Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus

Oren, Matan; Steindler, Laura; Ilan, Micha

doi:10.1007/s00227-005-0064-8

Cited by 53 publications

(50 citation statements)

References 16 publications

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“…Such a co-speciation pattern, where closely related sponges contain more similar microbial communities compared with distantly related sponges, would be expected if sponge symbionts were strictly transmitted via reproductive stages to the next generation. Vertical transmission of single lineages and of complex microbial communities has been shown for several sponges including some of the species investigated in this study (Usher et al, 2001;Oren et al, 2005;Enticknap et al, 2006;Schmitt et al, 2007;Sharp et al, 2007). However, it was previously proposed that vertical transmission is not the only mechanism of symbiont acquisition and that sponge symbionts may additionally be acquired from the seawater (Taylor et al, 2007;Schmitt et al, 2008;Webster et al, 2010).…”

Section: Resultsmentioning

confidence: 67%

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

et al. 2011

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Marine sponges are well known for their associations with highly diverse, yet very specific and often highly similar microbiota. The aim of this study was to identify potential bacterial sub-populations in relation to sponge phylogeny and sampling sites and to define the core bacterial community. 16S ribosomal RNA gene amplicon pyrosequencing was applied to 32 sponge species from eight locations around the world's oceans, thereby generating 2567 operational taxonomic units (OTUs at the 97% sequence similarity level) in total and up to 364 different OTUs per sponge species. The taxonomic richness detected in this study comprised 25 bacterial phyla with Proteobacteria, Chloroflexi and Poribacteria being most diverse in sponges. Among these phyla were nine candidate phyla, six of them found for the first time in sponges. Similarity comparison of bacterial communities revealed no correlation with host phylogeny but a tropical sub-population in that tropical sponges have more similar bacterial communities to each other than to subtropical sponges. A minimal core bacterial community consisting of very few OTUs (97%, 95% and 90%) was found. These microbes have a global distribution and are probably acquired via environmental transmission. In contrast, a large species-specific bacterial community was detected, which is represented by OTUs present in only a single sponge species. The species-specific bacterial community is probably mainly vertically transmitted. It is proposed that different sponges contain different bacterial species, however, these bacteria are still closely related to each other explaining the observed similarity of bacterial communities in sponges in this and previous studies. This global analysis represents the most comprehensive study of bacterial symbionts in sponges to date and provides novel insights into the complex structure of these unique associations.

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Section: Resultsmentioning

confidence: 67%

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

et al. 2011

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“…In an ontogenetic context, numerous studies have demonstrated vertical inheritance of putatively core symbionts during development of embryos and larvae, based on evidence from electron microscopy (see for example Ereskovsky et al, 2005;Oren et al, 2005;Maldonado, 2007;Schmitt et al, 2008) or sequencing of prokaryotic 16S rRNA gene amplicons (see for example Oren et al, 2005;Enticknap et al, 2006;Schmitt et al, 2007Schmitt et al, , 2008Sharp et al, 2007;Steger et al, 2008;Lee et al, 2009;Webster et al, 2010;Gloeckner et al, 2012). Horizontal transmission, characterized by de novo symbiont acquisition from the environment with each new generation, has also been identified in several sponges (de Caralt et al, 2007;Maldonado, 2007;Schmitt et al, 2007;Gloeckner et al, 2013) and could include the introduction into the microbiome of opportunistic, non-core bacterial species.…”

Section: Introductionmentioning

confidence: 99%

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

et al. 2016

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Vertical transmission of bacterial symbionts, which is known in many species of sponge (Porifera), is expected to promote strong fidelity between the partners. Combining 16S rRNA gene amplicon sequencing and electron microscopy, we have assayed the relative abundance of vertically-inherited bacterial symbionts in several stages of the life cycle of Amphimedon queenslandica, a tropical coral reef sponge. We reveal that adult A. queenslandica house a low diversity microbiome dominated by just three proteobacterial OTUs, with a single gammaprotebacterium clearly dominant through much of the life cycle. This ontogenetic perspective has revealed that, although vertical transmission occurs very early in development, the inherited symbionts do not maintain proportional dominance of the bacterial community at every developmental stage. A reproductive bottleneck in the A. queenslandica life cycle is larval settlement, when a free-swimming pelagic larva settles out of the water column onto the benthos and completes metamorphoses into the sessile body plan within just 3-4 days. During this dramatic life cycle transition, an influx of environmentally-derived bacteria leads to a major reorganization of the microbiome, potentially challenging the fidelity and persistence of the vertically-inherited symbiotic relationships. However, dominance of the primary, vertically-inherited symbionts is restored in adult sponges. The mechanisms underlying ontogenetic changes in the bacterial community are unknown, including how the dominance of the primary symbionts is restored in the adult sponge-does the host or symbiont regulate this process? Using high-resolution transcriptional profiling in multiple stages of the A. queenslandica life cycle combined with this natural perturbation of the microbiome immediately following larval settlement, we are beginning to identify candidate host genes associated with animal-bacterial crosstalk. Among the sponge host genes upregulated during the times of active microbiome assembly, there is an enrichment of genes potentially involved in innate immunity, including scavenger receptors, and of genes containing eukaryote-like domains, which have elsewhere Fieth et al.Sponge Microbiome Changes through Lifecycle been implicated in host-symbiont interactions. Intriguingly, we also see an enrichment of sponge genes arising from ancient horizontal transfer events from bacteria, which raises the possibility that host-bacterial associations in the evolutionary past may help to regulate host-bacterial associations in the ecological present.

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“…The Red Sea sponges have been studied during the past two decades for their natural products and bioactive compounds, as well as for their ecological importance to coral reefs (Ilan et al, 2004). There are about 240 sponge species recorded in the Red Sea (Radwan et al, 2010), yet only a few with their microbial communities have been studied (Hentschel et al, 2002;Oren et al, 2005;Radwan et al, 2010). In this study, we used the massively parallel tag pyrosequencing technology to better explore the diversity, stability and specificity of microbial communities associated with different sponge species from different locations of the Red Sea.…”

Section: Introductionmentioning

confidence: 99%

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

et al. 2010

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Marine sponges are associated with a remarkable array of microorganisms. Using a tag pyrosequencing technology, this study was the first to investigate in depth the microbial communities associated with three Red Sea sponges, Hyrtios erectus, Stylissa carteri and Xestospongia testudinaria. We revealed highly diverse sponge-associated bacterial communities with up to 1000 microbial operational taxonomic units (OTUs) and richness estimates of up to 2000 species. Altogether, 26 bacterial phyla were detected from the Red Sea sponges, 11 of which were absent from the surrounding sea water and 4 were recorded in sponges for the first time. Up to 100 OTUs with richness estimates of up to 300 archaeal species were revealed from a single sponge species. This is by far the highest archaeal diversity ever recorded for sponges. A non-negligible proportion of unclassified reads was observed in sponges. Our results demonstrated that the sponge-associated microbial communities remained highly consistent in the same sponge species from different locations, although they varied at different degrees among different sponge species. A significant proportion of the tag sequences from the sponges could be assigned to one of the sponge-specific clusters previously defined. In addition, the sponge-associated microbial communities were consistently divergent from those present in the surrounding sea water. Our results suggest that the Red Sea sponges possess highly sponge-specific or even sponge-species-specific microbial communities that are resistant to environmental disturbance, and much of their microbial diversity remains to be explored.

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Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus

Cited by 53 publications

References 16 publications

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

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