Plant Chlamydia relationships
Introduction
Back in the late 1960s as a raw Microbiology undergraduate, the early
theories relating bacteria to the evolution of subcellular organelles in
eukaryotes intrigued me. As the chlamydial genome was unravelled, it was
fascinating to find that chlamydiae had a large number of "plant-like" genes,
most of them associated with the plastid (chloroplast), the powerhouse of
photosynthesis on which human life itself depends. At the time I wrote the first
part of this article in 2002 and 2003, it was thought that chlamydiae and
cyanobacteria might share an ancestral relationship. Some of the evidence for
that is summarised in the original article, which I have chosen to leave
unrevised. Since then much more genomic data have become available, most notably
for an environmental Protochlamydia endosymbiotic in amoebae and for the
extremophilic red
alga Cyanidioschyzon merolae. In updating the original, I have
focussed on a milestone paper published in 2007 in which Jinling Huang and
Johann Gogarten argue that chlamydial endosymbiosis played a crucial role in the
establishment of primary plastids from cyanobacteria. This view is supported by
further work from the Bhattacharya group.
[MEW] February 2008
Part 1: August 2003 original: Chloroplasts
One of the most unexpected findings of the genome sequencing
of the Chlamydiaceae was the relatively high proportion of genes with highest
similarity to plant gene sequences [Stephens et al., 1998]. It
was suggested
that a Chlamydia ancestor might have acquired such genes from a plant or
plant-like amoebal host by horizontal gene transfer [Royo et
al., 2000; Stephens et al., 1998; Wolf
et al., 1999; see: last common ancestor]. Such a process would be facilitated by the intimate
association between Chlamydiaceae and their host cells. Brinkman
et al., 2002 developed software
tools to detect bacterial proteins which were more similar in their primary
sequence to eukaryotic proteins than to other bacterial or archaeal proteins
(and vice versa). They found that 65% of bacterial proteins identified with the
highest similarity to a eukaryotic protein involved Chlamydia, Chlamydophila,
Synechocystis, or Rickettsia, even though these organisms only
accounted for 14% of the genes analysed.
The associations with Rickettsia and
Synechocystis were not surprising. As long ago as 1885
Schimper suggested that chloroplasts were derived from symbiotic microorganisms,
while Mereschkowsky in 1905 argued
persuasively that chloroplasts developed from
different types of cyanobacteria. This whole concept of the endosymbiotic origin of
life has been vigorously championed by Margulis, [see Margulis
1981] and the evidence for it is now regarded as overwhelming [Archibald
& Keeling, 2002]. Mitochondria, the energy generators of our own cells, are
thought to be the end result of symbiosis between an intracellular bacterium
having an ancestral relationship to Rickettsia and a host eukaryote [Andersson et al., 1998]. Similarly land plants are thought to be the beneficiaries of a second
symbiosis between an ancestral blue green bacterium (cyanobacterium) related to Synechocystis
and a mitochondria-bearing host which eventually yielded the light harvesting
chloroplast characteristic of green plants [Reumann &
Keegstra, 1999]. It is thought most of these genes were transferred from the endosymbiotic bacterium to the host nucleus during the transition of
endosymbiont to organelle [Gray 1992; Martin
et al., 2002] but many genes of prokaryotic origin remain in the
eukaryotic nucleus [Martin et al., 2002]. Indeed the
estimated 4,500 cyanobacterial genes in the Arabidopsis genome is
approximately 1000 more genes than is present in the Synechocystis genome [Archibald
& Keeling, 2003]. As
Palenik, 2002 wittily put it, the hosts keep both the baby and
the bath water. Nevertheless, the number of
plant-like genes in the Chlamydiaceae genomes is puzzling as the Chlamydiaceae have no
known relationship with any eukaryotic organelle. Moreover, although
recombination events may occur within strains of C. trachomatis [Hayes
et al., 1994; see
recombination in MOMP] horizontal gene transfer outside the Chlamydiales
seems unlikely given both the high degree of conservation across known
chlamydial genomic sequences [Read et al., 2000] and
the fact that the Chlamydiaceae have a notably lower variance in the Guanine + Cytosine ratio for
their genes than is
observed for the genome of any other microbe sequenced to date [Brinkman
et al., 2002]. This apparently clonal nature
of Chlamydia and lack of horizontal gene transfer may be due to their
ecological isolation as a result of imprisonment in the inclusion vacuole [Read
et al., 2000]. Significantly, the apparent lack of horizontal
gene transfer involving Chlamydia indicates that chlamydiae
may be a useful model for studies of gene evolutionary rates [Jordan
et al., 2001] or for determining
to what degree factors other than horizontal gene transfer can affect certain
genomic properties [Brinkman et al., 2002].
