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The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like gamma-proteobacterium.

Marin B, Nowack EC, Glöckner G, Melkonian M - BMC Evol. Biol. (2007)

Bottom Line: Combined phylogenies using rbcL and the rDNA-operon resulted in a nearly fully resolved tree of the PS-clade.The gamma-proteobacterium Nitrococcus mobilis represents the closest known relative to the donor of the carboxysomal operon.The isolated position of the Paulinella chromatophore in molecular phylogenies as well as its elevated AT content suggests that the Paulinella chromatophore has already undergone typical steps in the reductive evolution of an endosymbiont.

View Article: PubMed Central - HTML - PubMed

Affiliation: Botanisches Institut, Lehrstuhl I, Universität zu Köln, Köln, Germany. birger.marin@uni-koeln.de

ABSTRACT

Background: Paulinella chromatophora is a freshwater filose amoeba with photosynthetic endosymbionts (chromatophores) of cyanobacterial origin that are closely related to free-living Prochlorococcus and Synechococcus species (PS-clade). Members of the PS-clade of cyanobacteria contain a proteobacterial form 1A RubisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase) that was acquired by horizontal gene transfer (HGT) of a carboxysomal operon. In rDNA-phylogenies, the Paulinella chromatophore diverged basal to the PS-clade, raising the question whether the HGT occurred before or after the split of the chromatophore ancestor.

Results: Phylogenetic analyses of the almost complete rDNA operon with an improved taxon sampling containing most known cyanobacterial lineages recovered the Paulinella chromatophore as sister to the complete PS-clade. The sequence of the complete carboxysomal operon of Paulinella was determined. Analysis of RubisCO large subunit (rbcL) sequences revealed that Paulinella shares the proteobacterial form 1A RubisCO with the PS-clade. The gamma-proteobacterium Nitrococcus mobilis was identified as sister of the Paulinella chromatophore and the PS-clade in the RubisCO phylogeny. Gene content and order in the carboxysomal operon correlates well with the RubisCO phylogeny demonstrating that the complete carboxysomal operon was acquired by the common ancestor of the Paulinella chromatophore and the PS-clade through HGT. The carboxysomal operon shows a significantly elevated AT content in Paulinella, which in the rbcL gene is confined to third codon positions. Combined phylogenies using rbcL and the rDNA-operon resulted in a nearly fully resolved tree of the PS-clade.

Conclusion: The HGT of the carboxysomal operon predated the divergence of the chromatophore ancestor from the PS-clade. Following HGT and divergence of the chromatophore ancestor, diversification of the PS-clade into at least three subclades occurred. The gamma-proteobacterium Nitrococcus mobilis represents the closest known relative to the donor of the carboxysomal operon. The isolated position of the Paulinella chromatophore in molecular phylogenies as well as its elevated AT content suggests that the Paulinella chromatophore has already undergone typical steps in the reductive evolution of an endosymbiont.

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Synapomorphy support in the 23S rRNA for the sister-group relationship between Paulinella and free-living α-cyanobacteria. Shown is the alignment and secondary structure diagram of Helix 837 in the 23S rDNA, with two RNA base pairs highlighted that represent synapomorphies of α-cyanobacterial clades to the exclusion of Paulinella and other prokaryotes. Sequence data and evolutionary changes are plotted on a simplified phylogram (NJ-bootstrap consensus tree). Pair 868/909 shows a uniquely derived CBC (compensatory base change: U-A → C-G) of all free-living α-cyanobacteria; the neighbouring pair 869/908 changed in the common ancestor of the marine PS-subclades (marine Synechococcus and Prochlorococcus) whereas the Cyanobium-clade and Paulinella are plesiomorphic. Pair 869/908 shows parallel changes in a few other cyanobacteria, (e.g. in Fischerella).
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Figure 2: Synapomorphy support in the 23S rRNA for the sister-group relationship between Paulinella and free-living α-cyanobacteria. Shown is the alignment and secondary structure diagram of Helix 837 in the 23S rDNA, with two RNA base pairs highlighted that represent synapomorphies of α-cyanobacterial clades to the exclusion of Paulinella and other prokaryotes. Sequence data and evolutionary changes are plotted on a simplified phylogram (NJ-bootstrap consensus tree). Pair 868/909 shows a uniquely derived CBC (compensatory base change: U-A → C-G) of all free-living α-cyanobacteria; the neighbouring pair 869/908 changed in the common ancestor of the marine PS-subclades (marine Synechococcus and Prochlorococcus) whereas the Cyanobium-clade and Paulinella are plesiomorphic. Pair 869/908 shows parallel changes in a few other cyanobacteria, (e.g. in Fischerella).

