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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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Maximum likelihood (RAxML) trees of Chlamydiae-derived genes in the Plantae.A) The tree of dimethyladenosine transferase (PFC1). B) The tree of queuine tRNA-ribosyltransferase. The results of a bootstrap analysis using RAxML are shown above the branches, whereas PHYML bootstrap support values are shown below the branches. Only bootstrap values ≥60% are shown. Branch lengths are proportional to the number of substitutions per site (see scale bars). Cyanobacteria are shown in blue text, green algae and land plants in green text, red algae in red, chromalveolates in brown, and Chamydiae in magenta. All other bacteria are shown in black text. The thick branches unite Chlamydiae and Plantae.
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pone-0002205-g002: Maximum likelihood (RAxML) trees of Chlamydiae-derived genes in the Plantae.A) The tree of dimethyladenosine transferase (PFC1). B) The tree of queuine tRNA-ribosyltransferase. The results of a bootstrap analysis using RAxML are shown above the branches, whereas PHYML bootstrap support values are shown below the branches. Only bootstrap values ≥60% are shown. Branch lengths are proportional to the number of substitutions per site (see scale bars). Cyanobacteria are shown in blue text, green algae and land plants in green text, red algae in red, chromalveolates in brown, and Chamydiae in magenta. All other bacteria are shown in black text. The thick branches unite Chlamydiae and Plantae.

Mentions: Examples of novel genes we found are shown in Figs. 2, 3, and 4. In Fig. 2A, we present the phylogeny of PFC1 (a plastid-targeted RNA methylase that is essential for low-temperature development of chloroplasts [35]) that shows a clear affiliation of green algae to Chlamydiae (RAxML bootstrap, RB = 80%, PHYML [36] bootstrap, PB = 84%) and this clade is sister to cyanobacteria (RB = 97%, PB = 87%). One possible explanation of cases with a cyanobacteria-Chlamydiae-Plantae connection is that Chlamydiae may be sister to or in the past exchanged genes with cyanobacteria (i.e., the plastid donor) and therefore their close relationship is a reflection of the bacterial tree rather than endosymbiotic gene transfer (EGT)/HGT from the former group (see [15] and [22] for a detailed discussion of this scenario). A different sort of topology is shown in Fig. 2B in which there are two types of queuine tRNA-ribosyltransferase genes (a tRNA-guanine transglycosylase; putatively mitochondrial targeted in algae and plants) in Plantae, one is putatively derived from cyanobacteria in chlorophytes (i.e., Chlamydomonas and Volvox) and another from Chlamydiae in red algae, chromalveolates, and prasinophytes (i.e., Ostreococcus spp.; PB, RB = 100%). This tree is likely explained by differential gene loss in green algae with red and prasinophyte algae retaining the Chlamydiae gene (that was subsequently transferred to chromalveolates via red or green algal secondary endosymbiosis) and green algae the cyanobacterial copy. A third example of the types of genes we found is glgA (glycogen synthase) that is shown in Fig. 3. This gene catalyzes starch synthesis and there are two gene copies in plants, one that is derived from Chlamydiae (specifically Candidatus Protochlamydia amoebophila UWE25; RB = 69%, PB = 75%) and another that is shared by many greens and is derived from an unknown prokaryotic source. Both genes function in the chloroplast. This is the second gene of chlamydial origin that is involved in a carbohydrate metabolic process (i.e., the first is the starch debranching enzyme ATISA3; Table 1). An interesting point about Fig. 3 is that it shows a specific relationship between UWE25 and Plantae (see also [22]). This environmental Chlamydiae species (symbiont in Acanthamoeba, [18]) was found to be sister to Plantae in 30/55 trees (Table S1) identifying it as the closest living relative in our data set of the endoparasite that donated the genes. Complete genomes from other environmental Chlamydiae are needed to more comprehensively address the issue of the potential gene donor(s) in Plantae. UWE25 is a member of ECL V clade of Chlamydiae [20] with a genome (2.4 Mb) that is twice the size of the more highly derived vertebrate pathogens and in contrast to the latter, retains a complete TCA cycle. UWE25 however, still encodes an ADP/ATP translocator and is presumably an endoparasite of Acanthamoeba [16]).