The vast majority of plant-like genes in the Chlamydiaceae are
related to chloroplast gene sequences [Brinkman et al.,
2002]. This might be due either to the acquisition of chloroplast related
genes which we have seen is unlikely, or to a
closer than suspected relationship with the ancestral cyanobacteria which
themselves gave rise to Synechocystis and chloroplasts. It has previously
been suggested that Synechocystis and the family Chlamydiaceae
form sister groups [Nelson et al., 2000], though not
with a high level of confidence. Analysis of an unspliced group I
intron in 23S rRNA also supported a possible link between the Chlamydiaceae
and the chloroplast lineage [Everett et al., 1999].
Following analysis of multiple bacterial and chloroplast genes and genomes,
Brinkman et al., 2002 concluded that there is a
substantial relationship between the Chlamydiaceae and cyanobacterial/chloroplast lineages.
It was suggested that the high proportion of plant-like
genes in the Chlamydiaceae is a reflection of an ancient, ancestral
relationship between the Chlamydiaceae and the cyanobacterial ancestor of the
chloroplast [Brinkman et al., 2002].
Clearly organellar ancestry must be considered in any case where a eukaryotic gene
shares higher-than-expected similarity to bacterial homologues. But why should
the Chlamydiaceae and other bacteria contain genes with notable sequence
similarity with organellar genes when there are other species, such as Synechocystis
and Rickettsia, with an even closer relationship with organellar ancestors? Firstly,
Brinkman et al., 2002 showed that the number of
eukaryotic organelle-related genes in the Chlamydiaceae is far lower than
in cyanobacterial or rickettsial genomes. Secondly, the effects of gene
loss on bacterial genome evolution have to be considered. Thus, Synechocystis
might have lost a gene that is still present in Chlamydiaceae and
the chloroplast, making the chlamydial gene appear most similar to the
chloroplast. Given that the analysis was
based on a single completed cyanobacterial genome and that most cases of plant-Chlamydiaceae gene-similarity lacked a
Synechocystis
homologue for comparison [Brinkman et al., 2002] this
seems quite likely. These isolated cases (far fewer than the number of cases of
Synechocystis genes resembling chloroplast genes) probably reflect gene loss in
the Synechocystis lineage. Thus, existing knowledge of cyanobacteria, to which the Chlamydiaceae
appear related, may stimulate new ways of thinking about the
function and control of pathogenic chlamydiae [Brinkman et al., 2002
]. However the finding of environmental chlamydia - like phylotypes in the plant
rhizosphere [Schmalenberger & Tebbe, 2002] indicates other possible mechanisms
by which environmental chlamydiae might acquire plant genes.
[MEW comment: Conversely,
because of obligate intracellular parasitism, genomic degradation must be far
more extensive in chlamydiae than in Synechocystis; see:
genomic degradation.
It is possible that some of the plant genes currently considered as
cyanobacterial might be more closely related to genes of the
last common chlamydial ancestor. Interestingly the
Glaucocystophyte algae, which have a primary prokaryote-derived plastid, are the
only algae to retain vestiges of characteristically bacterial
peptidoglycan in their chloroplast; Archibald & Keeling, 2002].
