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Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae.

Wei L, Xin Y, Wang D, Jing X, Zhou Q, Su X, Jia J, Ning K, Chen F, Hu Q, Xu J - BMC Genomics (2013)

Bottom Line: Pt genome diversification was driven by asymmetric evolution of two inverted repeats (IRa and IRb): psbV and clpC in IRb are highly conserved whereas their counterparts in IRa exhibit three lineage-associated types of structural polymorphism via duplication or disruption of whole or partial genes.This first comprehensive dataset of organelle genomes for a microalgal genus enabled exhaustive assessment and searches of all candidate phylogenetic markers on the organelle genomes.A new strategy for intragenus phylotyping of microalgae was proposed which might be generally applicable to other microalgal genera and should serve as a valuable tool in the expanding algal biotechnology industry.

View Article: PubMed Central - HTML - PubMed

Affiliation: BioEnergy Genome Center and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China.

ABSTRACT

Background: Microalgae are promising feedstock for production of lipids, sugars, bioactive compounds and in particular biofuels, yet development of sensitive and reliable phylotyping strategies for microalgae has been hindered by the paucity of phylogenetically closely-related finished genomes.

Results: Using the oleaginous eustigmatophyte Nannochloropsis as a model, we assessed current intragenus phylotyping strategies by producing the complete plastid (pt) and mitochondrial (mt) genomes of seven strains from six Nannochloropsis species. Genes on the pt and mt genomes have been highly conserved in content, size and order, strongly negatively selected and evolving at a rate 33% and 66% of nuclear genomes respectively. Pt genome diversification was driven by asymmetric evolution of two inverted repeats (IRa and IRb): psbV and clpC in IRb are highly conserved whereas their counterparts in IRa exhibit three lineage-associated types of structural polymorphism via duplication or disruption of whole or partial genes. In the mt genomes, however, a single evolution hotspot varies in copy-number of a 3.5 Kb-long, cox1-harboring repeat. The organelle markers (e.g., cox1, cox2, psbA, rbcL and rrn16_mt) and nuclear markers (e.g., ITS2 and 18S) that are widely used for phylogenetic analysis obtained a divergent phylogeny for the seven strains, largely due to low SNP density. A new strategy for intragenus phylotyping of microalgae was thus proposed that includes (i) twelve sequence markers that are of higher sensitivity than ITS2 for interspecies phylogenetic analysis, (ii) multi-locus sequence typing based on rps11_mt-nad4, rps3_mt and cox2-rrn16_mt for intraspecies phylogenetic reconstruction and (iii) several SSR loci for identification of strains within a given species.

Conclusion: This first comprehensive dataset of organelle genomes for a microalgal genus enabled exhaustive assessment and searches of all candidate phylogenetic markers on the organelle genomes. A new strategy for intragenus phylotyping of microalgae was proposed which might be generally applicable to other microalgal genera and should serve as a valuable tool in the expanding algal biotechnology industry.

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Hotspots of structural polymorphism that drive the diversification of organelle genomes. The phylogenetic tree on the left was based on whole-genome alignment of the seven complete mt genomes. (A) Structural and sequence polymorphism of inverted repeat in the pt genomes. (B) Structural and sequence polymorphism of the hotspot in the mt genomes. Within each sub-figure, genomic features were drawn proportionally to their actual length. Grey solid lines, inserted for alignment purposes, were not actual sequences.
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Figure 3: Hotspots of structural polymorphism that drive the diversification of organelle genomes. The phylogenetic tree on the left was based on whole-genome alignment of the seven complete mt genomes. (A) Structural and sequence polymorphism of inverted repeat in the pt genomes. (B) Structural and sequence polymorphism of the hotspot in the mt genomes. Within each sub-figure, genomic features were drawn proportionally to their actual length. Grey solid lines, inserted for alignment purposes, were not actual sequences.

Mentions: Despite the slow evolution of the Nannochloropsis organelle genomes, a single hotspot of structural polymorphism was found in the pt genomes. A large inverted repeat (IR), as a canonical structure of pt genome, was present in the vast majority of higher plants and algae studied so far [57]. In many stramenopile algae such as H. akashiwo, Thalassiosira oceanica and Skeletonema costatum, the IRs are large in size (22 kb, 18 kb and 20 kb, respectively) and include 17 ~ 20 genes (including rRNA genes such as rrn5, rrn16 and rrn23, ribosomal protein genes such as rpl32, rpl21 and rpl34, and photosynthetic genes such as psbA, psbY and psbC; [48,58]). However, a pair of short IRs (IRa and IRb) each of 5,122 ~ 7,380 bp in size was found in each of the Nannochloropsis pt genomes (Figure 3), suggesting dramatic IR-size contraction. This may be due to the fewer number of genes harbored in the IRs: the ribosomal operon (rrn5, rrn16 and rrn23) was present while ribosomal protein and photosystem genes were absent in each of the Nannochloropsis strains; moreover, psbV, petJ and clpC-I (which were absent in the IRs of diatoms and brown algae [8,26]) were present in only a subset of the strains (Figure 3A).


Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae.

