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The chloroplast genomes of Bryopsis plumosa and Tydemania expeditiones (Bryopsidales, Chlorophyta): compact genomes and genes of bacterial origin.

Leliaert F, Lopez-Bautista JM - BMC Genomics (2015)

Bottom Line: The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region.Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.The cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA. frederik.leliaert@ugent.be.

ABSTRACT

Background: Species of Bryopsidales form ecologically important components of seaweed communities worldwide. These siphonous macroalgae are composed of a single giant tubular cell containing millions of nuclei and chloroplasts, and harbor diverse bacterial communities. Little is known about the diversity of chloroplast genomes (cpDNAs) in this group, and about the possible consequences of intracellular bacteria on genome composition of the host. We present the complete cpDNAs of Bryopsis plumosa and Tydemania expeditiones, as well as a re-annotated cpDNA of B. hypnoides, which was shown to contain a higher number of genes than originally published. Chloroplast genomic data were also used to evaluate phylogenetic hypotheses in the Chlorophyta, such as monophyly of the Ulvophyceae (the class in which the order Bryopsidales is currently classified).

Results: Both DNAs are circular and lack a large inverted repeat. The cpDNA of B. plumosa is 106,859 bp long and contains 115 unique genes. A 13 kb region was identified with several freestanding open reading frames (ORFs) of putative bacterial origin, including a large ORF (>8 kb) closely related to bacterial rhs-family genes. The cpDNA of T. expeditiones is 105,200 bp long and contains 125 unique genes. As in B. plumosa, several regions were identified with ORFs of possible bacterial origin, including genes involved in mobile functions (transposases, integrases, phage/plasmid DNA primases), and ORFs showing close similarity with bacterial DNA methyltransferases. The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region. Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.

Conclusions: The cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta. The presence of bacterial genes, including genes typically found in mobile elements, suggest that these have been acquired through horizontal gene transfer, which may have been facilitated by the occurrence of obligate intracellular bacteria in these siphonous algae.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic trees of Chlorophyta inferred from a 50-gene dataset. (A) Bayesian majority rule tree showing all compatible partitions, inference from the protein alignment of 50 concatenated chloroplast genes (9,300 amino acid positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values of the protein analyses (above branches), and the nucleotide analyses (below branches); values <0.9 and 50, respectively, are not shown; asterisks indicated full support in both the Bayesian and ML analyses. (B) Bayesian tree inference from the nucleotide alignment (first two codon positions) of 50 concatenated chloroplast genes (18,600 nucleotide positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values, and asterisks indicate full support in both analyses.
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Fig9: Phylogenetic trees of Chlorophyta inferred from a 50-gene dataset. (A) Bayesian majority rule tree showing all compatible partitions, inference from the protein alignment of 50 concatenated chloroplast genes (9,300 amino acid positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values of the protein analyses (above branches), and the nucleotide analyses (below branches); values <0.9 and 50, respectively, are not shown; asterisks indicated full support in both the Bayesian and ML analyses. (B) Bayesian tree inference from the nucleotide alignment (first two codon positions) of 50 concatenated chloroplast genes (18,600 nucleotide positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values, and asterisks indicate full support in both analyses.

Mentions: The phylogenetic trees resulting from the analyses of the 50-gene dataset are summarized in Figure 9. The 50-gene dataset differs from the 79-dataset mainly in the inclusion of species of Trentepohliales and Dasycladales (both orders of Ulvophyceae) and Tetraselmis (Chlorodendrophyceae). Overall, the 50-gene phylogenies recovered the same main clades as the 79-gene phylogenies, in addition to two extra clades of Ulvophyceae (Trentepohliales and Dasycladales), and Tetraselmis. Similar to the 79-gene phylogenies, the relationships among the main clades of core Chlorophyta (including the different clades of Ulvophyceae) received little statistical support, and therefore the monophyly of the Ulvophyceae cannot be confirmed nor rejected by our data. The phylogenies inferred from the nucleotide alignment (Figure 9B) recovered the same main clades as the protein analyses, but the topology and branch support differs in several aspects, including a well-supported Trentepohliales + Dasycladales clade, and a different phylogenetic position of Tetraselmis.Figure 9


The chloroplast genomes of Bryopsis plumosa and Tydemania expeditiones (Bryopsidales, Chlorophyta): compact genomes and genes of bacterial origin.

