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Journal of Bacteriology, January 2001, p. 785-790, Vol. 183, No. 2
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.2.785-790.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Vertical Transmission of Biosynthetic Plasmids in
Aphid Endosymbionts (Buchnera)
Jennifer J.
Wernegreen* and
Nancy A.
Moran
Department of Ecology and Evolutionary
Biology, University of Arizona, Tucson, Arizona 85721
Received 2 February 2000/Accepted 16 October 2000
 |
ABSTRACT |
This study tested for horizontal transfer of plasmids among
Buchnera aphidicola strains associated with
ecologically and phylogenetically related aphid hosts
(Uroleucon species). Phylogenetic congruence of
Buchnera plasmid (trpEG and
leuABC) and chromosomal (dnaN and trpB) genes supports strictly vertical long-term
transmission of plasmids, which persist due to their contributions
to host nutrition rather than capacity for infectious
transfer. Synonymous divergences indicate elevated mutation on plasmids
relative to chromosomal genes.
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TEXT |
Bacterial genomes are
characterized by remarkable plasticity that allows rapid genetic
adaptations to environmental changes (reviewed in references
3, 33, 46). Plasmids, extrachromosomal DNA molecules that
replicate autonomously, contribute to this plasticity by mediating
lateral gene transfer among bacterial species and genera (15, 17,
21, 40, 57, 59, 65) and even between kingdoms (19,
24). In addition to their role in lateral gene transfer,
plasmids also function in gene amplification and overexpression
(46, 47). Just as chromosomal duplications are a common
mechanism for increasing gene dosage in response to fluctuations in the
environment (47, 54), amplification of loci on plasmids
may be adaptive when selection favors increased gene dosages (12,
20).
In Buchnera aphidicola, the primary endosymbiont of
aphids, genes for the biosynthesis of tryptophan
(trpEG) and leucine (leuABCD) often occur on multicopy plasmids (pTrpEG and pLeu,
respectively) (5, 6, 10, 31, 48, 49, 52, 63, 64).
Comparative sequence analysis indicates that the ancestral location for
both trpEG and leuABCD genes
was the Buchnera chromosome, not an exogenous plasmid
(7, 49, 63). This movement of chromosomal loci onto
plasmids is considered a host-beneficial adaptation of
Buchnera to overproduce these essential amino acids that are
lacking in the hosts' diet of plant sap.
The role of horizontal transfer in the evolution of Buchnera
biosynthetic plasmids remains unclear. In contrast to facultative symbionts such as Rhizobium and Vibrio, lateral
gene transfer in Buchnera may be highly constrained since
this obligate symbiont spends its entire life cycle within specialized
host cells (bacteriocytes) (11, 43). In accordance with
this hypothesis, several previous studies show phylogenetic congruence
among chromosomal (trpB and 16S rRNA) and plasmid
(trpEG and leuABCD) genes of
Buchnera associated with the family Aphididae and suggest a
lack of plasmid transfer in this symbiont group (5, 6, 10, 22,
48, 49, 51, 63, 64). However, recent work suggests
horizontal transfer of the plasmid-encoded repA1 gene in
Buchnera of Pemphigus spyrothecae (62).
Most previous studies were based on sampling Buchnera
associated with different aphid genera and cannot address the issue of
plasmid transfer among closely related strains, which may occur via
biological vectors or acquisition of DNA from the environment (60). In order to maximize the chance of detecting gene
transfer among related Buchnera lineages, we sampled
Buchnera of Uroleucon, a recent radiation of
aphids that specialize on Asteraceae and often share host
plants, habitats, secondary endosymbionts, and parasitoids (42,
50). We compare phylogenies of chromosomal genes
(dnaN and trpB) and plasmid-encoded genes
(trpEG and leuABC) to test
for plasmid transfer in this symbiont group.
Phylogeny reconstruction.
Collection data, aphid DNA
extractions, and standard PCR conditions were described previously
(42). The PCR was used to amplify three gene regions
of Buchnera: dnaN (1,107 bp),
leuABC (3,919 bp), and trpEG
(1,767 bp) (primer sequences available upon request). DNA sequences
were obtained as described previously (42) directly from
PCR products or TA clones of PCR fragments. GenBank numbers for
sequences obtained here and for previously published sequences are
given in Table 1. Translated DNA
sequences were aligned by using Megalign (DNAstar).
