Published online before print
February 12, 2003, 10.1101/gr.652803
Vol 13, Issue 3, 407-412, March 2003
LETTER
The Genetic Core of the Universal Ancestor
J. Kirk Harris1,2,4,
Scott T. Kelley1,4,
George B. Spiegelman3 and
Norman R. Pace1,5
1Department of Molecular, Cellular and Developmental
Biology, University of Colorado, Boulder, Colorado 80309-0347, USA;2
Graduate Group in Microbiology, University of California,
Berkeley, Berkeley, California 94720, USA; 3Department of
Microbiology and Immunology, University of British Columbia,
Vancouver, British Columbia, Canada V6T 1Z3
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ABSTRACT
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Molecular analysis of conserved sequences in the ribosomal RNAs of
modern organisms reveals a three-domain phylogeny that converges in a
universal ancestor for all life. We used the Clusters of Orthologous
Groups database and information from published genomes to search for
other universally conserved genes that have the same phylogenetic
pattern as ribosomal RNA, and therefore constitute the ancestral
genetic core of cells. Our analyses identified a small set of genes
that can be traced back to the universal ancestor and have coevolved
since that time. As indicated by earlier studies, almost all of these
genes are involved with the transfer of genetic information, and most
of them directly interact with the ribosome. Other universal genes have
either undergone lateral transfer in the past, or have diverged so much
in sequence that their distant past could not be resolved. The nature
of the conserved genes suggests innovations that may have been
essential to the divergence of the three domains of life. The analysis
also identified several genes of unknown function with phylogenies that
track with the ribosomal RNA genes. The products of these genes are
likely to play fundamental roles in cellular processes.
Phylogenetic studies of ribosomal RNA (rRNA)
revolutionized our understanding of biological diversity by revealing
that modern organisms fall into three phylogenetic domains: Archaea,
Bacteria, and Eucarya (Woese and Fox 1977 ; Woese et al. 1990). rRNA
sequence information in principle is well suited for determining deep
phylogenetic relationships for several reasons. The rRNA sequences
occur in all organisms, they have evolved at a sufficiently slow rate
to retain phylogenetic information between distantly related organisms,
and the rRNA genes have undergone limited or no horizontal transfer
(i.e., transfer between distantly related organisms; Asai et al. 1999).
Since the original description of the three-domain phylogeny,
correlations of biochemical properties between organisms and data from
genomic sequences have lent support to this classification of life
(Woese et al. 1990; Wettach et al. 1995; Brown et al. 2001b).
At the same time, it also has become evident that many genes do not
exhibit the same phylogenetic pattern as rRNA genes. Data from complete
genomic sequences and phylogenetic studies of particular genes have
revealed that genomes contain many genes that have undergone horizontal
as well as vertical evolutionary change (Brown and Doolittle 1997).
Moreover, a large number of genes appear to have been lost from, or
never acquired by, various lineages over evolutionary time (Snel et al.
2002). Although gene loss or gain and horizontal transfer are common
themes in evolution, phylogenetic analyses nonetheless have identified
a number of genes in the nucleic acid-based information-processing
pathway that have phylogenetic histories congruent with that of rRNA.
For instance, the phylogenetic relationships among the core subunits of
the DNA-dependent RNA polymerases, or most ribosomal protein genes, are
the same as those seen in phylogenetic analyses of rRNA sequences
(Iwabe et al. 1991; Klenk et al. 1993; Liao and Dennis 1994).
Additionally, recent studies of concatenated datasets recovered the
three-domain topology even when component members analyzed separately
clearly demonstrated lateral transfers between organisms (Brown et al.
2001a). Collectively, the results indicate that the phylogenetic
pattern of rRNA is representative of the evolutionary history of some
portion of cellular components, which we term the ‘genetic core.’