Leliaert F, Lopez-Bautista JM - BMC Genomics (2015)

Phylogenetic trees of Chlorophyta inferred from a 50-gene dataset. (A) Bayesian majority rule tree showing all compatible partitions, inference from the protein alignment of 50 concatenated chloroplast genes (9,300 amino acid positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values of the protein analyses (above branches), and the nucleotide analyses (below branches); values <0.9 and 50, respectively, are not shown; asterisks indicated full support in both the Bayesian and ML analyses. (B) Bayesian tree inference from the nucleotide alignment (first two codon positions) of 50 concatenated chloroplast genes (18,600 nucleotide positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values, and asterisks indicate full support in both analyses.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4487195&req=5

Fig9: Phylogenetic trees of Chlorophyta inferred from a 50-gene dataset. (A) Bayesian majority rule tree showing all compatible partitions, inference from the protein alignment of 50 concatenated chloroplast genes (9,300 amino acid positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values of the protein analyses (above branches), and the nucleotide analyses (below branches); values <0.9 and 50, respectively, are not shown; asterisks indicated full support in both the Bayesian and ML analyses. (B) Bayesian tree inference from the nucleotide alignment (first two codon positions) of 50 concatenated chloroplast genes (18,600 nucleotide positions and 51 terminal taxa). Node support is given as Bayesian posterior probabilities and maximum-likelihood (ML) bootstrap values, and asterisks indicate full support in both analyses.
Mentions: The phylogenetic trees resulting from the analyses of the 50-gene dataset are summarized in Figure 9. The 50-gene dataset differs from the 79-dataset mainly in the inclusion of species of Trentepohliales and Dasycladales (both orders of Ulvophyceae) and Tetraselmis (Chlorodendrophyceae). Overall, the 50-gene phylogenies recovered the same main clades as the 79-gene phylogenies, in addition to two extra clades of Ulvophyceae (Trentepohliales and Dasycladales), and Tetraselmis. Similar to the 79-gene phylogenies, the relationships among the main clades of core Chlorophyta (including the different clades of Ulvophyceae) received little statistical support, and therefore the monophyly of the Ulvophyceae cannot be confirmed nor rejected by our data. The phylogenies inferred from the nucleotide alignment (Figure 9B) recovered the same main clades as the protein analyses, but the topology and branch support differs in several aspects, including a well-supported Trentepohliales + Dasycladales clade, and a different phylogenetic position of Tetraselmis.Figure 9

Bottom Line: The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region.Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.The cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA. frederik.leliaert@ugent.be.

ABSTRACT

Background: Species of Bryopsidales form ecologically important components of seaweed communities worldwide. These siphonous macroalgae are composed of a single giant tubular cell containing millions of nuclei and chloroplasts, and harbor diverse bacterial communities. Little is known about the diversity of chloroplast genomes (cpDNAs) in this group, and about the possible consequences of intracellular bacteria on genome composition of the host. We present the complete cpDNAs of Bryopsis plumosa and Tydemania expeditiones, as well as a re-annotated cpDNA of B. hypnoides, which was shown to contain a higher number of genes than originally published. Chloroplast genomic data were also used to evaluate phylogenetic hypotheses in the Chlorophyta, such as monophyly of the Ulvophyceae (the class in which the order Bryopsidales is currently classified).

Results: Both DNAs are circular and lack a large inverted repeat. The cpDNA of B. plumosa is 106,859 bp long and contains 115 unique genes. A 13 kb region was identified with several freestanding open reading frames (ORFs) of putative bacterial origin, including a large ORF (>8 kb) closely related to bacterial rhs-family genes. The cpDNA of T. expeditiones is 105,200 bp long and contains 125 unique genes. As in B. plumosa, several regions were identified with ORFs of possible bacterial origin, including genes involved in mobile functions (transposases, integrases, phage/plasmid DNA primases), and ORFs showing close similarity with bacterial DNA methyltransferases. The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region. Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.

Conclusions: The cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta. The presence of bacterial genes, including genes typically found in mobile elements, suggest that these have been acquired through horizontal gene transfer, which may have been facilitated by the occurrence of obligate intracellular bacteria in these siphonous algae.

No MeSH data available.


Related in: MedlinePlus