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

Handle URI:
http://hdl.handle.net/10754/596810
Title:
Phylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae.
Authors:
Huerlimann, Roger; Zenger, Kyall R; Jerry, Dean R; Heimann, Kirsten
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.
Citation:
Huerlimann R, Zenger KR, Jerry DR, Heimann K (2015) Phylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae. PLoS ONE 10: e0131099. Available: http://dx.doi.org/10.1371/journal.pone.0131099.
Publisher:
Public Library of Science (PLoS)
Journal:
PLoS ONE
Issue Date:
1-Jul-2015
DOI:
10.1371/journal.pone.0131099
PubMed ID:
26131555
PubMed Central ID:
PMC4489017
Type:
Article
ISSN:
1932-6203
Sponsors:
The ACCase sequence of Symbiodinium clade A was kindly supplied by Christian R. Voolstra, King Abdullah University of Science and Technology (KAUST), Saudi Arabia [44], while the sequences for clade B were supplied by Bill Leggat, James Cook University, Townsville, Australia.
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DC FieldValue Language
dc.contributor.authorHuerlimann, Rogeren
dc.contributor.authorZenger, Kyall Ren
dc.contributor.authorJerry, Dean Ren
dc.contributor.authorHeimann, Kirstenen
dc.date.accessioned2016-02-21T08:51:07Zen
dc.date.available2016-02-21T08:51:07Zen
dc.date.issued2015-07-01en
dc.identifier.citationHuerlimann R, Zenger KR, Jerry DR, Heimann K (2015) Phylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae. PLoS ONE 10: e0131099. Available: http://dx.doi.org/10.1371/journal.pone.0131099.en
dc.identifier.issn1932-6203en
dc.identifier.pmid26131555en
dc.identifier.doi10.1371/journal.pone.0131099en
dc.identifier.urihttp://hdl.handle.net/10754/596810en
dc.description.abstractThe 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.en
dc.description.sponsorshipThe ACCase sequence of Symbiodinium clade A was kindly supplied by Christian R. Voolstra, King Abdullah University of Science and Technology (KAUST), Saudi Arabia [44], while the sequences for clade B were supplied by Bill Leggat, James Cook University, Townsville, Australia.en
dc.publisherPublic Library of Science (PLoS)en
dc.rightsThis is an open access article distributed under the terms of the , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are crediteden
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titlePhylogenetic Analysis of Nucleus-Encoded Acetyl-CoA Carboxylases Targeted at the Cytosol and Plastid of Algae.en
dc.typeArticleen
dc.identifier.journalPLoS ONEen
dc.identifier.pmcidPMC4489017en
dc.contributor.institutionCollege 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.en
dc.contributor.institutionCollege of Marine and Environmental Sciences, James Cook University, Townsville, Queensland, Australia; Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland, Australia.en

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