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Transcriptome analyses to investigate symbiotic relationships between marine protists.

Balzano S, Corre E, Decelle J, Sierra R, Wincker P, Da Silva C, Poulain J, Pawlowski J, Not F - Front Microbiol (2015)

Bottom Line: Unigenes coding putative c-type lectin domains (CTLD) were found in the species bearing photosynthetic symbionts (A. elongata, Collozoum sp., and S. streptacantha) but not in the non-symbiotic one (A. scolymantha).More particularly, phylogenetic analyses group CTLDs from A. elongata and Collozoum sp. on a distinct branch from S. streptacantha CTLDs, which contained carbohydrate-binding motifs typically observed in other marine photosymbiosis.Our data suggest that similarly to other well-known marine photosymbiosis involving metazoans, the interactions of glycans with c-type lectins is likely involved in modulation of the host/symbiont specific recognition in Radiolaria.

View Article: PubMed Central - PubMed

Affiliation: UMR 7144, Université Pierre et Marie Curie Université Paris 06, Sorbonne Universités, Station Biologique de Roscoff Roscoff, France ; Centre National de la Recherche Scientifique, UMR 7144, Station Biologique de Roscoff Roscoff, France.

ABSTRACT
Rhizaria are an important component of oceanic plankton communities worldwide. A number of species harbor eukaryotic microalgal symbionts, which are horizontally acquired in the environment at each generation. Although these photosymbioses are determinant for Rhizaria ability to thrive in oceanic ecosystems, the mechanisms for symbiotic interactions are unclear. Using high-throughput sequencing technology (i.e., 454), we generated large Expressed Sequence Tag (EST) datasets from four uncultured Rhizaria, an acantharian (Amphilonche elongata), two polycystines (Collozoum sp. and Spongosphaera streptacantha), and one phaeodarian (Aulacantha scolymantha). We assessed the main genetic features of the host/symbionts consortium (i.e., the holobiont) transcriptomes and found rRNA sequences affiliated to a wide range of bacteria and protists in all samples, suggesting that diverse microbial communities are associated with the holobionts. A particular focus was then carried out to search for genes potentially involved in symbiotic processes such as the presence of c-type lectins-coding genes, which are proteins that play a role in cell recognition among eukaryotes. Unigenes coding putative c-type lectin domains (CTLD) were found in the species bearing photosynthetic symbionts (A. elongata, Collozoum sp., and S. streptacantha) but not in the non-symbiotic one (A. scolymantha). More particularly, phylogenetic analyses group CTLDs from A. elongata and Collozoum sp. on a distinct branch from S. streptacantha CTLDs, which contained carbohydrate-binding motifs typically observed in other marine photosymbiosis. Our data suggest that similarly to other well-known marine photosymbiosis involving metazoans, the interactions of glycans with c-type lectins is likely involved in modulation of the host/symbiont specific recognition in Radiolaria.

No MeSH data available.


Unrooted tree describing the relatedness of c-type lectins of radiolarians in the present study, other protists and Metazoa harboring photosynthetic symbionts. The consensus tree resulting from phyml analyses of 246 unambiguously aligned positions and 43 protein sequences. Topological support of >50% obtained from aLRT approach are shown in each branch label. Sequences corresponding to this study are in bold whereas sequences from other protists are underlined.
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Figure 5: Unrooted tree describing the relatedness of c-type lectins of radiolarians in the present study, other protists and Metazoa harboring photosynthetic symbionts. The consensus tree resulting from phyml analyses of 246 unambiguously aligned positions and 43 protein sequences. Topological support of >50% obtained from aLRT approach are shown in each branch label. Sequences corresponding to this study are in bold whereas sequences from other protists are underlined.

Mentions: The alignment of putative CTLD from our samples with CTLD from other marine holobionts or putative CTLD from other protists consisted of four highly conserved cysteine residues as well as four motifs (Supplementary Figure S3). The WIGL-like motif which is crucial in the identification of CTLD (Zelensky and Gready, 2005) was found to vary for our holobionts, being WIGV for A. elongata, WLGF for Collozoum sp. and WIGL, WLGL, and WVGL for the different CTLD from S. streptacantha (Supplementary Figure S3). The glucose/mannose binding motif EPN (Zelensky and Gready, 2005) was found only in S. streptacantha whereas such motif was replaced by DSS in A. elongata and by WSD in Collozoum sp. Similarly the galactose binding motif LND (Zelensky and Gready, 2005) was only found in S. streptacantha CTLD. In A. elongata the LND motif was replaced by VND whereas we could not find an equivalent motif in Collozoum sp. (Supplementary Figure S3). The resulting phylogenetic tree reconstruction is shown as an unrooted tree (Figure 5), and includes putative CTLD extracted from the holobionts as well as a range of reference sequences from Metazoa and protists. Five well-supported c-lectin groups can be identified from the phylogenetic tree. Group A strictly includes coral CTLDs that could be related to several ungrouped sequences from alveolates. In group B we find the protist CTDLs of A. elongata and A. anophagefferens more closely related to other metazoans CTDLs than to other acantharians and apicomplexan protists, respectively. Group C is almost exclusively composed by S. streptacantha except for a sequence from N. vectensis. Group D is an assembly of various metazoan CTDLs with the presence of the protist G. theta. Finally, group E contains the CTDLs of Collozoum sp. and the lectins of the Salpingoeca rosetta and Cyprinus carpio.


