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Critical Reviews in Microbiology, 31:101–135, 2005
c Taylor & Francis Inc.
Copyright ISSN: 1040-841X print / 1549-7828 online
DOI: 10.1080/10408410590922393
Protein Signatures Distinctive of Alpha Proteobacteria and
Its Subgroups and a Model for α-Proteobacterial Evolution
Radhey S. Gupta
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Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada
Alpha (α) proteobacteria comprise a large and metabolically
diverse group. No biochemical or molecular feature is presently
known that can distinguish these bacteria from other groups. The
evolutionary relationships among this group, which includes numerous pathogens and agriculturally important microbes, are also
not understood. Shared conserved inserts and deletions (i.e., indels
or signatures) in molecular sequences provide a powerful means
for identification of different groups in clear terms, and for evolutionary studies (see www.bacterialphylogeny.com). This review
describes, for the first time, a large number of conserved indels in
broadly distributed proteins that are distinctive and unifying characteristics of either all α-proteobacteria, or many of its constituent
subgroups (i.e., orders, families, etc.). These signatures were identified by systematic analyses of proteins found in the Rickettsia
prowazekii (RP) genome. Conserved indels that are unique to αproteobacteria are present in the following proteins: Cytochrome
c oxidase assembly protein Ctag, PurC, DnaB, ATP synthase αsubunit, exonuclease VII, prolipoprotein phosphatidylglycerol
transferase, RP-400, FtsK, puruvate phosphate dikinase, cytochrome b, MutY, and homoserine dehydrogenase. The signatures in
succinyl-CoA synthetase, cytochrome oxidase I, alanyl-tRNA synthetase, and MutS proteins are found in all α-proteobacteria, except the Rickettsiales, indicating that this group has diverged prior
to the introduction of these signatures. A number of proteins contain conserved indels that are specific for Rickettsiales (XerD integrase and leucine aminopeptidase), Rickettsiaceae (Mfd, ribosomal
protein L19, FtsZ, Sigma 70 and exonuclease VII), or Anaplasmataceae (Tgt and RP-314), and they distinguish these groups from
all others. Signatures in DnaA, RP-057, and DNA ligase A are
commonly shared by various Rhizobiales, Rhodobacterales, and
Caulobacter, suggesting that these groups shared a common ancestor exclusive of other α-proteobacteria. A specific relationship
between Rhodobacterales and Caulobacter is indicated by a large
insert in the Asn-Gln amidotransferase. The Rhizobiales group
of species are distinguished from others by a large insert in the
Trp-tRNA synthetase. Signature sequences in a number of other
proteins (viz. oxoglutarate dehydogenase, succinyl-CoA synthase,
LytB, DNA gyrase A, LepA, and Ser-tRNA synthetase) serve to
distinguish the Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae
families from Bradyrhizobiaceae and Methylobacteriaceae. Based
Received 20 December 2004; accepted 8 December 2005.
Address correspondence to Radhey S. Gupta, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton,
Ontario, Canada L8N 3Z5. E-mail: [email protected]
on the distribution patterns of these signatures, it is now possible to logically deduce a model for the branching order among
α-proteobacteria, which is as follows: Rickettsiales → Rhodospirillales-Sphingomonadales → Rhodobacterales-Caulobacterales
→ Rhizobiales (Rhizobiaceaea-Brucellaceae-Phyllobacteriaceae,
and Bradyrhizobiaceae). The deduced branching order is also consistent with the topologies in the 16 rRNA and other phylogenetic
trees. Signature sequences in a number of other proteins provide evidence that α-proteobacteria is a late branching taxa within Bacteria, which branched after the δ,-subdivisions but prior to the β,γproteobacteria. The shared presence of many of these signatures in
the mitochondrial (eukaryotic) homologs also provides evidence of
the α-proteobacterial ancestry of mitochondria.
Keywords
Bacterial Phylogeny; Alpha Proteobacteria Trees; Protein Signatures; Rickettsiales; Rhodobacterales; Branching Order; Mitochondrial Origin; Rickettsia prowazekii;
Rhizobiales
INTRODUCTION
The alpha (α) proteobacteria comprise an important group
within Bacteria, which has contributed seminally to many aspects of the history of life (Margulis 1970; Kersters et al. 2003).
It is now established that mitochondria, which enable eukaryotic cells to produce energy via oxidative phosphorylation, are
the result of endosymbitotic capture of an α-proteobacteria by
the primitive eukaryotic cell (Margulis 1970; Falah & Gupta
1994; Viale & Arakaki 1994; Andersson et al. 1998; Gray et al.
1999; Karlin & Brocchieri 2000; Emelyanov 2001a; Esser et al.
2004). There is also strong evidence indicating that the ancestral eukaryotic cell itself may have originated via a fusion, or
long-term symbiotic association, event between one or more αproteobacteria and an archaebacteria (or Archaea) (Gupta et al.
1994; Lake & Rivera 1994; Gupta & Golding 1996; Margulis
1996; Gupta 1998; Martin & Muller 1998; Ribeiro & Golding
1998; Andersson et al. 1998; Karlin et al. 1999; Lang et al. 1999;
Kurland & Andersson 2000; Emelyanov 2001a, 2003b). The
symbiosis between α-proteobacteria (viz. Rhizobiaceae species)
and plant root nodules plays a central role in the fixation of atmospheric nitrogen by plants (Sadowsky & Graham 2000; Van
Sluys et al. 2002; Kersters et al. 2003; Sawada et al. 2003). Additionally, many α-proteobacterial species (viz. Rickettsiales,
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Brucella, Bartonella) are adapted to intracellular life style and
are major human and animal pathogens (Moreno & Moriyon
2001; Kersters et al. 2003; Yu & Walker 2003).
The α-proteobacteria exhibit enormous diversity in terms of
their morphological and metabolic characteristics and they include numerous phototrophs, chemolithotrophs and chemoorganotrophs (Stackebrandt et al. 1988; De Ley 1992; Kersters et al.
2003). This group also harbors all known aerobic photoheterotrohic bacteria, which contain bacteriochlorophyll a, but are unable
to grow photosynthetically under anaerobic conditions (Yurkov
& Beatty 1998). These bacteria are abundant in the upper layers
of oceans (Kolber et al. 2001). The α-proteobacterial species are
presently recognized on the basis of their branching pattern in
the 16S rRNA trees, where they form a distinct clade within the
proteobacterial phylum (Woese et al. 1984; Stackebrandt et al.
1988; Olsen et al. 1994; Gupta 2000; Kersters et al. 2003). This
group has been given the rank of a Class or subdivision within
the Proteobacteria phylum (Stackebrandt et al. 1988; Murray
et al. 1990; De Ley 1992; Stackebrandt 2000; Ludwig & Klenk
2001; Garrity & Holt 2001; Kersters et al. 2003). Other than
their distinct branching in the 16S rRNA or other phylogenetic
trees (De Ley 1992; Viale et al. 1994; Eisen 1995; Gupta et al.
1997; Gupta 2000; Stepkowski et al. 2003; Emelyanov 2003a;
Battistuzzi et al. 2004), there is no reliable phenotypic or molecular characteristic known at present that is uniquely shared by
different α-proteobacteria which distinguish them from all other
bacteria (Kersters et al. 2003). On the basis of 16S rRNA trees the
α-proteobacteria have been divided into seven main subgroups
or orders (viz. Caulobacterales, Rhizobiales, Rhodobacterales,
Rhodospirillales, Rickettsiales, Sphingomondales, and Parvularucales) (Maidak et al. 2001; Garrity & Holt 2001; Kersters
et al. 2003). However, the branching order and interrelationships among these subgroups are presently not resolved and no
distinctive features that can distinguish these groups from each
other are known (Kersters et al. 2003).
In our recent work, we have been utilizing a new approach
based on identification of conserved indels (also referred to as
signatures) in proteins sequences that is proving very useful in
identifying different groups within Bacteria in clear molecular terms and clarifying evolutionary relationships among them
(see www.bacterialphylogeny.com) (Gupta 1998, 2003, 2004;
Griffiths & Gupta 2002, 2004a; Gupta & Griffiths 2002; Gupta
et al. 2003). We have previously described many protein signatures that are distinctive characteristics of the proteobacterial phylum and which also provided information regarding its
branching position relative to other bacterial groups (Gupta 1998,
2000; Griffiths & Gupta 2004b). This review focuses on examining the evolutionary relationships among α-proteobacteria
using the signature sequence as well as traditional phylogenetic approaches. In recent years, complete genomes of several α-proteobacteria (viz. Bartonella henselae, Bart. quintana,
Bradyrhizobium japonicum, Brucella melitensis, Bru. suis,
Caulobacter crescentus, Mesorhizobium loti, Sinorhizobium loti,
Rhodopseudomonas palustris, Agrobacterium tumefaciens, Rick-
ettsia conorii, Ri. prowazekii, Ri. typhi, and Wolbachia sp.