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TABLE 1.
Aphid hosts of Buchnera lineages included in
this study and GenBank accession numbers for gene regions sequences
here (bold) and previously
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Genealogies of each of the four gene regions and for combined data were
estimated by using maximum parsimony (MP) and maximum
likelihood (ML)
(Paup* 4 [56]). MP trees were estimated by heuristic
searching, and
confidence in nodes was assessed by bootstrapping
(100 replications).
MP trees estimated for the subset of taxa
available for each locus
(Fig.
1, taxa in bold) agree with
relationships
shown in the larger bootstrap trees for all available
taxa (Fig.
1). These MP trees were generally very similar across genes.
ML
phylogenies were estimated for the subset of
Buchnera
lineages
sequenced for each gene region after excluding third codon
positions.
ML parameters and topologies were alternatively estimated
until
there was no improvement in the likelihood score, according to
the successive approximation method suggested by Swofford
(
55).
The proportion of invariant sites and base
frequencies were set
to empirical levels, and substitution rates were
allowed to vary
among sites according to a gamma distribution (four
site categories)
under the Hasegawa-Kishino-Yano model of
substitution. Phylogenies
and the ML parameters alpha (the gamma shape
parameter) and transition/transversion
ratio were estimated separately
for each region. Only two ML topologies
were found: (i) that of
leuABC and
dnaN and (ii) that of
trpB,
trpEG, and combined data (Fig.
2).
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FIG. 1.
Maximum parsimony-based phylogeny of four
Buchnera gene regions: the chromosomal genes
dnaN (a) and trpB (b), the plasmid gene
regions trpEG (c) and
leuABC (d), and combined data
for the subset of taxa sequenced at each locus (e). Bootstrap values
(100 replications) are given at nodes. Taxa common to each data set are
given in bold. See Table 1 for abbreviations.
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FIG. 2.
Maximum likelihood-based phylogenies of first and second
codon positions of four Buchnera gene regions and
combined data. Parameters were estimated separately for each locus (see
the text). Branch lengths are proportional. Likelihood scores and ML
parameters were estimated as follows: (a) dnaN,
 Ln L = 3,731.411, ti/tv = 1.612 (k = 3.986),
a = 0.492; (b) trpB, Ln L = 1,492.105, ti/tv = 1.242 (k = 2.42), a = 0.177; (c)
trpEG, Ln L = 5,881.237, ti/tv = 1.09 (k = 2.283), a = 2.010; (d)
leuABC, Ln L = 9,962.228, ti/tv = 1.53 (k = 3.10), a = 0.198; (e) combined data, Ln L = 21,296.363, ti/tv = 1.363 (k = 2.836), a = 0.239. See
Table 1 for abbreviations.
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MP and ML estimates give similar phylogenies for all gene regions.
Notably, the MP and ML trees for combined data are identical.
Slight
discrepancies between MP and ML estimations result primarily
from the
placement of two taxa,
Buchnera of
Uroleucon
erigeronense and
Uroleucon caligatum. These
discrepancies are only weakly supported,
as seen in the low MP
bootstrap values (Fig.
1) and short internal
branches on ML trees (Fig.
2). The relationships at each gene
generally agree with relationships
among the
Uroleucon hosts (
14).
Phylogenetic congruence among loci.
Outgroup
species (Rhopalosiphum padi and Schizaphis
graminum) were excluded from tests of phylogenetic congruence to
avoid biasing the outcome towards congruence. First, we tested the null hypothesis, using TREEMAP (44), that MP trees for each
data set are no more congruent than expected by chance (i.e., randomly related). All pairs of MP trees were more similar than expected by
chance (P < 0.001 for each comparison). However,
disproving the null hypothesis of random relatedness provides only weak
evidence for congruence, since gene transfer may not erase all traces
of historical associations (see reference 14). We
therefore tested the null hypothesis that different gene regions
support the same topology. The Kishino-Hasegawa test evaluates whether
a data set has a significantly better likelihood score across its own
ML tree than across the alternative ML topology (28)
(using Paup*4). Similarity in likelihood scores for both ML trees
indicates that discrepancies between the two Buchnera ML
phylogenies are not statistically significant for any gene region
(Table 2).
