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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

Bayesian posterior predictive simulations for assessing model fit to the key enzymes implicated in the ménage à trois.Posterior predictive simulations25 are a technique for assessing model adequacy with respect to key properties of the sequence alignment, which has an impact on phylogenetic inference. Here we compared the ability of the LG and CAT+GTR models to adequately capture the site-specific biochemical constraints experienced by the genes implicated in the ‘ménage à trois’ hypothesis. In sequence alignments, these constraints are manifest in the reduced number of amino acids observed in any one alignment column, which is usually much less than the theoretical maximum of 20. (a) The mean observed number of different amino acids per site in the GlgC alignment was 7.78. Data simulated under the LG model showed mean per-site diversity values (dot) much higher than the real data, suggesting this model did a poor job of modelling site-specific constraints. In contrast, the range (bars) of site-specific diversities predicted under the CAT+GTR model was comparable to that of the real data (P=0.33), suggesting adequate model fit with respect to this important metric. (b–d) The results for our analyses of GlgP, GlgX and UhpC were similar, with the CAT+GTR model better able to capture site-specific constraints, although neither model produced realistic predictions for the GlgP alignment. (e) Analyses of three different GlgA alignments under the CAT+GTR model. The original data set contained a large and highly diverse outgroup, leading to a high per-site diversity and poor model fit. An outgroup consisting only of the sequences most closely related to the relevant GlgA clade reduced per-site diversity and enabled adequate model fit; Dayhoff recoding of the original alignment also resulted in improved model fit relative to the unrecoded data. In both analyses in which adequate model fit was achieved, we did not recover a specific Chlamydiae/Archaeplastida clade, as discussed in the main text. Error bars represent s.e. and P-values were calculated using the ‘ppred’ and ‘readpb_mpi’ programmes in the PhyloBayes and PhyloBayes-MPI packages, respectively.
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f2: Bayesian posterior predictive simulations for assessing model fit to the key enzymes implicated in the ménage à trois.Posterior predictive simulations25 are a technique for assessing model adequacy with respect to key properties of the sequence alignment, which has an impact on phylogenetic inference. Here we compared the ability of the LG and CAT+GTR models to adequately capture the site-specific biochemical constraints experienced by the genes implicated in the ‘ménage à trois’ hypothesis. In sequence alignments, these constraints are manifest in the reduced number of amino acids observed in any one alignment column, which is usually much less than the theoretical maximum of 20. (a) The mean observed number of different amino acids per site in the GlgC alignment was 7.78. Data simulated under the LG model showed mean per-site diversity values (dot) much higher than the real data, suggesting this model did a poor job of modelling site-specific constraints. In contrast, the range (bars) of site-specific diversities predicted under the CAT+GTR model was comparable to that of the real data (P=0.33), suggesting adequate model fit with respect to this important metric. (b–d) The results for our analyses of GlgP, GlgX and UhpC were similar, with the CAT+GTR model better able to capture site-specific constraints, although neither model produced realistic predictions for the GlgP alignment. (e) Analyses of three different GlgA alignments under the CAT+GTR model. The original data set contained a large and highly diverse outgroup, leading to a high per-site diversity and poor model fit. An outgroup consisting only of the sequences most closely related to the relevant GlgA clade reduced per-site diversity and enabled adequate model fit; Dayhoff recoding of the original alignment also resulted in improved model fit relative to the unrecoded data. In both analyses in which adequate model fit was achieved, we did not recover a specific Chlamydiae/Archaeplastida clade, as discussed in the main text. Error bars represent s.e. and P-values were calculated using the ‘ppred’ and ‘readpb_mpi’ programmes in the PhyloBayes and PhyloBayes-MPI packages, respectively.

Mentions: Under the ménage à trois hypothesis, archaeplastidal GlgC, GlgA, GlgP and GlgX originated as chlamydial effectors whose coding sequences were later transferred to the host nucleus; as a consequence, their modern-day archaeplastidal homologues are expected to cluster within, or as the sister to, chlamydial genes in single gene trees. Published phylogenies of these genes have made use of the single-matrix substitution models JTT13, WAG141523 and LG16, which all share the simplifying assumptions that the process of evolution is homogeneous across the sites of the alignment and the branches of the tree. These assumptions are frequently violated by real molecular sequences, in which sequence composition, and by inference evolutionary process, often varies extensively in both of these dimensions. Violation of these assumptions results in poor model fit and can lead to phylogenetic artefacts such as long-branch attraction, in which fast-evolving sequences (long branches) cluster together irrespective of true historical relationships; as a result, analyses with poorly fitting models can potentially lead to the recovery of strongly supported but incorrect phylogenetic trees24. To evaluate whether the assumptions of single-matrix models are met by the enzymes key to the ménage à trois hypothesis, we performed posterior predictive simulations25 on alignments of GlgC, GlgX, GlgA, GlgP and UhpC under the LG model, which according to analyses using the model selection tool ProtTest 3.4 (ref. 26) was the best-fitting single-matrix model in all cases. Posterior predictive simulations provide a test of model adequacy by comparing the properties of data simulated under the model to the real alignment; significant compositional differences between the observed and simulated data suggest that the assumptions of the model are unrealistic for the data at hand. Our simulations indicated that all five alignments contained significant across-site and across-branch compositional variation that was not adequately accounted for by the single-matrix LG model (see Fig. 2 and Supplementary Table 1). These results suggested that LG provided an inadequate fit to the data with respect to sequence composition, raising the possibility that the resulting phylogenies might be affected by phylogenetic artefacts such as long-branch attraction and motivating the use of more complex models.