(Drosophila endosymbiont)) have become available (Andersson et al. 1998; Kaneko et al. 2000, 2002; Nierman et al. 2001;
Wood et al. 2001; Ogata et al. 2001; Galibert et al. 2001;
DelVecchio et al. 2002; Paulsen et al. 2002; Larimer et al. 2004;
McLeod et al. 2004). These provide valuable resources for identifying novel molecular features that are likely distinctive characteristics of α-proteobacteria and its various subgroups, and
which may prove helpful in clarifying the evolutionary relationships among them. This article, describes for the first time,
a large number of conserved indels in widely distributed proteins that are either uniquely shared by all α-proteobacteria, or
which are shared by only particular subgroups (i.e., families or
orders) of this Class. These signatures provide novel and definitive molecular means for distinguishing α-proteobacteria and
many of its subgroups from all other bacteria. The distribution
of these signatures in different α-proteobacteria also enables one
to logically deduce the relative branching orders and interrelationships among different α-proteobacteria subgroups. Phylogenetic studies have also been carried out based on 16S rRNA
and a number of proteins sequences. Based on this information, a detailed model for the evolutionary relationships among
α-proteobacteria has been developed.
PHYLOGENETIC TREE FOR ALPHA PROTEOBACTERIA
BASED ON 16S rRNA SEQUENCES
Although α-Proteobacteria comprise a major group within
Bacteria (Garrity & Holt 2001) with >5200 sequences in the
Ribosomal Database Project II (Maidak et al. 2001), there is no
detailed review or article that discusses the evolutionary relationships among this group (i.e. indicating the relationships among
different subgroups and orders within this Class) (Kersters et al.
2003). Most of the articles on α-Proteobacteria are aimed at clarifying the phylogenetic placement of particular species at either
genus or family levels (Dumler et al. 2001; Gaunt et al. 2001;
Young et al. 2001; Taillardat-Bisch et al. 2003; van Berkum
et al. 2003; Broughton 2003; Stepkowski et al. 2003; Sawada
et al. 2003). The second edition of Bergey’s Manual (Ludwig &
Klenk 2001) and the third edition of Prokaryotes (Kersters et al.
2003) present condensed phylogenetic trees for the α-Proteobacteria (or Proteobacteria) as a whole to indicate presumed
relationships among different subgroups comprising this subdivision. However, most of these trees do not show any bootstrap scores or even individual species (Ludwig & Klenk 2001;
Kersters et al. 2003), making it difficult to get a clear sense of the
reliability of the observed (or indicated) relationships. Hence,
as an initial step toward understanding the evolutionary relationships among α-Proteobacteria, a phylogenetic tree based on
16S rRNA sequences was constructed from 65 α-proteobacterial
species, covering its major subgroups. The resulting neighborjoining bootstrapped consensus tree is presented in Figure 1.
The tree shown was rooted using the 16S rRNA sequences from
epsilon proteobacteria, which show deeper branching than the
α-subdivision in the rRNA as well as various other trees (Olsen
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
FIG. 1. A neighbor-joining bootstrap consensus tree for α-proteobacteria based on 16S rRNA sequences. The tree was bootstrapped 100 times and bootstrap
scores which were >60 are indicated on the nodes. The tree was rooted using H. pylori. However, the tree topologies was not altered on rooting with other
deep branching bacteria (e.g., Aq. aeolicus). The groups of species corresponding to some of the main subgroups within α-proteobacteria are marked. ∗ indicates
anomalous branching in the tree.
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et al. 1994; Viale et al. 1994; Eisen 1995; Gupta 1998). The
bootstrap scores for all nodes, which were >60 (out of 100) are
indicated on the tree.
In the resulting tree a number of different clades are either
clearly (>90% bootstrap score) or reasonably well resolved.
These included the clades corresponding to group of species
which are recognized as major orders within the α-Proteobacteria
(Rhizobiales, Rhodospirillales, Caulobacterales, Sphingomonadales, Rhodobacterales, and Rickettsiales) (Ludwig & Klenk
2001; Garrity & Holt 2001; Kersters et al. 2003). Within Rhizobiales, the Bradyrhizobiaceae family of species was clearly
separated from some of the other families within this order
(viz. Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae)
(Wang et al. 1998; Sadowsky & Graham 2000; Dumler et al.
2001; van Berkum et al. 2003; Stepkowski et al. 2003). Within
α-Proteobacteria, the deepest branching was observed for the
Rickettsiales group of species. Within the Rickettsiales, the Rickettsia, and Orientia genera, which form part of the Rickttsiaceae family, were clearly resolved from the Anaplasmataceae
family comprised of Ehrlichia, Wolbachia, Anaplasma, and Neorickettsia species (Dumler et al. 2001; Yu & Walker 2003). In
contrast to these well-resolved clades or relationships, various
nodes indicating the interrelationships among different orders
had lower bootstrap scores (<60%), indicating that interrelationships among them were not resolved. The relationships observed here are very similar to those reported in earlier studies
(Olsen et al. 1994; Sadowsky & Graham 2000; Dumler et al.
2001; Yu et al. 2001; Kersters et al. 2003; Yu & Walker 2003;
Stepkowski et al. 2003). The tree shown here will serve as a
useful reference for determining the evolutionary significance
of various signature sequences.
SIGNATURE SEQUENCES DISTINCTIVE OF
α-PROTEOBACTERIA
To identify conserved indels that might be distinctive of αProteobacteria, or a particular groups of species within this
Class, multiple sequence alignments of all proteins that are found
in the genome of Ri. prowazekii (Andersson et al. 1998) were created using the CLUSTAL X program (Jeanmougin et al. 1998).
These alignments were visually inspected for any conserved indels that were mainly restricted to the α-proteobacterial species.
The indels that we focussed on were generally of defined size
and they were present in the same position in a given protein.
The indels of interest were also required to be flanked on both
sides by conserved regions to ensure that the sequence alignment in the region was reliable and that the indel under consideration was not resulting from any alignment artefact (Gupta
1998, 2000; Rokas & Holland 2000; Gupta & Griffiths 2002).
The indels that appeared unique to other groups of bacteria, or
which were present in only a single α-proteobacterial species,
were not further investigated. This has led to identification of
many conserved indels that are specific for α-proteobacteria or
its subgroups. A brief description of these signatures as well as
of the proteins in which they are found is given below.
A. Signature Sequences That are Common to All
α-Proteobacteria
Signature sequences in the following proteins are uniquely
shared by different α-proteobacteria. Cytochrome c oxidase
(CoxI) is an integral component of the respiratory chain in mitochondria and various aerobic bacteria, and it serves as the
terminal electron acceptor (Stryer 1995; Andersson et al. 1998;
Emelyanov 2003a). This membrane-associated complex requires
the association of several protein subunits and the formation of
many different metal centers. One of the proteins involved in
its assembly is Ctag (Cox11), which is required for the formation of CuB and magnesium centers of Cox I (Hiser et al.
2000). In the Ctag protein, a 5 aa insert in a conserved region is
present in all α-proteobacteria, but not found in any other bacteria (Figure 2). Within bacteria the homologs of this protein are
mainly restricted to α, β, and γ -subdivisions of proteobacteria.
Although a protein which carries out a similar function (also
known as Ctag) is present in gram-positive bacteria, it does not
show any sequence similarity to the proteobacterial homologs
(Bengtsson et al. 2004). The observed insert in the Ctag protein
is also present in various eukaryotic homologs, supporting their
derivation from α-proteobacteria.
Another conserved insert that is specific for α-proteobacteria
is present in the enzyme 5 -phosphoribosyl-5-aminoimidazole4-N-succinocarboxamide (SAICAR or PurC) synthetase, which
carries out the seventh step in the de novo purine biosynthetic
pathway (Hui & Morrison 1993; Stryer 1995). The enzyme is encoded by the purC gene and it is broadly distributed in bacteria.
A 3 aa insert in this protein is present in various α-proteobacteria
(Figure 3), but not in any other bacteria, indicating that it is a
distinctive characteristic of the group. The eukaryotic homologs
of the SAICAR synthetase do not contain this insert, but their
overall similarity in this region is limited (not shown). In addition to α-proteobacteria, a 2 aa insert is also present in this
position in Magnetococcus sp. MC-1, suggesting that it may be
distantly related to this group. The phylogenetic assignment of
Magnetococcus sp. MC-1 is presently uncertain (Garrity & Holt
2001).