Although it is known that some cellular genes show the same
phylogenetic patterns as rRNA, the purpose of the present study was to
determine the entire set of universal genes with this property; this
set constitutes a ‘genetic core’ of the known cellular lines of
descent. Abundant new sequence information from a rapidly expanding
database of genome sequences allows a more complete assessment of the
genes that comprise such a genetic core that traces its ancestry back
to the last common ancestor (LCA) of life. We used the Clusters of
Orthologous Groups of proteins (COG) database (Tatusov et al. 2001) to
search for constituents of the genetic core by identifying the
universally conserved set of related genes that have the same
phylogenetic history as rRNA. If a gene that is universally present in
cells shares the same phylogenetic history as rRNA, two important
properties of the gene can be inferred: (1) The gene occurred in the
LCA and is not present in all organisms, as a result of subsequent
horizontal transfer between lineages; and (2) the gene has resisted
both nonorthologous displacement and extensive amino acid substitution
since that time of the LCA. We note that this analysis will not yield a
minimal genome for the LCA, because it should focus primarily on the
mechanisms of the universal function of transfer of genetic
information.
The analyses presented here were based exclusively on fully sequenced
genomes and have two primary advantages over single-gene surveys.
First, the complete set of genes from the organisms being examined is
known, which allowed for a comprehensive analysis of gene coevolution.
Second, the absence of a gene in an analysis of complete genome
sequences is not a negative result; rather, it is a finding that the
gene is truly not present in the organism. This contrasts with PCR- or
homology-based analyses of particular genes, where a negative result is
ambiguous.
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RESULTS
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Of the roughly 3100 COGs analyzed, only 80 were found to occur in
all organisms. Fifty of these universally present genes showed the same
phylogenetic relationships as rRNA (Fig. 1A
presents examples). For brevity, we refer to universally conserved
genes that share the rRNA topology as ‘three-domain’ genes. The
majority of universally conserved three-domain COG genes (37 of 50) are
physically associated with the ribosome in modern cells. For the 30
COGs that were not three-domain, there was no single evolutionary
pattern (e.g., Fig. 1B). In some cases the relationships were simply
unresolved, whereas for others one domain clearly separated and the
other two domains remained intermixed (Table
1). The 80 COGs were classified into six
groups based on phylogeny and known, or presumed, function (Table 1).
The six groups are described below.
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Figure 1. Examples of three-domain and non-three-domain phylogenetic trees from
analyses of the COG database protein alignments. The trees are the
single shortest trees found by a maximum parsimony (MP) analysis of the
amino acid alignments (neighbor-joining [NJ] analysis gave the same
topology). Names of organisms belonging to the Bacteria are in italics;
names of Archaea are in bold italics, and names of Eucarya are in all
capital letters. (A) The phylogeny of COG0231 (efp in
E. coli) recapitulates the basic three-domain topology given
by ribosomal RNA, and the numbers indicate bootstrap support for the
monophyly of the archaeal, bacterial, and eucaryal sequences in this
COG. Results from MP bootstrap analysis are given above the branches,
and results from NJ bootstrap analysis are given below. (B)
The phylogeny of COG0018 (argS in E. coli) violates
the three-domain paradigm, as none of the three domains are
monophyletic. Indications of horizontal gene transfer events are
presented in enlarged font along with corresponding bootstrap support
for the nodes demarking lateral transfer.
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Group 1: Ribosomal Proteins and Translation Initiation Factors
Group 1 contains genes that recapitulate the three-domain phylogeny
and whose products are directly linked to the function of the ribosome.
This group includes genes for 29 universally conserved ribosomal
proteins (rproteins) and the four universally conserved initiation and
elongation factors (RNAs were not considered in this compilation.) In
the case of the 30 small subunit rprotein COGs, 15 were universal, six
were found only in Bacteria, and nine were found only in Eucarya and
Archaea. The majority of universal COGs for small subunit rproteins
showed strong support for a three-domain phylogeny (14 of 15; Table 1).
The genes for large subunit ribosomal proteins were a more complex
group, and a smaller fraction of these were universally conserved (17
of 51 COGs, with 15 being three-domain). COGs encoding 11 large subunit
proteins appeared to be three-domain by either maximum parsimony or
neighbor-joining analysis, but bootstrap support for the three-domain
topology was not strong (< 50%). We presume that the lack of
statistical support in the calculations resulted from random
evolutionary convergence in the relatively small data sets (ranging
between 125 and 200 parsimony-informative characters) for these COGs.
Because the best and most resolved topology was three-domain, we
classified them as such.
