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Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges.

ABSTRACT: Many marine sponges are hosts to dense and phylogenetically diverse microbial communities that are located in the extracellular matrix of the animal. The candidate phylum Poribacteria is a predominant member of the sponge microbiome and its representatives are nearly exclusively found in sponges. Here we used single-cell genomics to obtain comprehensive insights into the metabolic potential of individual poribacterial cells representing three distinct phylogenetic groups within Poribacteria. Genome sizes were up to 5.4 Mbp and genome coverage was as high as 98.5%. Common features of the poribacterial genomes indicated that heterotrophy is likely to be of importance for this bacterial candidate phylum. Carbohydrate-active enzyme database screening and further detailed analysis of carbohydrate metabolism suggested the ability to degrade diverse carbohydrate sources likely originating from seawater and from the host itself. The presence of uronic acid degradation pathways as well as several specific sulfatases provides strong support that Poribacteria degrade glycosaminoglycan chains of proteoglycans, which are important components of the sponge host matrix. Dominant glycoside hydrolase families further suggest degradation of other glycoproteins in the host matrix. We therefore propose that Poribacteria are well adapted to an existence in the sponge extracellular matrix. Poribacteria may be viewed as efficient scavengers and recyclers of a particular suite of carbon compounds that are unique to sponges as microbial ecosystems.

SUBMITTER: Kamke J

PROVIDER: S-EPMC3834845 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges.

Kamke Janine J Sczyrba Alexander A Ivanova Natalia N Schwientek Patrick P Rinke Christian C Mavromatis Kostas K Woyke Tanja T Hentschel Ute U

The ISME journal 20130711 12

Many marine sponges are hosts to dense and phylogenetically diverse microbial communities that are located in the extracellular matrix of the animal. The candidate phylum Poribacteria is a predominant member of the sponge microbiome and its representatives are nearly exclusively found in sponges. Here we used single-cell genomics to obtain comprehensive insights into the metabolic potential of individual poribacterial cells representing three distinct phylogenetic groups within Poribacteria. Gen ...[more]

PMID: 23842652

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Project description:Marine sponges are recognized as valuable sources of bioactive metabolites and renowned as petri dishes of the sea, providing specialized niches for many symbiotic microorganisms. Sponges of the family Dysideidae are well documented to be chemically talented, often containing high levels of polyhalogenated compounds, terpenoids, peptides, and other classes of bioactive small molecules. This group of tropical sponges hosts a high abundance of an uncultured filamentous cyanobacterium, Hormoscilla spongeliae Here, we report the comparative genomic analyses of two phylogenetically distinct Hormoscilla populations, which reveal shared deficiencies in essential pathways, hinting at possible reasons for their uncultivable status, as well as differing biosynthetic machinery for the production of specialized metabolites. One symbiont population contains clustered genes for expanded polybrominated diphenylether (PBDE) biosynthesis, while the other instead harbors a unique gene cluster for the biosynthesis of the dysinosin nonribosomal peptides. The hybrid sequencing and assembly approach utilized here allows, for the first time, a comprehensive look into the genomes of these elusive sponge symbionts.IMPORTANCE Natural products provide the inspiration for most clinical drugs. With the rise in antibiotic resistance, it is imperative to discover new sources of chemical diversity. Bacteria living in symbiosis with marine invertebrates have emerged as an untapped source of natural chemistry. While symbiotic bacteria are often recalcitrant to growth in the lab, advances in metagenomic sequencing and assembly now make it possible to access their genetic blueprint. A cell enrichment procedure, combined with a hybrid sequencing and assembly approach, enabled detailed genomic analysis of uncultivated cyanobacterial symbiont populations in two chemically rich tropical marine sponges. These population genomes reveal a wealth of secondary metabolism potential as well as possible reasons for historical difficulties in their cultivation.

Project description:UNLABELLED:The "Candidatus Synechococcus spongiarum" group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a "Ca. Synechococcus spongiarum" group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, "Ca. Synechococcus spongiarum" includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of "Ca. Synechococcus spongiarum," each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of "Ca. Synechococcus spongiarum" members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the "Ca. Synechococcus spongiarum" group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack. IMPORTANCE:While the Synechococcus/Prochlorococcus-type cyanobacteria are widely distributed in the world's oceans, a subgroup has established its niche within marine sponge tissues. Recently, the first genome of sponge-associated cyanobacteria, "Candidatus Synechococcus spongiarum," was described. The sequencing of three representatives of different clades within this cyanobacterial group has enabled us to investigate intraspecies diversity, as well as to give a more comprehensive understanding of the common symbiotic features that adapt "Ca. Synechococcus spongiarum" to its life within the sponge host.

Dataset Information

Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges.

Publications

Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges.

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