Two other signatures that are specific for α-proteobacteria are
present in the replicative DNA helicase (DnaB) and the α subunit
of ATP synthase complex. DnaB helicase is a multifunctional
enzyme involved in the DNA replication process (Soni et al.
2003). It interacts with a number of proteins involved in DNA
replication and exhibits multiple enzymatic activities including
helicase, ATP hydrolysis and DNA binding. An insert of between
8 and 14 aa is present in a conserved region of DnaB, which is
unique to various α-proteobacteria (Figure 4). Most of the Rhizobiales as well as Rhodobacter and Caulobacter species are found
to contain the 14 aa insert, whereas a smaller insert is present in
various Rickettsiales and certain other α-proteobacteria. In Mag.
magnetotacticum, three different homologs of DnaB are found
and they all contained the 14 aa insert. Based upon the fact that
this insert is present in the same position in all α-proteobacteria,
it is likely that it was introduced only once in a common ancestor
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
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FIG. 2. Partial sequence alignment for Cytochrome c oxidase assembly protein (Ctag) showing a 5 aa insert (boxed), which is specific for α-proteobacteria.
Dashes in this sequence alignment as well as all others indicate identity with the amino acid on the top line. The position of this sequence in the protein is marked
on the top. The accession numbers of various sequences are shown in the second column. Only representative sequences from different bacteria are shown. The
identified insert is also present in various eukaryotic (mitochondrial) homologs indicating their derivation from an α-proteobacterial ancestor. The abbreviations
used in the species names are listed at the end of this review.
of the group and that subsequent genetic changes led to the observed variation in its length. The DnaB homologs are not found
in eukaryotic species.
The synthesis of ATP in different organisms is carried out
by F1 F0 ATP synthase, a multisubunit complex located in the
cytoplasmic membrane of bacteria or inner membrane of mitochondria (Stryer 1995; Leyva et al. 2003). The F1 portion of this
complex is a heteromer made up of five subunits, α, β, γ , δ and
with the stoichiometry α3 β3 γ δ. The α subunit of ATP synthase contains an 8 aa insert in a highly conserved region that
is commonly present in all α-proteobacteria, but which is not
found in any other proteobacterial species (Figure 5). Besides,
α-proteobacteria, inserts of variable lengths are also present in
this position in various Actinobacteria and Bacteriodetes (not
shown). In phylogenetic tree based on ATP synthase (α), these
latter groups do not show any affinity for each other or to the αproteobacteria (Gupta 2004), indicating that these inserts have
likely been introduced independently. The observed insert in
ATP synthase α is also present in various eukaryotic homologs
providing evidence of their α-proteobacterial ancestry.
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FIG. 3.
Partial sequence alignment of PurC (SAICAR synthetase) showing a 3 aa insert that is specific for various α-proteobacteria.
The enzyme exonuclease VII degrades single-stranded DNA
bidirectionally and processively (Chase et al. 1986). In the large
subunit of exonuclease VII, encoded by the xseA gene, a number
of useful signatures for α-proteobacteria are present. These signatures include a 3 aa insert and a 1 aa deletion that are present
in all known α-proteobacterial homologs (Figure 6A), but not
found in any other groups of bacteria. In the same position where
the 3 aa insert is found, an additional 3 aa insert is present in
all α-proteobacteria except the Rickettsiales. Elsewhere in this
protein, a 1 aa deletion (at position 141 in the Ri. prowazekii sequence) that is unique to various Rickettsia species is also found
(not shown). In a phylogenetic tree based on exonuclease VII sequences (Figure 7), all of the α-proteobacterial homologs formed
a well-defined clade, which was strongly supported by bootstrap
scores. Similar to the rRNA tree, the Rickettsiales species formed
the earliest branching group within the α-proteobacteria, and
both the Rickettsiales clade, as well as a clade comprising of the
remainder of the α-proteobacteria were clearly resolved in this
tree. The inferences from signature sequences are thus strongly
supported by the phylogenetic analysis. The evolutionary stages
where different identified signatures have likely been introduced
in this gene/protein are marked on the tree (Figure 7).
Another insert that is specific for α-proteobacteria is present
in the enzyme prolipoprotein-phosphatidylglycerol (PLPG) transferase, which carries out the first committed step in the pathway
leading to synthesis of lipid modified proteins (Figure 6B) (Qi
et al. 1995). The indicated 3 aa insert in PLPG- transferase is
unique to α-proteobacteria and not found in other bacteria. The
homologs of exonuclease VII and PLPG-transferase were not
detected in eukaryotes.
Two other proteins where α-proteobacteria-specific inserts
are found are, RP-400 and puryvuate phosphate dikinase (PPDK).
The first of these is a protein of unknown function present in the
Ri. prowazekii genome (RP-400), which is distantly related to
murein transglycosylases. This protein contains a 4–6 aa insert
in a conserved region that is a distinctive characteristic of various α-proteobacteria, except Zymomonas mobilis (Figure 8).
The absence of this insert in the latter species could result from
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
FIG. 4.
Partial sequence alignment of replicative DNA helicase, DnaB, showing an 8–14 aa insert that is specific for various α-proteobacteria.
either selective loss, or exchange of this gene from some other
species lacking the insert. PPDK is a key enzyme in photosynthesis, which catalyzes the reversible conversion of phosphoenolpyruvate to pyruvate (Ku et al. 1996). This enzyme is not
found in mammalian cells but it is broadly distributed in bacteria
and plants. A conserved insert in PPDK provides an informative
signature for α-proteobacteria. Rickettsiales species contain a
5 aa insert in this position, whereas a larger insert of 12 aa is
found in various other α-proteobacteria (Figure 9). Interestingly,
an insert of 10 aa is also present in the same position in various
δ-proteobacteria, suggesting a distant relationship of this group
to the α-proteobacteria. Because the insert sequence in various species appears to be related, it is possible that this insert
was originally introduced in a common ancestor of the α- and δproteobacteria. The varying lengths of the inserts in Rickettsiales
and other α-proteobacteria could then result from subsequent
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FIG. 5. Sequence alignment of ATP synthase α subunit showing an 8 aa insert in a highly conserved region that is present in various α-proteobacterial homologs,
but not found in any other proteobacteria. The shared presence of this insert in various eukaryotic homologs provides evidence of their α-proteobacterial ancestry.
genetic changes in the branches leading to these groups. Alternatively, the inserts of different lengths could have been independently introduced in these groups and the observed sequence
similarity may be a consequence of their related function. It is
of interest that in contrast to other α-proteobacteria, which contain only a single PPDK homolog, two homologs of this protein
are found in Bradyrhizobium (Brad.) japonicum. Of these, only
one contained the insert. The homolog lacking the insert is quite
divergent and it is possible that this may have been acquired by
means of lateral gene transfer (LGT) from other bacteria.
Two different proteins, FtsK and Cytochrome b (PetB) contain deletions which are mainly limited to the α-proteobacterial
species. In the FtsK protein, which plays a central role in cell
division and chromosome segregation in bacteria (Capiaux et al.
2002; Espeli et al. 2003), two 1 aa deletions are present in conserved regions that are largely distinctive of α-proteobacteria
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
FIG. 6. Signature sequence in exonucleaseVII (A) and prolipoprotein-phosphatidylglycerol (PLPG) transferase (B) proteins that are distinctive of αproteobacterial species. Exonuclease VII contains a 3 aa insert and a 1 aa deletion that is unique to all α-proteobacteria. The presence of an additional 3 aa
insert distinguishes Rickettsiales species from other α-proteobacteria. The enzyme PLPG-transferase also contains a 3 aa insert that is specific for α-proteobacteria.
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FIG. 7. A neighbor-joining bootstrap consensus tree based on exonucleaseVII sequences. Bootstrap scores >50% are indicated on various nodes. All inserts
and deletions were excluded from the sequence alignment used for phylogenetic analysis. The α-proteobacteria formed a well-defined clade in this tree, however,
their branching position relative to other groups was not resolved. The Rickettsiales order formed the deepest branch within α-proteobacteria and they were also
clearly resolved from other α-proteobacteria. The arrows mark the suggested positions where the identified signatures were introduced in this protein.
(Figure 10). One of these deletions is a distinctive characteristic of all α-proteobacteria and not found in any other bacteria.