Wei L, Xin Y, Wang D, Jing X, Zhou Q, Su X, Jia J, Ning K, Chen F, Hu Q, Xu J - BMC Genomics (2013)

Hotspots of structural polymorphism that drive the diversification of organelle genomes. The phylogenetic tree on the left was based on whole-genome alignment of the seven complete mt genomes. (A) Structural and sequence polymorphism of inverted repeat in the pt genomes. (B) Structural and sequence polymorphism of the hotspot in the mt genomes. Within each sub-figure, genomic features were drawn proportionally to their actual length. Grey solid lines, inserted for alignment purposes, were not actual sequences.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750441&req=5

Figure 3: Hotspots of structural polymorphism that drive the diversification of organelle genomes. The phylogenetic tree on the left was based on whole-genome alignment of the seven complete mt genomes. (A) Structural and sequence polymorphism of inverted repeat in the pt genomes. (B) Structural and sequence polymorphism of the hotspot in the mt genomes. Within each sub-figure, genomic features were drawn proportionally to their actual length. Grey solid lines, inserted for alignment purposes, were not actual sequences.
Mentions: Despite the slow evolution of the Nannochloropsis organelle genomes, a single hotspot of structural polymorphism was found in the pt genomes. A large inverted repeat (IR), as a canonical structure of pt genome, was present in the vast majority of higher plants and algae studied so far [57]. In many stramenopile algae such as H. akashiwo, Thalassiosira oceanica and Skeletonema costatum, the IRs are large in size (22 kb, 18 kb and 20 kb, respectively) and include 17 ~ 20 genes (including rRNA genes such as rrn5, rrn16 and rrn23, ribosomal protein genes such as rpl32, rpl21 and rpl34, and photosynthetic genes such as psbA, psbY and psbC; [48,58]). However, a pair of short IRs (IRa and IRb) each of 5,122 ~ 7,380 bp in size was found in each of the Nannochloropsis pt genomes (Figure 3), suggesting dramatic IR-size contraction. This may be due to the fewer number of genes harbored in the IRs: the ribosomal operon (rrn5, rrn16 and rrn23) was present while ribosomal protein and photosystem genes were absent in each of the Nannochloropsis strains; moreover, psbV, petJ and clpC-I (which were absent in the IRs of diatoms and brown algae [8,26]) were present in only a subset of the strains (Figure 3A).

Bottom Line: Pt genome diversification was driven by asymmetric evolution of two inverted repeats (IRa and IRb): psbV and clpC in IRb are highly conserved whereas their counterparts in IRa exhibit three lineage-associated types of structural polymorphism via duplication or disruption of whole or partial genes.This first comprehensive dataset of organelle genomes for a microalgal genus enabled exhaustive assessment and searches of all candidate phylogenetic markers on the organelle genomes.A new strategy for intragenus phylotyping of microalgae was proposed which might be generally applicable to other microalgal genera and should serve as a valuable tool in the expanding algal biotechnology industry.

View Article: PubMed Central - HTML - PubMed

Affiliation: BioEnergy Genome Center and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China.

ABSTRACT

Background: Microalgae are promising feedstock for production of lipids, sugars, bioactive compounds and in particular biofuels, yet development of sensitive and reliable phylotyping strategies for microalgae has been hindered by the paucity of phylogenetically closely-related finished genomes.

Results: Using the oleaginous eustigmatophyte Nannochloropsis as a model, we assessed current intragenus phylotyping strategies by producing the complete plastid (pt) and mitochondrial (mt) genomes of seven strains from six Nannochloropsis species. Genes on the pt and mt genomes have been highly conserved in content, size and order, strongly negatively selected and evolving at a rate 33% and 66% of nuclear genomes respectively. Pt genome diversification was driven by asymmetric evolution of two inverted repeats (IRa and IRb): psbV and clpC in IRb are highly conserved whereas their counterparts in IRa exhibit three lineage-associated types of structural polymorphism via duplication or disruption of whole or partial genes. In the mt genomes, however, a single evolution hotspot varies in copy-number of a 3.5 Kb-long, cox1-harboring repeat. The organelle markers (e.g., cox1, cox2, psbA, rbcL and rrn16_mt) and nuclear markers (e.g., ITS2 and 18S) that are widely used for phylogenetic analysis obtained a divergent phylogeny for the seven strains, largely due to low SNP density. A new strategy for intragenus phylotyping of microalgae was thus proposed that includes (i) twelve sequence markers that are of higher sensitivity than ITS2 for interspecies phylogenetic analysis, (ii) multi-locus sequence typing based on rps11_mt-nad4, rps3_mt and cox2-rrn16_mt for intraspecies phylogenetic reconstruction and (iii) several SSR loci for identification of strains within a given species.

Conclusion: This first comprehensive dataset of organelle genomes for a microalgal genus enabled exhaustive assessment and searches of all candidate phylogenetic markers on the organelle genomes. A new strategy for intragenus phylotyping of microalgae was proposed which might be generally applicable to other microalgal genera and should serve as a valuable tool in the expanding algal biotechnology industry.

Show MeSH
Related in: MedlinePlus