Institut für Genetik, Technische Universität Braunschweig, Spielmannstrasse 7, 38106 Braunschweig, Germany
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Abstract |
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Introduction |
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Notably, most eukaryotic GAPDH genes belong to types Gap I and Gap II. Within Gap I, the eukaryotic GapC gene of mainly glycolytic function is closely related to proteobacterial gap1 and was possibly acquired via endosymbiotic gene transfer from the alpha-proteobacterial antecedents of mitochondria (Smith 1989
; Martin et al. 1993
; Liaud et al. 1994
). Similarly, within Gap II, the nuclear genes GapA and GapB, encoding subunits A and B of Calvin cycle GAPDH (Cerff 1982
), most likely originated from cyanobacterial gap2 via gene transfer in the context of plastidal endosymbiosis (Brinkmann et al. 1989
; Martin et al. 1993
; Liaud et al. 1994
). Apart from these prominent members of the GAPDH gene family found in eukaryotic nuclei, three other eukaryotic GAPDH lineages exist that are clearly not of mitochondrial or chloroplast descent: (1) Some Parabasalia harbor a distinct eukaryotic GAPDH gene, the origin of which has so far remained obscure (Markos, Miretsky, and Müller 1993
; Viscogliosi and Müller 1998
). (2) A cytosolic GapC gene is present in some trypanosomes that is surprisingly close to gamma-proteobacterial gap1 (Michels et al. 1991
) and has probably been acquired via a recent lateral gene transfer (LGT) from a gamma-proteobacterial donor (Henze et al. 1995
; Figge et al. 1999
). (3) Cytosolic GapC in Euglena (Henze et al. 1995
) and its glycosomal equivalent in trypanosomes (Michels et al. 1991
) have recently been shown to be closely related to a eubacterial gap1 so far found only in the syphilis spirochete Treponema pallidum (Figge et al. 1999
). In order to explain this curious finding, LGT between a spirochetal and a euglenozoan ancestor has been invoked. The direction of this transfer, however, could not be clarified.
LGT has just recently been recognized as a major factor in eubacterial and eukaryotic evolution (Doolittle 1999a, 1999b
; Lake, Jain, and Rivera 1999
). For example, it has been suggested that about 18% of the Escherichia coli genome is lateral acquisitions that happened during the last 100 million years (Lawrence and Ochman 1998
). However, it seems that not all genes are affected by LGT to the same extent, as outlined by Rivera et al. (1998)
. According to these authors, operational genes (encoding functions such as energy metabolism, biosynthesis of amino acids, cofactors, etc.) are transferred easily and often, whereas informational genes (encoding genes that function in e.g., RNA, DNA synthesis and translation) are rarely passed on to another organism. Nevertheless, even informational genes such as 16S rRNA or ribosomal genes may not be safe from LGT. In fact, it was shown that 16S rRNA genes from Es. coli could be replaced with the corresponding genes from Proteus vulgaris (Asai et al. 1999
) and that the ribosomal rpS14 gene may have undergone multiple LGT events (Brochier, Philippe, and Moreira 2000
).
In order to determine the direction of the LGT between Euglenozoa and the spirochete T. pallidum, we have now determined gap genes from nine other spirochetes. Spirochetes are easily distinguishable on the basis of their unique morphology and mechanism of motility and have been shown to constitute a phylogenetically distinct eubacterial phylum (Paster et al. 1991
and references therein). The analysis of the spirochetal sequences in the context of all other eubacterial and a selection of eukaryotic sequences revealed that the GAPDH gene diversity within spirochetes is much broader than previously assumed. LGT between spirochetes and other eubacterial phyla, in addition to early gene duplications in the eubacterial ancestor, seems to account for the phylogenetic distribution of the spirochetal Gap genes presently observed.
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Material and Methods |
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Escherichia coli strains XL1-blue, and HB101 were grown with appropriate antibiotics according to standard procedures (Sambrook, Fritsch, and Maniatis 1989
). Cloning vectors used were pBluescript-SK (+) (Stratagene) and pUC18 (Vieira and Messing 1982
). Plasmid transformation, selection, and testing for recombinant clones were performed as described (Sambrook, Fritsch, and Maniatis 1989
).
DNA Isolation, Cloning, and Sequencing of Eubacterial gap Genes
DNA from spirochetes was isolated as follows: spirochete cultures were washed once in TES (10 mM Tris-HCl, pH 8.0; 0.1 M EDTA, pH 8.0; 0.15 M NaCl) and resuspended in the same buffer. Subsequently, lysozyme (ad [final concentration] 5 mg/ml), SDS (ad 1%), and proteinase K (ad 50 µg/ml) were added independently after 1-h incubation periods at 37°C. Then, samples were treated twice with phenol-chloroform-isoamylalcohol (25:24:1) and precipitated.
