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Plastid establishment did not require a chlamydial partner.

Domman D, Horn M, Embley TM, Williams TA - Nat Commun (2015)

Bottom Line: One hypothesis that has achieved recent prominence suggests that the first role of the cyanobiont was in energy provision for a host cell whose reserves were being depleted by an intracellular chlamydial pathogen.A pivotal claim is that it was chlamydial proteins themselves that converted otherwise unusable cyanobacterial metabolites into host energy stores.We test this hypothesis by investigating the origins of the key enzymes using sophisticated phylogenetics.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Ecosystem Science, University of Vienna, A-1090 Vienna, Austria.

ABSTRACT
Primary plastids descend from the cyanobacterial endosymbiont of an ancient eukaryotic host, but the initial selective drivers that stabilized the association between these two cells are still unclear. One hypothesis that has achieved recent prominence suggests that the first role of the cyanobiont was in energy provision for a host cell whose reserves were being depleted by an intracellular chlamydial pathogen. A pivotal claim is that it was chlamydial proteins themselves that converted otherwise unusable cyanobacterial metabolites into host energy stores. We test this hypothesis by investigating the origins of the key enzymes using sophisticated phylogenetics. Here we show a mosaic origin for the relevant pathway combining genes with host, cyanobacterial or bacterial ancestry, but we detect no strong case for Chlamydiae to host transfer under the best-fitting models. Our conclusion is that there is no compelling evidence from gene trees that Chlamydiae played any role in establishing the primary plastid endosymbiosis.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic analyses of the glycogen synthase GlgA.(a) Inference under the CAT+GTR model recovers a weakly supported (PP=0.74) clade comprising the chlamydial and Archaeplastidal sequences, but does not support horizontal transfer from Chlamydiae to Archaeplastida. This alignment was unusually heterogeneous in terms of sequence composition, and the CAT+GTR model failed our posterior predictive test for across-site compositional heterogeneity (P=0). (b) Inclusion of only the closest outgroup sequences improved the fit of the CAT+GTR model and collapsed this relationship, recovering an in-group trichotomy between the sequences from Archaeplastida, Chlamydiae and other bacteria. (c) Analysis of the Dayhoff-recoded data set under the CAT+GTR model; Dayhoff recoding ameliorated the observed compositional heterogeneity and also failed to recover a specific Chlamydiae/Archaeplastida relationship. (d) Joint modelling of across-site and across-branch compositional variation using the non-stationary CAT+BP model, which also failed to recover a specific relationship. These panels represent sub-trees derived from larger analyses showing the portion of the tree containing the chlamydial and archaeplastidal sequences; the root positions indicated are based on the topology of the complete analyses. Support values are summarized as Bayesian posterior probabilities, and branch lengths are proportional to the expected number of substitutions per site.
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f4: Phylogenetic analyses of the glycogen synthase GlgA.(a) Inference under the CAT+GTR model recovers a weakly supported (PP=0.74) clade comprising the chlamydial and Archaeplastidal sequences, but does not support horizontal transfer from Chlamydiae to Archaeplastida. This alignment was unusually heterogeneous in terms of sequence composition, and the CAT+GTR model failed our posterior predictive test for across-site compositional heterogeneity (P=0). (b) Inclusion of only the closest outgroup sequences improved the fit of the CAT+GTR model and collapsed this relationship, recovering an in-group trichotomy between the sequences from Archaeplastida, Chlamydiae and other bacteria. (c) Analysis of the Dayhoff-recoded data set under the CAT+GTR model; Dayhoff recoding ameliorated the observed compositional heterogeneity and also failed to recover a specific Chlamydiae/Archaeplastida relationship. (d) Joint modelling of across-site and across-branch compositional variation using the non-stationary CAT+BP model, which also failed to recover a specific relationship. These panels represent sub-trees derived from larger analyses showing the portion of the tree containing the chlamydial and archaeplastidal sequences; the root positions indicated are based on the topology of the complete analyses. Support values are summarized as Bayesian posterior probabilities, and branch lengths are proportional to the expected number of substitutions per site.

Mentions: In the ménage à trois, the original role of the glycogen synthase GlgA is proposed to have been the incorporation of ADP-glucose generated by GlgC into host glycogen for later exploitation by the chlamydial pathogen. This enzyme would therefore have established the intial link between host and cyanobiont metabolism by providing a route for the incorporation of a bacterial metabolite (ADP-glucose) into host energy stores. In agreement with the recent analyses of Ball et al.16, a phylogeny inferred under the LG model provides moderate support (PP=0.83) for chlamydial ancestry of the archaeplastid sequences, although this model was rejected in our posterior predictive simulations both for across-site and across-branch compositional heterogeneity (P=0 for across-site compositional heterogeneity, P=0.002 for across-branch heterogeneity; see Supplementary Table 1). Indeed, the GlgA alignment proved to be extremely heterogeneous in both across-site and across-branch composition; unusually, even the most general substitution model currently available (CAT+GTR) failed to provide an adequate fit with respect to across-site compositional variation (P=0, see Fig. 2e and Supplementary Table 1). Although the tree inferred under CAT+GTR did not fit the data, it did weakly (PP=0.74) support a Chlamydiae plus Archaeplastida clade, consistent with horizontal exchange (Fig. 4a and Supplementary Fig. 5).


Plastid establishment did not require a chlamydial partner.