Plastid establishment did not require a chlamydial partner.

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

Bayesian posterior predictive simulations for assessing model fit to the key enzymes implicated in the ménage à trois.Posterior predictive simulations25 are a technique for assessing model adequacy with respect to key properties of the sequence alignment, which has an impact on phylogenetic inference. Here we compared the ability of the LG and CAT+GTR models to adequately capture the site-specific biochemical constraints experienced by the genes implicated in the ‘ménage à trois’ hypothesis. In sequence alignments, these constraints are manifest in the reduced number of amino acids observed in any one alignment column, which is usually much less than the theoretical maximum of 20. (a) The mean observed number of different amino acids per site in the GlgC alignment was 7.78. Data simulated under the LG model showed mean per-site diversity values (dot) much higher than the real data, suggesting this model did a poor job of modelling site-specific constraints. In contrast, the range (bars) of site-specific diversities predicted under the CAT+GTR model was comparable to that of the real data (P=0.33), suggesting adequate model fit with respect to this important metric. (b–d) The results for our analyses of GlgP, GlgX and UhpC were similar, with the CAT+GTR model better able to capture site-specific constraints, although neither model produced realistic predictions for the GlgP alignment. (e) Analyses of three different GlgA alignments under the CAT+GTR model. The original data set contained a large and highly diverse outgroup, leading to a high per-site diversity and poor model fit. An outgroup consisting only of the sequences most closely related to the relevant GlgA clade reduced per-site diversity and enabled adequate model fit; Dayhoff recoding of the original alignment also resulted in improved model fit relative to the unrecoded data. In both analyses in which adequate model fit was achieved, we did not recover a specific Chlamydiae/Archaeplastida clade, as discussed in the main text. Error bars represent s.e. and P-values were calculated using the ‘ppred’ and ‘readpb_mpi’ programmes in the PhyloBayes and PhyloBayes-MPI packages, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Bayesian posterior predictive simulations for assessing model fit to the key enzymes implicated in the ménage à trois.Posterior predictive simulations25 are a technique for assessing model adequacy with respect to key properties of the sequence alignment, which has an impact on phylogenetic inference. Here we compared the ability of the LG and CAT+GTR models to adequately capture the site-specific biochemical constraints experienced by the genes implicated in the ‘ménage à trois’ hypothesis. In sequence alignments, these constraints are manifest in the reduced number of amino acids observed in any one alignment column, which is usually much less than the theoretical maximum of 20. (a) The mean observed number of different amino acids per site in the GlgC alignment was 7.78. Data simulated under the LG model showed mean per-site diversity values (dot) much higher than the real data, suggesting this model did a poor job of modelling site-specific constraints. In contrast, the range (bars) of site-specific diversities predicted under the CAT+GTR model was comparable to that of the real data (P=0.33), suggesting adequate model fit with respect to this important metric. (b–d) The results for our analyses of GlgP, GlgX and UhpC were similar, with the CAT+GTR model better able to capture site-specific constraints, although neither model produced realistic predictions for the GlgP alignment. (e) Analyses of three different GlgA alignments under the CAT+GTR model. The original data set contained a large and highly diverse outgroup, leading to a high per-site diversity and poor model fit. An outgroup consisting only of the sequences most closely related to the relevant GlgA clade reduced per-site diversity and enabled adequate model fit; Dayhoff recoding of the original alignment also resulted in improved model fit relative to the unrecoded data. In both analyses in which adequate model fit was achieved, we did not recover a specific Chlamydiae/Archaeplastida clade, as discussed in the main text. Error bars represent s.e. and P-values were calculated using the ‘ppred’ and ‘readpb_mpi’ programmes in the PhyloBayes and PhyloBayes-MPI packages, respectively.
Mentions: Under the ménage à trois hypothesis, archaeplastidal GlgC, GlgA, GlgP and GlgX originated as chlamydial effectors whose coding sequences were later transferred to the host nucleus; as a consequence, their modern-day archaeplastidal homologues are expected to cluster within, or as the sister to, chlamydial genes in single gene trees. Published phylogenies of these genes have made use of the single-matrix substitution models JTT13, WAG141523 and LG16, which all share the simplifying assumptions that the process of evolution is homogeneous across the sites of the alignment and the branches of the tree. These assumptions are frequently violated by real molecular sequences, in which sequence composition, and by inference evolutionary process, often varies extensively in both of these dimensions. Violation of these assumptions results in poor model fit and can lead to phylogenetic artefacts such as long-branch attraction, in which fast-evolving sequences (long branches) cluster together irrespective of true historical relationships; as a result, analyses with poorly fitting models can potentially lead to the recovery of strongly supported but incorrect phylogenetic trees24. To evaluate whether the assumptions of single-matrix models are met by the enzymes key to the ménage à trois hypothesis, we performed posterior predictive simulations25 on alignments of GlgC, GlgX, GlgA, GlgP and UhpC under the LG model, which according to analyses using the model selection tool ProtTest 3.4 (ref. 26) was the best-fitting single-matrix model in all cases. Posterior predictive simulations provide a test of model adequacy by comparing the properties of data simulated under the model to the real alignment; significant compositional differences between the observed and simulated data suggest that the assumptions of the model are unrealistic for the data at hand. Our simulations indicated that all five alignments contained significant across-site and across-branch compositional variation that was not adequately accounted for by the single-matrix LG model (see Fig. 2 and Supplementary Table 1). These results suggested that LG provided an inadequate fit to the data with respect to sequence composition, raising the possibility that the resulting phylogenies might be affected by phylogenetic artefacts such as long-branch attraction and motivating the use of more complex models.

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