Genomic DNA from Prochlorococcus marinus CCMP1375 was a gift from Wolfgang Hess, Humboldt Universität, Berlin. Isabelle St. Girons, Institut Pasteur, Paris, provided DNA from Leptospira biflexa and Brachyspira hyodysenteriae. Klaus Heuner, Klinikum Charité, Berlin, supplied the DNA from T. denticola.
Degenerate primers (G/AINGFG: 5'-GSNATHAAYGGNTTYGG-3'; WYDNEW: 5'-CCAYTCRTTRTCRTACCA-3') for two highly conserved regions at the N-terminal and C-terminal ends of GAPDH proteins (INGFGRI, WYDNE) were used for the amplification of gap genes (95% of the coding sequence) from genomic DNA samples. Polymerase chain reaction conditions were as followscycle 1: 93°C for 5 min; cycles 235: 93°C for 1 min, 50°C for 1 min, and 72°C for 2 min; and cycle 36: 72°C for 5 min for the amplification of gap genes from Prochlorococcus marinus. In the case of Sp. stenostrepta, Sp. aurantia, S. murdochii, and T. saccharophilum, the following conditions were usedcycle 1: 94°C for 3 min; cycles 235: 94°C for 30 s, 50°C for 30 s, and 72°C for 1 min; and cycle 36: 72°C for 7 min. For Leptospira biflexa, Leptospira interrogans, L. illini, B. hyodysenteriae, and T. denticola, the following conditions were appliedcycle 1: 96°C for 3 min; cycles 235: 96°C for 30 s, 48°C for 30 s, and 72°C for 1 min; and cycle 36: 72°C for 7 min. All reactions were performed in a Perkin-Elmer thermocycler with a Mg2+ concentration of 1.5 mM and 40200 ng of DNA per reaction (100 µl). Amplification products of appropriate size were eluted from agarose gels (Nucleospin, Macherey, and Nagel), treated with polynucleotide kinase and Klenow DNA polymerase using protocols of the supplier (New England Biolabs), and cloned into pBluescript-SK (+) or pUC18. Both strands of several independent PCR-generated clones for each gene were sequenced with appropriate oligonucleotides using the dideoxy chain termination method (Big dye, Perkin-Elmer).
The nucleotide sequences of the gap genes reported will appear in DDBJ/EMBL/GenBank International Nucleotide Sequence Database under the accession numbers AJ245541 (P. marinus CCMP1375); AJ245542 (Sp. aurantia DSM 1902); AJ245543 (Sp. stenostrepta DSM 2028); AJ245544 (T. saccharophilum DSM 2985); AJ245545 (S. murdochii ATCC 51284); AJ245546 (Leptospira biflexa Patoc 1); AJ245547 (L. illini); AJ245548 (Leptospira interrogans pathovar icterohaemorragiae); AJ245549 (B. hyodysenteriae ATCC 27164); AJ245550 (T. denticola ATCC 33521).
Phylogenetic Analysis
GAPDH sequences used for phylogenetic analysis were retrieved from Genbank with the following exceptions: Bordetella pertussis, Chlorobium tepidum, Clostridium acetobutylicum, Mycobacterium avium, Neisseria gonorrhoeae, Porphyromonas gingivalis, Salmonella typhi, Staphylococcus aureus, Streptococcus pneumoniae, Streptomyces coelicolor, and Yersinia pestis. These sequences were all obtained from TIGR (see The Institute for Genomic Research website at http://www.tigr.org) as preliminary sequence data.
Deduced amino acid sequences were aligned with CLUSTAL W (Thompson, Higgins, and Gibson 1994
) and refined by hand. The complete sequence alignment will appear at http://www.ebi.ac.uk:80/embl/Submission/alignment.html under the accession number DS45110. After the exclusion of gaps and the elimination of the N- and C-terminal regions including GINGFG and WYDNE, the resulting alignment contained 110 sequences with 250 positions. Protein phylogeny was inferred using maximum-likelihood (ML) (Molphy, version 2.3 [Adachi and Hasegawa 1996
]), starting with a Neighbor-Joining (NJ) tree that was subsequently improved using the local rearrangement option of ProtML.
The robustness of the tree topology was estimated by 100 NJ-bootstrap replicates (Saitou and Nei 1987
) that were calculated based on the JTT-F matrix. The same alignment was used in a maximum parsimony (MP) bootstrap (PAUP 4.0 alpha version, 2000) analysis (250 bootstrap replicates). To this end, a full heuristic search with four times random addition of the input order was performed, and only bootstrap values above 50% were retained. In order to investigate the relationship between species in the Gap IB subtree, data sets containing 10, 12, or 14 sequences with 293 positions were analyzed with TREE-PUZZLE (Strimmer and von Haeseler 1996
). The JTT-F amino acid substitution matrix (Jones, Taylor, and Thornton 1992
) was employed with an eight-category discrete gamma model of site rate heterogeneity.