Group 2: Proteins Associated With the Ribosome or Protein Modification
Group 2 includes universal three-domain genes that encode a diverse
set of nonribosomal proteins with known functions that potentially link
the genes to ribosome function or to modification of proteins. COG0024,
methionine aminopeptidase (map, in E. coli), cleaves
the initiator methionine during the process of translation (Lowther and
Matthews 2000). COG0006, XaaPro amino peptidase (pepP in
E. coli), also encodes a protease, initially identified by
enzymatic activity against dipeptides with proline as the penultimate
residue (Yaron and Mlynar 1968). COG0112 encodes the GlyA protein in
E. coli. GlyA is required for amino acid catabolism and for
donation of methyl groups to S-adenosyl-methionine-dependent
methyltransferases and other methylating enzymes. In modern organisms,
proteins encoded by three members of Group 2 (COG0201
[secY], COG0552 [ffh, SRP54], and COG0541
[ftsY SRP54 receptor]) are involved in protein export or
insertion into membranes, guiding leader peptides to the membrane
during translation (Walter and Johnson 1994).
Group 3: Proteins Associated With Transcription and Replication of DNA
Four of the universally conserved three-domain COGs in Group 3
encode proteins involved in transcription, including three subunits of
DNA-dependent RNA polymerase (COG0085, COG0086, and COG0202
[RpoB, RpoC, and RpoA, respectively
in E. coli]), and the gene for a transcription
anti-terminator (COG0250, NusG in E. coli).
The number of universal genes involved in DNA replication and repair
was surprisingly small, only four. Of these universal genes, only three
were found to be three-domain: COG0592 (DnaN, in E.
coli) that encodes the sliding clamp subunit of DNA polymerase III,
COG0258 (Pol1-A in E. coli) that encodes the 5'-3'
exonuclease function of the DNA polymerase I, and COG0468 that encodes
the recombination enzyme RecA.
Group 4: Uncharacterized Proteins
Two universally conserved genes that displayed three-domain
phylogeny (> 95% bootstrap for all domains) but have no known
functions were also found. In both cases, at least one property of the
COG proteins could be predicted from its sequences. COG0037 (mesJand ydaO in E. coli) encodes a predicted
ATPase, and COG0012 (ychF in E. coli) encodes a
predicted GTPase.
Group 5: Universal, Non-Three-Domain Proteins
Twenty-eight universally conserved COGs did not show three-domain
phylogeny. Presumably, therefore, these genes encode essential
functions and have been subjected to lateral gene transfer at some
point in evolution (Doolittle 1999; Glansdorff 2000). For example, 14
of the eucaryal amino acyl tRNA synthetase genes did not form a
monophyletic group, and rather were always nested within either the
bacterial or the archaeal groups (Woese et al. 2000). The
non-three-domain universal COGs also include COG0125 (thymidine
kinase), COG0550 (topoisomerase 1A), and COG1109 (phosphomanomutase;
mrsA in E. coli). COG0533 has been predicted to
encode a metal-dependent protease (ygjD in E. coli),
but the precise function of the gene product has not been identified in
any organism. The remaining COG representing a subunit of DNA
polymerase III that was found to be universal was COG0470
(holB in E. coli). In modern organisms this subunit
is required to load the modern sliding clamp, but, like the rest of the
essential DNA polymerase genes, COG0470 has been transferred between
domains. Groups 5 also includes a number of COGs that are missing from
only one of the 36 genomes included in the survey and do not show
three-domain phylogeny (Table 1).
Group 6: Protein Families and Domain Families
The COG database contains two gene families that occur universally,
COG0073 (EMAP domain) and COG0526 (thiodisulfide isomerases). These
were not analyzed in this study due to the large number of paralogs in
these COGs.
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DISCUSSION
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Systematic phylogenetic analyses of the universally conserved COG
proteins revealed a genetic core of organisms containing a
small number of genes that coevolved with the ribosomal RNAs since
their divergence from a common ancestor. As expected, most of the
three-domain genes belong to the nucleic acid-based central information
pathway (ribosomal proteins, DNA/RNA polymerase subunits, elongation
factors). However, we also discovered a number of three-domain COG
proteins with little apparent connection to genetic transmission or
gene expression (e.g., membrane insertion factors and proteases).