The other deletion, in addition to the α-proteobacteria, is
also commonly present in the two Desulfovibrio species
(δ-proteobacteria), suggesting a distant relationship of this group
to α-proteobacteria, as also seen with the PPDK protein (Figure
9). In addition to these deletions, the FtsK protein also contains a 5–6 aa insert that is unique to various α-proteobacteria
in comparison to the other groups of proteobacteria (present in
position corresponding to aa 513–520 in Ri. prowazekii protein).
Since the region where this insert is found exhibits variability
in other bacteria, this signature is not shown. The FtsK protein
has also been previously shown to contain an 8–9 aa insert in a
different region of the protein that is a distinctive characteristic
of various Bacteriodetes and Chlorobium species (Gupta 2004).
The FtsK homologs are not found in most eukaryotic organisms.
However, a homolog of this protein is present in Plasmodium
yoelii (Genebank accession number 23485217). The origin and
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
FIG. 8.
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Partial sequence alignment of RP-400 protein showing a 4–6 aa insert that is specific for various α-proteobacteria, except Z. mobilis.
possible significance of this gene/protein is presently unclear.
A 1 aa deletion that is specific for various α-proteobacteria is
also present in the Cytochrome b (Cyt b; PetB) protein (Figure 11), which is a subunit of the cytochrome reductase, which
is an integral part of the electron transport chain (Daldal et al.
1987; Stryer 1995; Emelyanov 2003a). This indel is not present
in other bacteria including that from Aquifex aeolicus, indicating that it is a deletion in α-proteobacteria, rather than an insert
in other bacteria. Cyt b is one of the 13 proteins that is still
encoded by mitochondrial DNA (Lang et al. 1999). Sequence
information for Cyt b is available from a large number (>500)
of mitochondrial genomes and phylogenetic studies based on
this protein provides evidence for the origin of mitochondria
from within the Rickettsiaceae (Sicheritz-Ponten et al. 1998;
Emelyanov 2003a). Similar to the α-proteobacteria, Cyt b from
all eukaryotic mitochondrial homologs was found to lack this 1
aa indel, providing evidence of their specific relationship to the
α-proteobacteria.
B. Signature Sequences Distinguishing Rickettsiales from
Other α-Proteobacteria
In phylogenetic trees based on 16S rRNA, as well as many
protein sequences, the Rickettsiales are found to form the deepest
branching clade within α-proteobacteria (see Figures 1 and 7)
(Dumler et al. 2001; Gaunt et al. 2001; Yu et al. 2001; Kersters
et al. 2003; Yu & Walker 2003; Stepkowski et al. 2003). We
have identified several signatures that are present in various αproteobacteria, except the Rickettsiales. These signatures are
described below.
The enzyme succinyl CoA-synthetase, which is part of the
citric acid cycle, carries out cleavage of the thioester bond in
succinyl-CoA in a coupled reaction to generate succinate and
producing GTP (Bridger et al. 1987; Stryer 1995). It is the
only step in the citric acid cycle that directly leads to the formation of a high-energy phosphate bond. The beta subunit of
this protein contains a conserved insert of 10 aa, that is commonly present in all other α-proteobacteria, except the Rickettsiales (Figure 12). Surprisingly, this insert is also present
in Ral. metallidurans (a β-proteobacterium), but not in any
other β-proteobacteria, including the closely related species Ral.
solanacearum. This suggests that the Succ-CoA synthetase gene
in Ral. metallidurans has likely originated by non-specific means
such as LGT. A smaller unrelated insert in this region, which is
presumably of independent origin, is also present in Cytophaga
and Rhodopirellula species (not shown). It is of interest that a
7–8 aa insert is also present in this position in various eukaryotic homologs. It is unclear at present, whether this latter insert
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FIG. 9. Excerpt from sequence alignment for pyruvate phosphate dikinase (PPDK) protein showing a signature for α-proteobacteria. The Rickettsiales species
contain a 5 aa long insert, where all other α-proteobacteria have a 12 aa insert in the same position. Two different homologs of PPDK are found in Brad. japonicum,
only one of which is found to contain the insert. A smaller conserved insert of 10 aa is also present in this position in various δ-proteobacteria suggesting that they
may be specifically, but distantly, related to the α-proteobacteria.
has originated from an α-proteobacterial ancestor or it is of independent origin. If these inserts are of common origin, then
this would suggest that the eukaryotic homologs of Succ-CoAsynthetase have originated from an α-proteobacterial ancestor
other than the Rickettsiales. This observation will be at variance
with other evidence pointing to a closer relationship of mitochondria to the Rickettsiales species (Viale & Arakaki 1994;
Gupta 1995; Andersson et al. 1998; Sicheritz-Ponten et al. 1998;
Gray et al. 1999; Lang et al. 1999; Emelyanov 2001a, 2001b,
2003a). Emelyanov (2001a, 2001b) has observed a closer relationship of mitochondrial homologs to certain rickettsial species
(e.g. Holospora obtusa, Caedibactera caryophila), for which
sequence information for this protein is lacking at present. It
is possible that Succ-CoA synthetase from these species may
contain this insert. Presently, the possibility that the insert in
eukaryotic homologs was independently introduced also cannot
be excluded.
Another signature showing a similar distribution pattern has
been identified in cytochrome oxidase polypeptide I (Cox I).
In this case, a 5 aa insert in a conserved region is commonly
present in various α-proteobacterial species except the Rickettsiales (Figure 13). It should be noted that α-proteobacteria
contain two different related proteins. One of these, which harbors this insert seems to correspond to Cox I, whereas the other
homologs lacking the insert are mainly those from Cytochrome
o ubiquinol oxidase (Davidson & Daldal 1987). However, all
Rickettsiales species contain only a single homolog of this protein, corresponding to Cox I. The observed insert in both SuccCoA-synthetase and Cox I were thus likely introduced in a common ancestor of the remainder of the α-proteobacteria after the
branching of Rickettsiales. Similar to the Cyt b, the Cox I in eukaryotic cells is also encoded by mitochondrial DNA (Andersson
et al. 1998; Gray et al. 1999) and sequence information for
this protein is available from a large number of mitochondrial
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FIG. 10. Partial sequence alignments of FtsK protein showing two different signatures (1 aa deletions) that are informative characteristics of α-proteobacteria.
The deletion on the left is unique to various α-proteobacteria, whereas the one on the right is also commonly shared by two Desulfovibrio species (δ-proteobacteria)
suggesting their relatedness to the α-proteobacteria.
genomes. The eukaryotic homologs of Cox I do not contain
the identified insert (results not shown) indicating their possible
derivation from Rickettsiales (Emelyanov 2003a).
Two other proteins were found to contain inserts of variable
lengths in highly conserved regions in various α-proteobacterial
species, with the exception of Rickettsiales (Figure 14). In
alanyl-tRNA synthetase (AlaRS), which is ubiquitously found
in all organisms, an insert of between 5–11 aa is present in
a highly conserved region in various α-proteobacteria, except
the Rickettsiales (and also Mag. magnetotacticum) (Figure 14A).
Another signature showing a similar distribution pattern is found
in the MutS protein, which is involved in the DNA mismatch repair (Sixma 2001; Martins-Pinheiro et al. 2004). In this case, a
conserved insert of 2–5 aa is present in various α-proteobacteria
(Figure 14B), but not in Rickettsiales. The simplest explanation
for these signatures is that they were introduced in an ancestral
α-proteobacterial lineage, after the branching of Rickettsiales
(and also possibly Mag. magnetotacticum). The observed variations in the lengths of these inserts have presumably resulted
from subsequent genetic changes.
We have also identified a number of α-proteobacteria-specific
signatures in proteins for which no homologs are found
in the Rickettsiales. In the MutY protein, which is an A-G
specific DNA glycosylase involved in DNA repair (Parker &
Eshleman 2003; Martins-Pinheiro et al. 2004), a 4–9 aa insert in a conserved region is present in various α-proteobacteria
(Figure 15A). An insert of similar length is also present in most
eukaryotic homologs (with the exception of Anopheles gambiae)
indicating their possible derivation from α-proteobacteria. Another signature showing similar species distribution is present in
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FIG. 11. Partial sequence alignment for Cyt b protein showing a 1 aa deletion that is specific for various α-proteobacteria. This deletion is also present in all
mitochondrial homologs (Cyt b is encoded by mitochondrial DNA) providing strong evidence of their α-proteobacterial ancestry.
the protein homoserine dehydrogenase (Figure 15B). This indel
consists of a 1 aa insert in a conserved region that is present
in various α-proteobacteria, but not any other proteobacteria.
