Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “
            <i>Candidatus</i>
            Synechococcus spongiarum”

Gao, Zhaoming; Wang, Yong; Tian, Renmao; Wong, Yue Him; Batang, Zenon B.; Al-Suwailem, Abdulaziz M.; Bajic, Vladimir B.; Qian, Pei‐Yuan

doi:10.1128/mbio.00079-14

Cited by 82 publications

(96 citation statements)

References 60 publications

(112 reference statements)

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“…In contrast, the seawater metagenome revealed higher abundances of Alphaproteobacteria, Flavobacteria , and Cyanobacteria compared to the sponge metagenomes. With increasing availability of sequence data and the completion of draft genomes by single cell genomics (Kamke et al, 2014) or binning approaches (Gao et al, 2014; Burgsdorf et al, 2015), the assignment of complete reads rather than single gene markers should become widely acceptable.…”

Section: Discussionmentioning

confidence: 99%

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes

et al. 2016

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Many marine sponges are populated by dense and taxonomically diverse microbial consortia. We employed a metagenomics approach to unravel the differences in the functional gene repertoire among three Mediterranean sponge species, Petrosia ficiformis, Sarcotragus foetidus, Aplysina aerophoba and seawater. Different signatures were observed between sponge and seawater metagenomes with regard to microbial community composition, GC content, and estimated bacterial genome size. Our analysis showed further a pronounced repertoire for defense systems in sponge metagenomes. Specifically, clustered regularly interspaced short palindromic repeats, restriction modification, DNA phosphorothioation and phage growth limitation systems were enriched in sponge metagenomes. These data suggest that defense is an important functional trait for an existence within sponges that requires mechanisms to defend against foreign DNA from microorganisms and viruses. This study contributes to an understanding of the evolutionary arms race between viruses/phages and bacterial genomes and it sheds light on the bacterial defenses that have evolved in the context of the sponge holobiont.

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Section: Discussionmentioning

confidence: 99%

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes

et al. 2016

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“…Single-cell genomic and metagenomics studies have contributed to correlating particular traits with specific symbiont lineages Siegl et al, 2011;Kamke et al, 2013;Gao et al, 2014;Tian et al, 2014;Wilson et al, 2014;Burgsdorf et al, 2015;Britstein et al, 2016), revealing functional gene convergence in phylogenetically-distinct microbial communities with core features that likely reflect adaptation of microorganisms to the sponge host environment Hentschel et al, 2012). Traits that have repeatedly been reported in prokaryote symbionts of poriferans include versatile nutrient utilization, protection from environmental and host-specific stress, and eukaryotic-like proteins Hentschel et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

2016

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Amphimedon queenslandica is a coral reef demosponge that houses a low complexity and low abundance microbiota dominated by a proteobacterial duo for which draft genomes are presented here. The most prevalent symbiont, AqS1, is a sulfur-oxidizing gammaproteobacterium closely related to other demosponge symbionts and to free-living Ectothiorhodospiraceae (Chromatiales). The predicted gene repertoire of AqS1 indicates that it is capable of sulfur oxidation, carbon monoxide oxidation and inorganic phosphate assimilation, and that some of its metabolic capabilities may have been acquired via horizontal gene transfer from alphaproteobacteria. The second most prevalent symbiont, AqS2, is a betaproteobacterium whose closest known relatives are other demosponge symbionts. AqS1 has characteristic sponge symbiont features, including a versatile nutrient use with large number of transporters, ankyrin-repeat-containing proteins, and a CRISPR system. Based on the size of its genome assembly, AqS2 is predicted to have a much smaller genome with many fewer symbiotic features than AqS1. The smaller is reflected in its more limited metabolic capabilities that include carbohydrate metabolism, but not sulfur oxidation or phosphorus metabolism. Within-pathway complementation and resource partitioning potentially occur between the two bacteria. The addition of these symbiont genomes to extensive genome and transcriptome resources already available for the sponge host now permits the development of mixed-species genome-scale metabolic models as a foundation for experimental investigations of resource partitioning between symbionts and host.

