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Horizontal transfer of a eukaryotic plastid-targeted protein gene to cyanobacteria.

Rogers MB, Patron NJ, Keeling PJ - BMC Biol. (2007)

Bottom Line: This eukaryotic-type FBA once replaced the plastid/cyanobacterial type in photosynthetic eukaryotes, hinting at a possible functional advantage in Calvin cycle reactions.A gene for plastid-targeted FBA has been transferred from red algae to cyanobacteria, where it has inserted itself beside its non-homologous, functional analogue.Its current distribution in Prochlorococcus and Synechococcus is punctate, suggesting a complex history since its introduction to this group.

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Affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, BC, Canada. mbrogers@interchange.ubc.ca

ABSTRACT

Background: Horizontal or lateral transfer of genetic material between distantly related prokaryotes has been shown to play a major role in the evolution of bacterial and archaeal genomes, but exchange of genes between prokaryotes and eukaryotes is not as well understood. In particular, gene flow from eukaryotes to prokaryotes is rarely documented with strong support, which is unusual since prokaryotic genomes appear to readily accept foreign genes.

Results: Here, we show that abundant marine cyanobacteria in the related genera Synechococcus and Prochlorococcus acquired a key Calvin cycle/glycolytic enzyme from a eukaryote. Two non-homologous forms of fructose bisphosphate aldolase (FBA) are characteristic of eukaryotes and prokaryotes respectively. However, a eukaryotic gene has been inserted immediately upstream of the ancestral prokaryotic gene in several strains (ecotypes) of Synechococcus and Prochlorococcus. In one lineage this new gene has replaced the ancestral gene altogether. The eukaryotic gene is most closely related to the plastid-targeted FBA from red algae. This eukaryotic-type FBA once replaced the plastid/cyanobacterial type in photosynthetic eukaryotes, hinting at a possible functional advantage in Calvin cycle reactions. The strains that now possess this eukaryotic FBA are scattered across the tree of Synechococcus and Prochlorococcus, perhaps because the gene has been transferred multiple times among cyanobacteria, or more likely because it has been selectively retained only in certain lineages.

Conclusion: A gene for plastid-targeted FBA has been transferred from red algae to cyanobacteria, where it has inserted itself beside its non-homologous, functional analogue. Its current distribution in Prochlorococcus and Synechococcus is punctate, suggesting a complex history since its introduction to this group.

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Protein maximum likelihood tree of class I FBA. Protein maximum likelihood phylogeny of class I FBA. The cyanobacterial and plastid-targeted red algal class I FBA genes are indicated by boxes, and all other groups are bracketed and labelled to the right. Numbers at node correspond to bootstrap support over 50% for major nodes from ML (above) and distance (below). Methods and parameters used are detailed in the Methods section.
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Figure 2: Protein maximum likelihood tree of class I FBA. Protein maximum likelihood phylogeny of class I FBA. The cyanobacterial and plastid-targeted red algal class I FBA genes are indicated by boxes, and all other groups are bracketed and labelled to the right. Numbers at node correspond to bootstrap support over 50% for major nodes from ML (above) and distance (below). Methods and parameters used are detailed in the Methods section.

Mentions: The relatively restricted distribution of this eukaryotic gene in a few strains of Synechococcus and Prochlorococcus suggests either a very recent origin in these genera, or horizontal gene transfer between strains. To determine if the genes originated once in cyanobacteria and from what kind of eukaryote they might be derived, phylogenetic analyses were performed to determine the position of the cyanobacterial genes relative to eukaryotic class I FBAs. Class I FBA phylogeny has been shown previously to lack sufficient resolution between many major subgroups [14,16], and the present analysis was no exception to this (Figure 2). However, the cyanobacterial genes formed a unique clade with 100% support, indicating a single origin of the gene in Synechococcus and Prochlorococcus. Most importantly, the cyanobacterial genes formed a specific and strongly-supported group with the nuclear-encoded, plastid-targeted FBAs from red algae (100% support). These genes are very distantly related to the discrete clade of class I FBAs already known from some prokaryotes, which is also present in three cyanobacteria Trichodesmium erythraeum, Crocosphaera watsonii, and Synechococystis PCC6803. These genera are not closely related to Prochlorococcus and Synechococcus. The Prochlorococcus and Synechococcus genes show elevated rates of evolution, but with the exception of the possible pseudogene in Prochlorococcus MIT9303, none show any signs of being non-functional or otherwise unusual.


Horizontal transfer of a eukaryotic plastid-targeted protein gene to cyanobacteria.