The homologs of both these proteins were not detected in the
Rickettsiales species and their absence is very likely due to selective loss of these genes in a common ancestor of the Rickettsiales
(Martins-Pinheiro et al. 2004), presumably due to the intracellular life-style of these organisms (Boussau et al. 2004). The
observed inserts in these genes could have been introduced in a
common ancestor of the α-proteobacteria, either before or after
the loss of these genes in Rickettsiales.
Several proteins contain conserved inserts that are either unique
for the Rickettsiales or for the two main families, Rickettsiaceae and Anaplasmataceae, comprising this order (Dumler
et al. 2001; Yu & Walker 2003). The Rickettsiales-specific signatures are present in the proteins XerD and leucine aminopeptidase
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FIG. 12. Partial sequence alignment of Succ-CoA synthase showing a 10 aa insert that is present in various α-proteobacteria, except the Rickettsiales. This insert
is not found in other bacteria, except Ral. metallidurans, which has likely acquired it by non-specific means. A smaller insert is also present in this position in
various eukaryotic homologs.
(Figure 16). XerD protein (Figure 16B) is a part of the XerCD
integrase/recombinase that is involved in the cell division process and decatenation of DNA duplexes (Ip et al. 2003). A 7 aa
insert is present in a conserved region of this protein which is
uniquely shared by all Rickettsiales and not found in any other
bacteria (Figure 16A). Another 2 aa insert that is specific for
Rickettsiales is present in leucine aminopeptidase (Figure 16A),
which is an exopeptidase that selectively releases N-terminal
amino acids from peptides and proteins (Gonzales & RobertBaudouy 1996). The signatures that are specific for Rickettsia
include a 4 aa insert in a highly conserved region of the transcription repair coupling factor (Mfd) (Martins-Pinheiro et al.
2004) (Figure 17A), a 10 aa insert in ribosomal protein L19
(Figure 17B) and a 1 aa insert in the FtsZ protein (Figure 17C).
Two additional Rickettsia-specific signatures consisting of a 1
aa insert in the major sigma factor-70 (at position 141 in the R.
prowazekii sequence) and a 1 aa deletion in exouclease VII (at
position 137 in the Ri. prowazekii homolog) were also identified, but they are not shown here. The identified signatures in
these proteins are present only in various Rickettsiaceae species
and not found in other Rickettsiales (viz. Ehrlichia, Wolbachia,
Anaplasma) or other groups of bacteria. Within eukaryotes, a
homolog of the transcription repair-coupling factor is only detected in Arabidoposis thaliana and it lacks the identified insert
(results not shown). The homologs of ribosomal protein L19 are
found in various plants and algae but not in any of the animal
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FIG. 13. Partial sequence alignment of Cox I showing a 5 aa insert that is present in various α-proteobacteria, except Rickettsiales. The other α-proteobacteria
also contains a second more distantly related homolog that lacks this insert.
species. Of these, an 8 aa insert in the same position is present
only in the homolog from Cyanophora paradox (not shown). The
significance and possible origin of this insert is not clear. Similar to the ribosomal protein L19, FtsZ homologs are also found
only in plants but not in animals. These homologs also lacked the
insert that is present in Rickettsiaceae. The plant homologs of
these proteins likely correspond to those of the plastids, which
because of their cyanobacterial ancestry (Gray 1989; Morden
et al. 1992; Margulis 1993; Gupta et al. 2003) are expected to
be lacking Rickettsia-specific signatures.
We have also identified two large inserts that are commonly
shared by the Ehrlichia, Wolbachia, and Anaplasma species but
not found in any of the Rickettsia species or other bacteria. These
signatures include a 15 aa insert in the HlyD family of secretory
protein (Figure 18A) and a 10–11 aa insert in the tRNA guanine
transglycosylase (Tgt) protein (Figure 18B), involved in the synthesis of hypermodified nucleoside queousine (Reuter & Ficner
1995). The eukaryotic homologs of Tgt do not contain this insert
providing evidence against their origin from Anaplasmatacaea
family of species (results not shown). The homologs of HlyD are
not found in eukaryotes. These signatures point to a close relationship between Ehrlichia, Wolbachia, and Anaplasma species,
which is also seen in phylogenetic trees based on many other sequences (Dumler et al. 2001; Gaunt et al. 2001; Yu et al. 2001;
Taillardat-Bisch et al. 2003; Yu & Walker 2003; Stepkowski
et al. 2003; Emelyanov 2003a). These signatures were likely introduced in a common ancestor of the Anaplasmataceae family,
which now includes all Ehrlichia, Anaplasma, Cowdria, Wolbachia, and Neorickettsia species (Dumler et al. 2001; Yu &
Walker 2003).
C. Signature Sequences for Other Subgroups of
α-Proteobacteria and Providing Information Regarding
Their Interrelationships
Signature sequences in a number of other proteins are useful in distinguishing other subgroups of α-proteobacteria and
they also provide information clarifying the interrelationships
among them. In the DnaA protein involved in chromosomal
replication (Messer 2002), a 5 aa insert is present in various Rhizobiales and Caulobacter/Rhodobacter species (Figure 19A).
However, this insert is not found in any of the Rickettsiales, as
well most α-proteobacterial species belonging to the orders Sphingomonadales and Rhodospirillales. The species Mag. magnetotacticum contains two different homologs of this protein,
only one of which is found to contain the insert. Another insert
showing a similar distribution pattern is present in the protein
RP057, which is a homolog of the glucose-inhibited division
protein B (Romanowski et al. 2002). This protein contains a 3 aa
insert that is common to the same subgroups of α-proteobacteria
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FIG. 14. Signature sequences in alanyl-tRNA synthetase (AlaRS) and MutS proteins that are informative for the α-proteobacteria. In AlaRS (upper panel)
an insert of variable length in a highly conserved region is present in various α-proteobacteria, except the Rickettsiales and Mag. magentotacticum. The DNA
mismatch repair protein MutS (lower panel) also contains a 3–5 aa insert in various α-proteobacteria, except Rickettsiales. The inserts lengths in this case also
serve to differentiate Rhodospirillales and Sphingomonadales species from the Rickettsiales, Rhodobacterales, and Caulobacterales.
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FIG. 15. Partial sequence alignments of MutY (upper panel) and homoserine dehydrogenase (lower panel) proteins showing inserts (boxed) in conserved regions
that are specific for α-proteobacteria. The homologs of both these proteins are not found in the Rickettsiales. For MutY, an insert of approximately similar length
is also present in various eukaryotic homologs, with the exception of Anopheles gambiae.
as the insert in the DnaA protein, but which is not found in
the Rickettsiales or Rhodospirillales/Sphingomonadales species
(Figure 19B). The variable length inserts are also present in
this position in other bacteria (not shown). However, within
proteobacteria this insert is limited to the above subgroups of
α-proteobacteria. Based on the distribution patterns of these
signatures, these inserts were likely introduced in a common
ancestor of the Rhizobiales and Caulobacter/Rhodobacter
after the branching of Rickettsiales and Rhodospirillales/
Sphingomonadales orders (Figure 19C).
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FIG. 16. Signature sequences in XerD integrase (upper panel) and leucine aminopeptidase (lower panel) that are distinctive of the Rickettsiales order and not
found in other α-proteobacteria or other bacteria.
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FIG. 17. Signature sequences in transcription repair coupling factor Mfd (A), Ribosomal protein L19 (B), and FtsZ (C) proteins that are distinctive of Rickettsia
species and not found in other α-proteobacteria including Anaplasmataceae family (e.g., Wolbachia, Ehrlichia, Anaplasma) of species. Two additional signatures
showing similar distribution are found in the sigma factor-70 and exonuclease VII proteins.
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FIG. 18. Signature sequences in RP-314 (A) and tRNA guanine transglycosylase (Tgt) (B) proteins that are distinctive of the Anaplasmataceae family of species
and not found in Rickettsia or various other bacteria.
The protein DNA ligase (NAD dependent; Lig A) contains a
12 aa insert in a highly conserved region that is commonly shared
by various Rhizobiales as well as Rhodobacterales species
(Figure 20A), but which is not found in C. crescentus, Rhodospirillales (Rhodo. rubrum, Mag. magnetotacticum), and Sph-
ingomonadales (Z. mobilis, Novo. armoaticivorans). The absence of this insert in the Mesorhizobium sp. BNC1, is somewhat surprising, but it could result from non-specific mechanisms. This signature suggests that Rhizobiales species may
be more closely related to Rhodobacterales in comparison to
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FIG. 19. Partial sequence alignments of DnaA (panel A) and RP-057 (panel B) proteins showing inserts in conserved regions (boxed) that are only present in
various Rhizobiales, Rhodobacterales, and Caulobacter, but not found in other α-proteobacteria or bacteria. These inserts were likely introduced in a common
ancestor of the above groups after the branching of Rickettsiales, Rhodospirillales, and Sphingomonadales as indicated in panel C.