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“…S4 and Table S5 in the supplemental material). High abundances of eukaryotic-like proteins (e.g., ankyrin repeats) are hypothesized to shield sponge symbionts from host digestion (26), and ankyrin repeats were also found to be abundant in the genomes of other uncultured spongesymbiotic bacteria (80)(81)(82)(83). CRISPRs are defense mechanisms against the introduction of foreign DNA, including that of phages, and were previously found to be a common feature for many sponge microbiomes and some sponge symbionts (26,(83)(84)(85); similarly, they were found also in the genome of Rhodobacterales bacterium TS309 (see Table S5 in the supplemental material).…”

Section: Discussionmentioning

confidence: 99%

A NewN-Acyl Homoserine Lactone Synthase in an Uncultured Symbiont of the Red Sea Sponge Theonella swinhoei

Britstein

Devescovi

Handley

et al. 2016

Appl Environ Microbiol

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i Sponges harbor a remarkable diversity of microbial symbionts in which signal molecules can accumulate and enable cell-cell communication, such as quorum sensing (QS). Bacteria capable of QS were isolated from marine sponges; however, an extremely small fraction of the sponge microbiome is amenable to cultivation. We took advantage of community genome assembly and binning to investigate the uncultured majority of sponge symbionts. We identified a complete N-acyl-homoserine lactone (AHL)-QS system (designated TswIR) and seven partial luxI homologues in the microbiome of Theonella swinhoei. The TswIR system was novel and shown to be associated with an alphaproteobacterium of the order Rhodobacterales, here termed Rhodobacterales bacterium TS309. The tswI gene, when expressed in Escherichia coli, produced three AHLs, two of which were also identified in a T. swinhoei sponge extract. The taxonomic affiliation of the 16S rRNA of Rhodobacterales bacterium TS309 to a sponge-coral specific clade, its enrichment in sponge versus seawater and marine sediment samples, and the presence of spongespecific features, such as ankyrin-like domains and tetratricopeptide repeats, indicate a likely symbiotic nature of this bacterium. Symbiosis between metazoans and microbes exists in virtually every environment, including in marine sponges (phylum Porifera) (1). Marine sponges are important members of shallow and deep reef communities and are a rich source of secondary metabolites with pharmaceutical potential, and these metabolites are often produced by the sponges' microbial symbionts (2, 3). These host-associated bacteria are sponge specific and can comprise up to 35% of the sponge volume (4), spanning at least 47 bacterial phyla (5).In recent years, symbioses between microorganisms and eukaryotic hosts have received growing attention. The host, together with all its symbionts, is now seen as a single entity designated the holobiont, defined as the sum of the genetic information of the host and its microbiota (6). Sponge holobionts provide an enclosed niche in which extensive interactions among dense and diverse microbial populations are accomplished (7). The mechanisms underlying cell-cell interactions among bacteria within the sponge and the genetic regulation systems controlling gene expression in sponge symbionts are largely unknown. One of the best understood microbial quorum-sensing (QS) systems is the one that uses N-acyl-homoserine lactones (AHLs) as signals (e.g., 8-10). QS enables bacteria to regulate their gene expression in a population density-dependent manner. At a low cell density, low levels of AHLs, which diffuse in and out of the bacterial cell, are present. As the bacterial density increases, especially for bacteria enclosed in niches, AHLs accumulate, and once they reach a critical level (quorum), they interact with LuxR cognate receptor proteins, which then affect target gene expression (11). A canonical AHL-QS system produces AHLs via the LuxI family AHL synthase protein and responds to them via the LuxR co...

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Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “ Candidatus Synechococcus spongiarum”

Cited by 82 publications

References 60 publications

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

A NewN-Acyl Homoserine Lactone Synthase in an Uncultured Symbiont of the Red Sea Sponge Theonella swinhoei

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