Mentions: Phylogenetic analyses revealed basal cyanobacterial branches (e.g. Gloeobacter), and two moderately supported lineages, one combining the majority of the β-cyanobacteria including all plastids (branch 1 in Figure 1), the other containing Paulinella and the PS-clade nested within a radiation of a few β-cyanobacteria, representing the clades PHOR, PRCHX and SELONG (branch 2 in Figure 1). Paulinella is monophyletic with the PS-clade (branch 4). Our previous study [1] had already revealed the monophyly of both marine PS-subclades to the exclusion of the Paulinella chromatophore, as confirmed here (see branch 9). The present investigation includes five sequences of the third PS-subclade, the Cyanobium-clade, which is sister to the marine subclades, with Paulinella still diverging in a basal position. The monophyly of the entire PS-clade to the exclusion of Paulinella, however, receives only moderate to low bootstrap support (branch 5), but is corroborated by unique synapomorphies in the 23S rRNA (Figure 2). As previously shown, both marine PS-subclades are characterized by unique compensatory base changes (CBCs in pairs 868/909 and 869/908), whereas Paulinella is plesiomorphic in both pairs [1]. Interestingly, the Cyanobium-clade is intermediate in sharing the unique CBC in position 868/909 with marine PS-subclades, but displaying the ancestral character state in positions 869/908, in congruence with the tree topology (Figure 2).


The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like gamma-proteobacterium.

Marin B, Nowack EC, Glöckner G, Melkonian M - BMC Evol. Biol. (2007)

Synapomorphy support in the 23S rRNA for the sister-group relationship between Paulinella and free-living α-cyanobacteria. Shown is the alignment and secondary structure diagram of Helix 837 in the 23S rDNA, with two RNA base pairs highlighted that represent synapomorphies of α-cyanobacterial clades to the exclusion of Paulinella and other prokaryotes. Sequence data and evolutionary changes are plotted on a simplified phylogram (NJ-bootstrap consensus tree). Pair 868/909 shows a uniquely derived CBC (compensatory base change: U-A → C-G) of all free-living α-cyanobacteria; the neighbouring pair 869/908 changed in the common ancestor of the marine PS-subclades (marine Synechococcus and Prochlorococcus) whereas the Cyanobium-clade and Paulinella are plesiomorphic. Pair 869/908 shows parallel changes in a few other cyanobacteria, (e.g. in Fischerella).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC1904183&req=5