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TABLE 2.
Results of the Kishino-Hasegawa (KH) test, comparing the
likelihood score of four datasets and combined data across the two
alternative ML phylogenies
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This phylogenetic congruence of plasmid and chromosomal genes strongly
supports a lack of plasmid transfer among
Buchnera strains associated with aphid hosts that share habitats, host
plants, and parasitoids and secondary endosymbionts (
50).
A
recent study found congruence of gene genealogies in
Buchnera of
Uroleucon ambrosiae, suggesting
strictly vertical transfer
even within the same host species
(
22). These results support
previous conclusions of
congruence among
Buchnera genealogies
and contribute to the
larger picture of vertical plasmid transmission
across millions of
years (
5,
6,
10,
48,
49,
52,
63,
64). Our data suggest
that the single proposed instance
of plasmid transfer in
Buchnera may represent a very rare event
that occurred early
in the evolution of the Pemphigidae (
62).
This plasmid
stability in
Buchnera contrasts with genome fluidity
in most
bacterial species, where plasmids mobilize ecologically
important
features such as pathogenic and symbiotic capacities
(
69)
and antibiotic resistance (
4,
37) and contribute to
the
mosaic-like genome structure of some bacterial genomes (
26,
32,
34,
41). For example, in
Escherichia coli, the close
free-living relative of
Buchnera, incongruence among
genealogies
of chromosomal and plasmid-encoded genes indicates several
recombination
and horizontal transfer events (
35).
Selection for plasmid maintenance.
The maintenance of
bacterial plasmids has been attributed to a combination of infectious
transfer and selection for plasmid-encoded traits (38).
Since the two biosynthetic plasmids of Buchnera experience
little if any lateral transfer, they must be maintained solely by
selection for plasmid-encoded traits. In endosymbionts, selection may occur within hosts (resulting from differential replication of different endosymbiont genotypes within an individual host) and between hosts (resulting from differential reproductive rates
of hosts that contain different symbiont genotypes) (1, 45). At the level of within-host selection, plasmid
amplification of biosynthetic genes in Buchnera is probably
neutral or deleterious, since the overproduction of tryptophan and
leucine and the replication of plasmids may be costly to
individual Buchnera cells (36, 53).
Any selection favoring plasmid maintenance in Buchnera must
occur between aphids, which require symbiont biosynthetic functions for
adequate nutrition. This impact of host-level selection may explain the
prevalence of these two plasmids in Buchnera of the
Aphididae, in which relatively rapid growth and high fecundity may
increase physiological demands for amino acids (7).
Host-level selection may also explain the parallel changes in level of
amplification of trpEG and
leuABCD in particular aphid species
(58).
With the above reasoning, selection on bacterial cells will tend to
favor plasmid loss while selection on aphid hosts will
favor plasmid
maintenance. Such conflict may be partially resolved
by an attenuation
of negative effects of plasmids on bacterial
fitness (e.g., see
reference
9). Based on the divergence times
of aphids with
plasmid-bearing
Buchnera (about 50 to 70 million
years for the family Aphididae) and the estimated generation
time
of
Buchnera (about 50 doublings per year
[
13]), pTrpEG and pLeu
have been vertically
transmitted with the
Buchnera chromosome
for approximately
2.5 to 3.5 billion bacterial generations, over
which time selection may
have minimized deleterious effects of
plasmids on bacterial fitness.
One possible mechanism by which
individual
Buchnera
cells may benefit from (or be "addicted" to)
pTrpEG is
through selection to preserve
dnaA boxes borne by
this
plasmid (
30). These sites may titrate DnaA, a protein
that is
also involved in initiation of chromosomal
replication.
Elevated divergence at plasmid-borne genes.
