MBE Advance Access originally published online on May 19, 2007
Molecular Biology and Evolution 2007 24(8):1761-1768; doi:10.1093/molbev/msm096
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Research Articles |
Evidence for a Gram-positive, Eubacterial Root of the Tree of Life
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* Department of Molecular, Cellular, and Developmental Biology, University of California, Los Angeles
Molecular Biology Institute, University of California, Los Angeles
Department of Human Genetics, University of California, Los Angeles
UCLA Astrobiology Institute, University of California, Los Angeles
E-mail: Lake{at}mbi.ucla.edu.
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Abstract |
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Directed indels, insertions, and deletions within paralogous genes, have the potential to root the tree of life. Here we apply a newly developed rooting algorithm, top-down rooting, to indels found in informational and operational gene sets, introduce new computational tools for indel analyses, and present evidence (P < .01) that the root of the tree of life is not present in its traditional location, between the Eubacteria and the Archaebacteria. Using indels contained in the dihydroorotate dehydrogenase/uroporphyrinogen decarboxylase gene pair and in the ribosomal protein S12/beta prime subunit of the RNA polymerase gene pair, we exclude the root from within the clade consisting of the Firmicutes plus the Archaebacteria and their most recent common ancestor. These results, plus previous directed indel studies excluding the root from the eukaryotes, restrict the root to just four possible sites. One potential root is on the branch leading to the double-membrane prokaryotes, another is on the branch leading to the Actinobacteria, another is within the Actinobacteria, and the fourth is on the branch leading to the Firmicutes–Archaea clade. These results imply (1) that the cenancestral population was not hyperthermophilic, but moderate thermophily cannot be excluded for the root on the branch leading to the Firmicutes–Archaea clade, (2) that the cenancestral population was surrounded by ester lipids and a peptidoglycan layer, and (3) that parts of the mevalonate synthesis pathway were present in the population ancestral to the Bacilli and the Archaebacteria, including geranylgeranylglyceryl phosphate synthase, an enzyme thought to be partially responsible for the unique sn-1 stereochemistry of the archaeal glycerol phosphate backbone.
Key Words: tree of life • root • indels • cenancestor • Firmicutes • Archaebacteria • double-membrane prokaryotes
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Introduction |
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TOPAbstractIntroductionAnalyses and ResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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The root of the tree of life allows one to test theories for the order of appearance of novel biological innovations. With a root one can synthesize past geological, paleontological, and climatological events with genomic phylogenies and thereby reconstruct and better understand significant genetic, biochemical, and metabolic events in the evolution of life on Earth.
Traditionally the root of the prokaryotic tree of life is placed between the Archaebacteria and the Eubacteria (Gogarten et al. 1989
; Iwabe 1989). As a result, it is thought that archaebacterial metabolisms, such as methanogenesis and extreme thermophily, may reflect the energy sources utilized in earlier eons. At the same time, there is a growing awareness that the traditional root might be an artifact of phylogenetic reconstruction resulting from long branch attraction (Felsenstein 1978) and other sequence analysis artifacts (Philippe and Forterre 1999; Zhaxybayeva, Lapierre, and Gogarten 2005). Thus there is uncertainty about whether the Archaebacteria are phylogenetically ancient, or whether they have evolved rapidly after diverging from eubacterial ancestors. Furthermore, the traditional root leads to predictions that conflict with other results. For example, it predicts that the cenancestor was a hyperthermophile, and this prediction conflicts with molecular stability arguments (Miller and Lazcano 1995) and with correlations between phylogenetic analyses and ribosomal RNA G/C compositions (Galtier, Tourasse, and Gouy 1999) that suggest that life started at mesophilic temperatures. These findings call the traditional root of the tree of life into question and make it important to examine other types of rooting data.
Here we present evidence based on the distribution of directed indels, insertions, or deletions in paralogous genes, that restrict the root to four locations on the tree of life. Applying top-down rooting (Lake et al. 2007) to indel-containing informational (ribosomal protein S12) and operational (dihydroorotate dehydrogenase) genes, we present statistically significant evidence excluding the root from a clade containing the Firmicutes, the Archaebacteria, and their last common ancestor. In combination with previous results excluding the root from the eukaryotes (Rivera and Lake 1992; Skophammer et al. 2006; Lake et al. 2007), the root of the tree/ring of life is restricted (1) to the branch leading to the double-membrane prokaryotes; (2) on the branch leading to the Actinobacteria; (3) to the branch leading to the clade of the Firmicutes plus the Archaebacteria; or (4) within the Actinobacteria. These restricted root locations parsimoniously imply that cenancestral prokaryotes, the last common ancestors of life, were surrounded by ester-linked lipid membranes and covered by a peptidoglycan layer. They are inconsistent with a root adjacent to the Aquificae, and they rule out a hyperthermophilic cenancestral origin but do not necessarily exclude a moderately thermophilic cenancestor.