Figure 2: Synapomorphy support in the 23S rRNA for the sister-group relationship between Paulinella and free-living α-cyanobacteria. Shown is the alignment and secondary structure diagram of Helix 837 in the 23S rDNA, with two RNA base pairs highlighted that represent synapomorphies of α-cyanobacterial clades to the exclusion of Paulinella and other prokaryotes. Sequence data and evolutionary changes are plotted on a simplified phylogram (NJ-bootstrap consensus tree). Pair 868/909 shows a uniquely derived CBC (compensatory base change: U-A → C-G) of all free-living α-cyanobacteria; the neighbouring pair 869/908 changed in the common ancestor of the marine PS-subclades (marine Synechococcus and Prochlorococcus) whereas the Cyanobium-clade and Paulinella are plesiomorphic. Pair 869/908 shows parallel changes in a few other cyanobacteria, (e.g. in Fischerella).
Mentions: Phylogenetic analyses revealed basal cyanobacterial branches (e.g. Gloeobacter), and two moderately supported lineages, one combining the majority of the β-cyanobacteria including all plastids (branch 1 in Figure 1), the other containing Paulinella and the PS-clade nested within a radiation of a few β-cyanobacteria, representing the clades PHOR, PRCHX and SELONG (branch 2 in Figure 1). Paulinella is monophyletic with the PS-clade (branch 4). Our previous study [1] had already revealed the monophyly of both marine PS-subclades to the exclusion of the Paulinella chromatophore, as confirmed here (see branch 9). The present investigation includes five sequences of the third PS-subclade, the Cyanobium-clade, which is sister to the marine subclades, with Paulinella still diverging in a basal position. The monophyly of the entire PS-clade to the exclusion of Paulinella, however, receives only moderate to low bootstrap support (branch 5), but is corroborated by unique synapomorphies in the 23S rRNA (Figure 2). As previously shown, both marine PS-subclades are characterized by unique compensatory base changes (CBCs in pairs 868/909 and 869/908), whereas Paulinella is plesiomorphic in both pairs [1]. Interestingly, the Cyanobium-clade is intermediate in sharing the unique CBC in position 868/909 with marine PS-subclades, but displaying the ancestral character state in positions 869/908, in congruence with the tree topology (Figure 2).

Bottom Line: Combined phylogenies using rbcL and the rDNA-operon resulted in a nearly fully resolved tree of the PS-clade.The gamma-proteobacterium Nitrococcus mobilis represents the closest known relative to the donor of the carboxysomal operon.The isolated position of the Paulinella chromatophore in molecular phylogenies as well as its elevated AT content suggests that the Paulinella chromatophore has already undergone typical steps in the reductive evolution of an endosymbiont.

View Article: PubMed Central - HTML - PubMed

Affiliation: Botanisches Institut, Lehrstuhl I, Universität zu Köln, Köln, Germany. birger.marin@uni-koeln.de

ABSTRACT

Background: Paulinella chromatophora is a freshwater filose amoeba with photosynthetic endosymbionts (chromatophores) of cyanobacterial origin that are closely related to free-living Prochlorococcus and Synechococcus species (PS-clade). Members of the PS-clade of cyanobacteria contain a proteobacterial form 1A RubisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase) that was acquired by horizontal gene transfer (HGT) of a carboxysomal operon. In rDNA-phylogenies, the Paulinella chromatophore diverged basal to the PS-clade, raising the question whether the HGT occurred before or after the split of the chromatophore ancestor.

Results: Phylogenetic analyses of the almost complete rDNA operon with an improved taxon sampling containing most known cyanobacterial lineages recovered the Paulinella chromatophore as sister to the complete PS-clade. The sequence of the complete carboxysomal operon of Paulinella was determined. Analysis of RubisCO large subunit (rbcL) sequences revealed that Paulinella shares the proteobacterial form 1A RubisCO with the PS-clade. The gamma-proteobacterium Nitrococcus mobilis was identified as sister of the Paulinella chromatophore and the PS-clade in the RubisCO phylogeny. Gene content and order in the carboxysomal operon correlates well with the RubisCO phylogeny demonstrating that the complete carboxysomal operon was acquired by the common ancestor of the Paulinella chromatophore and the PS-clade through HGT. The carboxysomal operon shows a significantly elevated AT content in Paulinella, which in the rbcL gene is confined to third codon positions. Combined phylogenies using rbcL and the rDNA-operon resulted in a nearly fully resolved tree of the PS-clade.

Conclusion: The HGT of the carboxysomal operon predated the divergence of the chromatophore ancestor from the PS-clade. Following HGT and divergence of the chromatophore ancestor, diversification of the PS-clade into at least three subclades occurred. The gamma-proteobacterium Nitrococcus mobilis represents the closest known relative to the donor of the carboxysomal operon. The isolated position of the Paulinella chromatophore in molecular phylogenies as well as its elevated AT content suggests that the Paulinella chromatophore has already undergone typical steps in the reductive evolution of an endosymbiont.

Show MeSH