Rogers MB, Patron NJ, Keeling PJ - BMC Biol. (2007)

Protein maximum likelihood tree of class I FBA. Protein maximum likelihood phylogeny of class I FBA. The cyanobacterial and plastid-targeted red algal class I FBA genes are indicated by boxes, and all other groups are bracketed and labelled to the right. Numbers at node correspond to bootstrap support over 50% for major nodes from ML (above) and distance (below). Methods and parameters used are detailed in the Methods section.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1919352&req=5

Figure 2: Protein maximum likelihood tree of class I FBA. Protein maximum likelihood phylogeny of class I FBA. The cyanobacterial and plastid-targeted red algal class I FBA genes are indicated by boxes, and all other groups are bracketed and labelled to the right. Numbers at node correspond to bootstrap support over 50% for major nodes from ML (above) and distance (below). Methods and parameters used are detailed in the Methods section.
Mentions: The relatively restricted distribution of this eukaryotic gene in a few strains of Synechococcus and Prochlorococcus suggests either a very recent origin in these genera, or horizontal gene transfer between strains. To determine if the genes originated once in cyanobacteria and from what kind of eukaryote they might be derived, phylogenetic analyses were performed to determine the position of the cyanobacterial genes relative to eukaryotic class I FBAs. Class I FBA phylogeny has been shown previously to lack sufficient resolution between many major subgroups [14,16], and the present analysis was no exception to this (Figure 2). However, the cyanobacterial genes formed a unique clade with 100% support, indicating a single origin of the gene in Synechococcus and Prochlorococcus. Most importantly, the cyanobacterial genes formed a specific and strongly-supported group with the nuclear-encoded, plastid-targeted FBAs from red algae (100% support). These genes are very distantly related to the discrete clade of class I FBAs already known from some prokaryotes, which is also present in three cyanobacteria Trichodesmium erythraeum, Crocosphaera watsonii, and Synechococystis PCC6803. These genera are not closely related to Prochlorococcus and Synechococcus. The Prochlorococcus and Synechococcus genes show elevated rates of evolution, but with the exception of the possible pseudogene in Prochlorococcus MIT9303, none show any signs of being non-functional or otherwise unusual.

Bottom Line: This eukaryotic-type FBA once replaced the plastid/cyanobacterial type in photosynthetic eukaryotes, hinting at a possible functional advantage in Calvin cycle reactions.A gene for plastid-targeted FBA has been transferred from red algae to cyanobacteria, where it has inserted itself beside its non-homologous, functional analogue.Its current distribution in Prochlorococcus and Synechococcus is punctate, suggesting a complex history since its introduction to this group.

View Article: PubMed Central - HTML - PubMed

Affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, BC, Canada. mbrogers@interchange.ubc.ca

ABSTRACT

Background: Horizontal or lateral transfer of genetic material between distantly related prokaryotes has been shown to play a major role in the evolution of bacterial and archaeal genomes, but exchange of genes between prokaryotes and eukaryotes is not as well understood. In particular, gene flow from eukaryotes to prokaryotes is rarely documented with strong support, which is unusual since prokaryotic genomes appear to readily accept foreign genes.

Results: Here, we show that abundant marine cyanobacteria in the related genera Synechococcus and Prochlorococcus acquired a key Calvin cycle/glycolytic enzyme from a eukaryote. Two non-homologous forms of fructose bisphosphate aldolase (FBA) are characteristic of eukaryotes and prokaryotes respectively. However, a eukaryotic gene has been inserted immediately upstream of the ancestral prokaryotic gene in several strains (ecotypes) of Synechococcus and Prochlorococcus. In one lineage this new gene has replaced the ancestral gene altogether. The eukaryotic gene is most closely related to the plastid-targeted FBA from red algae. This eukaryotic-type FBA once replaced the plastid/cyanobacterial type in photosynthetic eukaryotes, hinting at a possible functional advantage in Calvin cycle reactions. The strains that now possess this eukaryotic FBA are scattered across the tree of Synechococcus and Prochlorococcus, perhaps because the gene has been transferred multiple times among cyanobacteria, or more likely because it has been selectively retained only in certain lineages.

Conclusion: A gene for plastid-targeted FBA has been transferred from red algae to cyanobacteria, where it has inserted itself beside its non-homologous, functional analogue. Its current distribution in Prochlorococcus and Synechococcus is punctate, suggesting a complex history since its introduction to this group.

Show MeSH
Related in: MedlinePlus