Dataset Information

Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges.

ABSTRACT: Certain species of marine sponges in the order Dictyoceratida harbor large populations of the cyanobacterial symbiont Oscillatoria spongeliae in the mesohyl (interior) of the sponge. We show that in four of these sponge species (Lamellodysidea herbacea, Lamellodysidea chlorea, Lendenfeldia chondrodes, and Phyllospongia papyracea) from Palau there is a consistent community of alpha-proteobacteria in addition to O. spongeliae that fall within the Rhodobacter group based on 16S rRNA gene analysis. Some of the alpha-proteobacteria in Lendenfeldia chondrodes and P. papyracea but not in the Lamellodysidea spp. contained site-specific insertions in the 16S rRNA gene. Reverse transcription-PCR experiments demonstrated that the largest insertion found in this study (63 bp) is present in the mature rRNA. Lendenfeldia chondrodes was the only sponge found to have another cyanobacterium in the tissue, a Synechocystis sp. We found that the Synechocystis sp. was present in both the pinacoderm (surface epithelial tissue) and mesohyl, in contrast to O. spongeliae, which was only found in the mesohyl through the use of specific fluorescence in situ hybridization experiments. Of the four sponge species, only P. papyracea was found to contain a significant number of gamma-proteobacteria. These results demonstrate that O. spongeliae-dominated bacterial communities in different sponge species can vary considerably and increase our understanding of the bacterial communities found in marine invertebrates.

SUBMITTER: Ridley CP

PROVIDER: S-EPMC1287642 | biostudies-literature | 2005 Nov

REPOSITORIES: biostudies-literature

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Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges.

Ridley Christian P CP John Faulkner D D Haygood Margo G MG

Applied and environmental microbiology 20051101 11

Certain species of marine sponges in the order Dictyoceratida harbor large populations of the cyanobacterial symbiont Oscillatoria spongeliae in the mesohyl (interior) of the sponge. We show that in four of these sponge species (Lamellodysidea herbacea, Lamellodysidea chlorea, Lendenfeldia chondrodes, and Phyllospongia papyracea) from Palau there is a consistent community of alpha-proteobacteria in addition to O. spongeliae that fall within the Rhodobacter group based on 16S rRNA gene analysis. ...[more]

PMID: 16269779

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Project description:Marine sponges host dense, diverse, and species-specific microbial communities around the globe; however, most of the current knowledge is restricted to species from tropical and temperate waters. Only recently, some studies have assessed the microbiome of a few Antarctic sponges; however, contrary to low mid-latitude sponges, the knowledge about temporal (stability) patterns in the bacterial communities of Antarctic sponges is absent. Here, we studied the temporal patterns of bacterial communities in the Antarctic sponges Mycale (Oxymycale) acerata, Isodictya sp., Hymeniacidon torquata, and Tedania (Tedaniopsis) wellsae that were tagged in situ and monitored during three austral summers over a 24-month period. By using amplicon sequencing of the bacterial 16S rRNA gene we found that the microbiome differed between species. In general, bacterial communities were dominated by gammaproteobacterial OTUs; however, M. acerata showed the most distinct pattern, being dominated by a single betaproteobacterial OTU. The analysis at OTU level (defined at 97% sequence similarity) showed a highly stable bacterial community through time, despite the abnormal seawater temperatures (reaching 3°C) and rates of temperature increase of 0.15°C day-1 recorded in austral summer 2017. Sponges were characterized by a small core bacterial community that accounted for a high percentage of the abundance. Overall, no consistent changes in core OTU abundance were recorded for all studied species, confirming a high temporal stability of the microbiome. In addition, predicted functional pathway profiles showed that the most abundant pathways among all sponges belonged mostly to metabolism pathway groups (e.g., amino acid, carbohydrate, energy, and nucleotide). The predicted functional pathway patterns differed among the four sponge species. However, no clear temporal differences were detected supporting what was found in terms of the relatively stable composition of the bacterial communities.

Project description:Recent studies have unravelled the diversity of sponge-associated bacteria that may play essential roles in sponge health and metabolism. Nevertheless, our understanding of this microbiota remains limited to a few host species found in restricted geographical localities, and the extent to which the sponge host determines the composition of its own microbiome remains a matter of debate. We address bacterial abundance and diversity of two temperate marine sponges belonging to the Irciniidae family--Sarcotragus spinosulus and Ircinia variabilis--in the Northeast Atlantic. Epifluorescence microscopy revealed that S. spinosulus hosted significantly more prokaryotic cells than I. variabilis and that prokaryotic abundance in both species was about 4 orders of magnitude higher than in seawater. Polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) profiles of S. spinosulus and I. variabilis differed markedly from each other--with higher number of ribotypes observed in S. spinosulus--and from those of seawater. Four PCR-DGGE bands, two specific to S. spinosulus, one specific to I. variabilis, and one present in both sponge species, affiliated with an uncultured sponge-specific phylogenetic cluster in the order Acidimicrobiales (Actinobacteria). Two PCR-DGGE bands present exclusively in S. spinosulus fingerprints affiliated with one sponge-specific phylogenetic cluster in the phylum Chloroflexi and with sponge-derived sequences in the order Chromatiales (Gammaproteobacteria), respectively. One Alphaproteobacteria band specific to S. spinosulus was placed in an uncultured sponge-specific phylogenetic cluster with a close relationship to the genus Rhodovulum. Our results confirm the hypothesized host-specific composition of bacterial communities between phylogenetically and spatially close sponge species in the Irciniidae family, with S. spinosulus displaying higher bacterial community diversity and distinctiveness than I. variabilis. These findings suggest a pivotal host-driven effect on the shape of the marine sponge microbiome, bearing implications to our current understanding of the distribution of microbial genetic resources in the marine realm.

Dataset Information

Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges.

Publications

Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges.

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