Horizontal Gene Transfer of Chlamydial-Like tRNA Genes into
Early Vascular Plant Mitochondria
Nils Knie,1 Monika Polsakiewicz,1 and Volker Knoop*,1
1
Abteilung Molekulare Evolution, Institut f€ur Zellul€are und Molekulare Botanik, Universit€at Bonn, Bonn, Germany
*Corresponding author: E-mail: [email protected].
Associate editor: Andrew Roger
Abstract
Mitochondrial genomes of lycophytes are surprisingly diverse, including strikingly different transfer RNA (tRNA) gene
complements: No mitochondrial tRNA genes are present in the spikemoss Selaginella moellendorffii, whereas 26 tRNAs
are encoded in the chondrome of the clubmoss Huperzia squarrosa. Reinvestigating the latter we found that trnL(gag)
and trnS(gga) had never before been identified in any other land plant mitochondrial DNA. Sensitive sequence comparisons showed these two tRNAs as well as trnN(guu) and trnS(gcu) to be very similar to their respective counterparts in
chlamydial bacteria. We identified homologs of these chlamydial-type tRNAs also in other lycophyte, fern, and gymnosperm DNAs, suggesting horizontal gene transfer (HGT) into mitochondria in the early vascular plant stem lineages.
These findings extend plant mitochondrial HGT to affect individual tRNA genes, to include bacterial donors, and suggest
that Chlamydiae on top of their recently proposed key role in primary chloroplast establishment may also have participated in early tracheophyte genome evolution.
Key words: Chlamydiae, horizontal gene transfer (HGT), mitochondrial tRNA genes, lycophytes, monilophytes, gymnosperms, Class II tRNAs.
independent tRNA gene losses in other lineages in the light
of a modern understanding of plant phylogeny (Qiu et al.
2006), a scenario which appeared very unlikely to us.
Initially, two tRNA genes in the H. squarrosa mtDNA
caught our attention in particular: trnL(gag) and trnS(gga).
A mitochondrial trnL(gag) gene had never before been reported for the land plant (embryophyte) lineage but had only
sporadically been observed before in distant algae (fig. 1). A
mitochondrial trnS(gga) gene tracing back to the original
-proteobacterial endosymbiont that gave rise to mitochondria has, to our knowledge, in fact never before been reported
for any plant sensu lato (Viridiplantae) mitochondrial
genome. In fact, trnS(gga) homologs are also rare among protist mtDNAs. The orphan trnS(gga) in the mtDNA of the
protist Naegleria gruberi (Gray et al. 2004) is a unique conversion of a cognate trnS(uga), whereas the trnS(gga) genes in
Andalucia godoyi and Seculamonas ecuadoriensis (Burger et al.
2013) and in Tsukubamonas globosa (Kamikawa et al. 2014)
are as yet of unclear origin. The trnS(gga) genes present in
flowering plant mtDNAs in contrast are promiscuous copies
of their chloroplast counterparts (see Knoop 2012).
To exclude potential artifacts of the H. squarrosa mitochondrial genome assembly, we first strived to retrieve homologous sequences from independent biological material of
this and three further related species of the Lycopodiaceae
available in our laboratory (H. selago, H. megastachys, and H.
hippuris) through polymerase chain reaction (PCR). We easily
obtained the corresponding trnL(gag) and trnS(gga) loci from
these taxa, whereas control amplification attempts failed for
other plant nucleic acids included as negative controls.