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Analyses and Results |
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TOPAbstractIntroductionAnalyses and ResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Taxon Selection
Gene transfers affect almost every aspect of prokaryotic systematics (Doolittle 1999
; Gogarten, Murphey, and Olendzenski 1999; Ochman, Lawrence, and Groisman 2000) including the evolution of sequences and indels (Doolittle 1999; Zhaxybayeva and Gogarten 2004; Lake et al. 2005; Inagaki, Susko, and Roger 2006), thereby making prokaryotic evolution much more like eukaryotic evolution. However, because gene transfers are less likely between phylogenetically and functionally distant groups (Jain 2003), it is possible to reduce the effects of gene transfers by choosing taxonomic groups for indel analyses that minimize intergroup gene/indel transfers.
Recent indel studies have focused on four natural, phylogenetically well-separated groups: Archaebacteria, Firmicutes, Actinobacteria, and double-membrane (Gram-negative) prokaryotes (Skophammer et al. 2006; Lake et al. 2007). Together, these four encompass all known prokaryotic life (Boone and Castenholz 2001). Archaebacteria are primarily extremophiles and include many hyperthermophiles; Firmicutes, formerly named the low GC Gram positives, contain organisms like Clostridia and Bacilli; Actinobacteria, formerly named the high GC Gram positives, are diverse and contain many human pathogens; and double-membrane prokaryotes are a speciose, possibly primitively photosynthetic taxon exclusively containing all prokaryotes surrounded by double membranes. Using these groups is key to top-down indel rooting studies, and in previous studies it has reduced within-group homoplasies to 1%–5% for informational genes and 3%–20% for operational genes. This indicates that gene transfers between these four large taxonomic groups are fairly limited. The distributions of the 36 known prokaryotic taxa within these four groups are shown in Table 1.
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Ribosomal Protein S12 and RNA Polymerase RpoC
Ribosomal protein S12 is a ubiquitous protein, present in both prokaryotic and eukaryotic ribosomes, where it functions in the regulation of the fidelity of protein synthesis. The gene is a member of a highly conserved operon (Itoh et al. 1999
) that includes other protein synthesis-related genes, such as ribosomal protein S7 and protein synthesis factors EF-Tu and EF-G. Ribosomal protein S12 contains an insert within the region that corresponds to amino acid positions 7–38 in the Escherichia coli sequence. This insert is exclusively present in Firmicutes and Archaebacteria (Gupta 1998). Although this indel is well known, no S12 paralogs have been identified previously. Here we identify and analyze a portion of the beta prime subunit of DNA-dependent RNA polymerase, RpoC, which is paralogous to the amino terminus of S12. In Eubacteria, the core polymerase consists of two copies of the polymerase alpha subunit, one copy of the beta subunit, and one copy of the beta prime subunit. The beta prime subunit is the largest RNA polymerase subunit in most Eubacteria, with an approximate molecular weight of 160 kD and length of about 1,350 amino acids. The paralogous region of the beta prime subunit occurs in domain 5, at positions 868–899 in the E. coli numbering system. In Archaebacteria, the large RpoC protein is present as several smaller proteins, but the region orthologous to positions 868–899 is missing. From the observed distributions of BLAST bit scores and of LogBit distances (related to paralinear/LogDet distances) for S12 and RpoC, we calculate an expect score of 0.002 for our ortholog/paralog sets (for details see the Supplementary Material online, sections S1 and S3). The alignments of S12 and the beta prime polymerase subunit are summarized in Table 2 (comprehensive alignments are presented in the Supplementary Material online, section S6).