Perhaps the most surprising finding of this analysis was the relatively
small number of the COG gene sets that were three-domain in this
analysis. Of the nearly 3100 COG gene sets in the database, only 80
were universal and, of these, only 50 were three-domain.
Comparison of the gene sets used in the analysis suggested four main
reasons for the paucity of three-domain COG proteins. First, many of
the proteins in the COG database are unique to subsets of organisms, a
reflection of the enormous phenotypic diversity of modern cell types.
For example, genes required for synthesis of cell membranes, a required
function for all modern organisms, are not universally conserved among
the phylogenetic domains. This is because the biochemistry of archaeal
ether-linked lipids is fundamentally different from that used in the
other two domains, which produce ester-linked lipids (Koga et al.
1993). Second, the amino acid sequences of some proteins have diverged
so radically since the LCA that the sequences are no longer
recognizably homologous in different organisms (e.g.,
F1F0 ATP synthetase; Gruber et al. 2001). Third,
gene loss without replacement is a common phenomenon in many genomes
and appears to play an important role in shaping genome content (Snel
et al. 2002). Finally, the low number of three-domain COG proteins
reflects the importance of gene replacement by genes of independent
origins through nonorthologous displacement by lateral gene transfer.
As examples of the latter, DNA primase, DNA polymerization activity,
and ribonuclease H activity all appear to have multiple independent
origins (Leipe et al. 1999). This may also be true for other
ribonucleases and reverse transcriptase. As pointed out earlier, it is
certain that the LCA contained many genes other than the 80
three-domain COGs and that some of the COGs were added after the three
domains diverged. However, by and large we found that late additions to
the COGs and lateral transfers were obvious from their phylogenetic
patterns.
Three-Domain Ribosome-Associated Proteins
Most of the 50 three-domain COGs identified were ribosomal proteins
(29 of 50). This finding supports previous conclusions that the
divergence of the three types of ribosomes (bacterial, archaeal, and
eukaryal) occurred after a relatively efficient ribosome structure was
in place (Ouzounis and Kyrpides 1996; Olsen and Woese 1997). The
abundance of three-domain ribosomal proteins may be attributable to the
specific physical association of these proteins with the rRNA. The
crystal structure of the Thermus thermophilis 30S subunit
suggests that many of the three-domain ribosomal proteins in the small
subunit (SSU) are found at junctions between helices, such as S4, S7,
and the cluster of proteins S8, S15, and S17. Other three-domain
SSU proteins penetrate the RNA structural core, providing
functional stability (Wimberly et al. 2000). The interactions of the
SSU proteins with the 16S ribosomal RNA, as well as with each other,
suggest a strong mutual dependency and perhaps a powerful selective
constraint inhibiting radical sequence evolution or nonorthologous
displacement.
In contrast to the three-domain SSU proteins, considerably fewer of the
large ribosome subunit proteins were three-domain. In general, the
large subunit (LSU) proteins tend to be less physically clustered in
the ribosome than are those of the small subunit. The crystal structure
of the Haloarcula marismortui 50S ribosomal subunit shows that
only a few proteins, such as L3, L13, and L14, are sufficiently close
to one another to interact physically. The primary interaction of the
LSU proteins is with RNA rather than other proteins (Ban et al. 2000).
This provides some rationale for the lower frequency of the large
ribosome subunit proteins in the three-domain set. We note that the
collection of three-domain rproteins emphasizes the deep divergence of
the three domains of life, arguing against evolution models in which
the Eucarya are derived from a fusion of other cell types.
In addition to many ribosomal proteins, a number of other proteins
associated with the ribosome also are three-domain. As might be
expected considering the relatively sophisticated protein synthesis
machine of the LCA, the basic initiation and elongation factors are
three-domain (Kyrpides and Woese 1998). More surprisingly, several
proteins used for proteolytic modification of nascent peptides and for
methylation events are three-domain. Methionine aminopeptidase
(COG0024, map) is responsible for the proteolytic processing
of nascent peptides during translation to remove the initiator
methionine. In three genomes, the pepP (COG0006) gene
(proteolytic modification) has been found directly adjacent to the gene
for one of the universal three-domain elongation factors, implying a
link to maturation of proteins during translation (Matos et al. 1998).
