Marine sponges and their microbial symbionts: love and other relationships

Webster, Nicole S.; Taylor, Michael W.

doi:10.1111/j.1462-2920.2011.02460.x

Cited by 506 publications

(439 citation statements)

References 117 publications

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“…Sponge-specific and species-specific symbiont associations Our analyses confirmed a clear sponge-specific and species-specific signature of bacterial community composition, in agreement with previous studies employing less sequencing coverage (Webster et al, 2010;Erwin et al, 2011Erwin et al, , 2012Lee et al, 2011;Webster and Taylor, 2012). Sponge samples stored in a variety of ways also clustered by species, suggesting the signal override the preservatives, as previously shown (Simister et al, 2011).…”

Section: Discussionsupporting

confidence: 78%

Host-specificity among abundant and rare taxa in the sponge microbiome

Réveillaud¹,

Maignien²,

Eren³

et al. 2014

The ISME Journal

235

208

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Microbial communities have a key role in the physiology of the sponge host, and it is therefore essential to understand the stability and specificity of sponge-symbiont associations. Host-specific bacterial associations spanning large geographic distance are widely acknowledged in sponges. However, the full spectrum of specificity remains unclear. In particular, it is not known whether closely related sponges host similar or very different microbiota over wide bathymetric and geographic gradients, and whether specific associations extend to the rare members of the sponge microbiome. Using the ultra-deep Illumina sequencing technology, we conducted a comparison of sponge bacterial communities in seven closely related Hexadella species with a well-resolved host phylogeny, as well as of a distantly related sponge Mycale. These samples spanned unprecedentedly large bathymetric (15-960 m) gradients and varying European locations. In addition, this study included a bacterial community analysis of the local background seawater for both Mycale and the widespread deep-sea taxa Hexadella cf. dedritifera. We observed a striking diversity of microbes associated with the sponges, spanning 47 bacterial phyla. The data did not reveal any Hexadella microbiota co-speciation pattern, but confirmed sponge-specific and species-specific host-bacteria associations, even within extremely low abundant taxa. Oligotyping analysis also revealed differential enrichment preferences of closely related Nitrospira members in closely related sponges species. Overall, these results demonstrate highly diverse, remarkably specific and stable spongebacteria associations that extend to members of the rare biosphere at a very fine phylogenetic scale, over significant geographic and bathymetric gradients.

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Section: Discussionsupporting

confidence: 78%

Host-specificity among abundant and rare taxa in the sponge microbiome

Réveillaud¹,

Maignien²,

Eren³

et al. 2014

The ISME Journal

235

208

View full text Add to dashboard Cite

show abstract

“…However, the ascidian microbiota also maintained distinguishing characteristics in comparison to other host-associated communities. For example, the phylum Planctomycetes exhibited high diversity in ascidian hosts, whereas members of this phylum are typically rare in microbiota of sponge (Schmitt et al, 2012;Webster and Taylor, 2012) and coral hosts (Sunagawa et al, 2010;Barott et al, 2011). Further, 11 of the 56 most common OTUs in the ascidian microbiota exhibited high sequence divergence (45%) from any previously described marine microbe.…”

Section: Discussionmentioning

confidence: 99%

“…The advent of high-throughput, next-generation DNA sequencing platforms offers new opportunities for in-depth microbial diversity evaluation across large sample sets. Deep sequencing of microbial communities from soils, seawater and sponges has revealed diversity estimates over an order of magnitude higher than that recovered by traditional sequencing techniques (Huber et al, 2007;Roesch et al, 2007;Webster et al, 2010), including the detection of bacterial phyla not represented in firstgeneration sequencing datasets (e.g., Webster and Taylor, 2012). Similarly, the recent application of next generation sequencing to the ascidian microbiota has revealed a high diversity of symbiotic microbes and uncovered new ascidian-associated microbial lineages in the colonial host Lissoclinum patella and solitary host Styela plicata (Erwin et al, 2013), highlighting the depth of microbial biodiversity and unknown facultative and obligate symbiotic microbes awaiting discovery within ascidian hosts.…”