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In protein S12, a 13 amino acid insert is present in the Firmicutes (F) and the Archaebacteria (R) and absent in the double-membrane prokaryotes (D) and the Actinobacteria (A). The S12 insert is absent from all RpoC paralogs including the double-membrane prokaryotes (D'), the Actinobacteria (A'), and the Firmicutes (F'). This region of the RpoC gene is missing in the Archaebacteria (R'). The 13 amino acid insert is present in the Mollicutes and Bacilli (B) and absent, except for a few sequences, in the Clostridia (C). Thus, the Clostridia are analyzed as a separate group, distinct from the other Firmicutes. Given this distribution of indels, and that of the PyrD indel, discussed next, the most parsimonious unrooted tree is ((D,A),C, (B,R)), in Newick notation. The S12 taxa (D, A, C, B, R) are coded as (–, –, –, +, +), respectively, (or as (–, –, +, +, +) for the variant) and the RpoC taxa (D', A', C', B', R') are coded as (–, –, –, –, m), respectively, where "–" corresponds to insert missing, "+" corresponds to insert present, and "m" corresponds to gene region missing (Lake et al. 2007
). The most parsimonious rooted trees for each of the 12 possible rootings are shown in figure 1. Note that the leaves of the unrooted trees are divided into two separate regions because the five groups, D, A, C, B, and R, represent higher level phylogenetic clades, rather than single sequences. Hence, the roots within the distal portions of the leaves (roots 1, 2, 6, 11, and 12, respectively) are shown as two lines to represent the branching within the crown groups. The proximal portions of the leaves correspond to roots, 3, 4, 7, 9, and 10, and the internal branches correspond to roots 5 and 8. Thus there are 12 possible distinct roots, rather than the 7 roots that would normally be present if one were simply comparing five individual sequences. As shown by large X's in figure 1, the four least parsimonious rooted trees, roots 9, 10, 11, and 12, require three changes each. Hence these results eliminate the root from the clade defined by the last common ancestor of the Mollicutes, the Bacilli, and the Archaebacteria. (Only the most conservative interpretation is presented here.) As analyzed in the Supplementary Material online (section S3), the S12 indel provides statistically significant (P < .005) support excluding the root from this clade.
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Gene transfers do not appear to have significantly affected the analysis of the S12/RpoC gene set, as no Actinobacteria and no double-membrane prokaryotes contain the S12 insert. Similarly, among the Archaebacteria, the Bacilli, and the Mollicutes, only one S12 sequence lacks the insert, corresponding to a low rate of gene transfer. (For sequences and exceptions see Supplementary Material online, section S6.)
The absence of the S12 insert in most Clostridia is not the first indication that the Firmicutes may be paraphyletic. Ribonuclease P, the RNA enzyme that induces maturation of the 5' end of transfer RNA shows a similar distribution. It exists in two forms in the Eubacteria (Westhof and Massire 2004). Type A occurs uniformly throughout the double-membrane prokaryotes and is also present within the Actinobacteria and the Clostridia, matching the distribution of the S12 deletion. Type B occurs in the Bacilli and the Mollicutes, matching the distribution of the S12 insertion.
Dihydroorotate Dehydrogenase and Uroporphyrinogen Decarboxylase
Dihydroorotate dehydrogenase, PyrD, is a central enzyme involved in the de novo biosynthesis of pyrimidines. It catalyzes the conversion of dihydroorotate to orotate, a substrate for uridylate synthesis. PyrD contains a deletion that separates the Firmicutes and the Archaebacteria from the remaining prokaryotes and eukaryotes (Gupta 1998), but PyrD paralogs have not been previously identified. Here we identify a portion of uroporphyrinogen decarboxylase, HemE, that is paralogous to the indel-containing region of PyrD (for details, see Supplementary Material online, sections S3 and S5), and analyze this gene pair using top-down rooting.
HemE catalyzes a step in the biosynthetic pathway from tetrapyrroles to heme by sequentially decarboxylating the four acetate side chains of uroporphyrinogen III to produce coproporphyrinogen. The paralogous regions of PyrD and HemE, in the vicinity of the PyrD indel, correspond to E. coli amino acid positions 302–353 and 114–165, respectively. Three-dimensional X-ray structures of PyrD and HemE (Whitby et al. 1998; Hansen et al. 2004) show that both molecules utilize identical beta-alpha barrel motifs (ß
)8. In HemE and in PyrD the paralogous regions consist of an alpha helix, a beta sheet, and a second alpha helix. These correspond to alpha helix 2, beta sheet 3, and alpha helix G in HemE (Whitby et al. 1998). In PyrD, they correspond to alpha helix 6, beta sheet 7, and alpha helix 7 (Hansen et al. 2004). In both paralogs, the beta sheets start at the PLIG sequence. From the observed distributions of bit scores and LogBit distances for PyrD and HemE, we calculate an expect score of 0.0003 for our ortholog/paralog sets (for details, see the Supplementary Material online, sections S1 and S3).