Methylated nucleotides are a universal property of ribosomal RNA, and
the presence of a methyl donor (COG0112, glyA) among the three-domain
COGs suggests that methylation was required for the early function of
the ribosome.
Finally, components of two systems for insertion of proteins into
membranes were found among the three-domain COG proteins (COG0201,
SecY; COG0541 and COG0552, Ffh and FtsY, respectively). The
three-domain nature of these membrane insertion factors suggests that
functions linked to membranes were an ancient, required activity prior
to the establishment of the three domains of life.
Three-Domain Proteins Not Directly Associated With the Ribosome
In contrast to the coordinated structure of the ribosome, relatively
few genes encoding proteins involved in DNA replication or
transcription from DNA to RNA proved to be three-domain. The majority
of RNA polymerases found in modern organisms are not three-domain,
which illustrates the diversity of proteins that can carry out this
catalytic activity. Indeed, a number of studies have pointed to
multiple origins for RNA polymerases (McAllister and Raskin 1993; Zhang
et al. 1999; Cramer et al. 2000). We identified in this study only
three subunits of the core DNA-dependent RNA polymerase as
three-domain, as seen previously (Iwabe et al. 1991; Klenk et al.
1993). The three-domain nature of the core RNA polymerase subunits
indicates that the LCA used DNA for genetic continuity. This
supposition is supported by the occurrence in the three-domain set of
two enzymes of DNA metabolism, RecA and Pol1A (Eisen and Hanawalt
1999). The only component of the replicative DNA polymerase in modern
cells that was found to be three-domain is DnaN (COG0592), the
gene for the "sliding clamp." Considerable evidence supports the
idea that this protein is necessary for the high degree of processivity
of DNA polymerase during replication (Kuriyan and O'Donnell 1993;
Hingorani and O'Donnell 2000). Others have noted the sequence
divergence of the subunits of the replicative DNA polymerase, where it
has been suggested that the capacity for DNA polymerization arose
several times (Leipe et al. 1999).
This collection of three-domain DNA metabolism and transcription
enzymes suggests that the ability to synthesize and transcribe long DNA
molecules was an important property of the LCA. This innovation would
have increased genetic linkage, which in turn would have increased the
ability to transmit genetic information through vertical inheritance.
In particular, the sliding clamp function would have been required to
allow accurate replication of linked genes. Additionally, both RecA and
Pol1A would contribute to genetic continuity by gene conversion after
recombination, and would become increasingly useful in the maintenance
of genetic information as the lengths of DNA strands increased (Eisen
and Hanawalt 1999). A final protein that may have contributed to this
general innovation is the three-domain COG protein NusG. As a
transcription anti-terminator, NusG improves transcriptional
efficiency. Moreover, NusG (along with other proteins, such as the
ribosomal protein S4) has been proposed as a link between the ribosome
and the process of transcription (Squires and Zaporojets 2000).
Two universal COGs consist of genes with functions predicted solely on
the basis of sequence similarity to other functionally described
protein motifs. These genes likely encode proteins involved in the
central information processing of the cell. One of these COGs is a
predicted GTPase (COG0012, YchF in E. coli) that
could be disrupted in a Mycoplasma genitalium
mutagenesis study, and so is not an essential gene for laboratory
growth (Hutchison et al. 1999). The other COG is a predicted ATPase
(COG0037, YdaO and MesJ in E. coli). The
universal three-domain conservation of these genes suggests that they
encode ancient and fundamental properties of all organisms, and
identifies them as potentially fruitful targets for further
experimentation.
The universal COGs that are not three-domain primarily contain genes
that encode proteins that are not integrated into specific large
macromolecular complexes, for instance, the aminoacyl tRNA synthetases
(14 of 28 COGs, reviewed by Woese et al. 2000). One of the
non-three-domain COGs represents a metal-dependent protease that is
universally conserved, but of unknown specific function. The
universality of this protein indicates that it is an important cellular
component that is not highly integrated into a specific macromolecular
complex. The function of this protein could be a useful subject for
further investigation. Although lateral gene transfer is evident in
this group of universally conserved non-three-domain genes, the numbers
of transfers are still relatively low, indicating that lateral gene
transfer was not extensive among these genes (Table 1; Snel et al.
