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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

The evolutionary history of chlamydia–eukaryote interactions and the ménage à trois hypothesis for plastid establishment.Chlamydiae have probably been associated with eukaryotes for at least 700 million years (1717) so it appears reasonable to suggest that they also infected even more ancient eukaryotes. Extant Chlamydiae can infect a tremendously diverse range of eukaryotic hosts such as humans, cattle, pigs, birds, koala, fish, insects and unicellular protists. Notably, Chlamydiae have not been found infecting any member of the Archaeplastida. A proposed evolutionary scenario, coined the ‘ménage à trois’ hypothesis16, posits that an early eukaryotic cell was host to both a chlamydial and cyanobacterial partner. Key metabolic genes that enabled the symbiotic capture of the cyanobacterium are proposed to have been horizontally transferred from chlamydia primarily to the host, but also to the cyanobacterium. Once these genes were transferred, the chlamydial partner was no longer needed and was subsequently lost. The newly formed relationship between cyanobacterium and host led to the modern plastid and the evolution of Archaeplastida.
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f1: The evolutionary history of chlamydia–eukaryote interactions and the ménage à trois hypothesis for plastid establishment.Chlamydiae have probably been associated with eukaryotes for at least 700 million years (1717) so it appears reasonable to suggest that they also infected even more ancient eukaryotes. Extant Chlamydiae can infect a tremendously diverse range of eukaryotic hosts such as humans, cattle, pigs, birds, koala, fish, insects and unicellular protists. Notably, Chlamydiae have not been found infecting any member of the Archaeplastida. A proposed evolutionary scenario, coined the ‘ménage à trois’ hypothesis16, posits that an early eukaryotic cell was host to both a chlamydial and cyanobacterial partner. Key metabolic genes that enabled the symbiotic capture of the cyanobacterium are proposed to have been horizontally transferred from chlamydia primarily to the host, but also to the cyanobacterium. Once these genes were transferred, the chlamydial partner was no longer needed and was subsequently lost. The newly formed relationship between cyanobacterium and host led to the modern plastid and the evolution of Archaeplastida.

Mentions: Recently, a detailed, metabolically explicit hypothesis for the initial selective pressure driving endosymbiosis was proposed in which the heterotrophic host cell that engulfed the cyanobacterial endosymbiont was already infected with an ancient member of the Chlamydiae1213141516. In this ‘ménage à trois’16 (Fig. 1), named with reference to the proposed tripartite nature of the endosymbiosis, the chlamydial partner secreted a series of effectors that manipulated the host cell, rerouting host energy through glycogen metabolism for subsequent conversion to maltotetraose and import into the pathogen16. The proposed first step in this process was the conversion of host glucose-1-phosphate to the bacterial metabolite adenine diphosphoglucose (ADP-glucose) by the chlamydial effector GlgC; ADP-glucose was subsequently polymerized to glycogen and then processed for import by the pathogen through a series of downstream reactions catalysed by the effectors GlgA, GlgP and GlgX, all secreted by the pathogen into the host cytoplasm. In this scenario, an engulfed cyanobacterium could have provided immediate relief to the infected host cell through the provision of ADP-glucose generated as a byproduct of its own metabolism, preventing further depletion of host energy stores, that is, the energy sink represented by the chlamydial pathogen would provide the initial selective pressure for capture and retention of the cyanobiont. Although the immediate effect would have been to rescue the host cell, this tripartite metabolic interaction might also have potentiated the development of long-term endosymbiosis by establishing an initial metabolic link between host and cyanobiont, through the incorporation of cyanobacterial ADP-glucose into host glycogen stores.


Plastid establishment did not require a chlamydial partner.

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

The evolutionary history of chlamydia–eukaryote interactions and the ménage à trois hypothesis for plastid establishment.Chlamydiae have probably been associated with eukaryotes for at least 700 million years (1717) so it appears reasonable to suggest that they also infected even more ancient eukaryotes. Extant Chlamydiae can infect a tremendously diverse range of eukaryotic hosts such as humans, cattle, pigs, birds, koala, fish, insects and unicellular protists. Notably, Chlamydiae have not been found infecting any member of the Archaeplastida. A proposed evolutionary scenario, coined the ‘ménage à trois’ hypothesis16, posits that an early eukaryotic cell was host to both a chlamydial and cyanobacterial partner. Key metabolic genes that enabled the symbiotic capture of the cyanobacterium are proposed to have been horizontally transferred from chlamydia primarily to the host, but also to the cyanobacterium. Once these genes were transferred, the chlamydial partner was no longer needed and was subsequently lost. The newly formed relationship between cyanobacterium and host led to the modern plastid and the evolution of Archaeplastida.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: The evolutionary history of chlamydia–eukaryote interactions and the ménage à trois hypothesis for plastid establishment.Chlamydiae have probably been associated with eukaryotes for at least 700 million years (1717) so it appears reasonable to suggest that they also infected even more ancient eukaryotes. Extant Chlamydiae can infect a tremendously diverse range of eukaryotic hosts such as humans, cattle, pigs, birds, koala, fish, insects and unicellular protists. Notably, Chlamydiae have not been found infecting any member of the Archaeplastida. A proposed evolutionary scenario, coined the ‘ménage à trois’ hypothesis16, posits that an early eukaryotic cell was host to both a chlamydial and cyanobacterial partner. Key metabolic genes that enabled the symbiotic capture of the cyanobacterium are proposed to have been horizontally transferred from chlamydia primarily to the host, but also to the cyanobacterium. Once these genes were transferred, the chlamydial partner was no longer needed and was subsequently lost. The newly formed relationship between cyanobacterium and host led to the modern plastid and the evolution of Archaeplastida.
Mentions: Recently, a detailed, metabolically explicit hypothesis for the initial selective pressure driving endosymbiosis was proposed in which the heterotrophic host cell that engulfed the cyanobacterial endosymbiont was already infected with an ancient member of the Chlamydiae1213141516. In this ‘ménage à trois’16 (Fig. 1), named with reference to the proposed tripartite nature of the endosymbiosis, the chlamydial partner secreted a series of effectors that manipulated the host cell, rerouting host energy through glycogen metabolism for subsequent conversion to maltotetraose and import into the pathogen16. The proposed first step in this process was the conversion of host glucose-1-phosphate to the bacterial metabolite adenine diphosphoglucose (ADP-glucose) by the chlamydial effector GlgC; ADP-glucose was subsequently polymerized to glycogen and then processed for import by the pathogen through a series of downstream reactions catalysed by the effectors GlgA, GlgP and GlgX, all secreted by the pathogen into the host cytoplasm. In this scenario, an engulfed cyanobacterium could have provided immediate relief to the infected host cell through the provision of ADP-glucose generated as a byproduct of its own metabolism, preventing further depletion of host energy stores, that is, the energy sink represented by the chlamydial pathogen would provide the initial selective pressure for capture and retention of the cyanobiont. Although the immediate effect would have been to rescue the host cell, this tripartite metabolic interaction might also have potentiated the development of long-term endosymbiosis by establishing an initial metabolic link between host and cyanobiont, through the incorporation of cyanobacterial ADP-glucose into host glycogen stores.

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