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The genome of Cardinium cBtQ1 provides insights into genome reduction, symbiont motility, and its settlement in Bemisia tabaci.

Santos-Garcia D, Rollat-Farnier PA, Beitia F, Zchori-Fein E, Vavre F, Mouton L, Moya A, Latorre A, Silva FJ - Genome Biol Evol (2014)

Bottom Line: This was followed in Cardinium by smaller losses, associated with settlement in arthropods.The genome also contains a chromosomal duplication and a multicopy plasmid, which harbors several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity.As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.

View Article: PubMed Central - PubMed

Affiliation: Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Spain.

ABSTRACT
Many insects harbor inherited bacterial endosymbionts. Although some of them are not strictly essential and are considered facultative, they can be a key to host survival under specific environmental conditions, such as parasitoid attacks, climate changes, or insecticide pressures. The whitefly Bemisia tabaci is at the top of the list of organisms inflicting agricultural damage and outbreaks, and changes in its distribution may be associated to global warming. In this work, we have sequenced and analyzed the genome of Cardinium cBtQ1, a facultative bacterial endosymbiont of B. tabaci and propose that it belongs to a new taxonomic family, which also includes Candidatus Amoebophilus asiaticus and Cardinium cEper1, endosymbionts of amoeba and wasps, respectively. Reconstruction of their last common ancestors' gene contents revealed an initial massive gene loss from the free-living ancestor. This was followed in Cardinium by smaller losses, associated with settlement in arthropods. Some of these losses, affecting cofactor and amino acid biosynthetic encoding genes, took place in Cardinium cBtQ1 after its divergence from the Cardinium cEper1 lineage and were related to its settlement in the whitefly and its endosymbionts. Furthermore, the Cardinium cBtQ1 genome displays a large proportion of transposable elements, which have recently inactivated genes and produced chromosomal rearrangements. The genome also contains a chromosomal duplication and a multicopy plasmid, which harbors several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity. As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.

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Bayesian phylogenetic tree for Cardinium from different arthropods species. Phylogenetic relationships among different Cardinium supergroups are shown. The Cardinium group A strains (green vertical arrow) seem the most widespread group, infecting different arthropod orders including the subclass Neoptera (which includes whiteflies). Groups C (blue arrow) and D (red arrow) showed a more restricted pattern of hosts. Group C is restricted to the order Diptera, whereas Group D is detected on subclass Copepoda. On the 16S rRNA phylogeny, Cardinium endosymbionts of Bemisia tabaci are grouped in two different strains, the C1 (red dot) that belongs to the Mediterranean species (Q biotype) and the CI1 (blue dot) that belongs to the Asia II species. The GTR+I+G model was selected for 16S rRNA and the LG+G model for gyrB. Cardinium strain cBtQ1, endosymbiont of B. tabaci QHC-VLC, is displayed in bold type. In both cases, Amoebophilus asiaticus was used as the outgroup but was excluded from the figure for plotting reasons. Triangles represent collapsed branches of the same species or genus with the number of collapsed sequences between square brackets. Arthropoda taxonomic names and their respective colors are shown in the upper box. Accession numbers for noncollapsed branches are displayed. Only Bayesian posterior values above 0.5 are displayed (blue), and branches under this score were condensed. Bootstrap values from maximum likelihood phylogenetic reconstruction above 50% are also displayed (black).
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evu077-F2: Bayesian phylogenetic tree for Cardinium from different arthropods species. Phylogenetic relationships among different Cardinium supergroups are shown. The Cardinium group A strains (green vertical arrow) seem the most widespread group, infecting different arthropod orders including the subclass Neoptera (which includes whiteflies). Groups C (blue arrow) and D (red arrow) showed a more restricted pattern of hosts. Group C is restricted to the order Diptera, whereas Group D is detected on subclass Copepoda. On the 16S rRNA phylogeny, Cardinium endosymbionts of Bemisia tabaci are grouped in two different strains, the C1 (red dot) that belongs to the Mediterranean species (Q biotype) and the CI1 (blue dot) that belongs to the Asia II species. The GTR+I+G model was selected for 16S rRNA and the LG+G model for gyrB. Cardinium strain cBtQ1, endosymbiont of B. tabaci QHC-VLC, is displayed in bold type. In both cases, Amoebophilus asiaticus was used as the outgroup but was excluded from the figure for plotting reasons. Triangles represent collapsed branches of the same species or genus with the number of collapsed sequences between square brackets. Arthropoda taxonomic names and their respective colors are shown in the upper box. Accession numbers for noncollapsed branches are displayed. Only Bayesian posterior values above 0.5 are displayed (blue), and branches under this score were condensed. Bootstrap values from maximum likelihood phylogenetic reconstruction above 50% are also displayed (black).