CMP-KDO Synthetase
The eight-carbon acid sugar 3-deoxy-D-manno-octulosonate
(KDO) is an essential component of the endotoxic lipopolysaccharide or,
occasionally, capsular polysaccharide found on the outer surface of
Gram-negative bacteria. However, it has recently been realised that this sugar
is also present in the cell wall polysaccharides of green algae and in the
pectin component of the cell walls of higher plants. A key enzyme in the
synthesis of KDO is CMP-KDO synthetase, without which KDO cannot be incorporated
into cell wall polymers. Royo et al., 2000 identified a
maize gene which encodes a protein analogous to CMP-KDO synthetase.
Phylogenetic analysis of genes in prokaryotic gene databases indicated that
chlamydial CMP-KDO synthetase is most closely related to this plant gene. Two
explanations are offered for this observation.
- The endosymbiont hypothesis suggests eukaryotes were
derived from the association of an archaea-like host with eubacteria.
Subsequently, a number of genes from the endosymbionts were transferred to the
host genome. Neither Rickettsiae (mitochondria) nor Synechocystis
(chloroplasts) encode CMP-KDO synthetase; thus the plant CMP-KDO genes could
only originate from the endosymbiont precursor of mitochondria. It is
suggested that the eukaryotic lineage leading to animals and yeast lost the
gene because it was of no advantage, whereas it was retained in plants because
the sugar KDO became a component of their extracellular polysaccharides.
- Horizontal transfer of the gene encoding CMP-KDO synthetase
from a chlamydial ancestor to the plant. This must have occurred soon after
the separation of the plant lineage from other eukaryotes since the gene is
present in every major plant group. However, as argued in the previous
section, horizontal gene transfer to chlamydiae is considered to be rare.
At the present time the significance of this intriguing
observation is unclear. As Royo et al., 2000 suggest,
analysis of the plant genes coding for other enzymes of the KDO synthetic
pathway may help interpretation of the evolutionary significance of this
finding.
[MEW] August 2003
Part 2: Update Feb 2008
The evolutionary history of the chloroplast (plastid) unfolded over a billion
years ago, when a previously non-photosynthetic protist engulfed and
subsequently maintained a free-living cyanobacterium in its cytoplasm.
Chloroplasts allowed the evolution of algae and the plants that form the base of
the food chain for most of the ecosystems on planet Earth. For this symbiosis to
have survived, it is clear the host must early on have derived some advantage,
such as integration of the host and parasite metabolic systems. Completion of the relatively primitive environmental Protochlamydia
genome and the genome for a red green alga, Cyanidioschyzon merolae has thrown additional insight onto
how this evolutionary process may have occurred.
It has
already been remarked that an unexpected number of chlamydial genes are most
similar to plant homologues and, interestingly, often contain a plastid-targeting
signal. This might be accounted for by gene transfer between chlamydiae and
plant-related groups and an ancestral relationship between chlamydiae and
cyanobacteria, which are thought to be the primitive ancestors of
photosynthesis. Huang & Gogarten (2007) conducted phylogenomic
analyses of the red alga Cyanidioschyzon merolae genomic sequence to identify genes
specifically related to chlamydial homologues. Among the 4771 predicted protein
coding genes of the alga, using strict criteria, 16 of these were probably
Chlamydiales-related genes of which 14 were also found in green plants. Most
of these genes were related to plastids. 5 other previously reported genes from
green plants were reclassified as probably Chlamydiales-related.
Chlamydiales-like genes were present in all primary photosynthetic
eukaryotic lineages examined including a glycophyte, euglenids, a diatom and a
haptophyte. Further, a Chlamydiales-like ADP/ATP translocase has been
retained in at least some secondary photsynthetic groups also (i.e. eukaryotic
lineages that emerged by engulfing another algal cell as endosymbiont). Not
surprisingly, the Chlamydiales-related genes were most similar to those
of the environmental Protochlamydia which are found in amoebae.