Caulobacter and other α-proteobacteria. However, another prominent insert (11 aa) in a highly conserved region of the protein
aspargine-glutamine amidotransferase points to a specific relationship between Rhodobacterales and Caulobacter species
(Figure 20B), to the exclusion of all other α-proteobacteria.
Martins-Pinheiro et al. (2004) have reported phylogenetic analysis based on LigA sequences. The α-proteobacteria formed
a distinct clade in the tree, but they consisted of only certain
Rhizobiaceace and Caulobacter species (Martins-Pinheiro et al.
2004). To fully understand the evolutionary significance of these
signatures, it would be necessary to obtain sequence information
for these proteins from additional Caulobacterales.
We have also identified many conserved inserts that are
specific for species belonging to the Rhiziobiales order. The
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FIG. 20. Signature sequences in DNA ligase A and (upper panel) and Asn-Gln amidotransferase (lower panel) that are informative for α-proteobacteria. The
signature in DNA ligase is commonly shared by various Rhizobiales as well as C. crescentus species, while that in the Asn-Gln amidotransferase is uniquely shared
by Rhodobacterales and Caulobacter, indicating a specific relationship between these subgroups.
Trp-tRNA synthetase (TrpRS) contains a large insert in a
highly conserved region which is uniquely shared by various
Rhizobiales species (Figure 21A), but not found in any of the
other α-proteobacteria or other groups of bacteria (results for
other groups of bacteria not shown). The absence of this insert in
various Rickettsiales, Rhodospirillales, Sphingomonadales, and
Rhodobacterales as well as Caulobacter provides evidence that
these groups have branched off prior to the introduction of this
insert (Figure 21A). The length of the insert in TrpRS also serves
to distinguish the Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae family of species from those belonging to Bradyrhizobiaceae and Methylobacteriaceae. The insert in the former group
of species is 19 aa long, whereas the latter species contain only a
9–10 aa insert. Because the insert sequence in all of these species
is conserved, it is likely that the insert was introduced only once
in a common ancestor of the Rhizobiales and subsequent modification has led to the observed length variation. The distinctness
of Bradyrhizobium and Rhodopseudomonas from other Rhizobiales is also supported by a signature (3 aa insert) in Seryl-tRNA
synthetase (SerRS), which is uniquely present in these species
(Figure 21B) and it serves to distinguish them from other Rhizobiales as well as other α-proteobacteria. A schematic diagram
indicating the suggested positions where signatures described in
Figures 20 to 23 have been introduced is presented in Figure 21C.
We have also identified several signatures that are uniquely
present in the Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae families of species, but not found in other α-proteobacteria
including Bradyrhizobium and Rhodopseudomonas. These signatures include a 7 aa insert in Oxoglutarate dehydrogenease
(Figure 22A), a 5 aa insert in Succ-CoA synthase (Figure 22B),
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FIG. 21. Signature sequences in Trp-tRNA synthetase (upper panel) and Ser-tRNA synthetase (lower panel) that are informative for α-proteobacteria. The first
of these signatures is specific for Rhizobiales. The insert length in this signature also distinguishes Bradyrhizobiaceae and Methylobacteriaceae species from other
Rhizobiales. The insert in the Ser-tRNA synthetase is specific for the Bradyrhizobiaceae species and distinguishes this family from other Rhizobiales.
a 3 aa insert in LytB metalloproteinase (Figure 23A) and a 2 aa
insert in DNA gyrase A subunit (Figure 23B). A smaller insert
in oxoglutarate dehydrogenase is also present in Novosphingobacteria, but since its sequence is unrelated, it is either of independent origin or could have resulted from LGT. In addition
to these proteins, a 1–2 aa insert that is specific for Rhizobiaceae is also found in a conserved region of the LepA protein
(Figure 23C). The evolutionary positions where these signatures have been introduced are indicated in Figure 21C. It is
of interest that in contrast to other Rhizobiaceae species, which
contain only 1 aa inserts, Sinorhizobium meliloti and Agrobacterium tumefacienes are found to contain 2 aa inserts in the LepA
protein (Figure 23C). This observation points to a specific relationship between these two Rhizobiaceae species, as has been
suggested based on other lines of evidences (Young et al. 2001).
A 2 aa insert in the DnaK protein, which is commonly shared
by species belonging to Rhizobium and Sinrhizobium genera, as
well as Ehrlichia and a few other proteobacteria, has also been
described by Stepkowski et al. (2003).
D. Signature Sequences Indicating the Phylogenetic
Placement of α-Proteobacteria
A number of signatures described in earlier work have indicated that proteobacteria is a late branching phylum in comparison to other main groups within Bacteria (Gupta 1998, 2000,
2003; Gupta & Griffiths 2002; Griffiths & Gupta 2004b). These
signatures included a 4 aa insert in alanyl-tRNA synthetase, an
insert of >100 aa in RNA polymerase β (RpoB) subunit, a 10
aa insert in CTP synthase, a 2 aa insert in inorganic pyrophosphatase, and a 2 aa insert in Hsp70 protein. The identified signatures in these proteins were present in all proteobacterial homologs, but they were absent from most other bacterial phyla
(viz. Firmicutes, Actinobacteria, Thermotogae, DeinococcusThermus, Cyanobacteria, Spirochetes). In a number of cases,
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125
FIG. 22. Signature sequences in Oxoglutarate dehydrogenase (upper panel) and Succ-CoA synthase (lower panel) proteins that are commonly shared by only
certain Rhizobiales families (e.g., Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae), and not found in Bradyrhizobiaceae or other α-proteobacteria.
where the corresponding proteins were present in Archaea (viz.
RpoB, Hsp70, AlaRS), the archael homologs also lacked the indicated inserts, indicating that the absence of these indels constitute the ancestral states and that these signatures were introduced after branching of the groups lacking these indels (Gupta
& Griffiths 2002; Gupta 2003; Griffiths & Gupta 2004b). A number of identified signatures (7 aa insert in SecA, 1 aa deletion in
the Lon protease) were uniquely shared by only the α, β, and
γ -proteobacteria, providing evidence of the later branching of
these subdivisions (Gupta 2000, 2001, 2003). Two additional
signatures that are helpful in understanding the phylogenetic
placement of α-proteobacteria are described in the following
section.
Figure 24 shows the excerpt from a sequence alignment for
the transcription termination factor Rho, which is an RNAbinding protein that plays a central role in the RNA chain
termination (Opperman & Richardson 1994). This protein is
present in all main groups of bacteria, except cyanobacteria
(Gupta & Griffiths 2002; Gupta 2003), where RNA chain termination presumably occurs via a Rho-independent mechanism.
A 3 aa insert is present in a highly conserved region of Rho,
which is a distinctive characteristic of all α, β, and γ -proteobacteria. The length of this insert is 2–3 aa longer in various
Rickettsiales species, which suggests an additional insert in this
group of bacteria. In contrast to the α, β, and γ -proteobacteria,
this insert is not present in δ, ε-proteobacteria or any other
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FIG. 23. Signature sequences in LytB (A), DNA gyrase A (B) and LepA proteins that are distinctive characteristics of only certain Rhizobiales families (e.g.,
Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae), but not found in Bradyrhizobiaceae or other α-proteobacteria.
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FIG. 24. Partial sequence alignment of Rho protein showing a conserved insert that is commonly shared by various α, β, and γ -proteobacteria, but not found in
any other groups of bacteria including the δ,-proteobacteria and all other phyla of gram-positive and gram-negative bacteria. This insert was likely introduced in a
common ancestor of the α, β, and γ -proteobacteria after the branching of other bacterial phyla (see Figure 26). Many other signatures showing similar distribution
pattern and supporting the indicated branching position of α, β, and γ -proteobacteria have been described in earlier work.
groups of Gram-negative and Gram-positive bacteria. This
signature provides evidence that the groups consisting of α,
β, and γ -proteobacteria have branched off late in comparison to the other groups of bacteria. Another novel signature
that is useful in understanding the branching position of αproteobacteria is present in the ATP synthase alpha subunit.