Section: Introductionmentioning

confidence: 99%

Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians

et al. 2013

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Ascidians are ecologically important components of marine ecosystems yet the ascidian microbiota remains largely unexplored beyond a few model species. We used 16S rRNA gene tag pyrosequencing to provide a comprehensive characterization of microbial symbionts in the tunic of 42 Great Barrier Reef ascidian samples representing 25 species. Results revealed high bacterial biodiversity (3 217 unique operational taxonomic units (OTU 0.03 ) from 19 described and 14 candidate phyla) and the widespread occurrence of ammonia-oxidizing Thaumarchaeota in coral reef ascidians (24 of 25 host species). The ascidian microbiota was clearly differentiated from seawater microbial communities and included symbiont lineages shared with other invertebrate hosts as well as unique, ascidian-specific phylotypes. Several rare seawater microbes were markedly enriched (200-700 fold) in the ascidian tunic, suggesting that the rare biosphere of seawater may act as a conduit for horizontal symbiont transfer. However, most OTUs (71%) were rare and specific to single hosts and a significant correlation between host relatedness and symbiont community similarity was detected, indicating a high degree of host-specificity and potential role of vertical transmission in structuring these communities. We hypothesize that the complex ascidian microbiota revealed herein is maintained by the dynamic microenvironments within the ascidian tunic, offering optimal conditions for different metabolic pathways such as ample chemical substrate (ammonia-rich host waste) and physical habitat (high oxygen, low irradiance) for nitrification. Thus, ascidian hosts provide unique and fertile niches for diverse microorganisms and may represent an important and previously unrecognized habitat for nitrite/nitrate regeneration in coral reef ecosystems.

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“…Animal-plant/microbe symbioses are vital to these ecosystems as they facilitate photosynthetic productivity, mineral recycling, nutrient provision to the host and secondary metabolite production (Smith and Douglas, 1987). Although patterns of microbial diversity and putative symbiotic functions have been well explored in corals and sponges (Sunagawa et al, 2009;Mouchka et al, 2010;Webster and Taylor, 2012;Bourne and Webster, 2013), there is a lack of data on microbial associations in other reef taxa including Bivalves, Foraminifera and Ascidians.…”

mentioning

confidence: 99%

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

et al. 2013

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Coral reefs provide habitat for an array of marine invertebrates that host symbiotic microbiomes. Photosynthetic symbionts including Symbiodinium dinoflagellates and diatoms potentially influence the diversity of their host-associated microbiomes by releasing carbon-containing photosynthates and other organic compounds that fuel microbial metabolism. Here we used 16S ribosomal RNA (rRNA) gene amplicon pyrosequencing to characterise the microbiomes of 11 common Great Barrier Reef marine invertebrate species that host photosynthetic symbionts and five taxa in which they are absent. The presence of photosynthetic symbionts influenced the composition but not the species richness, evenness and phylogenetic diversity of invertebrateassociated microbiomes. Invertebrates without photosynthetic symbionts were dominated by Alphaproteobacteria, whereas those hosting photosynthetic symbionts were dominated by Gammaproteobacteria. Interestingly, many microbial species from photosymbiont-bearing invertebrates, including Oceanospirillales spp., Alteromonas spp., Pseudomonas spp., Halomonas spp., are implicated in the metabolism of dimethylsulfoniopropionate (DMSP). DMSP is produced in high concentrations by photosynthetic dinoflagellates and is involved in climate regulation by facilitating cloud formation. Microbiomes correlated with host taxa and replicate individuals from most sampled species grouped in distance-based redundancy analysis of retrieved 16S rRNA gene sequences. This study highlights the complex nature of invertebrate holobionts and confirms the importance of photosynthetic symbionts in structuring marine invertebrate bacterial communities.

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Marine sponges and their microbial symbionts: love and other relationships

Cited by 506 publications

References 117 publications

Host-specificity among abundant and rare taxa in the sponge microbiome

Host-specificity among abundant and rare taxa in the sponge microbiome

Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

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