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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.

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.

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ITS Phylogeny of Prochlorococcus and Synechococcus showing gene order surrounding FBA I locus. Phylogeny of Prochlorococcus and Synechococcus strains showing the distribution of class I and class II FBA. Maximum likelihood tree based on rRNA ITS sequences with bootstrap support shown for major nodes with greater than 70% support. The branch leading to one clade of Prochlorococcus (indicated by double hatch marks) has been truncated to fit. The genomic context of FBA genes is shown for completely sequenced genomes. Class I FBA (eukaryotic) is shown in red and class II (prokaryotic) is shown in green. Black arrows correspond to up and downstream genes that are conserved in order and direction in most genomes, whereas grey arrows are the few exceptions to this conservation.
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Figure 1: ITS Phylogeny of Prochlorococcus and Synechococcus showing gene order surrounding FBA I locus. Phylogeny of Prochlorococcus and Synechococcus strains showing the distribution of class I and class II FBA. Maximum likelihood tree based on rRNA ITS sequences with bootstrap support shown for major nodes with greater than 70% support. The branch leading to one clade of Prochlorococcus (indicated by double hatch marks) has been truncated to fit. The genomic context of FBA genes is shown for completely sequenced genomes. Class I FBA (eukaryotic) is shown in red and class II (prokaryotic) is shown in green. Black arrows correspond to up and downstream genes that are conserved in order and direction in most genomes, whereas grey arrows are the few exceptions to this conservation.

Mentions: Cyanobacterial genomes typically encode a class II FBA for use in both glycolysis and the Calvin cycle. However, in two closely related genera, Synechococcus and Prochlorococcus, we have found the situation is more complex. The order of genes surrounding the FBA locus is highly conserved among completely sequenced representative genomes from both genera. While many strains encode only the ancestral cyanobacterial class II FBA, in three Synechococcus strains (BL107, CC9902, and 9311) and three Prochlorococcus strains (SS120, AS9601, and MIT9515), a eukaryote-derived class I FBA is found immediately upstream of the ancestral cyanobacterial gene (Figure 1). Moreover, in two Prochlorococcus strains (NATL1A and NATL2A) the cyanobacterial class II FBA has been lost, effectively leaving the eukaryotic class I FBA in its place (Figure 1). Prochlorococcus MIT9303 also has a homologue of this gene elsewhere in the genome, but both it and the canonical class II FBA contain several stop codons, indicating either they are pseudogenes or sequencing errors.


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

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

ITS Phylogeny of Prochlorococcus and Synechococcus showing gene order surrounding FBA I locus. Phylogeny of Prochlorococcus and Synechococcus strains showing the distribution of class I and class II FBA. Maximum likelihood tree based on rRNA ITS sequences with bootstrap support shown for major nodes with greater than 70% support. The branch leading to one clade of Prochlorococcus (indicated by double hatch marks) has been truncated to fit. The genomic context of FBA genes is shown for completely sequenced genomes. Class I FBA (eukaryotic) is shown in red and class II (prokaryotic) is shown in green. Black arrows correspond to up and downstream genes that are conserved in order and direction in most genomes, whereas grey arrows are the few exceptions to this conservation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: ITS Phylogeny of Prochlorococcus and Synechococcus showing gene order surrounding FBA I locus. Phylogeny of Prochlorococcus and Synechococcus strains showing the distribution of class I and class II FBA. Maximum likelihood tree based on rRNA ITS sequences with bootstrap support shown for major nodes with greater than 70% support. The branch leading to one clade of Prochlorococcus (indicated by double hatch marks) has been truncated to fit. The genomic context of FBA genes is shown for completely sequenced genomes. Class I FBA (eukaryotic) is shown in red and class II (prokaryotic) is shown in green. Black arrows correspond to up and downstream genes that are conserved in order and direction in most genomes, whereas grey arrows are the few exceptions to this conservation.
Mentions: Cyanobacterial genomes typically encode a class II FBA for use in both glycolysis and the Calvin cycle. However, in two closely related genera, Synechococcus and Prochlorococcus, we have found the situation is more complex. The order of genes surrounding the FBA locus is highly conserved among completely sequenced representative genomes from both genera. While many strains encode only the ancestral cyanobacterial class II FBA, in three Synechococcus strains (BL107, CC9902, and 9311) and three Prochlorococcus strains (SS120, AS9601, and MIT9515), a eukaryote-derived class I FBA is found immediately upstream of the ancestral cyanobacterial gene (Figure 1). Moreover, in two Prochlorococcus strains (NATL1A and NATL2A) the cyanobacterial class II FBA has been lost, effectively leaving the eukaryotic class I FBA in its place (Figure 1). Prochlorococcus MIT9303 also has a homologue of this gene elsewhere in the genome, but both it and the canonical class II FBA contain several stop codons, indicating either they are pseudogenes or sequencing errors.

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