In this case, an 11 aa insert in a highly conserved region
is present in various β and γ -proteobacteria, but it is not
found in any α-proteobacteria or other groups of bacteria (Figure 25). The absence of this insert in various other bacteria as
well as archael homologs provides evidence that it was introduced in a common ancestor of the β and γ -proteobacteria after the divergence of other bacteria, including α-proteobacteria
(Figure 26).
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FIG. 25. Partial sequence alignment of ATP synthase α-subunit showing a highly conserved insert that is commonly shared by various β and γ -proteobacteria,
but not found in any other groups of bacteria including the α- and δ,-proteobacteria and all other phyla of Gram-positive and Gram-negative bacteria. This insert
is also not present in archael or eukaryotic homologs indicating that it was introduced in a common ancestor of the β and γ -proteobacteria after the branching of
all other groups including α-proteobacteria. Other signatures showing similar relationships have been described in earlier work (Gupta 1998, 2000, 2001, 2003).
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
FIG. 26. Evolutionary relationships among α-proteobacteria based on signature sequences in different proteins. The branching position of α-proteobacteria
relative to other groups of bacteria is based on signature sequences such as those shown in Figures 24 and 25. The evolutionary stages where these signatures have
been introduced are indicated by thick arrows. Many other signatures that are helpful in resolving the branching order of other groups have been described in our
earlier work (Gupta 1998, 2000, 2001, 2003, 2004; Gupta & Griffiths 2002; Griffiths & Gupta 2004b (see also www.bacterialphylogeny.com)). The evolutionary
relationship among α-proteobacteria shown here was deduced based on the distribution patterns of different signatures described in this review. The long thin
arrows mark the positions where the signature sequences in various proteins have likely been introduced.
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CONCLUSIONS
The α-proteobacteria are a morphologically and metabolically very diverse group of organisms, which are presently recognized as a distinct group solely on the basis of their branching
pattern in the 16S rRNA tree (Woese et al. 1984; Stackebrandt
et al. 1988; Murray et al. 1990; De Ley 1992; Ludwig & Klenk
2001; Kersters et al. 2003). No biochemical, molecular or other
features are presently known, which are uniquely shared by
various α-proteobacteria and that can clearly distinguish this
group from all others. The evolutionary relationships within
this group of bacteria are also presently not understood. This
review describes many novel signatures consisting of conserved
inserts and deletions in widely distributed proteins that provide
definitive means for defining the α-proteobacteria and many of
its subgroups, and for understanding evolutionary relationships
among them. Because of the rarity and highly specific nature of
these genetic changes, the possibility of their arising independently by either convergent or parallel evolution is low (Gupta
1998; Rokas & Holland 2000). The simplest and most parsimonious explanation for such rare genetic changes, when restricted to a particular clade(s), is that they were introduced
only once in common ancestors of the particular group(s) and
then passed on to various descendants. The signature approach
has proven very useful in the past in clarifying a number of
important evolutionary relationships, which could not be reliably resolved based on phylogenetic trees (Rivera & Lake 1992;
Baldauf & Palmer 1993). Our earlier work has identified many
signatures that are either specific for particular groups of bacteria (viz. chlamydiae, cyanobacteria, Bacteroidetes-ChlorobiFibrobacter, Deinococcus-Thermus, Proteobacteria) (Gupta
2000, 2004; Griffiths & Gupta 2002, 2004a; Gupta et al. 2003),
or which are commonly shared by certain bacterial phyla providing information regarding their interrelationships (Gupta 1998,
2003; Gupta & Griffiths 2002; Griffiths & Gupta 2004b).
A summary of the different signatures that were described
in this review and the overall picture of α-proteobacterial evolution that emerges based upon them is presented in Figure 26.
Most of the signatures described here were unique for either all
α-proteobacteria or certain of its subgroups, and except for a few
isolated instances, they were not found in other bacteria. These
finding provides evidence that the genes containing these signatures have not been laterally transferred from α-proteobacteria
to other bacteria, although LGT for certain other genes have
been previously reported (Wolf et al. 1999). A large number
of these signatures, present in broadly distributed proteins (cytochrome assembly protein Ctag, SAICAR synthetase, DnaB,
ATP synthase α, exonuclease VII, PLPG transferase, RP-400,
puruvate phosphate dikinase, FtsK, and Cyt b) were distinctive
characteristics of all α-proteobacteria. Two additional proteins,
MutY and homoserine dehydrogenase, also contain signatures
that were specific for α-proteobacteria. However, the homologs
of these proteins were not found in Rickettsiales. These signatures, for the first time, describe molecular characteristics that
unify all α-proteobacteria, and provide means to clearly distin-
guish them from all other bacteria. The unique presence of these
signatures in various α-proteobacteria, which is a very diverse
group (Kersters et al. 2003), strongly suggests that these indels
should be functionally important for this group of organisms.
Hence, studies examining their functional effects should be of
much interest.
Signature sequences in other proteins are helpful in defining
many of the α-proteobacteria subgroups and in clarifying evolutionary relationships among them. A number of proteins, which
include, Succ-CoA synthetase, Cox I, AlaRS, and MutS, contain
conserved inserts that are shared by all other α-proteobacteria,
except the Rickettsiales. The homologs of these proteins from
other bacteria also lack these indels providing evidence that these
signatures were introduced in a common ancestor of other αproteobacteria after the divergence of Rickettsiales. The Rickettsiales order also consistently forms the deepest branching
lineage in 16S rRNA and various protein trees (Dumler et al.
2001; Gaunt et al. 2001; Kersters et al. 2003; Yu & Walker
2003; Stepkowski et al. 2003). Signature sequences in a number of proteins were found to be specific for either the Rickettsiales order (viz. XerD integrase and leucine aminopeptidase)
or the two main families, Rickettsiaceae (viz. transcription repair
coupling factor, ribosomal protein L19, and FtsZ proteins) and
Anaplasmataceae (RP-314 and Tgt proteins). These signatures
were likely introduced in the common ancestors of these groups.
These groups are also clearly distinguished in the phylogenetic
trees based on 16S rRNA (Figure 1) (Dumler et al. 2001; Yu &
Walker 2003) and various proteins (Figure 7) (Stepkowski et al.
2003; Emelyanov 2003a).
Signature sequences in a number of proteins (viz. chromosomal replication factor, RP-057 and DNA ligase) were commonly
shared by various Rhizobiales, Rhodobacterales, and in most
cases Caulobacterales (currently represented by only C. crescentus), but they were not present in Rickettsiales, Rhodospirillales as well as Sphingomonadales species. These results provide evidence that the groups lacking these signatures diverged
prior to the introduction of these signatures. A unique signature
has also been identified for the Rhizobiales order (viz. TrpRS),
and one which is commonly shared by Rhodobacterales and C.
crescentus. The latter signature suggests a specific relationship
between the Rhodobacterales and Caulobacter groups. The relationships indicated by these signatures are also generally supported by the phylogenetic trees based on 16S rRNA and various
proteins (Gaunt et al. 2001; Kersters et al. 2003; Stepkowski et al.
2003; Emelyanov 2003a). Signatures sequences in a number
of other proteins (viz. oxoglutarate dehydrogenase, Succ-CoA
synthase, DNA gyrase A, LepA, and LytB), are able to distinguish the Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae
families from the Bradyrhizobiaceae species. The distinctness
of Bradyrhizobiaceae from other Rhizobiales is also clearly
indicated by a signature sequence in seryl-tRNA synthetase
that is specific for this group. These signatures are also consistent with the observation that Bradyrhizobiaceae species are
only distantly related to other Rhizobiales (viz. Rhizobeaceae,
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PHYLOGENY AND SIGNATURES DISTINCTIVE OF α-PROTEOBACTERIA
Brucellaceae, and Phyllobacteriaceae) (Figure 1) (Sadowsky
& Graham 2000; Gaunt et al. 2001; van Berkum et al. 2003;
Kersters et al. 2003; Stepkowski et al. 2003; Moulin et al. 2004).
A specific relationship between Sinorhizobium and Agrobacterium species was also indicated by the signature sequence in
the LepA protein.