Mentions: To establish the relationship of Cardinium cBtQ1 to other Cardinium endosymbionts based on 16S rRNA sequences, a covariance model aligner was employed. The 16S rRNA alignment was used to infer a phylogeny, showing that almost all Cardinium endosymbionts of B. tabaci (including cBtQ1) were present in a clade with other Cardinium endosymbionts of several Encarsia species (99.14% identity with the whole 16SrRNA of Cardinium from E. pergandiella) (fig. 2, left). A phylogeny with gyrB was also performed, which corroborated the close phylogenetic relation with Cardinium from Encarsia spp. and also showed that Cardinium cBtQ1 was embedded in the Cardinium–Encarsia clade (fig. 2, right). Because 16S rRNA sequences of Cardinium cBtQ1 and the species type C. hertigii (symbiont of E. hispida) show only 1.2% of differences, we propose that Cardinium cBtQ1 is a strain of the latter, in agreement with previous reports (Zchori-Fein and Perlman 2004). The Bemisia/Encarsia clade belongs to the Cardinium group A, which is well differentiated from the other two groups included in the analysis: Group C, which is specific to the genus Culicoides (Nakamura et al. 2009) and group D, which is present in some Copepoda spp. (Edlund et al. 2012) (fig. 2).Fig. 2.—


The genome of Cardinium cBtQ1 provides insights into genome reduction, symbiont motility, and its settlement in Bemisia tabaci.

Santos-Garcia D, Rollat-Farnier PA, Beitia F, Zchori-Fein E, Vavre F, Mouton L, Moya A, Latorre A, Silva FJ - Genome Biol Evol (2014)

Bayesian phylogenetic tree for Cardinium from different arthropods species. Phylogenetic relationships among different Cardinium supergroups are shown. The Cardinium group A strains (green vertical arrow) seem the most widespread group, infecting different arthropod orders including the subclass Neoptera (which includes whiteflies). Groups C (blue arrow) and D (red arrow) showed a more restricted pattern of hosts. Group C is restricted to the order Diptera, whereas Group D is detected on subclass Copepoda. On the 16S rRNA phylogeny, Cardinium endosymbionts of Bemisia tabaci are grouped in two different strains, the C1 (red dot) that belongs to the Mediterranean species (Q biotype) and the CI1 (blue dot) that belongs to the Asia II species. The GTR+I+G model was selected for 16S rRNA and the LG+G model for gyrB. Cardinium strain cBtQ1, endosymbiont of B. tabaci QHC-VLC, is displayed in bold type. In both cases, Amoebophilus asiaticus was used as the outgroup but was excluded from the figure for plotting reasons. Triangles represent collapsed branches of the same species or genus with the number of collapsed sequences between square brackets. Arthropoda taxonomic names and their respective colors are shown in the upper box. Accession numbers for noncollapsed branches are displayed. Only Bayesian posterior values above 0.5 are displayed (blue), and branches under this score were condensed. Bootstrap values from maximum likelihood phylogenetic reconstruction above 50% are also displayed (black).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4007549&req=5