2002).
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METHODS
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Phylogenetic Analyses
More than 3100 COGs from 34 sequenced bacterial, archaeal, and
eucaryal genomes available in the COG database were surveyed. Although
additional genome sequences continue to be determined, the generality
of these results is unlikely to be affected substantially by additional
genomic sequences. Eighty of the COGs surveyed were found to occur in
all organisms (Table 1). The phylogenetic relationships of these COGs
were then examined using PAUP version 4.0b8 (Swofford 1998). Alignments
were obtained from the COG database, and orthologs from Drosophila
melanogaster and Caenorhabditis elegans genomes
(identified in the COG database) were added to the alignment using the
CLUSTAL W program (Aiyar 2000).
Phylogenetic analyses were performed on all of the final alignments of
the amino acid sequences. A maximum parsimony (MP) heuristic search
with 10 random addition sequence searches was performed to find the
most parsimonious tree or sets of trees (summarized by strict
consensus). A distance analysis of the sequence was also performed
using the neighbor-joining (NJ) method. To determine the confidence
levels for each tree, an MP bootstrap analysis with 100 replicates (10
random addition sequence searches per replicate) and an NJ bootstrap
with 500 replicates were conducted. Although the sequence alignments
used in the phylogenetic analyses contained clear regions of homology
between all of the sequences, they sometimes also contained poorly
aligned sections due to insertions or deletions that had accumulated
over evolutionary time. To test the effect of these poorly aligned
regions on the phylogenetic analyses, we repeated the NJ and MP
phylogenetic analyses on a selection of 10 different COG data sets
after excluding the poorly aligned regions in these alignments
(three-domain: COG0048, CO0080, COG0180, COG0198, COG0201;
non-three-domain: COG0013, COG0092, COG0143, COG0495, COG0550). These
particular alignments were chosen because they included a broad array
of alignment sizes, varying from 248 positions in the smallest multiple
sequence alignment to 1488 positions in the largest. Excluding poorly
aligned regions of these alignments did not significantly alter the
resulting phylogenetic topologies and had no effect on the
interpretation of whether any of these particular COG protein groups
were three-domain. Based on these results, we concluded that the
CLUSTAL W alignments were appropriate for answering the question of
whether particular COGs were three-domain and that the poorly aligned
sections had a negligible effect on the phylogenetic analyses.
Because MP and uncorrected NJ analyses underestimate the rates of
change in amino acid sequences, we tested whether rate-corrected
distance and maximum likelihood (ML) analyses affected the
interpretation of phylogenetic relationships within COG protein groups.
NJ analyses using PAM amino acid distance corrections, available with
the Phylip phylogeny package (Felsenstein 1993), were preformed with
the various COG alignments. In addition, we used the ML approach for
protein sequence data sets, available with the Molphy phylogenetic
analysis package
(http://www.ism.ac.jp/software/ismlib/softother.e.html#molphy), to
determine whether there was support for alternative topologies. The
protein ML analyses utilized the JTT (Jones, Taylor, and Thornton)
model of protein sequence evolution (Jones et al. 1992). Because ML
analyses tend to be computationally intensive, we used the NJ trees
with the PAM distance corrections as starting trees and assessed the
likelihood of local topology rearrangements. None of the rate-corrected
analyses found tree topologies significantly different from the
uncorrected analyses.
The publication costs of this article
were defrayed in part by payment of page charges. This article must
therefore be hereby marked "advertisement" in accordance with 18
USC section 1734 solely to indicate this fact.
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WEB SITE REFERENCES
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http://www.ism.ac.jp/software/ismlib/softother.e.html#molphy;
MOLPHY computer package that allows the user to run either the ProtML
or NucML programs on their sequence data.
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Footnotes
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4 These authors contributed equally to this work. 
5 Corresponding author.
E-MAIL nrpace{at}colorado.edu; FAX (303) 492-7744.
Article and publication are at
http://www.genome.org/cgi/doi/10.1101/gr.652803. Article published online before print in February
2003.
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Received July 24, 2002;
accepted in revised format December 11, 2002.
13:407-412 © by 2003 Cold Spring Harbor Laboratory Press ISSN 1088-9051/03 $5.00
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