Cloning and sequencing perfectly confirmed conservation
ß The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please
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Mol. Biol. Evol. 32(3):629–634 doi:10.1093/molbev/msu324 Advance Access publication November 20, 2014
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Letter
Extant lycophytes (club mosses, quillworts, and spike mosses)
represent the most ancient surviving lineage of early vascular
plants with an origin dating back to Devonian times more
than 400 Ma. Their common names are misleading given that
lycophytes do not belong to bryophytes, or mosses in particular, but are true vascular plants, tracheophytes. The evolutionary innovation of long-distance water-conducting tissue
in tracheophytes gave rise to one of the most dramatic
changes of the biosphere on our planet. Concomitantly, the
ancestral bryophyte lifestyle dominated by a haploid gametophyte growth-phase changed to a plant life-cycle dominated by the diploid sporophyte generation. Surprisingly,
these evolutionary transitions were accompanied by major
changes in the mitochondrial DNA (mtDNA) as recently documented with the first completely determined mitochondrial
genome sequences of the quillwort Isoetes engelmannii
(Grewe et al. 2009), the spikemoss Selaginella moellendorffii
(Hecht et al. 2011), and the club moss Huperzia squarrosa (Liu
et al. 2012). In essence, the Isoetes and Selaginella mtDNAs are
characterized by extensive mitochondrial genome recombination, trans-splicing introns and frequent endosymbiotic
gene transfer also characteristic of flowering plants. In contrast, the Huperzia mtDNA turned out to be much more
conservative in evolution, even retaining numerous ancient
bryophyte mitochondrial gene syntenies (Liu et al. 2012;
Knoop 2013). One of the most surprising discrepancies
among the lycophyte mtDNAs is the particularly large set
of 26 transfer RNA (tRNA) genes in H. squarrosa, which contrasts their complete absence in S. moellendorffii. Notably, to
account for some of the tRNA genes present in the H. squarrosa mtDNA one would have to postulate numerous
Knie et al. . doi:10.1093/molbev/msu324
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FIG. 1. Native mitochondrial (mt) genes for trnL(gag) and trnS(gga) tracing back to the -proteobacterial endosymbiont are entirely unknown in the
completely sequenced mtDNAs (bold) of embryophytes (E). Native mitochondrial trnN(guu) and trnS(gcu) genes are present in liverworts but were
obviously lost in the stem lineage of all other embryophytes (). The presence of these four tRNA genes in early vascular plant mtDNAs as reported
here is parsimoniously explained by a gain through HGT from chlamydial bacteria (CHLAM) in the tracheophyte stem lineage (node label 1).
Alternatively, trnS(gcu) may have been gained exclusively in the lycophyte stem lineage (node label 2) and trnS(gga) exclusively in the
Lycopodiaceae stem lineage (node label 3). Flowering plants or seed plants, respectively, carry chloroplast (CP) copies of trnN(guu) and trnS(gga) in
their mtDNAs. The superscript (a) indicates that a chlamydial-like trnS(gga) pseudogene coexists in the Cycas taitungensis mtDNA (see supplementary
fig. S3, Supplementary Material online). Chlamydial-type trnN(ggu) and trnL(gag) sequences were also detected in monilophyte and gymnosperm taxa
as described in the text. None of the four tRNAs is present in hornwort or moss chondromes, very recently also further corroborated by 12 additional
complete moss mtDNAs sequences of wide taxon sampling (Liu et al. 2014).
of both tRNA identities among Lycopodiaceae (fig. 2 and
supplementary fig. S1, Supplementary Material online).
Based on the current insights on plant phylogeny (fig. 1)
and assuming that these tRNA genes trace back to the original endosymbiont, the presence of trnL(gag) and trnS(gga)
tRNA genes in Lycopodiaceae would imply numerous independent losses from mtDNAs among Viridiplantae alone (in
several Chlorophytes as well as in Mesostigma, Chlorokybus,
Chaetosphaeridium, Charales, Liverworts, Mosses and
Hornworts, Isoetales, and Euphyllophytes), obviously a
nonparsimonious scenario. We used the Lycopodiaceae
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tRNA sequences for sensitive BLASTN searches (word
size = 7 and experimentally variable matching and gapping
parameters). These searches conclusively revealed top similarity hits (i.e., random similarity probabilities consistently
below expectancies of 10 10) for trnL(gag) and trnS(gga)
among the homologous genes of Chlamydiae, with top
scores most frequently in the recently determined genomes
of three chlamydial bacteria genera (Parachlamydia,
Simkania, and Waddlia), here further referred to as “PSWChlamydiae,” which are distinctly set apart from the wellknown Chlamydia/Chlamydophila clade of human and
Chlamydial tRNAs in tracheophyte mtDNAs . doi:10.1093/molbev/msu324
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FIG. 2. The Huperzia mitochondrial chlamydial-like trnS(gga) is shown in the cloverleaf secondary structure model. Near-universal tRNA signature
nucleotides are consistently conserved (bold, see supplementary fig. S1, Supplementary Material online). The “PSW-chlamydial” (genera Parachlamydia,
Simkania, and Waddlia) trnS(gga) homologs differ in seven positions (italics and underlined) of the core structure (20:C; 25:A; 31:C; 39:G; 40:C; 57:G; and
63:C) and diverge among each other at several positions in the highly variable extra-arm (shaded) characteristic of most serine, leucine and tyrosine
tRNAs. As in Huperzia, the CCA acceptor end is not genomically encoded in the Chlamydiae. The corresponding chloroplast-like trnS(gga) in
mitochondria of flowering plants (right) differs from its chlamydial or Huperzia counterpart, respectively, in numerous core positions (shaded) and
has an entirely different, one nucleotide shorter variable extra-arm.
