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Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions.

Moustafa A, Reyes-Prieto A, Bhattacharya D - PLoS ONE (2008)

Bottom Line: The chlamydial gene distribution and protein tree topologies provide evidence for both endosymbiotic gene transfer and a horizontal gene transfer ratchet driven by recurrent endoparasitism as explanations for gene origin.Our findings paint a more complex picture of gene origin than can easily be explained by endosymbiotic gene transfer from an organelle-like point source.This strain, Candidatus Protochlamydia amoebophila UWE25 is an endosymbiont of Acanthamoeba and likely represents the type of endoparasite that contributed the genes to Plantae.

View Article: PubMed Central - PubMed

Affiliation: Interdisciplinary Program in Genetics, University of Iowa, Iowa City, Iowa, United States of America.

ABSTRACT

Background: The photosynthetic organelle (plastid) originated via primary endosymbiosis in which a phagotrophic protist captured and harnessed a cyanobacterium. The plastid was inherited by the common ancestor of the red, green (including land plants), and glaucophyte algae (together, the Plantae). Despite the critical importance of primary plastid endosymbiosis, its ancient derivation has left behind very few "footprints" of early key events in organelle genesis.

Methodology/principal findings: To gain insights into this process, we conducted an in-depth phylogenomic analysis of genomic data (nuclear proteins) from 17 Plantae species to identify genes of a surprising provenance in these taxa, Chlamydiae bacteria. Previous studies show that Chlamydiae contributed many genes (at least 21 in one study) to Plantae that primarily have plastid functions and were postulated to have played a fundamental role in organelle evolution. Using our comprehensive approach, we identify at least 55 Chlamydiae-derived genes in algae and plants, of which 67% (37/55) are putatively plastid targeted and at least 3 have mitochondrial functions. The remainder of the proteins does not contain a bioinformatically predicted organelle import signal although one has an N-terminal extension in comparison to the Chlamydiae homolog. Our data suggest that environmental Chlamydiae were significant contributors to early Plantae genomes that extend beyond plastid metabolism. The chlamydial gene distribution and protein tree topologies provide evidence for both endosymbiotic gene transfer and a horizontal gene transfer ratchet driven by recurrent endoparasitism as explanations for gene origin.

Conclusions/significance: Our findings paint a more complex picture of gene origin than can easily be explained by endosymbiotic gene transfer from an organelle-like point source. These data significantly extend the genomic impact of Chlamydiae on Plantae and show that about one-half (30/55) of the transferred genes are most closely related to sequences emanating from the genome of the only environmental isolate that is currently available. This strain, Candidatus Protochlamydia amoebophila UWE25 is an endosymbiont of Acanthamoeba and likely represents the type of endoparasite that contributed the genes to Plantae.

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Pie chart showing the distribution of Chlamydiae-like genes among Plantae and chromalveolates.
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pone-0002205-g001: Pie chart showing the distribution of Chlamydiae-like genes among Plantae and chromalveolates.

Mentions: Thirty-one of the Chlamydiae genes were present in the green algae plus plants clade (with or without chromalveolates) and 20 were shared by at least red and green algae, thereby suggesting their ancient origins in the Plantae (see Figure 1). An expanded list of protein characteristics is provided in Table S1 and the RAxML bootstrap trees are presented in Table S2. Our ability to identify a larger set of Chlamydiae genes than Huang and Gogarten [22] likely reflected the fact that we used the combined protein set from 17 Plantae genomes, thereby including as large a diversity of query sequences as possible. As also noted by Huang and Gogarten [22], C. merolae has a highly reduced nuclear genome (16.5 Mb; 5,331 genes [33]), therefore some genes (e.g., Fig. 1A, 1C) absent from this species could still be present in the “normal-sized” genomes of mesophilic green algae (e.g., Chlamydomonas reinhardtii, 120 Mb; >15,000 genes [34]) and plants. Consistent with this idea, 32 of the genes we found of Chlamydiae origin were undetected in red algae. Many of these genes may have been lost from the Cyanidiales, or diverged beyond detection using our bioinformatic pipeline, or are independent gains in the green lineage. More extensive data are needed from mesophilic red algae to address this issue. Currently we only had available partial EST data from non-Cyanidiales red algae.


Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions.