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

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

Maximum likelihood (RAxML) trees of Chlamydiae-derived genes in the Plantae.A) The tree of dimethyladenosine transferase (PFC1). B) The tree of queuine tRNA-ribosyltransferase. The results of a bootstrap analysis using RAxML are shown above the branches, whereas PHYML bootstrap support values are shown below the branches. Only bootstrap values ≥60% are shown. Branch lengths are proportional to the number of substitutions per site (see scale bars). Cyanobacteria are shown in blue text, green algae and land plants in green text, red algae in red, chromalveolates in brown, and Chamydiae in magenta. All other bacteria are shown in black text. The thick branches unite Chlamydiae and Plantae.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002205-g002: Maximum likelihood (RAxML) trees of Chlamydiae-derived genes in the Plantae.A) The tree of dimethyladenosine transferase (PFC1). B) The tree of queuine tRNA-ribosyltransferase. The results of a bootstrap analysis using RAxML are shown above the branches, whereas PHYML bootstrap support values are shown below the branches. Only bootstrap values ≥60% are shown. Branch lengths are proportional to the number of substitutions per site (see scale bars). Cyanobacteria are shown in blue text, green algae and land plants in green text, red algae in red, chromalveolates in brown, and Chamydiae in magenta. All other bacteria are shown in black text. The thick branches unite Chlamydiae and Plantae.
Mentions: Examples of novel genes we found are shown in Figs. 2, 3, and 4. In Fig. 2A, we present the phylogeny of PFC1 (a plastid-targeted RNA methylase that is essential for low-temperature development of chloroplasts [35]) that shows a clear affiliation of green algae to Chlamydiae (RAxML bootstrap, RB = 80%, PHYML [36] bootstrap, PB = 84%) and this clade is sister to cyanobacteria (RB = 97%, PB = 87%). One possible explanation of cases with a cyanobacteria-Chlamydiae-Plantae connection is that Chlamydiae may be sister to or in the past exchanged genes with cyanobacteria (i.e., the plastid donor) and therefore their close relationship is a reflection of the bacterial tree rather than endosymbiotic gene transfer (EGT)/HGT from the former group (see [15] and [22] for a detailed discussion of this scenario). A different sort of topology is shown in Fig. 2B in which there are two types of queuine tRNA-ribosyltransferase genes (a tRNA-guanine transglycosylase; putatively mitochondrial targeted in algae and plants) in Plantae, one is putatively derived from cyanobacteria in chlorophytes (i.e., Chlamydomonas and Volvox) and another from Chlamydiae in red algae, chromalveolates, and prasinophytes (i.e., Ostreococcus spp.; PB, RB = 100%). This tree is likely explained by differential gene loss in green algae with red and prasinophyte algae retaining the Chlamydiae gene (that was subsequently transferred to chromalveolates via red or green algal secondary endosymbiosis) and green algae the cyanobacterial copy. A third example of the types of genes we found is glgA (glycogen synthase) that is shown in Fig. 3. This gene catalyzes starch synthesis and there are two gene copies in plants, one that is derived from Chlamydiae (specifically Candidatus Protochlamydia amoebophila UWE25; RB = 69%, PB = 75%) and another that is shared by many greens and is derived from an unknown prokaryotic source. Both genes function in the chloroplast. This is the second gene of chlamydial origin that is involved in a carbohydrate metabolic process (i.e., the first is the starch debranching enzyme ATISA3; Table 1). An interesting point about Fig. 3 is that it shows a specific relationship between UWE25 and Plantae (see also [22]). This environmental Chlamydiae species (symbiont in Acanthamoeba, [18]) was found to be sister to Plantae in 30/55 trees (Table S1) identifying it as the closest living relative in our data set of the endoparasite that donated the genes. Complete genomes from other environmental Chlamydiae are needed to more comprehensively address the issue of the potential gene donor(s) in Plantae. UWE25 is a member of ECL V clade of Chlamydiae [20] with a genome (2.4 Mb) that is twice the size of the more highly derived vertebrate pathogens and in contrast to the latter, retains a complete TCA cycle. UWE25 however, still encodes an ADP/ATP translocator and is presumably an endoparasite of Acanthamoeba [16]).

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