Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

The role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater. Results Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity. Conclusion This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large.info:eu-repo/semantics/publishedVersio

Abstracts from the 20th International Symposium on Signal Transduction at the Blood-Brain Barriers

https://deepblue.lib.umich.edu/bitstream/2027.42/138963/1/12987_2017_Article_71.pd

Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome.

BackgroundThe role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater.ResultsSymbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity.ConclusionThis is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large. Video Abstract

Additional file 1 of Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

Additional file 1: Figure S1. Phylogenomic analysis of the Ca. Thioglobaceae family using SpeciesTreeBuilder v.01.0. Figure S2. COG functions (N=76) significantly enriched (q-value < 0.05) in the octocoral-derived Ca. Gorgonimonas (Endozoicomonadaceae) MAGs (N= 11, green), compared with all other MAGs (N=55) of this dataset. Figure S3. KEGG metabolic pathway map of the Ca. Gorgonimonas (Endozoicomonadaceae) MAGs of this study. Figure S4. Phylogeny of 101 full-length, bacterial endo-chitinase (EC 3.2.1.14) encoding genes, including the 11 endo-chitinase (GH18-family) genes from Endozoicomonadaceae MAGs (grey shadings) of this study. Figure S5. COG functions (N=34) significantly enriched (p-value < 0.05) in the Ca. Thioglobaceae MAGs (N= 6, dark green), compared with all other MAGs (N=60) of this dataset. An one-sided Welch’s t-test for unequal variances was performed in STAMP v.2.1.3. Multiple test correction was performed using the Benjamini-Hochberg correction (FDR). To further limit the displayed number of significant entries, an effect size filter was also applied, setting the “ratio of proportions” to 5.00. Figure S6. KEGG metabolic pathway map of the Ca. Thioglobaceae MAGs of this study. The metabolic map features glycolysis, pyruvate, nitrogen, sulfur, and taurine metabolism. EC numbers of enzymes catalyzing the reactions are given in rectangular boxes. EC numbers highlighted in green represent enzymes encoded on Ca. Thioglobaceae MAGs. Beige boxes indicate connections to other metabolic pathways active in these MAGs. Figure S7. KEGG carbon fixation map of Ca. Thiocorallibacter gorgonii MAG EG15H_Bin1 (Ca. Thioglobaceae). EC numbers of enzymes catalyzing the reactions are given in rectangular boxes. EC numbers highlighted in green represent enzymes encoded on this MAG. Beige boxes indicate connections to other metabolic pathways active in these MAGs. Orange dots highlight the substrates (Ribulose-1,5-bisphosphate, CO2, and H2O) and product (2 Glycerate-3-phosphate, 2 H+) of Rubisco (EC 4.1.1.39)

Additional file 2 of Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

Additional file 2: Table S1. General genomic features, taxonomic classification and genome assembly accession numbers of each of the 66 metagenome-assembled genomes (MAGs) obtained from octocoral- and seawater-derived microbial metagenomes. Table S2. Overview of the number and quality of MAGs obtained from octocoral- and seawater-derived microbial metagenome samples. Table S3. Clusters of Orthologous Groups of proteins (COGs) annotation of the 66 MAGs analysed in this study. Table S4. Results of the SIMPER test performed on COG profiles (Hellinger-transformed abundances; Euclidean distances) of the 66 MAGs grouped at order level. Table S5A. Absolute abundances (counts) of COG functions shown in Figure 4 that distinguished the 66 MAGs the most (based on SIMPER and Welch's tests). Table S5B. Relative abundances of COG functions shown in Figure 4 that distinguished the 66 MAGs the most (based on SIMPER and Welch's tests). Table S6A. Features of the endo-chitinase (EC 3.2.1.14) genes found on the 11 Endozoicomonadaceae MAGs of this study. Table S6B. Genes involved in chitin degradation present on the 11 Endozoicomonadaceae MAGs of this study and other, publicly available Endozoicomonadaceae genomes. Table S7. Amino acid (n= 20) and B vitamin (n = 8) biosynthesis capacities (based on genomic evidence) of the 11 bacterial species recovered from the microbiomes of healthy octocoral tissue. Table S8. Secondary metabolite biosynthetic gene clusters (SM-BGCs) present on the 66 MAGs, annotated using antiSMASH bacterial version 5.0. Table S9. List of SM-BGCs with some level of homology to MIBiG database entries