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Phylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae.

Huerlimann R, Zenger KR, Jerry DR, Heimann K - PLoS ONE (2015)

Bottom Line: Nucleus-encoded homomeric ACCase is also found in plastids of algae that arose from a secondary/tertiary endosymbiotic event.These two ACCase based, phylogenetic relationships suggest that the plastidial homomeric ACCase was acquired by the Haptophyta, Cryptophyta and SAR, before the photosynthetic Rhizaria acquired their green plastid.Additionally, plastidial ACCase was derived by HGT from an ancestor or relative of the Prasinophyceae and not by duplication of cytosolic ACCase.

View Article: PubMed Central - PubMed

Affiliation: College of Marine and Environmental Sciences, James Cook University, Townsville, Queensland, Australia; Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland, Australia; Comparative Genomics Centre, James Cook University, Townsville, Queensland Australia.

ABSTRACT
The understanding of algal phylogeny is being impeded by an unknown number of events of horizontal gene transfer (HGT), and primary and secondary/tertiary endosymbiosis. Through these events, previously heterotrophic eukaryotes developed photosynthesis and acquired new biochemical pathways. Acetyl-CoA carboxylase (ACCase) is a key enzyme in the fatty acid synthesis and elongation pathways in algae, where ACCase exists in two locations (cytosol and plastid) and in two forms (homomeric and heteromeric). All algae contain nucleus-encoded homomeric ACCase in the cytosol, independent of the origin of the plastid. Nucleus-encoded homomeric ACCase is also found in plastids of algae that arose from a secondary/tertiary endosymbiotic event. In contrast, plastids of algae that arose from a primary endosymbiotic event contain heteromeric ACCase, which consists of three nucleus-encoded and one plastid-encoded subunits. These properties of ACCase provide the potential to inform on the phylogenetic relationships of hosts and their plastids, allowing different hypothesis of endosymbiotic events to be tested. Alveolata (Dinoflagellata and Apicomplexa) and Chromista (Stramenopiles, Haptophyta and Cryptophyta) have traditionally been grouped together as Chromalveolata, forming the red lineage. However, recent genetic evidence groups the Stramenopiles, Alveolata and green plastid containing Rhizaria as SAR, excluding Haptophyta and Cryptophyta. Sequences coding for plastid and cytosol targeted homomeric ACCases were isolated from Isochrysis aff. galbana (TISO), Chromera velia and Nannochloropsis oculata, representing three taxonomic groups for which sequences were lacking. Phylogenetic analyses show that cytosolic ACCase strongly supports the SAR grouping. Conversely, plastidial ACCase groups the SAR with the Haptophyta, Cryptophyta and Prasinophyceae (Chlorophyta). These two ACCase based, phylogenetic relationships suggest that the plastidial homomeric ACCase was acquired by the Haptophyta, Cryptophyta and SAR, before the photosynthetic Rhizaria acquired their green plastid. Additionally, plastidial ACCase was derived by HGT from an ancestor or relative of the Prasinophyceae and not by duplication of cytosolic ACCase.

No MeSH data available.


Phylogenetic consensus tree (MrBayes; WAG+G) based on 55 ACCase sequences and 564 amino acids positions.Cytosolic and plastidial ACCase are indicated. Sequences produced in this study are shown in bold. Statistical support for internal nodes was determined by Bayesian inference posterior probabilities (first, shown as % values) and bootstrap analysis for ML (second, Model LG+G+F). Only support values ≥50% are shown.
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pone.0131099.g001: Phylogenetic consensus tree (MrBayes; WAG+G) based on 55 ACCase sequences and 564 amino acids positions.Cytosolic and plastidial ACCase are indicated. Sequences produced in this study are shown in bold. Statistical support for internal nodes was determined by Bayesian inference posterior probabilities (first, shown as % values) and bootstrap analysis for ML (second, Model LG+G+F). Only support values ≥50% are shown.

Mentions: The Chromalveolate hypothesis is still hotly debated [6,28]. The traditional view fails to explain recent genetic evidence (e.g. the relationship of the SAR species to the exclusion of the Haptophyta and Cryptophyta), and the latest phylogenetic explanations invoke additional endosymbiotic events to explain inconsistencies [6]. In order to unravel the phylogenetic relationship of acetyl-CoA carboxylase (ACCase) between the different taxa, a phylogenetic consensus tree for plastidial and cytosolic ACCase was constructed using the Bayesian Inference (BI) and Maximum Likelihood (ML) methods (Fig 1). This dataset included all algal sequences of ACCase found on Genbank and JGI (accessed March 2013), to the exclusion of all the sequences of Ectocarpus siliculosus, the plastidial sequence of Emiliania huxleyi and the cytosolic sequence of one Toxoplasma gondii strain, which were incomplete and missed important binding regions. The sequence for the cytosolic ACCase of Chromera velia was also in three fragments, but included all four important binding regions (Table 2). Of the five major nodes (A to E), nodes B to E were strongly supported (BI = 100%, ML ≥ 99%), while node A was strongly supported by BI (BI = 100%, ML > 50%) (Fig 1). Node A, B, C and D contain cytosolic ACCase only, with the exception of the plastidial ACCase from plants. Conversely, node E contains mainly plastidial ACCase. Therefore, nodes A through D show the relationship of the hosts, while node E provides information on the origin of the plastidial ACCase.


Phylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae.

Huerlimann R, Zenger KR, Jerry DR, Heimann K - PLoS ONE (2015)

Phylogenetic consensus tree (MrBayes; WAG+G) based on 55 ACCase sequences and 564 amino acids positions.Cytosolic and plastidial ACCase are indicated. Sequences produced in this study are shown in bold. Statistical support for internal nodes was determined by Bayesian inference posterior probabilities (first, shown as % values) and bootstrap analysis for ML (second, Model LG+G+F). Only support values ≥50% are shown.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4489017&req=5

pone.0131099.g001: Phylogenetic consensus tree (MrBayes; WAG+G) based on 55 ACCase sequences and 564 amino acids positions.Cytosolic and plastidial ACCase are indicated. Sequences produced in this study are shown in bold. Statistical support for internal nodes was determined by Bayesian inference posterior probabilities (first, shown as % values) and bootstrap analysis for ML (second, Model LG+G+F). Only support values ≥50% are shown.
Mentions: The Chromalveolate hypothesis is still hotly debated [6,28]. The traditional view fails to explain recent genetic evidence (e.g. the relationship of the SAR species to the exclusion of the Haptophyta and Cryptophyta), and the latest phylogenetic explanations invoke additional endosymbiotic events to explain inconsistencies [6]. In order to unravel the phylogenetic relationship of acetyl-CoA carboxylase (ACCase) between the different taxa, a phylogenetic consensus tree for plastidial and cytosolic ACCase was constructed using the Bayesian Inference (BI) and Maximum Likelihood (ML) methods (Fig 1). This dataset included all algal sequences of ACCase found on Genbank and JGI (accessed March 2013), to the exclusion of all the sequences of Ectocarpus siliculosus, the plastidial sequence of Emiliania huxleyi and the cytosolic sequence of one Toxoplasma gondii strain, which were incomplete and missed important binding regions. The sequence for the cytosolic ACCase of Chromera velia was also in three fragments, but included all four important binding regions (Table 2). Of the five major nodes (A to E), nodes B to E were strongly supported (BI = 100%, ML ≥ 99%), while node A was strongly supported by BI (BI = 100%, ML > 50%) (Fig 1). Node A, B, C and D contain cytosolic ACCase only, with the exception of the plastidial ACCase from plants. Conversely, node E contains mainly plastidial ACCase. Therefore, nodes A through D show the relationship of the hosts, while node E provides information on the origin of the plastidial ACCase.

Bottom Line: Nucleus-encoded homomeric ACCase is also found in plastids of algae that arose from a secondary/tertiary endosymbiotic event.These two ACCase based, phylogenetic relationships suggest that the plastidial homomeric ACCase was acquired by the Haptophyta, Cryptophyta and SAR, before the photosynthetic Rhizaria acquired their green plastid.Additionally, plastidial ACCase was derived by HGT from an ancestor or relative of the Prasinophyceae and not by duplication of cytosolic ACCase.

View Article: PubMed Central - PubMed

Affiliation: College of Marine and Environmental Sciences, James Cook University, Townsville, Queensland, Australia; Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland, Australia; Comparative Genomics Centre, James Cook University, Townsville, Queensland Australia.

ABSTRACT
The understanding of algal phylogeny is being impeded by an unknown number of events of horizontal gene transfer (HGT), and primary and secondary/tertiary endosymbiosis. Through these events, previously heterotrophic eukaryotes developed photosynthesis and acquired new biochemical pathways. Acetyl-CoA carboxylase (ACCase) is a key enzyme in the fatty acid synthesis and elongation pathways in algae, where ACCase exists in two locations (cytosol and plastid) and in two forms (homomeric and heteromeric). All algae contain nucleus-encoded homomeric ACCase in the cytosol, independent of the origin of the plastid. Nucleus-encoded homomeric ACCase is also found in plastids of algae that arose from a secondary/tertiary endosymbiotic event. In contrast, plastids of algae that arose from a primary endosymbiotic event contain heteromeric ACCase, which consists of three nucleus-encoded and one plastid-encoded subunits. These properties of ACCase provide the potential to inform on the phylogenetic relationships of hosts and their plastids, allowing different hypothesis of endosymbiotic events to be tested. Alveolata (Dinoflagellata and Apicomplexa) and Chromista (Stramenopiles, Haptophyta and Cryptophyta) have traditionally been grouped together as Chromalveolata, forming the red lineage. However, recent genetic evidence groups the Stramenopiles, Alveolata and green plastid containing Rhizaria as SAR, excluding Haptophyta and Cryptophyta. Sequences coding for plastid and cytosol targeted homomeric ACCases were isolated from Isochrysis aff. galbana (TISO), Chromera velia and Nannochloropsis oculata, representing three taxonomic groups for which sequences were lacking. Phylogenetic analyses show that cytosolic ACCase strongly supports the SAR grouping. Conversely, plastidial ACCase groups the SAR with the Haptophyta, Cryptophyta and Prasinophyceae (Chlorophyta). These two ACCase based, phylogenetic relationships suggest that the plastidial homomeric ACCase was acquired by the Haptophyta, Cryptophyta and SAR, before the photosynthetic Rhizaria acquired their green plastid. Additionally, plastidial ACCase was derived by HGT from an ancestor or relative of the Prasinophyceae and not by duplication of cytosolic ACCase.

No MeSH data available.