The phylogenetic analysis of the PyrD/HemE gene pair is complicated by alternative indels. As summarized in Table 3, PyrD contains a two amino acid insertion in double-membrane prokaryotic and actinobacterial sequences, whereas firmicute and archaeal sequences lack this insertion. Eukaryotic PyrD sequences follow the double-membrane pattern, reflecting their relationship with double-membrane prokaryotes typically observed for operational proteins. In addition, some double-membrane PyrD sequences, class 1, contain a 3-amino-acid insertion.
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All HemE sequences contain insertions related to those present in the double-membrane and actinobacterial PyrD sequences. A two amino acid HemE insert is contained in double-membrane prokaryotes and in some actinobacteria. Other actinobacteria contain a one amino acid insert. The Bacilli contain the HemE gene with a one amino acid insert and the Clostridia and the Mollicutes lack the HemE gene.
PyrD/HemE indels have similar distributions to S12/RpoC indels, except that two PyrD variants and two HemE variants are explicitly considered in its analysis. Two PyrD variants occur in the double-membrane prokaryotes (D). Variant gene sets 1 and 2 of PyrD taxa (D,A,C,B,R) are coded as (++, ++, –, –, –) and (+++, ++, –, –, –), respectively, where "++" represents the two amino acid insert, "+++" represents the three amino acid insert, taxon C corresponds to the Clostridia and the Mollicutes, and taxon B corresponds to the Bacilli. Variant gene sets 1 and 2 of HemE taxa (D', A', C', B', and R') are coded as (++, ++, m, +, m) and as (++, +, m, +, m), respectively, where "++" represents the two amino acid insert, "+" indicates the single amino acid insert, and "m" indicates that the gene is missing. The most parsimonious unrooted tree, ((D,A),C, (B,R)) in Newick notation, is used for the rooting calculations.
Because we do not know which variants correspond to the ancestral indel character states, we consider, in turn, the four possible combinations of PyrD and HemE variants and interpret the results conservatively. Specifically, a root is eliminated only if it is rejected by all four possible combinations of character states. The results of these analyses are summarized in figure 2. (The detailed analyses on which figure 2 is based are provided in the Supplementary Material online, section S8). The unrooted phylogenetic tree is shown at the top of the diagram, with the possible roots labeled 1–12. A root is rejected when all boxes in a column, corresponding to the four variants, are red (dark). If even a single yellow (light) box is present, the root is not rejected, because it is possible that it corresponds to an acceptable root. Figure 2 also shows that roots 6–12 are rejected for all possible character states. Thus, even though we do not know for sure which character state sets are correct, the conclusion remains valid, because any rejected roots are excluded by all possible data sets. These analyses exclude the root from the clade that includes the Firmicutes (C+B), the Archaebacteria (R), and their last common ancestor. As determined in section S3 of the Supplementary Material online, the PyrD indel provides statistically significant (P < .01) support for excluding the root of the tree of life from this clade.
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Gene transfers do not appear to have appreciably affected these results. All firmicute and archaebacterial PyrD sequences contain the relevant deletion, except for four species of Staphylococcus, corresponding to a possible gene transfer rate of 4/70 = 5.7%. Among the Actinobacteria and double-membrane prokaryotes, which lack the PyrD deletion, 27 sequences were found which contain the deletion, corresponding to a possible gene transfer rate of 27/234 = 11.5%. (For sequences and exceptions, see the Supplementary Material online, section S7.).