Domman D, Horn M, Embley TM, Williams TA - Nat Commun (2015)

Phylogenetic analyses of the glycogen synthase GlgA.(a) Inference under the CAT+GTR model recovers a weakly supported (PP=0.74) clade comprising the chlamydial and Archaeplastidal sequences, but does not support horizontal transfer from Chlamydiae to Archaeplastida. This alignment was unusually heterogeneous in terms of sequence composition, and the CAT+GTR model failed our posterior predictive test for across-site compositional heterogeneity (P=0). (b) Inclusion of only the closest outgroup sequences improved the fit of the CAT+GTR model and collapsed this relationship, recovering an in-group trichotomy between the sequences from Archaeplastida, Chlamydiae and other bacteria. (c) Analysis of the Dayhoff-recoded data set under the CAT+GTR model; Dayhoff recoding ameliorated the observed compositional heterogeneity and also failed to recover a specific Chlamydiae/Archaeplastida relationship. (d) Joint modelling of across-site and across-branch compositional variation using the non-stationary CAT+BP model, which also failed to recover a specific relationship. These panels represent sub-trees derived from larger analyses showing the portion of the tree containing the chlamydial and archaeplastidal sequences; the root positions indicated are based on the topology of the complete analyses. Support values are summarized as Bayesian posterior probabilities, and branch lengths are proportional to the expected number of substitutions per site.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4374161&req=5

f4: Phylogenetic analyses of the glycogen synthase GlgA.(a) Inference under the CAT+GTR model recovers a weakly supported (PP=0.74) clade comprising the chlamydial and Archaeplastidal sequences, but does not support horizontal transfer from Chlamydiae to Archaeplastida. This alignment was unusually heterogeneous in terms of sequence composition, and the CAT+GTR model failed our posterior predictive test for across-site compositional heterogeneity (P=0). (b) Inclusion of only the closest outgroup sequences improved the fit of the CAT+GTR model and collapsed this relationship, recovering an in-group trichotomy between the sequences from Archaeplastida, Chlamydiae and other bacteria. (c) Analysis of the Dayhoff-recoded data set under the CAT+GTR model; Dayhoff recoding ameliorated the observed compositional heterogeneity and also failed to recover a specific Chlamydiae/Archaeplastida relationship. (d) Joint modelling of across-site and across-branch compositional variation using the non-stationary CAT+BP model, which also failed to recover a specific relationship. These panels represent sub-trees derived from larger analyses showing the portion of the tree containing the chlamydial and archaeplastidal sequences; the root positions indicated are based on the topology of the complete analyses. Support values are summarized as Bayesian posterior probabilities, and branch lengths are proportional to the expected number of substitutions per site.
Mentions: In the ménage à trois, the original role of the glycogen synthase GlgA is proposed to have been the incorporation of ADP-glucose generated by GlgC into host glycogen for later exploitation by the chlamydial pathogen. This enzyme would therefore have established the intial link between host and cyanobiont metabolism by providing a route for the incorporation of a bacterial metabolite (ADP-glucose) into host energy stores. In agreement with the recent analyses of Ball et al.16, a phylogeny inferred under the LG model provides moderate support (PP=0.83) for chlamydial ancestry of the archaeplastid sequences, although this model was rejected in our posterior predictive simulations both for across-site and across-branch compositional heterogeneity (P=0 for across-site compositional heterogeneity, P=0.002 for across-branch heterogeneity; see Supplementary Table 1). Indeed, the GlgA alignment proved to be extremely heterogeneous in both across-site and across-branch composition; unusually, even the most general substitution model currently available (CAT+GTR) failed to provide an adequate fit with respect to across-site compositional variation (P=0, see Fig. 2e and Supplementary Table 1). Although the tree inferred under CAT+GTR did not fit the data, it did weakly (PP=0.74) support a Chlamydiae plus Archaeplastida clade, consistent with horizontal exchange (Fig. 4a and Supplementary Fig. 5).

Bottom Line: One hypothesis that has achieved recent prominence suggests that the first role of the cyanobiont was in energy provision for a host cell whose reserves were being depleted by an intracellular chlamydial pathogen.A pivotal claim is that it was chlamydial proteins themselves that converted otherwise unusable cyanobacterial metabolites into host energy stores.We test this hypothesis by investigating the origins of the key enzymes using sophisticated phylogenetics.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Ecosystem Science, University of Vienna, A-1090 Vienna, Austria.

ABSTRACT
Primary plastids descend from the cyanobacterial endosymbiont of an ancient eukaryotic host, but the initial selective drivers that stabilized the association between these two cells are still unclear. One hypothesis that has achieved recent prominence suggests that the first role of the cyanobiont was in energy provision for a host cell whose reserves were being depleted by an intracellular chlamydial pathogen. A pivotal claim is that it was chlamydial proteins themselves that converted otherwise unusable cyanobacterial metabolites into host energy stores. We test this hypothesis by investigating the origins of the key enzymes using sophisticated phylogenetics. Here we show a mosaic origin for the relevant pathway combining genes with host, cyanobacterial or bacterial ancestry, but we detect no strong case for Chlamydiae to host transfer under the best-fitting models. Our conclusion is that there is no compelling evidence from gene trees that Chlamydiae played any role in establishing the primary plastid endosymbiosis.

No MeSH data available.


Related in: MedlinePlus