As discussed earlier, it was originally thought that chlamydiae might have
acquired their plant-related genes by transfer from plants. However most of
these genes are predominantly distributed in bacteria, suggesting that the
reverse might be the case. However the picture is made complex by a lack of data
and because of probable gene loss during evolution. Plastid to chlamydiae
transfer implies a cyanobacterial origin for the transferred genes, but this
does not explain why for many of the genes there is a strong relationship of
chlamydiae-like genes to the Protochlamydia homologues (eg Fig 1a). It is
also incompatible with the fact that the cyanobacterial homologues form a
distinct group (eg Fig 1b). This is unexpected since, as plastids are believed
to be of cyanobacterial origin, it would be normally expected that any gene
acquired from plastids by chlamydiae should be more closely related to
cyanobacteria than to other bacterial sequences. Moreover 5 of the
Chlamydiales-like genes in photosynthetic eukaryotes lacked identifiable
cyanobacterial homologues. Thus it was considered more likely that the majority
of these Chlamydiales-like genes were probably transferred from
(presumably aquatic) Chlamydiales to primary photosynthetic eukaryotes.
Fig 1. Example genes of plastidic and chlamydial origin.
|
 |
 |
| Figure 1. (Double click to enlarge the
thumbnails). Primary photosynthetic eukaryotes contain gene copies of
both plastidic and chlamydial origin. Figures above the branch show
bootstrap values for maximum likelihood and distance analyses
respectively. Asterisks indicate values <50%. (a) gcpE
diphosphate synthetase. Sequences from red algae and glaucophytes are of
plastidic origin whereas those from green plants, apicomplexans,
haptophytes and chlorarachniophytes are of chlamydial origin. |
(b) Enoyl-ACP reductase (fabl).
Here sequences from green plants, diatoms, chlorarachniophytes and
apicomplexans form a strongly supported group whereas cyanobacterial and
red alga Cyanidoschyzon homologues form another distinct group. The
colours represent different phylogenetic affiliations. These figures
reproduced by kind permission from the paper of Huang and
Gogarten, 2007. |
The results exemplified in Fig 1 raise the question as to whether there is an
ancestral relationship between the Chlamydiales and the Cyanobacteria?
Although this has been postulated, it has not been rigorously tested. If
chlamydiae and cyanobacteria shared a common ancestor then it would be expected
that sequences of a plastidic nature would have a stronger relationship to
cyanobacteria, which with the exception of the genes in Fig 1, is usually not
the case. Huang and Gogarten (2007) discuss the issue at
length and conclude that chlamydiae and cyanobacteria are not ancestrally
related. Chlamydial genes might have been transferred to the cyanobacterial
progenitor of plastids, perhaps being transferred from plastids to the nucleus
of photosynthetic eukaryotes. This was considered unlikely as thus far no
chlamydiae-like genes have been found in extant cyanobacteria. The presence of
chlamydiae-like genes in red algae and glaucophytes, which are not food sources
for insects, makes participation of an insector vector of chlamydial gene
transfer to these plants also unlikely while also contradicting the molecular
and fossil record.
The high number of genes transferred between chlamydiae and photosynthetic
eukaryotes implies that there was a stable association of these two groups in
the past. Symbiosis is the most likely explanation given that all known
chlamydiae are obligate endosymbionts of eukaryotic cells. Huang
and Gogarten (2007) therefore proposed that the Chlamydiales-like
genes in plants arose as an ancient chlamydial endosymbiosis with the ancestral primary
photosynthetic eukaryote. They suggest that three organisms were involved
in establishing the primary photosynthetic lineage: the eukaryotic host cell, a
cyanobacterial endosymbiont that provided photosynthetic capability, and a
chlamydial endosymbiont or parasite that facilitated the establishment of the
cyanobacterial endosymbiont. The complex interactions that may have been
necessary to establish the primary endosymbiotic relationship between plastid
and host cytoplasms, and thereby explaining the rarity with which long-term
successful endosymbiotic relationships between heterotrophs and photoautotrophs
were established, are illustrated in Figure 2.
