Sponge‐specific clusters revisited: a comprehensive phylogeny of sponge‐associated microorganisms

Simister, Rachel L.; Deines, Peter; Botté, Emmanuelle S.; Webster, Nicole S.; Taylor, Michael W.

doi:10.1111/j.1462-2920.2011.02664.x

Cited by 236 publications

(390 citation statements)

References 36 publications

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“…In addition, the ascidian microbiota demonstrated some overlap with other host-associated microbial communities yet clear distinction from ambient planktonic communities in coral reef seawater, except for the widespread presence of Cyanobacteria from the Prochlorococcus genus. Consistently, previous studies have noted multiple shared symbiont lineages among microbiota of sponges and corals (Taylor et al, 2007;Simister et al, 2012), indicating microbial lineages adapted to host-associated lifestyles may disperse among disparate host organisms. However, the ascidian microbiota also maintained distinguishing characteristics in comparison to other host-associated communities.…”

Section: Discussionsupporting

confidence: 65%

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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Section: Discussionsupporting

confidence: 65%

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

et al. 2013

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“…are nitrite oxidizers and are proposed to have key roles in nitrogen fixing and cycling within the ascidian tunics Lucker et al, 2013). Another group that was slightly enriched in L. badium samples specifically in PNG_11062 (22%) is the Acidimicrobiales class of actinobacteria, a group that was previously described as a sponge-specific bacterial group (Simister et al, 2012). All the analyses for identifying the most abundant species-specific bacteria were further confirmed by Metastats analyses for the statistical identification of differentially abundance OTUs (data not shown).…”

Section: Bacterial Composition Of Ascidiansmentioning

confidence: 99%

Species specificity of symbiosis and secondary metabolism in ascidians

et al. 2014

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Ascidians contain abundant, diverse secondary metabolites, which are thought to serve a defensive role and which have been applied to drug discovery. It is known that bacteria in symbiosis with ascidians produce several of these metabolites, but very little is known about factors governing these 'chemical symbioses'. To examine this phenomenon across a wide geographical and species scale, we performed bacterial and chemical analyses of 32 different ascidians, mostly from the didemnid family from Florida, Southern California and a broad expanse of the tropical Pacific Ocean. Bacterial diversity analysis showed that ascidian microbiomes are highly diverse, and this diversity does not correlate with geographical location or latitude. Within a subset of species, ascidian microbiomes are also stable over time (R ¼ À 0.037, P-value ¼ 0.499). Ascidian microbiomes and metabolomes contain species-specific and location-specific components. Location-specific bacteria are found in low abundance in the ascidians and mostly represent strains that are widespread. Location-specific metabolites consist largely of lipids, which may reflect differences in water temperature. By contrast, species-specific bacteria are mostly abundant sequenced components of the microbiomes and include secondary metabolite producers as major components. Species-specific chemicals are dominated by secondary metabolites. Together with previous analyses that focused on single ascidian species or symbiont type, these results reveal fundamental properties of secondary metabolic symbiosis. Different ascidian species have established associations with many different bacterial symbionts, including those known to produce toxic chemicals. This implies a strong selection for this property and the independent origin of secondary metabolite-based associations in different ascidian species. The analysis here streamlines the connection of secondary metabolite to producing bacterium, enabling further biological and biotechnological studies.

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“…Numerous studies have reported the existence of monophyletic sponge-specific 16S ribosomal RNA (rRNA) gene sequence clusters, representing bacteria found in sponges but not detected in other environments, such as seawater (Hentschel et al, 2002;Taylor et al, 2007;Simister et al, 2012). In a recent 16S rRNA gene tag pyrosequencing study (Webster et al, 2010), we revealed the presence of sequences affiliated with 'sponge-specific' clusters in seawater.…”

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confidence: 99%

“…The analysed data demonstrate the power of next-generation sequencing technologies Figure 2 Occurrence of 'sponge-specific' 16S rRNA gene sequence clusters in ICoMM samples. Heatmap showing the distribution of representatives of previously described 'sponge-specific' 16S rRNA gene sequence clusters (Simister et al, 2012) among the V6 pyrotag sequences downloaded from the ICoMM website. Clusters with an SC prefix contain sequences previously reported only from sponges; SCC prefix signifies clusters containing only sponge-and coral-derived sequences.…”

