococcus spongiarum.” More reliable metagenomic data further revealed that poribacterial symbionts were highly abundant and only secondary to the cyanobacterial symbiont. One draft genome for each of the Cyanobacteria, Chloroflexi and Acidobacteria and three poribacterial genomes were extracted from the metagenomes. Among them, genomes affiliated with the Chloroflexi and Acidobacteria were reported for the first time in sponge symbionts. Eukaryotic-like domains were found in all the binned genomes, indicating their potential symbiotic roles with the sponge host. The high quality of the six recovered genomes of sponge symbionts from the sponge D. elegans makes it possible to understand their symbiotic roles and interactions with the sponge host as well as among one another.

Pangenomic comparison of globally distributed Poribacteria associated with sponge hosts and marine particles

“…Other studies, using only broader "universal" primers, found much lower relative abundances in samples from the same sponge host species [19,28]. These differences may reflect natural biological variation, but could also be the result of reduced sensitivity due to amplification primer mismatches [1,9,12,29], raising concerns that historical surveys relying exclusively on unsuitable primers may have systematically under-reported Poribacteria abundance.…”

“…Ultrastructure and molecular characterization studies to date have relied heavily on samples obtained from a single host, Aplysina aerophoba, but Poribacteria-related 16S rRNA genes have also been detected in numerous other sponge genera, including Agelas, Astrosclera, Dactylospongia, Geodia, Ircinia, Plaktoris, Pseudoceratina, Rhabdastrella, Theonella, Vaceletia, and Xestospongia [2,[11][12][13][14][15][16][17][18][19]. Closely related 16S rRNA sequences have also been observed, albeit at much lower levels, in corals, seawater, and marine sediment samples [2,3,[19][20][21][22].…”

“…Phylogenetic trees constructed from partial 16S rRNA sequences suggest that sponge-associated Poribacteria may fall into four [16,23] or five [24] distinct subclasses, but no correlations have been observed between these classes and sponge host taxonomy or geographical location. Several studies analyzing sponge-associated microbial communities with specifically targeted 16S rRNA gene primers observed Poribacteria-related sequences at relative abundances of 20-30% [1,12,[25][26][27]. Other studies, using only broader "universal" primers, found much lower relative abundances in samples from the same sponge host species [19,28].…”

New Microbial Lineages Capable of Carbon Fixation and Nutrient Cycling in Deep-Sea Sediments of the Northern South China Sea

“…RNase-and DNase-free sterile tubes and tips were used in the operation to avoid contaminants from the environment. DNA in the RNA extractions was removed by a Turbo DNA-free kit (Ambion, Carlsbad, CA, USA) and was checked by PCR using universal primer 341F (5=-CCTAYGGGRBGCASCAG-3=) and reverse fusion primer 802R (5=-TACNVGGGTATCTAATCC-3=) targeting V3-V4 region of 16S rRNA genes (52). The primers were examined in Silva (https://www.arb -silva.de/) for primer coverage of Asgard archaea and novel bacterial phyla.…”

In situ meta‐omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench

“…Raw paired-end reads were trimmed using Btrim (Kong, 2011) with default parameters and further assembled using FLASH with at least 40 bp overlap (Magoc and Salzberg, 2011). Assembled reads were subjected to QIIME 1.8.0 pipelines for downstream bioinformatics analysis (Caporaso et al, 2010) with the same modifications mentioned in our previous work (Gao et al, 2017). The SILVA database for taxonomic assignment was updated to version 128 .…”