animal pathogens (Collingro et al. 2011). Only few positions in
the core tRNA structures of trnS(gga) and trnL(gag) are conserved differently among the PSW-Chlamydiae aside from
the sequences of the extra arms, which are highly variable
among the Chlamydiae (fig. 2 and supplementary fig. S1,
Supplementary Material online). Like their Lycopodiaceae
pendants, the chlamydial tRNA genes also lack a genomically
encoded CCA aminoacyl acceptor end.
The above findings, indicating that an ancestral
Lycopodiaceae mitochondrial genome may have functionally
integrated chlamydial DNA sequences after horizontal gene
transfer (HGT), made us reinvestigate the entire H. squarrosa
mtDNA sequence in detail. We used sensitive sequence comparisons in small sequence intervals to detect further evidence for transfer of chlamydial (or any other) foreign
sequence integrations. Nearly all coding regions expectedly
shared highest similarity with homologs in the plant lineage
or, when restricted to bacterial sequences, to proteobacterial
sequences supporting their mitochondrial genealogy.
However, there were two further striking exceptions: The
tRNA genes for trnN(guu) and trnS(gcu) again showed highest similarities to chlamydial instead of other mitochondrial
or proteobacterial counterparts. Significantly, both these
tRNA genes are present in algal and liverwort but absent
in moss and hornwort mitochondrial genomes (fig. 1 and
supplementary fig. S2, Supplementary Material online).
Most notably, we now identified a homolog of the
Huperzia trnS(gcu) also in the I. engelmannii mtDNA, which
had previously been overlooked (Grewe et al. 2009), very likely
due to its unique chlamydial nature (supplementary fig. S2,
Supplementary Material online).
Like trnS(gcu), the trnN(guu) gene in H. squarrosa gene is
only distantly related to the native mitochondrial homologs
in liverworts and algae but revealed closely related homologs
in mitochondrial sequences of two other species: In the gymnosperm Cycas taitungensis (Chaw et al. 2008) and in the fern
FIG. 3. The trnN(guu) gene has an interesting evolutionary history featuring native mitochondrial gene copies in liverworts and algae, chloroplast-derived paralogs in flowering plants and chlamydial xenologs in
lycophytes, ferns and gymnosperms clearly set apart. The plant xenologs
of the latter type are nested within the “PSW clade” of “environmental”
Chlamydiae including endosymbionts of protists.
Asplenium nidus (accession AM600641, Panarese S, Rainaldi
G, De Benedetto C and Gallerani R unpublished data).
Interestingly, trnN(guu) is functionally replaced by its chloroplast homolog promiscuously copied into the mitochondrial
genomes in angiosperms (fig. 1). Although naturally very limited in phylogenetic resolution owing to their short sequences, the different plant mitochondrial trnN gene
sequences very clearly reveal their three different genetic origins (fig. 3 and supplementary fig. S2, Supplementary
Material online). The lycophyte, fern, and gymnosperm chlamydial trnN xenologs cluster within the PSW-Chlamydiae
clade to the exclusion of the native mitochondrial homologs
in liverworts and streptophyte algae and the previously
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Knie et al. . doi:10.1093/molbev/msu324
known angiosperm homologs which are nearly identical to
their chloroplast source loci (fig. 3).
The chlamydial-type trnN(guu) genes in C. taitungensis and
A. nidus suggested an early gain of this xenolog through HGT
in the tracheophyte stem lineage (fig. 1). We hence wished to
investigate this evolutionary scenario using primers targeting
the four chlamydial tRNA genes in a sampling of monilophytes and gymnosperms. Although we were unable to
obtain any PCR products for trnS(gga) and consistently
only obtained the native mitochondrial trnS(gcu) gene in
ferns, we retrieved the chlamydial-type sequences of
trnN(guu) in two further gymnosperms and six fern taxa
covering most of the extant monilophyte diversity (fig. 1).