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confidence: 99%

“…These sequences were screened against a manually curated SILVA 16S rRNA database (Pruesse et al, 2007) containing 366 026 bacterial sequences, using a phylogenetic assignment procedure based on those described previously (Webster et al, 2010;Schmitt et al, 2012). One-hundred and seventy-three sponge-specific clusters (SC1-SC173) and 32 sponge-coralspecific clusters (SCC 1-SCC 32) were identified in an earlier study (Simister et al, 2012) and were represented in the SILVA database. In brief, each ICoMM-derived pyrotag was subjected to a BLAST (Altschul et al, 1990) search against the curated SILVA database, and the 50 best hits were aligned in order to determine sequence similarities.…”

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confidence: 99%

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‘Sponge-specific’ bacteria are widespread (but rare) in diverse marine environments

et al. 2012

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Numerous studies have reported the existence of sponge-specific 16S ribosomal RNA (rRNA) gene sequence clusters, representing bacteria found in sponges but not detected in other environments, such as seawater. The advent of deep-sequencing technologies allows us to examine the rare microbial biosphere in order to establish whether these bacteria are truly sponge specific, or are more widely distributed but only at abundances below the detection limit of conventional molecular approaches. We screened 412 million publicly available 16S rRNA gene pyrotags derived from 649 seawater, sediment, hydrothermal vent and coral samples from temperate, tropical and polar regions. We detected 77 of the 173 previously described sponge-specific clusters in seawater or other non-sponge samples, albeit generally at extremely low abundances. Sequences representing the candidate phylum 'Poribacteria', previously thought to be largely restricted to sponges, were recovered from 46 (out of 411) seawater and 41 (out of 129) sediment samples. While the presence of an organism does not imply that it is active in situ, our results do suggest that many 'spongespecific' bacteria occur more widely outside of sponge hosts than previously thought. The ISME Journal (2013) 7, 438-443; doi:10.1038/ismej.2012.111; published online 4 October 2012Subject Category: microbe-microbe and microbe-host interactions Keywords: marine sponge; bacteria; specificity; 16S rRNA pyrosequencing Marine sponges form relationships with a diverse range of microbes (Taylor et al., 2007;Webster and Taylor, 2012), and many of these associations are highly host specific (Schmitt et al., 2012). Numerous studies have reported the existence of monophyletic sponge-specific 16S ribosomal RNA (rRNA) gene sequence clusters, representing bacteria found in sponges but not detected in other environments, such as seawater (Hentschel et al., 2002;Taylor et al., 2007;Simister et al., 2012). In a recent 16S rRNA gene tag pyrosequencing study (Webster et al., 2010), we revealed the presence of sequences affiliated with 'sponge-specific' clusters in seawater. While this finding suggests that 'sponge-specific' bacteria can in fact reside outside of these hosts, the seawater was collected only 10 m away from the sampled sponges at the time of sponge spawning and thus a sponge origin for these bacteria could not be unequivocally ruled out. To clarify this fundamental issue in sponge symbiont biology, we examined 412 million 16S rRNA gene pyrotags (V6 region) generated under the auspices of the International Census of Marine Microbes (ICoMM; http://icomm.mbl.edu/). These sequences were derived from a range of seawater, sediment, hydrothermal vent and coral samples obtained from temperate, tropical and polar regions (Figure 1). The absence of 'sponge-specific' bacteria from these samples would provide strong additional evidence for their host specificity, whereas their widespread occurrence among non-sponge samples would imply that they are capable of at least surviving in a free-living state...

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Sponge‐specific clusters revisited: a comprehensive phylogeny of sponge‐associated microorganisms

Cited by 236 publications

References 36 publications

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

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

Species specificity of symbiosis and secondary metabolism in ascidians

‘Sponge-specific’ bacteria are widespread (but rare) in diverse marine environments

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