On the basis of 16S rRNA or various genes/proteins trees, it
has proven difficult to reliably determine the interrelationships
among different α-proteobacterial subgroups (Ludwig & Klenk
2001; Kersters et al. 2003). However, based upon the distribution patterns of various signatures, it is now possible to logically
deduce the branching order of the main α-proteobacterial subgroups (Figure 26). The model for α-proteobacterial evolution,
which has been developed here is based upon a large number of
proteins, which are involved in different functions. This model
is internally highly consistent and it is difficult to logically explain the observed distributions of these signatures by alternate
means. The model developed here is also consistent with the relationships, which are resolved in the 16S rRNA or other phylogenetic trees (viz. deep branching and distinctness of Rickettsiales,
a closer relationship between Rhizobiaceae, Brucellaceae, and
Phyllobacteriaceae as compared to Bradyrhizobiaceae; a closer
relationship between Rhodobacterales and Caulobacterales; distinctness of Rickettsiaceae from Anaplasmataceae species; distinctness of Rhizobiales order containing various root nodule
bacteria, etc.) (Sadowsky & Graham 2000; Dumler et al. 2001;
Kersters et al. 2003; Yu & Walker 2003; Moulin et al. 2004).
A few minor inconsistencies seen at present (e.g., phylogenetic placement of Ca. crescentus) should be clarified when
sequence information from additional species becomes available. In this context, it is important to acknowledge that sequence information is available at present from only a limited
number of α-proteobacterial species. Although, these species
include representatives from different α-proteobacterial orders,
it is necessary to obtain sequence information for many other
species from different genera and families to test and validate this
model.
Signature sequences in a number of proteins, a few of which
are described here, also provide evidence that α-proteobacteria
is a late diverging group within Bacteria (Gupta 1998, 2000,
2003; Gupta & Griffiths 2002). Within proteobacteria, δ and
-subdivisions are indicated to have branched prior to α-proteobacteria, whereas β and γ -subdivisions are indicated as later
branching groups (see also www.bacterialphylogeny.com). The
branching of α-proteobacteria in this position is also supported
by the16S rRNA and various protein trees (Olsen et al. 1994;
Viale et al. 1994; Eisen 1995; Kersters et al. 2003). The αproteobacteria, which is a very large group within Bacteria
(>5000 entries in the RDP-II database) (Maidak et al. 2001),
are presently recognized as a Class within the Proteobacteria
phylum (Woese et al. 1984; Stackebrandt et al. 1988; Murray
et al. 1990; Ludwig & Schleifer 1999; Boone et al. 2001;
Kersters et al. 2003). However, presently there are no clearly defined criteria for the higher taxa (viz. Phylum, Class, Order, etc.)
131
within Bacteria (Woese et al. 1985; Stackebrandt 2000; Ludwig
& Klenk 2001; Gupta & Griffiths 2002; Gupta 2002). Based on
the observations that α-proteobacteria can now be clearly distinguished from all other bacteria based upon a large number of
molecular characteristics, and that this group also branches distinctly from all other groups of bacteria including the β, γ - and
δ,-proteobacteria, it is suggested that α-proteobacteri should be
recognized as a main group or phylum within Bacteria, rather
than as a subdivision or class of the Proteobacteria (Gupta 2000,
2004; Gupta & Griffiths 2002). Signature sequences in a few
proteins (viz. PPDK and FtsK) indicate that α-proteobacteria
might have shared a distant ancestry with the δ-proteobacteria
exclusive of other bacteria, but this relationship needs to be further investigated and confirmed.
The α-proteobacteria have also given rise to mitochondria
(Margulis 1970; Gray & Doolittle 1982; Andersson et al. 1998;
Sicheritz-Ponten et al. 1998; Gray et al. 1999; Gupta 2000;
Emelyanov 2001a, 2003a, 2003b) and very likely played a central role in the origin of the ancestral eukaryotic cell (Gupta
& Singh 1994; Gupta & Golding 1996; Margulis 1996; Gupta
1998; Martin & Muller 1998; Lopez-Garcia & Moreira 1999;
Karlin et al. 1999; Lang et al. 1999; Emelyanov 2003b; Rivera
& Lake 2004). Many of the α-proteobacteria specific signatures identified in the present work are also present in the mitochondrial/eukaryotic homologs, providing additional evidence
of their derivation from an α-proteobacterial ancestor. In a few
cases, the α-proteobacterial signatures are present in genes which
are encoded by the mitochondrial DNA (viz. Cox I and Cyt b).
The shared presence of these signatures in the mitochondrial homologs provides further strong evidence for the α-proteobacterial
ancestry of mitochondria, as previously shown by phylogenetic
analysis (Andersson et al. 1998; Sicheritz-Ponten et al. 1998;
Emelyanov 2003a). The current evidence suggests that within
α-proteobacteria, the Rickettsiales group of species are the closest relatives of mitochondria (Gupta 1995; Andersson et al. 1998;
Sicheritz-Ponten et al. 1998; Gray et al. 1999; Lang et al. 1999;
Emelyanov 2001a, 2001b). However, this view is supported by
only some of the identified signatures and further work is needed
to clarify this aspect.
LIST OF ABBREVIATIONS
AlaRS, alanyl-tRNA synthetase; CFBG, ChlamydiaFibrobacter-Bacteroidetes-Green sulfur bacteria; Cyt., Cytochrome; Cox I, Cytochrome oxidase polypeptide I; LGT, lateral gene transfer; PLPG, Prolipoprotein-phosphatidylgycerol;
PPDK, pyruvate phosphate dikinase; RP, Rickettsia prowazekii;
SerRS, serine-tRNA synthetase; Succ-CoA, Succinyl-CoA; Tgt,
tRNA-guanine transglycosylase; TrpRS, tryptophanyl-tRNA
synthetase; Abbreviations in the species names are: A., Agrobacterium; Ana., Anaplasma; Aqu., Aquifex; Azo., Azotobacter;
Azospir., Azospirillum; Bac., Bacillus; Bact., Bacteroides; Bart.,
Bartonella; Bdello., Bdeollovibrio; Bif., Bifidobacterium; Bor.,
Borrelia; Bord., Bordetella; Brad. Bradyrhizobium; Bru.,
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132
R. S. GUPTA
Brucella; Buch., Buchnera; Burk., Burkholderia; Ca., Caulobacter; Camp., Campylobacter; Cb., Chlorobium; Cfx., Chloroflexus; Chl., Chlamydia; Chlam, Chlamydophila; Chromo.,
Chromo-bacterium; Clo., Clostridium; Cor., Cornyebacterium;
Cox., Coxiella; Cyt., Cytophaga; Dei., Deinococcus; Dechloro.,
Dechloromonas; Des., Desulfovibrio; Desulf., Desulfitobacterium; Dros. endo., Drosophila endosymbiont; E., Escherichia; Ent., Enterococcus; Fuso., Fusobacterium; Geo., Geobacter; H., Haemophilus; Hel., Helicobacter; Lac., Lactococcus; Lactobac., Lactobacillus; Lep., Leptospira; Lis., Listeria;
Leg., Legionella; Mag., Magnetococcus; Meso., Mesorhizobium;
Methano., Methanobacterium; Methyl., Methylobacillus; Microbul., Microbulbifer; Myc., Mycobacterium; Myx., Myxococcus; Nei., Neisseria; Nit., Nitrosomonas; Nitro., Nitrosospira;
Novo., Novosphingobacterium; Olig., Oligotropha; Para., Paracoccus; Pas., Pasteurella; Photobac., Photobacterium; Por.,
Porphyromonas; Pse., Pseudomonas; Ral., Ralstonia; Rhi., Rhizobium; Rho., Rhodobacter; Rhodo., Rhodospirillum; Rhodopseud., Rhodopseudomonas; Ri., Rickettsia; Shew., Shewanella;
Sino., Sinorhizobium; Sta., Staphylococcus; Str., Streptomyces;
Strep., Streptococcus; Syn., Synechococcus; Sulfo., Sulfolobus;
T., Thermotoga; Thermoan., Thermoanaerobacter; Thermosyn.,
Thermosynechococcus; Tre., Treponema; Vib., Vibrio; Xan.,
Xanthomonas; Thiobac., Thiobacillus; Wol., Wolinella; Xyl.,
Xylella; Yer., Yersinia; Z., Zymomonas.
ACKNOWLEDGMENTS
The competent technical assistance of Pinay Kanth, Jeveon
Clements, Larissa Shamseer, and Adeel Mahmood in creating
sequence alignments of proteins from Rickettsia prowazekii and
other genomes is thankfully acknowledged. I am also thankful to
Yan Li for developing certain computer programs that facilitated
the creation of signature sequence files and for help in setting up
the bacterial signatures website (www.bacterialphylogeny.com).
Thanks are also due to Emma Griffiths and Pinay Kanth for
helpful comments on the manuscript. The work on signature
sequences described here was mostly completed by August
2004. This work was supported by a research grant from the
National Science and Engineering Research Council of Canada
and the Canadian Institute of Health Research.
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