Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission

Summary Marine sponges host diverse communities of microorganisms that are often vertically transmitted from mother to oocyte or embryo. Horizontal transmission has often been proposed to co‐occur in marine sponges, but the mechanism is poorly understood. To assess the impact of the mode of transmis...

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Published inEnvironmental microbiology Vol. 17; no. 10; pp. 3807 - 3821
Main Authors Sipkema, Detmer, de Caralt, Sònia, Morillo, Jose A., Al-Soud, Waleed Abu, Sørensen, Søren J., Smidt, Hauke, Uriz, María J.
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.10.2015
Wiley Subscription Services, Inc
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Summary:Summary Marine sponges host diverse communities of microorganisms that are often vertically transmitted from mother to oocyte or embryo. Horizontal transmission has often been proposed to co‐occur in marine sponges, but the mechanism is poorly understood. To assess the impact of the mode of transmission on the microbial assemblages of sponges, we analysed the microbiota in sympatric sponges that have previously been reported to acquire bacteria via either vertical (Corticium candelabrum and Crambe crambe) or horizontal transmission (Petrosia ficiformis). The comparative study was performed by polymerase chain reaction‐denaturing gradient gel electrophoresis and pyrosequencing of barcoded PCR‐amplified 16S rRNA gene fragments. We found that P. ficiformis and C. candelabrum each harbour their own species‐specific bacteria, but they are similar to other high‐microbial‐abundance sponges, while the low‐microbial‐abundance sponge C. crambe hosts microbiota of a very different phylogenetic signature. In addition, nearly 50% of the reads obtained from P. ficiformis were most closely related to bacteria that were previously reported to be vertically transmitted in other sponges and comprised vertical–horizontal transmission phylogenetic clusters (VHT clusters). Therefore, our results provide evidence for the hypothesis that similar sponge‐associated bacteria can be acquired via both vertical and horizontal transmission.
Bibliography:Fig. S1. Denaturing gradient gel electrophoresis profile of PCR-amplified partial 16S rRNA gene fragments from five Petrosia ficiformis (Pf) specimens, four C. candelabrum (co) specimens, five C. crambe (cr) specimens and four seawater samples (sw). The P. ficiformis samples were run on a different gel. They were aligned with the other samples by using reference samples. Numbers placed left of DGGE bands indicate DGGE bands that were successfully excised and amplified. Band number of Pf are in black only to improve their visibility. The observed bacterial richness of especially C. candelabrum and C. crambe is lower than suggested by the DGGE profile as a number of artifactual double DGGE bands were identified by sequencing of excised and PCR re-amplified bands (e.g. Co22-Co74, Co87-Co88, Co50-Co8, Co116-Co13 and Cr50-Cr65). Fig. S2. Richness of sponge-associated microbial communities. Rarefaction curves are based on OTUs at a 97% sequence similarity threshold, while singletons (OTUs with one read in the total dataset) were excluded. Fig. S3. Bayesian phylogram based on 16S rRNA gene sequences of OTUs representing more than 1% of the reads in P. ficiformis and C. candelabrum and their nearest neighbours. Operational taxonomic units that include reads from C. crambe and seawater are only included if they also represent more than 1% of the reads in P. ficiformis or C. candelabrum. Operational taxonomic units from this study are in bold and 'Pf' indicates that the OTU contains reads derived from P. ficiformis individuals, 'Co' from C. candelabrum, 'Cr' from C. crambe and 'sw' from seawater. Numbers in parenthesis after the sample type indication refer to the percentage of reads that are included in the corresponding OTU per sample [9381 Pf(0/0.9) means that 0% of the reads of Pf1 and 0.9% of the reads of Pf3 are included in OTU9381]. Yellow boxes indicate vertical-horizontal transmission (VHT) clusters that are supported by posterior probability (PP) values > 95%. These clusters comprise OTUs from both Pf adults and sequences derived from other sponge's larvae or embryos. Grey boxes indicate potential VHT clusters that have PP values < 95%. Numbers above or below the branches correspond to PP values of the Bayesian analysis. Nodes with PP values of < 50 are not indicated. Fig. S4. Heat map of the OTUs that represented more than 1% of the reads in at least one of the P. ficiformis, C. candelabrum, C. crambe or seawater samples. Table S1. Average similarity (%) of DGGE band patterns within groups (Petrosia ficiformis = Pf, Corticium candelabrum = Co, Crambe crambe = Cr, seawater = sw) (in grey) and between groups (in white) based on simper analysis. Table S2. blastn result of DGGE band sequences indicated in Fig. S1 against the NCBI nr/nt nucleotide collection (performed at 3 May 2013). Denaturing gradient gel electrophoresis bands in bold are closely related to OTUs present in VHT clusters (number VHT cluster indicated in parentheses). Species names always refer to sponges and corals. The DGGE band sequences were compared with a database containing reference sequences from the OTUs obtained from pyrosequencing using a locally installed version of blast2-2-4 at a minimal similarity of 90%. The per cent of identity compared with pyrosequencing OTUs and nearest neighbours is in parentheses behind the OTU/neighbour identifier. Occasional low similarities are caused by low quality of sequenced DGGE bands rather than novelty of the DGGE sequence. Table S3. Per cent similarity matrix of all sequences that are present in VHT clusters (see. Fig. 3A-D). Vertical-horizontal transmission clusters are depicted in yellow and similarity of the P. ficiformis (Pf) OTUs with other members of the cluster is depicted in green. When similarity of Pf OTUs within the cluster is lower than 97%, they are indicated in light green. When other similarities within VHT clusters are below 97% they are indicated in orange. Table S4. Species diversity, richness estimates and coverage obtained at genetic distances of 3%. a Singletons have been excluded for counting the number of observed OTUs. b The coverage of richness was estimated by dividing the average observed species by average expected species multiplied by 100.
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ark:/67375/WNG-V2PHMFKK-K
Spanish Government - No. JCI-2008-2342
ArticleID:EMI12827
European Union - No. 222625; No. MOIF-CT-2005-022164
Dutch Government - No. 93519009
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
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ISSN:1462-2912
1462-2920
1462-2920
DOI:10.1111/1462-2920.12827