Some plasmids may
experience elevated rates of sequence evolution compared to chromosomal
genes due to higher rates of adaptive fixation or higher mutation rates
(18, 61). The latter might arise from more frequent
recombination (27), greater densities of transposons
(2), dependence on different, more error-prone polymerases
(25, 29), or higher rates of transcription
(16). The vertical transmission of Buchnera
plasmids provides a rare opportunity to contrast rates of sequence
divergence among completely linked, autonomously replicating DNA
molecules. In many bacterial species, selection for codon usage at
particular loci (adaptive codon bias) may lead to differences in
rates of synonymous divergence among genes (50). However,
since Buchnera lacks adaptive codon bias
(66), synonymous substitution rates are expected to
approximate neutral mutation rates. Under the hypothesis that different
replicons have equal mutation rates, divergence at synonymous sites is
expected to be similar for plasmid and chromosomal genes.
Synonymous divergences were estimated for each gene region across
phylogenetically independent pairs of
Buchnera. Synonymous
divergences were estimated using the method of Li (
39),
adjusting
for moderate levels of sequence divergence (using the program
Molecular Evolutionary Analysis [E. Moriyama, Yale
University])
and the maximum-likelihood-based method of Goldman
and Yang (
23)
(codeML package of PAML
[
67]). Compared to other methods, this
likelihood
approach accounts for unequal base (codon) frequencies
and biased
transition/transversion ratios and provides a more
realistic
evolutionary model for DNA sequences with extreme base
compositions (reviewed in reference
68). Assumptions of
the
likelihood method as implemented here include a constant base
composition and a uniform rate of substitution across codons
of
a particular gene (the shape parameter alpha =
infinity).
Discrepancies between Goldman and Yang's (
23) and Li's
(
39) methods illustrate the effects of accounting for base
composition
when calculating sequence divergences (Table
3). However, both
methods show higher
divergences at
trpEG and
leuABC compared to
those at
dnaN and
trpB for four of the six pairwise comparisons
(Fig.
3; Table
3). Higher synonymous
divergence at
trpEG than
at
chromosomal genes agrees with previous studies based on smaller,
more
divergent data sets (
13,
48) and suggests elevated neutral
mutation rates on pTrpEG. In contrast with the elevated
synonymous
divergence at
leuABC in our data set,
previous studies based on
fewer and more divergent taxa did not find
elevated rates at leucine
biosynthesis genes (
5,
13). The
Uroleucon sample used here
consists of numerous recently
diverged isolates, provides low
standard errors for divergence
estimates, and offers improved
ability to compare divergence levels
among loci. Overall, our
analysis suggests that the mutation rates for
both pTrpEG and
pLeu may show a moderate increase over that
of the chromosome,
at least in
Buchnera of
Uroleucon. Mechanisms for higher mutation
rates at plasmid
loci may include the use of different DNA polymerases
that vary in
error rate (
29) or higher levels of transcription,
which
may elevate mutation rates (
8,
16).
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TABLE 3.
Pairwise estimates of synonymous divergences at
chromosomal (dnaN and trpB) and plasmid
(leuABC and trpEg) genes for
six phylogenetically independent pairs of Buchnera isolates,
showing generally higher divergences at the plasmid-encoded loci
for any given
pairwise comparison
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FIG. 3.
Phylogenetically independent pairwise estimates of
synonymous divergence at Buchnera dnaN,
trpB, leuABC, and
trpEG genes, using a maximum likelihood-based
estimation (67, 68). Error bars indicate the standard
errors of individual pairwise estimates. See Table 1 for
abbreviations.
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Nucleotide sequence accession numbers.
GenBank numbers for
sequences obtained in this study and for previously published sequences
are given in Table 1.
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ACKNOWLEDGMENTS |
This work was supported by a National Institutes of Health
postdoctoral training grant in Molecular Insect Science (Center for
Insect Science, University of Arizona) to J.J.W. and a National Science
Foundation grant (DEB-9815413) to N.A.M.
We thank J. Sandström for obtaining most of the original
Uroleucon samples and P. Baumann for DNA extractions.
Three anonymous reviewers gave helpful comments.
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FOOTNOTES |
*
Corresponding author. Present address: JBP Center for
Comparative Molecular Biology and Evolution, The Marine Biological Lab, 7 MBL St., Woods Hole, MA 02543. Phone: (508) 548-3705, ext. 6650. Fax:
(508) 457-4727. E-mail: jwernegreen{at}mbl.edu.
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Journal of Bacteriology, January 2001, p. 785-790, Vol. 183, No. 2
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.2.785-790.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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