The Phylogeny of Glyceraldehyde-3-Phosphate Dehydrogenase Indicates Lateral Gene Transfer from Cryptomonads to Dinoflagellates

Fagan, Thomas F.; Hastings, J. Woodland; Morse, David

doi:10.1007/pl00006420

Cited by 41 publications

(25 citation statements)

References 45 publications

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“…2B, closed circles) show a clear tendency toward synonymous changes, indicating a purifying selection. It also is interesting that the two sequences with the largest number of synonymous mutations, the RuBisCo and glyceraldehyde-3-phosphate dehydrogenase sequences, are both thought to be derived from horizontal gene transfer (HGT) (18,19).…”

Section: Resultsmentioning

confidence: 99%

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

Beauchemin

Roy

Daoust

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Dinoflagellates are an important component of the marine biota, but a large genome with high–copy number (up to 5,000) tandem gene arrays has made genomic sequencing problematic. More importantly, little is known about the expression and conservation of these unusual gene arrays. We assembled de novo a gene catalog of 74,655 contigs for the dinoflagellate Lingulodinium polyedrum from RNA-Seq (Illumina) reads. The catalog contains 93% of a Lingulodinium EST dataset deposited in GenBank and 94% of the enzymes in 16 primary metabolic KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways, indicating it is a good representation of the transcriptome. Analysis of the catalog shows a marked underrepresentation of DNA-binding proteins and DNA-binding domains compared with other algae. Despite this, we found no evidence to support the proposal of polycistronic transcription, including a marked underrepresentation of sequences corresponding to the intergenic spacers of two tandem array genes. We also have used RNA-Seq to assess the degree of sequence conservation in tandem array genes and found their transcripts to be highly conserved. Interestingly, some of the sequences in the catalog have only bacterial homologs and are potential candidates for horizontal gene transfer. These presumably were transferred as single-copy genes, and because they are now all GC-rich, any derived from AT-rich contexts must have experienced extensive mutation. Our study not only has provided the most complete dinoflagellate gene catalog known to date, it has also exploited RNA-Seq to address fundamental issues in basic transcription mechanisms and sequence conservation in these algae.

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Section: Resultsmentioning

confidence: 99%

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

Beauchemin

Roy

Daoust

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…It is possible that this gene may have arisen in some of the species by lateral gene transfer (Fig. 1C) because a growing number of examples suggest lateral gene transfer of dinoflagellate genes may be relatively frequent (Fagan et al, 1998;Keeling and Inagaki, 2004;Waller et al, 2006). In any event, it is noteworthy that, to date, the d-CA family appears restricted to marine algae.…”

Section: Discussionmentioning

confidence: 99%

An External δ-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition

2008

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The oceans globally constitute an important sink for carbon dioxide (CO2) due to phytoplankton photosynthesis. However, the marine environment imposes serious restraints to carbon fixation. First, the equilibrium between CO2 and bicarbonate (HCO3 −) is pH dependent, and, in normal, slightly alkaline seawater, [CO2] is typically low (approximately 10 μ m). Second, the rate of CO2 diffusion in seawater is slow, so, for any cells unable to take up bicarbonate efficiently, photosynthesis could become carbon limited due to depletion of CO2 from their immediate vicinity. This may be especially problematic for those dinoflagellates using a form II Rubisco because this form is less oxygen tolerant than the usually found form I enzyme. We have identified a carbonic anhydrase (CA) from the free-living marine dinoflagellate Lingulodinium polyedrum that appears to play a role in carbon acquisition. This CA shares 60% sequence identity with δ-class CAs, isoforms so far found only in marine algae. Immunoelectron microscopy indicates that this enzyme is associated exclusively with the plasma membrane. Furthermore, this enzyme appears to be exposed to the external medium as determined by whole-cell CA assays and vectorial labeling of cell surface proteins with 125I. The fixation of 14CO2 is strongly pH dependent, suggesting preferential uptake of CO2 rather than HCO3 −, and photosynthetic rates decrease in the presence of 1 mm acetazolamide, a non-membrane-permeable CA inhibitor. This constitutes the first CA identified in the dinoflagellates, and, taken together, our results suggest that this enzyme may help to increase CO2 availability at the cell surface.