Transcriptome analyses to investigate symbiotic relationships between marine protists.

Balzano S, Corre E, Decelle J, Sierra R, Wincker P, Da Silva C, Poulain J, Pawlowski J, Not F - Front Microbiol (2015)

Unrooted tree describing the relatedness of c-type lectins of radiolarians in the present study, other protists and Metazoa harboring photosynthetic symbionts. The consensus tree resulting from phyml analyses of 246 unambiguously aligned positions and 43 protein sequences. Topological support of >50% obtained from aLRT approach are shown in each branch label. Sequences corresponding to this study are in bold whereas sequences from other protists are underlined.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4362344&req=5

Figure 5: Unrooted tree describing the relatedness of c-type lectins of radiolarians in the present study, other protists and Metazoa harboring photosynthetic symbionts. The consensus tree resulting from phyml analyses of 246 unambiguously aligned positions and 43 protein sequences. Topological support of >50% obtained from aLRT approach are shown in each branch label. Sequences corresponding to this study are in bold whereas sequences from other protists are underlined.
Mentions: The alignment of putative CTLD from our samples with CTLD from other marine holobionts or putative CTLD from other protists consisted of four highly conserved cysteine residues as well as four motifs (Supplementary Figure S3). The WIGL-like motif which is crucial in the identification of CTLD (Zelensky and Gready, 2005) was found to vary for our holobionts, being WIGV for A. elongata, WLGF for Collozoum sp. and WIGL, WLGL, and WVGL for the different CTLD from S. streptacantha (Supplementary Figure S3). The glucose/mannose binding motif EPN (Zelensky and Gready, 2005) was found only in S. streptacantha whereas such motif was replaced by DSS in A. elongata and by WSD in Collozoum sp. Similarly the galactose binding motif LND (Zelensky and Gready, 2005) was only found in S. streptacantha CTLD. In A. elongata the LND motif was replaced by VND whereas we could not find an equivalent motif in Collozoum sp. (Supplementary Figure S3). The resulting phylogenetic tree reconstruction is shown as an unrooted tree (Figure 5), and includes putative CTLD extracted from the holobionts as well as a range of reference sequences from Metazoa and protists. Five well-supported c-lectin groups can be identified from the phylogenetic tree. Group A strictly includes coral CTLDs that could be related to several ungrouped sequences from alveolates. In group B we find the protist CTDLs of A. elongata and A. anophagefferens more closely related to other metazoans CTDLs than to other acantharians and apicomplexan protists, respectively. Group C is almost exclusively composed by S. streptacantha except for a sequence from N. vectensis. Group D is an assembly of various metazoan CTDLs with the presence of the protist G. theta. Finally, group E contains the CTDLs of Collozoum sp. and the lectins of the Salpingoeca rosetta and Cyprinus carpio.

Bottom Line: Unigenes coding putative c-type lectin domains (CTLD) were found in the species bearing photosynthetic symbionts (A. elongata, Collozoum sp., and S. streptacantha) but not in the non-symbiotic one (A. scolymantha).More particularly, phylogenetic analyses group CTLDs from A. elongata and Collozoum sp. on a distinct branch from S. streptacantha CTLDs, which contained carbohydrate-binding motifs typically observed in other marine photosymbiosis.Our data suggest that similarly to other well-known marine photosymbiosis involving metazoans, the interactions of glycans with c-type lectins is likely involved in modulation of the host/symbiont specific recognition in Radiolaria.

View Article: PubMed Central - PubMed

Affiliation: UMR 7144, Université Pierre et Marie Curie Université Paris 06, Sorbonne Universités, Station Biologique de Roscoff Roscoff, France ; Centre National de la Recherche Scientifique, UMR 7144, Station Biologique de Roscoff Roscoff, France.

ABSTRACT
Rhizaria are an important component of oceanic plankton communities worldwide. A number of species harbor eukaryotic microalgal symbionts, which are horizontally acquired in the environment at each generation. Although these photosymbioses are determinant for Rhizaria ability to thrive in oceanic ecosystems, the mechanisms for symbiotic interactions are unclear. Using high-throughput sequencing technology (i.e., 454), we generated large Expressed Sequence Tag (EST) datasets from four uncultured Rhizaria, an acantharian (Amphilonche elongata), two polycystines (Collozoum sp. and Spongosphaera streptacantha), and one phaeodarian (Aulacantha scolymantha). We assessed the main genetic features of the host/symbionts consortium (i.e., the holobiont) transcriptomes and found rRNA sequences affiliated to a wide range of bacteria and protists in all samples, suggesting that diverse microbial communities are associated with the holobionts. A particular focus was then carried out to search for genes potentially involved in symbiotic processes such as the presence of c-type lectins-coding genes, which are proteins that play a role in cell recognition among eukaryotes. Unigenes coding putative c-type lectin domains (CTLD) were found in the species bearing photosynthetic symbionts (A. elongata, Collozoum sp., and S. streptacantha) but not in the non-symbiotic one (A. scolymantha). More particularly, phylogenetic analyses group CTLDs from A. elongata and Collozoum sp. on a distinct branch from S. streptacantha CTLDs, which contained carbohydrate-binding motifs typically observed in other marine photosymbiosis. Our data suggest that similarly to other well-known marine photosymbiosis involving metazoans, the interactions of glycans with c-type lectins is likely involved in modulation of the host/symbiont specific recognition in Radiolaria.

No MeSH data available.