Fig 2. Hypothetical stages showing the involvement of chlamydiae in
the origin and establishment of plastids. From Huang and Gogarten
(2007) and reproduced by kind permission of Jinling Huang.
|
 |
(A). The initial target
was a mitochondrion-containing eukaryote. The mitochondrion, of alpha-proteobacterial
origin, is shown in white. |
|
 |
(B). A Chlamydiales
bacterium (yellow), similar to the extant Protochlamydia, entered
as a bacterial parasite but became transiently symbiotic. It had the
metabolic capability to gain nutrients from the host cell. By chance a
once free-living photoautotrophic cyanobacterium (green) was captured by
the cell, perhaps ingested as food. The arrows indicate which of the
symbiotic partners received benefit. Gene transfer occurred between the
chlamydiae and host because of proximity. The host acquired transporters
from the chlamydiae facilitating communication with the cyanobacterial
captive. Dashed lines indicate direction of intracellular transfer
whereas solid lines show protein targeting of the transferred genes. |
|
 |
(C). Gene transfer
occurred between the cyanobacterium and host cell. The cyanobacterial
captive gradually transformed into a photosynthetic organelle (a
plastid) which provided product to the host. In turn from the host it
gained shelter, metabolites and transported protein products of the
transferred genes originating from the chlamydiae and the cyanobacteria. |
|
 |
(D). With the plastid
established, the chlamydial endosymbiont became less important to the
host. It may have reverted to being primarily a bacterial parasite. |
|
 |
(E). The chlamydial
parasitism could not be indefinitely sustained, leading to its
degeneration. Crosses indicate chlamydial endosymbiont and gene transfer
processes that might not exist in extant photosynthetic eukaryotes. It
is possible that the chlamydial parasite became an as yet unrecognised
organelle in photosynthetic eukaryotes. |
The work of Huang and Gogarten (2007) provides strong
support for a common origin of all primary photosynthetic eukaryotes and of the
plastids they harbour. It is the most satisfying explanation to date for
the anomalous presence of such large numbers of plant gene homologues in
chlamydiae and is consistent with current theories on the evolution of plastids
from cyanobacteria, see
Nozaki, 2005.
Note added 7/2/2008: I am grateful to Danielle Corsaro who, via the
contact form, drew my attention to the
paper of Tyra et al., 20007. These authors postulated
that the re-targeting of existing host solute transporters to the plastid
fore-runner must have been crucial for the early success of the primary
endosymbiosis, allowing the host to harvest endosymbiont primary metabolic production.
Accordingly they conducted a comprehensive analysis of the plastid permeome in
the brassica, Arabidopsis thaliana, (Thale Cress) the first higher
plant to have its genome sequenced. Of 137 well-annotated transporter
proteins that were initially considered, 83 that are broadly distributed in
plants were submitted to phylogenetic analysis. The results indicated that 58%
of Arabidopsis transporters, including all carbohydrate transporters,
were of host origin, whereas only 12% arose from the cyanobacterial
endosymbiont. However, four transporter genes were derived from a
Chlamydiales-like source (2 of which are shown below), suggesting that establishment of the primary
plastid likely involved contributions from at least two prokaryotic
sources. This therefore supports the hypothesis of Huang and Gogarten
(2007) that important contributions in the evolution of the chloroplast came
from the cyanobacterial endosymbiont and Protochlamydia-like bacteria
co-resident in the first algae.
Fig 3. Phyllogeny of two plastid targeted solute transporters of
putative "Chlamydia-like" origin in plants.
|
 |
 |
| Fig 3 (a). ADP/ATP translocase. The
different photosynthetic groups are coloured: blue-cyanobacteria,
red-red algae, green-green algae and land plants, magenta-glaucophytes,
brown-chromalveolates. |
Fig 3 (b). As 3 (a).
Heavy metal ATPase (HMA1) copper transporter.
Figure 3 reproduced from Tyra et al., 2007. |
[MEW] February 2008
NEXT:
Evolution Index
Main
Index Biology Index
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