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“…It is possible that psbO was still retained in the chloroplast genome at the time of endosymbiosis, but this seems unlikely given that psbO is a nuclear-encoded gene family in known photosynthetic eukaryotes (Ishida and Green 2002). For the GAPDH gene, chloroplast to nucleus transfer is unlikely because in the dinoflagellates (Fagan et al 1998), haptophytes (Harper and Keeling 2003), heterokonts (Fast et al 2001) and cryptophytes (Liaud et al 1997) the cyanobacterial version of this gene is thought to have been lost and a substitute cytosolic version has been targeted to the plastid. The GAPDH evolutionary history suggests direct transfer from the nucleus of the previous plastid host to the nucleus of the new host (Fast et al 2001;Harper and Keeling 2003).…”

Section: Iv4 Discussionmentioning

confidence: 99%

“…In addition to these Calvin-cycle genes, genes encoding triosephosphate isomerase and fructose-1,6-biphosphate aldolase were also present and are necessary for the regeneration of ribulose, but these ESTs do not provide enough information to determine if these are cyanobacterial or cytosolic forms of the enzymes. A substitution of a cytosolic glyceraldehyde 3-phosphate dehydrogenase (GAPDH) in dinoflagellate chloroplasts has been documented (Fagan et al 1998;Fast et al 2001 Other plastid-associated pathways include fatty acid biosynthesis and the DOXP/MEP pathway, and genes corresponding to both of these pathways were found.…”

Section: Cyanobacterial Genes and Biochemistrymentioning

confidence: 99%

5  The origin of the dinoflagellate plastid

Bachvaroff

Concepcion

Rogers

et al. 2003

Journal of Phycology

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The peridinin pigmented dinoflagellate chloroplasts are the result of a secondary endosymbiotic event between a photosynthetic eukaryote and a dinoflagellate.Dinoflagellate chloroplast and nuclear evolution were independent before this endosymbiotic event. To reconstruct the evolution of the dinoflagellate chloroplast, phylogenies were constructed with a chloroplast gene psbB. The gene phylogeny should reflect the evolution of the chloroplast and indicate the plastid donor lineage. Gene sequences derived from the dinoflagellate chloroplast were extremely divergent but suggested that the plastid donor could have been a haptophyte. In an attempt to find better genes for analysis and to further understand gene transfer about 4900 randomly selected expressed genes were sequenced from two dinoflagellates, Lingulodinium polyedra and Amphidinium carterae. From these genes, thirty typically plastid-encoded genes were found, including eight otherwise known only from plastid genomes. Based on poly-A tails, gene families, and leader sequences these genes appear to be nuclearencoded in dinoflagellates. This result suggests that dinoflagellate chloroplasts may have the smallest protein-coding potential yet known. These genes and the partially sequenced chloroplast genome of a haptophyte were used in a phylogenetic analysis. There is strong conflict between genes encoded in the chloroplast and those in the nucleus. The chloroplast genes suggest relationship between haptophyte and dinoflagellate plastids, while the nuclear-encoded genes suggest a relationship with heterokonts. Chromophyte plastid monophyly is supported by these data but the single origin of the chromophyte plastid from red algae does not mean that the host lineages are monophyletic. These results are consistent with at least two different scenarios: either dinoflagellates and haptophytes independently acquired a plastid from the heterokonts, or dinoflagellates acquired their plastids from haptophtyes, who in turn acquired their plastids from heterokonts. The evolutionary rate of the remaining plastid-encoded genes was compared with formerly plastid-encoded genes. These relative rate tests revealed strong incongruence between minicircle genes, formerly plastid-encoded genes and genes that were likely to have been acquired from the nucleus of the plastid donor lineage.

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The Phylogeny of Glyceraldehyde-3-Phosphate Dehydrogenase Indicates Lateral Gene Transfer from Cryptomonads to Dinoflagellates

Cited by 41 publications

References 45 publications

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

An External δ-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition

5  The origin of the dinoflagellate plastid

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The Phylogeny of Glyceraldehyde-3-Phosphate Dehydrogenase Indicates Lateral Gene Transfer from Cryptomonads to Dinoflagellates

Cited by 41 publications

References 45 publications

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic

An External δ-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition

5 The origin of the dinoflagellate plastid

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5  The origin of the dinoflagellate plastid