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Discussion |
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TOPAbstractIntroductionAnalyses and ResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Our indel analyses argue against a root within the clade consisting of the Archaebacteria plus the Firmicutes (PPyrD < 0.01 and PS12 < 0.005), and previous studies argue against roots within the double-membrane prokaryotes, against roots within the archaebacteria and, against roots on the two ring segments connecting eukaryotes to the prokaryotes (Rivera and Lake 2004; Skophammer et al. 2006
; Lake et al. 2007). Four roots are not excluded and remain viable candidates for the root of the tree of life. These are shown on the tree of life and on the ring of life in figures 3A and 3B, respectively. The roots are located on the branch leading to the double-membrane prokaryotes, root 1; on the branch leading to the Actinobacteria, root 2; on the branch leading to the Firmicutes–Archaea clade, root 3; and within the Actinobacteria, root 4. For reference, the classical root marked by an X, based on sequence analyses of anciently duplicated gene paralogs (Gogarten et al. 1989; Iwabe 1989), is between the Archaebacteria and the Eubacteria (Olsen et al. 1985). An alternative root based on a postulated irreversible evolutionary transition (Cavalier-Smith 2002, 2006) is within the double-membrane prokaryotes and generates an Actinobacteria–Archaebacteria clade rather than the Firmicutes-Archaebacteria clade obtained here.
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These four non-excluded roots suggest some properties of the cenancestral population. Roots 1, 2, and 4 parsimoniously imply that the cenancestral population is mesophilic because the double-membrane prokaryotes and the Actinobacteria are primitively mesophilic. A hyperthermophilic cenancestor is excluded by root 3, but a moderately thermophilic cenancestor cannot be excluded for this root, as two recently discovered thermophilic Clostridia occupy a position adjacent to root 3 in concatenated protein sequence trees (Wu et al. 2005
).
Carboxydothemus hydrogenoformans (Wu et al. 2005) grows optimally at 78°C, and Symbiobacterium thermophilum (Ohno et al. 2000) grows optimally at 60°C. Thus definitive parsimony based estimations of the growth temperature of the cenancestor will, at a minimum, require the elimination of additional roots. However these results, together with other evidence and arguments for mesophilic origins (Miller and Lazcano 1995; Galtier, Tourasse, and Gouy 1999; Philippe and Forterre 1999), make lower temperature hydrothermal sites, such as the Lost City field (Russell and Martin 2004; Kelly et al. 2005), increasingly attractive for the cenancestral evolution of life.
Parsimonious reasoning applied to the four potential roots also indicates that members of the cenancestral population were enclosed by ester-linked lipid membranes and surrounded by a peptidoglycan layer, because the Firmicutes, the double-membrane prokaryotes, and the Actinobacteria all share these character states. The locations of the potential roots imply that during the transition to the Archaebacteria the peptidoglycan layer was lost and the ester-linked membrane lipids were replaced with ether-linked lipid membranes. If ester-linked lipid membranes were replaced with ether-linked ones, then it is possible that remnants of this transition still exist in the lipid biosynthetic pathways found in the Firmicutes today.
This possibility caused us to reexamine the taxonomic distributions of genes coding for archaeal lipid pathways, and led us to conclude that detailed genome studies of lipid biosynthetic pathways point toward some novel lipid-based archaeal–firmicute connections (Lange et al. 2000; Smit and Mushegian 2000; Boucher et al. 2003; Boucher, Kamekura, and Doolittle 2004; Daiyasu et al. 2005). The findings reported in these studies suggest that parts of the mevalonate (MVA) synthesis pathway, central to archaeal lipid synthesis, may have been present in the common population immediately ancestral to the Bacilli and the Archaebacteria. They also imply that one of the enzymes responsible for the unique archaeal sn-1 stereochemistry, was present in this ancestral population as shown in the rooted Archaea–Firmicutes tree in figure 4.
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Many Bacilli have complete, or nearly complete, MVA lipid synthesis pathways like those found in Archaebacteria (Smit and Mushegian 2000
; Boucher, Kamekura, and Doolittle 2004), whereas most Eubacteria utilize the DXPS lipid synthesis pathway (Lange et al. 2000). In detailed phylogenetic analyses of the genes present in the prokaryotic MVA pathways (Boucher, Kamekura, and Doolittle 2004), few double-membrane prokaryotes contain MVA genes. Furthermore the MVA genes that are present in double-membrane prokaryotes are nonparsimoniously distributed throughout the trees in no particular phylogenetic order, suggesting that they arose from multiple gene transfers. In contrast, the Bacilli form a single clade in most MVA gene trees (Boucher, Kamekura, and Doolittle 2004). The phylogenetic distribution of MVA biosynthetic genes within the Bacilli parsimoniously suggests that many genes in the pathway were vertically inherited from the last common ancestral population relating the Bacilli and the Archaebacteria.