evu077-F2: Bayesian phylogenetic tree for Cardinium from different arthropods species. Phylogenetic relationships among different Cardinium supergroups are shown. The Cardinium group A strains (green vertical arrow) seem the most widespread group, infecting different arthropod orders including the subclass Neoptera (which includes whiteflies). Groups C (blue arrow) and D (red arrow) showed a more restricted pattern of hosts. Group C is restricted to the order Diptera, whereas Group D is detected on subclass Copepoda. On the 16S rRNA phylogeny, Cardinium endosymbionts of Bemisia tabaci are grouped in two different strains, the C1 (red dot) that belongs to the Mediterranean species (Q biotype) and the CI1 (blue dot) that belongs to the Asia II species. The GTR+I+G model was selected for 16S rRNA and the LG+G model for gyrB. Cardinium strain cBtQ1, endosymbiont of B. tabaci QHC-VLC, is displayed in bold type. In both cases, Amoebophilus asiaticus was used as the outgroup but was excluded from the figure for plotting reasons. Triangles represent collapsed branches of the same species or genus with the number of collapsed sequences between square brackets. Arthropoda taxonomic names and their respective colors are shown in the upper box. Accession numbers for noncollapsed branches are displayed. Only Bayesian posterior values above 0.5 are displayed (blue), and branches under this score were condensed. Bootstrap values from maximum likelihood phylogenetic reconstruction above 50% are also displayed (black).
Mentions: To establish the relationship of Cardinium cBtQ1 to other Cardinium endosymbionts based on 16S rRNA sequences, a covariance model aligner was employed. The 16S rRNA alignment was used to infer a phylogeny, showing that almost all Cardinium endosymbionts of B. tabaci (including cBtQ1) were present in a clade with other Cardinium endosymbionts of several Encarsia species (99.14% identity with the whole 16SrRNA of Cardinium from E. pergandiella) (fig. 2, left). A phylogeny with gyrB was also performed, which corroborated the close phylogenetic relation with Cardinium from Encarsia spp. and also showed that Cardinium cBtQ1 was embedded in the Cardinium–Encarsia clade (fig. 2, right). Because 16S rRNA sequences of Cardinium cBtQ1 and the species type C. hertigii (symbiont of E. hispida) show only 1.2% of differences, we propose that Cardinium cBtQ1 is a strain of the latter, in agreement with previous reports (Zchori-Fein and Perlman 2004). The Bemisia/Encarsia clade belongs to the Cardinium group A, which is well differentiated from the other two groups included in the analysis: Group C, which is specific to the genus Culicoides (Nakamura et al. 2009) and group D, which is present in some Copepoda spp. (Edlund et al. 2012) (fig. 2).Fig. 2.—

Bottom Line: This was followed in Cardinium by smaller losses, associated with settlement in arthropods.The genome also contains a chromosomal duplication and a multicopy plasmid, which harbors several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity.As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.

View Article: PubMed Central - PubMed

Affiliation: Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Spain.

ABSTRACT
Many insects harbor inherited bacterial endosymbionts. Although some of them are not strictly essential and are considered facultative, they can be a key to host survival under specific environmental conditions, such as parasitoid attacks, climate changes, or insecticide pressures. The whitefly Bemisia tabaci is at the top of the list of organisms inflicting agricultural damage and outbreaks, and changes in its distribution may be associated to global warming. In this work, we have sequenced and analyzed the genome of Cardinium cBtQ1, a facultative bacterial endosymbiont of B. tabaci and propose that it belongs to a new taxonomic family, which also includes Candidatus Amoebophilus asiaticus and Cardinium cEper1, endosymbionts of amoeba and wasps, respectively. Reconstruction of their last common ancestors' gene contents revealed an initial massive gene loss from the free-living ancestor. This was followed in Cardinium by smaller losses, associated with settlement in arthropods. Some of these losses, affecting cofactor and amino acid biosynthetic encoding genes, took place in Cardinium cBtQ1 after its divergence from the Cardinium cEper1 lineage and were related to its settlement in the whitefly and its endosymbionts. Furthermore, the Cardinium cBtQ1 genome displays a large proportion of transposable elements, which have recently inactivated genes and produced chromosomal rearrangements. The genome also contains a chromosomal duplication and a multicopy plasmid, which harbors several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity. As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.

Show MeSH
Related in: MedlinePlus