Likewise, we retrieved chlamydial-type PCR products and sequences also for trnL(gag) in the early branching monilophyte
genera Angiopteris and Equisetum. Hence, at least trnN(guu)
and trnL(gag) indeed seem to be early chlamydial gains in
mitochondria of the tracheophyte stem lineage (fig. 1).
The likelihood of HGT early in the tracheophyte mtDNAs
is supported by a noteworthy additional finding: Searches
with the Huperzia trnS(gga) among plant sequences identified
a stretch of 91% identity corresponding to tRNA positions
13–55 as a single significant additional hit in an intergenic
region of the C. taitungensis mtDNA (supplementary fig. S3,
Supplementary Material online), strongly indicative of a pseudogene leftover in the gymnosperm after a chlamydial HGT in
the tracheophyte stem lineage. An additional intriguing observation along similar lines is that three of the chlamydial
tRNA xenologs, trnL(gag), trnS(gcu), and trnS(gga), are all located within 20 kb of the H. squarrosa mitochondrial genome,
devoid of other functional coding sequences (supplementary
fig. S4, Supplementary Material online). This observation
might suggest a joint gain of at least those three tRNA
genes in a single HGT event. In fact, a gain of all four chlamydial tRNA genes in a single event of HGT at the origin of
tracheophytes (Label 1 in fig. 1), followed by differential retention of the xenologs would be a parsimonious scenario.
Indeed, trnS(gcu) and trnS(gga) are encoded in the same orientation and in a similar distance only 3.8 kb apart in the
Waddlia chondrophila genome. In contrast, however, the
other genes for the tRNAs under consideration here are separated by large distances in the genomes of the extant PSWChlamydiae, possibly reflecting millions of years of bacterial
genome recombination. Interestingly, however, two sequence
stretches of approximately 260 bp downstream of trnS(gga)
show additional significant similarities with intergenic regions
in the genome of Parachlamydia acanthamoebae strain UV-7,
an extant species that may be closely related to the ancestral
PSW-chlamydial taxon that donated the plant tRNA gene
xenologs (fig. 3 and supplementary fig. S4, Supplementary
Material online).
The four plant mitochondrial tRNAs under consideration
here were consistently found to be most similar to their chlamydial counterparts setting them apart from more distant
homologs (supplementary table S1 and fig. S5, Supplementary
Material online). The short lengths of tRNA genes necessarily
restrict individual statistical supports. A concatenated alignment of the four tRNA loci including their respective
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top-scoring homologs in gram-positive bacteria, Escherichia
coli, Azospirillum spp., Rickettiales, mitochondria and chloroplasts or cyanobacteria, respectively, in addition to the chlamydial homologs rather clearly demonstrates the distance to
the former and their being nested among the latter, however
(fig. 4). Taken together, we here report the HGT of four tRNA
genes, very likely originating from Chlamydiae (and most
likely of the “PSW clade” in particular) into mitochondria of
the vascular plant stem lineage.
The import of tRNAs into mitochondria is particularly
prominent in plants where many tRNA genes are lacking
from the mtDNAs (Duch^ene et al. 2009; Rubio and Hopper
2011; Schneider 2011; Sieber et al. 2011; Knoop 2012). In fact,
no tRNA genes at all were found in the mitochondrion of S.
moellendorffii (Hecht et al. 2011), suggesting that the entire
tRNA set has to be imported from the cytosol. It is all the
more surprising to now identify the four chlamydial tRNA
xenologs in the mtDNA of H. squarrosa where they coexist
with 22 native tRNA genes addressing other codons. A general propensity for more flexible and promiscuous tRNA
import into mitochondria of the one versus the other lycophyte may be a possible explanation for this peculiar evolutionary outcome. Other than import from the cytosol or
acquiring the homologous chloroplast tRNA genes through
lateral gene transfer between the endosymbiont genomes
within the same cell, the gain of bacterial xenolog tRNA
genes through HGT obviously adds a third option for
plants to complete their set of mitochondrial tRNAs.