Similar evidence suggests that at least one antecedent of the enzymes contributing the unique sn-1 stereochemistry existed in the ancestral population common to the Bacilli and the Archaebacteria. Geranylgeranylglyceryl phosphate (GGGP) synthase, a terminal member of the MVA pathway is one of the enzymes thought to be responsible for the unique sn-1 stereochemistry of the archaeal glycerol phosphate backbone (Boucher, Kamekura, and Doolittle 2004). Further, GGGP synthase appears to have been vertically inherited from the ancestral population common to the Bacilli and the Archaebacteria because, except for a single Cytophaga species (Boucher, Kamekura, and Doolittle 2004), only the Bacilli and the Archaebacteria contain genes for GGGP synthase. Furthermore, the Bacilli and the Archaebacteria are not intermixed in the GGGP synthase tree, as would be expected if extensive gene transfer from either group had been the source of GGGP synthase; instead, they are resolved into their respective groups. Although the GGGP synthase genes cannot polarize the root, they are consistent with our indel evidence excluding the root from the firmicute–archaeal clade. We parsimoniously infer that the ancestral population contained a nearly complete archaeal-like MVA pathway, and one of the genes necessary for producing the unique archaeal lipid backbone stereochemistry.
It is also helpful to consider factors that might argue against these conclusions. A potential criticism of this work is that the phylogenetic relationships observed in the MVA gene trees, and particularly in the GGGP synthase tree, are not due to common descent but are the result of ancient gene transfers that either occurred early in the evolution of the Firmicutes or early in the evolution of the Archaebacteria, thereby mimicking vertical descent. This would fit well with the importance of gene transfer in early, and present-day, evolution, but those arguments are not parsimonious. If we accept that the spotty, nonphylogenetic, patterns observed for the double-membrane prokaryotes in MVA pathway gene trees provide support for gene transfers, because they are not parsimoniously consistent with vertical descent, then we must also accept that the sister relationships observed within the Bacilli and within the Archaebacteria in the GGGP synthase gene tree parsimoniously provide support for vertical descent, because this interpretation does not require invoking additional gene transfers. Although one might reason that the results of the S12 and PyrD indel analyses could be explained by an early gene transfer between the Firmicutes and the Archaebacteria, nevertheless that scenario nonparsimoniously requires one more change than vertical descent.
Our rooting data also indicate that the Archaebacteria are not "ancient," as their name implies, and as has been discussed in detail by others (Cavalier-Smith 2002). The "uniqueness" of the Archaebacteria does not establish that they date back to the cenancestor. Just as a taxon that is found at the tip of a long branch in a tree may be the result of a fast-evolving gene, so too the "uniqueness" of a higher taxonomic group only indicates that the group has diverged extensively from other groups, and not that it is old.
The relationships derived here raise many unresolved question, such as why the Archaebacteria became so divergent. In studies of eukaryotic speciation, the role of geographical isolation, allopatric speciation, is commonly emphasized (Mayr 1963), but the prokaryotic equivalents of geographical isolation are just becoming known. Genomic studies have indicated that the ability of prokaryotes to exchange genes is greatest when hosts and donors share similar environmental, genetic, or metabolic properties. Some of the positively correlated, associative properties of prokaryotes include carbon heterotrophy, phototrophy, optimal growth temperatures, oxygen usage, and genomic GC composition (Jain 2003). But none of these properties define the Archaebacteria, so it is difficult to imagine an associative property shared by all Archaebacteria that might alter gene exchange. Perhaps, in some as yet unknown way, the very properties that define the Archaebacteria, such as their novel membrane lipids and the lack of a peptidoglycan layer, reduced their genetic contact with the outside prokaryotic world, thereby initiating their speciation and allowing them to blaze a new, more isolated, and more extreme, evolutionary pathway. We hope that this study will stimulate others to rethink the events involved in the origin of the Archaebacteria.
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Supplementary Material |
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Supplementary materials are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).
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Acknowledgements |
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TOPAbstractIntroductionAnalyses and ResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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This work was supported by grants from the National Science Foundation (NSF) and the UCLA NASA (National Aeronautics and Space Administration) Astrobiology Institute to J.A.L. Support was also provided by an IGERT training grant from NSF (R.G.S.), a Cell and Molecular Biology Training Grant from the National Institutes of Health (NIH) (J.A.S.), and a Genomic Interpretation and Analysis Training Grant from NIH (C.W.H.).
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Footnotes |
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Martin Embley, Associate Editor
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References |
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