An Anaerobic World in Sponges

Hoffmann, Friederike; Larsen, Ole; Thiel, Volker; Rapp, Hans Tore; Pape, Thomas; Michaelis, Walter; Reitner, Joachim

doi:10.1080/01490450590922505

Cited by 194 publications

(224 citation statements)

References 69 publications

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“…Both ammonia-oxidizing and nitrite-oxidizing bacteria were found in sponges before using specific primers (Bayer et al, 2008;Hoffmann et al, 2009), however, our data suggest that only the genus Nitrospira (which contains nitrite oxidizers) is widely distributed in these hosts. Potential sulfate reducers were also detected, for example, 97% OTUs in the genus Desulfovibrio and the family Desulfobulbaceae, confirming previous data on sulfate reduction in other sponges (Hoffmann et al, 2005). However, with few exceptions (for example, nitrifying microbes), 16S rRNA gene data can generally not be used to make inferences about metabolic capabilities of microbes.…”

Section: Resultssupporting

confidence: 78%

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: Resultssupporting

confidence: 78%

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

et al. 2011

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“…However, despite this interest, there is still little known about the nature of these symbioses. The function of sponge-specific microbes has only been determined for certain microbial groups that are responsible for, for example, photosynthesis, nitrification or sulphate reduction in sponges (Wilkinson, 1983;Hoffmann et al, 2005;Bayer et al, 2008). This study suggests that in fact many of the sponge-specific symbionts are active within their respective host sponges.…”

Section: U N C E R T L I N E a G E S P I R O C H A E T E S B A C T mentioning

confidence: 92%

“…Although our understanding of the microbial diversity in sponges is rapidly improving, much remains unknown about the activity of these microbes (Taylor et al, 2007a). Specific microbially mediated processes within sponges, such as photosynthesis, sulphate reduction, nitrogen fixation and nitrification, have been quantified and in many cases the relevant microbes have been identified (Wilkinson and Fay, 1979;Wilkinson, 1983;Diaz and Ward, 1997;Wilkinson et al, 1999;Hoffmann et al, 2005Hoffmann et al, , 2009Hallam et al, 2006;Bayer et al, 2008;Mohamed et al, 2008aMohamed et al, , 2009Steger et al, 2008). These studies, which have utilized methods such as isotope enrichments, metagenomics and functional gene analyses, have extended our knowledge of symbiont function in sponges, yet they remain focused on specific processes or particular functional groups of organisms.…”

Section: Introductionmentioning

confidence: 99%

Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons

2010

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The phylogenetic diversity of microorganisms in marine sponges is becoming increasingly well described, yet relatively little is known about the activities of these symbionts. Given the seemingly favourable environment provided to microbes by their sponge hosts, as indicated by the extraordinarily high abundance of sponge symbionts, we hypothesized that the majority of spongeassociated bacteria are active in situ. To test this hypothesis we compared, for the first time in sponges, 16S rRNA gene-vs 16S rRNA-derived bacterial community profiles to gain insights into symbiont composition and activity, respectively. Clone libraries revealed a highly diverse bacterial community in Ancorina alata, and a much lower diversity in Polymastia sp., which were identified by electron microscopy as a high-and a low-microbial abundance sponge, respectively. Substantial overlap between DNA and RNA libraries was evident at both phylum and phylotype levels, indicating in situ activity for a large fraction of sponge-associated bacteria. This active fraction included uncultivated, sponge-specific lineages within, for example, Actinobacteria, Chloroflexi and Gemmatimonadetes. This study shows the potential of RNA vs DNA comparisons based on the 16S rRNA gene to provide insights into the activity of sponge-associated microorganisms.

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“…Many of these symbiont lineages are primarily hostassociated (i.e., obligate symbionts) and represent novel microbial taxa from species level (e.g., Synechococcus spongiarum in sponges, Usher et al, 2004) to phylum level, (e.g., Poribacteria, Fieseler et al, 2004) while others exist in both freeliving and host-associated states, (i.e., facultative symbionts) though generally enriched in the invertebrate microhabitat and rare in seawater communities (Sunagawa et al, 2010). The phylogenetic diversity of symbiotic microbes is associated with a diversity of metabolic pathways in the carbon, (Wilkinson, 1983) nitrogen (Hoffmann et al, 2009) and sulfur cycles (Hoffmann et al, 2005), spurred by the utilization of host waste products (e.g., ammonia), the presence of dimethylsulfoniopropionate (DMSP, Raina et al, 2010) and physico-chemical conditions of the host microenvironment (e.g., oxygen gradients; Hoffmann et al, 2008;Kü hl et al, 2012). The structural and functional diversity of symbiotic microbial communities indicate that invertebrate hosts provide fertile microbial niches that contribute to prokaryotic biodiversity and nutrient cycling in coastal marine ecosystems.…”

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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An Anaerobic World in Sponges

Cited by 194 publications

References 69 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

Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons

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

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