After initial reports of HGT between seed plant mitochondria (Bergthorsson et al. 2003; Won and Renner 2003) several
further examples of plant-to-plant mitochondrial HGT have
been documented (e.g., Davis and Wurdack 2004; Mower
et al. 2004; Davis et al. 2005; Barkman et al. 2007; Mower
et al. 2010; Hao and Palmer 2011; Sanchez-Puerta et al.
2011; Hepburn et al. 2012; Renner and Bellot 2012). The
most prominent example for extensive mitochondrial HGT
is the case of the basal angiosperm Amborella trichopoda with
an enormously expanded mtDNA featuring extensive sequences originating through HGT from mitochondria of
other angiosperms, a moss and even algae (Bergthorsson
et al. 2004; Rice et al. 2013). Fewer reports have documented
HGT affecting plant nuclear DNA. As in the examples of mitochondrial HGT, intimate plant–plant contacts such as
host–parasite relationships are likely key to interpretation
of the known examples of plant nuclear HGT (Yoshida
et al. 2010; Xi et al. 2012).
The possibly most significant example for plant-to-plant
HGT on a much deeper evolutionary level is the recently
reported acquisition of a neochrome gene in ferns originating
from hornworts (Cooper 2014; Li et al. 2014) adding a significant item to the list of novel functionalities acquired through
HGT in eukaryotes (recently summarized by Sch€onknecht
et al. 2014). Microorganisms have likely served as donors of
HGT into plants much more frequently than other plants
(Broothaerts et al. 2005; Emiliani et al. 2009; Yue et al. 2012).
Most interestingly, Chlamydiae have already been identified earlier as likely sources for HGT of more than 50
protein-encoding genes into plant nuclear genomes
Chlamydial tRNAs in tracheophyte mtDNAs . doi:10.1093/molbev/msu324
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FIG. 4. A maximum-likelihood phylogenetic tree (GTR+G+I model of sequence evolution) based on the concatenated alignment of the four plant
mitochondrial tRNA genes trnL(gag), trnN(guu), trnS(gcu), and trnS(gga) under consideration here, which likely originated by HGT from chlamydial
bacteria. The respective top-scoring most similar homologs for each Huperzia squarrosa tRNA have been selected for inclusion in the alignment of the
compound taxon homologs (i.e., the respective most similar mitochondrial, chloroplast or cyanobacterial, Escherichia coli, Rickettiales, Azospirillum, and
gram-positive bacterial homologs, respectively). Node support from 1,000 bootstrap replicates is indicated on branches where exceeding 50%.
Phylogenetic tree was constructed using MEGA 5 (Tamura et al. 2011).
(Greub and Raoult 2003; Becker et al. 2008; Moustafa et al.
2008; Collingro et al. 2011). In fact, it is now assumed that
endosymbiotic Chlamydiae have played a decisive key role
in the establishment of the chloroplast in the ancestral
primary photosynthetic eukaryote (Huang and Gogarten
2007; Fournier et al. 2009; Price et al. 2012; Ball et al. 2013;
Baum 2013; Facchinelli et al. 2013; Subtil et al. 2014).
Chlamydiae may have acted also elsewhere in the eukaryote world as donors of genetic material as has recently
been shown for HGT of a tRNA guanine methyl-transferase protein domain into the slime mould Dictyostelium
discoideum (Manna and Barth 2013).
The here reported gain of four mitochondrial tRNA genes
from chlamydial bacteria, two of which had never entered the
land plant lineage in their native mitochondrial form, now
demonstrates that at least one further major event later in the
evolution of plant life, the origin of vascular plants, was associated with a close contact and the uptake of genetic material
from Chlamydiae, in this case targeting the mitochondrial
genome. The ancient chlamydial donor appears to be most
closely related to modern chlamydial taxa that have originally
been identified as endosymbionts of amoebae. Our new finding serves as an alert to closer inspection also of genes encoding small structural RNAs as possible candidate subjects for
interkingdom HGT.
Supplementary Material
Supplementary figures S1–S5 and table S1 are available at
Molecular Biology and Evolution online (http://www.mbe.
oxfordjournals.org/).
Acknowledgment
The authors gratefully acknowledge the very helpful suggestions for improvement of the manuscript in the review
process. Research reported here relied on basic funds of the
University of Bonn.
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