Moustafa A, Reyes-Prieto A, Bhattacharya D - PLoS ONE (2008)

Pie chart showing the distribution of Chlamydiae-like genes among Plantae and chromalveolates.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2376095&req=5

pone-0002205-g001: Pie chart showing the distribution of Chlamydiae-like genes among Plantae and chromalveolates.
Mentions: Thirty-one of the Chlamydiae genes were present in the green algae plus plants clade (with or without chromalveolates) and 20 were shared by at least red and green algae, thereby suggesting their ancient origins in the Plantae (see Figure 1). An expanded list of protein characteristics is provided in Table S1 and the RAxML bootstrap trees are presented in Table S2. Our ability to identify a larger set of Chlamydiae genes than Huang and Gogarten [22] likely reflected the fact that we used the combined protein set from 17 Plantae genomes, thereby including as large a diversity of query sequences as possible. As also noted by Huang and Gogarten [22], C. merolae has a highly reduced nuclear genome (16.5 Mb; 5,331 genes [33]), therefore some genes (e.g., Fig. 1A, 1C) absent from this species could still be present in the “normal-sized” genomes of mesophilic green algae (e.g., Chlamydomonas reinhardtii, 120 Mb; >15,000 genes [34]) and plants. Consistent with this idea, 32 of the genes we found of Chlamydiae origin were undetected in red algae. Many of these genes may have been lost from the Cyanidiales, or diverged beyond detection using our bioinformatic pipeline, or are independent gains in the green lineage. More extensive data are needed from mesophilic red algae to address this issue. Currently we only had available partial EST data from non-Cyanidiales red algae.

Bottom Line: The chlamydial gene distribution and protein tree topologies provide evidence for both endosymbiotic gene transfer and a horizontal gene transfer ratchet driven by recurrent endoparasitism as explanations for gene origin.Our findings paint a more complex picture of gene origin than can easily be explained by endosymbiotic gene transfer from an organelle-like point source.This strain, Candidatus Protochlamydia amoebophila UWE25 is an endosymbiont of Acanthamoeba and likely represents the type of endoparasite that contributed the genes to Plantae.

View Article: PubMed Central - PubMed

Affiliation: Interdisciplinary Program in Genetics, University of Iowa, Iowa City, Iowa, United States of America.

ABSTRACT

Background: The photosynthetic organelle (plastid) originated via primary endosymbiosis in which a phagotrophic protist captured and harnessed a cyanobacterium. The plastid was inherited by the common ancestor of the red, green (including land plants), and glaucophyte algae (together, the Plantae). Despite the critical importance of primary plastid endosymbiosis, its ancient derivation has left behind very few "footprints" of early key events in organelle genesis.

Methodology/principal findings: To gain insights into this process, we conducted an in-depth phylogenomic analysis of genomic data (nuclear proteins) from 17 Plantae species to identify genes of a surprising provenance in these taxa, Chlamydiae bacteria. Previous studies show that Chlamydiae contributed many genes (at least 21 in one study) to Plantae that primarily have plastid functions and were postulated to have played a fundamental role in organelle evolution. Using our comprehensive approach, we identify at least 55 Chlamydiae-derived genes in algae and plants, of which 67% (37/55) are putatively plastid targeted and at least 3 have mitochondrial functions. The remainder of the proteins does not contain a bioinformatically predicted organelle import signal although one has an N-terminal extension in comparison to the Chlamydiae homolog. Our data suggest that environmental Chlamydiae were significant contributors to early Plantae genomes that extend beyond plastid metabolism. The chlamydial gene distribution and protein tree topologies provide evidence for both endosymbiotic gene transfer and a horizontal gene transfer ratchet driven by recurrent endoparasitism as explanations for gene origin.

Conclusions/significance: Our findings paint a more complex picture of gene origin than can easily be explained by endosymbiotic gene transfer from an organelle-like point source. These data significantly extend the genomic impact of Chlamydiae on Plantae and show that about one-half (30/55) of the transferred genes are most closely related to sequences emanating from the genome of the only environmental isolate that is currently available. This strain, Candidatus Protochlamydia amoebophila UWE25 is an endosymbiont of Acanthamoeba and likely represents the type of endoparasite that contributed the genes to Plantae.

Show MeSH
Related in: MedlinePlus