Signature sequences were defined on the basis of their presence in at least 90% of all sequences pertaining to the corresponding type of GAPDH and no more than 10% of all other GAPDH sequences included in this analysis.
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Results |
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Spirochetal Gap Sequences Are Closely Related to Eukaryotic Gap Sequences from Euglenozoa and Parabasalia
Recently, we showed that a Gap1 sequence from the syphilis-spirochete T. pallidum is very closely related to GAPDH genes from the eukaryotic Euglenozoa, indicating that an interkingdom gene transfer may have occurred between these organisms (Figge et al. 1999
). To further our understanding of this curious finding, we have now analyzed this relationship in the presence of all available eubacterial and nine new spirochetal Gap sequences. Our analysis shows that, in addition to T. pallidum Gap1, three other spirochetal Gap sequences cluster with the Gap sequences from Euglenozoa. Sequences from S. murdochii and B. hyodysenteriae seem to be more closely related to Euglenozoan GapC than the two Treponema sequences. However, further analyses demonstrate that the outgroup species sampling influences the position of the Treponema species. In the presence of closely related outgroup sequences (Leptospira Gap IA), Treponema sequences cluster with the Euglenozoa with high bootstrap support (84%, fig. 3A
). When two more outgroup sequences are added, bootstrap support for this relationship drops to 53%. Finally, the addition of further, more distant outgroup sequences separates the fast-evolving Treponema species from the Euglenozoa (fig. 3C,
and even more prominently in fig. 1
) and counterfeits a close relationship between GAPDH from Brachyspira/Serpulina and the Euglenozoa.
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Discussion |
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As spirochetes are part of three highly distinct gene clusters within the Gap I subtree, are found in the Gap IV subtree, and belong to two other groupings with lower bootstrap support, the phylogenetic distribution of spirochetes in the GAPDH tree can hardly be explained by organismal evolution. Therefore, it is likely that several spirochetes, which notably all seem to harbor a single gap gene, obtained their present gap gene via LGT from donors that belong to other eubacterial phyla. With the present data we cannot determine with certainty which of the spirochetes (if any) harbors the gap gene that was present in the spirochetal ancestor. However, the Gap IB subtree includes sequences from three different spirochete genera, and therefore it is possible that these organisms have retained the gap gene originally present in the spirochetal ancestor. As a consequence, all other spirochetes may have adopted gap genes from the following bacterial phyla: Bacteroides/Cytophaga/Flavobacterium (L. illini), chlamydia (two Leptospira species), gram positives with low GC or gamma-proteobacteria (T. saccharophilum), and gram positives with high GC (two Spirochaeta species). Thus LGT of gap genes seems to be especially frequent between spirochetes and other eubacterial phyla. Nevertheless, LGT probably also occurred between other eubacterial phyla, e.g., between proteobacteria (E. coli) and the gram positives (Lactobacillus delbrueckii) in the Gap IV subtree or in the Gap I subtree between proteobacteria (Ralstonia solanacearum) and Cytophaga/Bacteroides/Flexibacter (Bacteroides fragilis), as recently described by Figge et al. (1999)
. In conclusion, the data presented clearly underscore the importance of LGT in bacterial evolution (Ochman et al. 2000
) and are in agreement with a recent analysis conducted by Rivera et al. (1998)
who show that the genes encoding operational functions, such as GAPDH, are exchanged with much higher frequency than the so-called informational genes encoding the components of transcription, translation, and replication.
In contrast to the indications presented above, several other lines of evidence let us assume that part of the extant gap gene diversity is not the result of LGT, but was already present in the eubacterial ancestor. First of all, several eubacterial species harbor multiple, up to four, highly divergent gap genes as in the case of Vibrio cholerae (Heidelberg et al. 2000
; indicated by asterisks in fig. 1
). If these multiple gap genes have already been present in the common eubacterial ancestor, today each of these paralogous genes may be expected to form a distinct GAPDH subtree that in itself represents a eubacterial phylogeny. Indeed, the Gap I subtree has features resembling a eubacterial phylogeny (Woese 1987
; Hugenholtz, Goebel, and Pace 1998
) because it includes Gap sequences from five different phyla: proteobacteria (subgroups beta, gamma), cyanobacteria, chlamydiae, spirochetes, and Bacteroides/Cytophaga/Flavobacteria. Even though all other type trees (with the exception of Gap II) comprise species from only two or three eubacterial phyla, it is conceivable for two reasons that these type trees also represent rudimentary eubacterial phylogenies. First, several species may have reduced their original GAPDH gene diversity to one functional copy, a phenomenon termed reductive genome evolution, that is especially frequent within pathogens (Andersson and Kurland 1998
). Second, only a minor fraction of the extant gene diversity is known, and thus the increase in sequence data may generate other type trees that resemble eubacterial phylogenies. Taken together, both LGT and gene duplications in the common eubacterial ancestor seem to account for the extremely broad GAPDH gene diversity presently observed. The fact that few gene phylogenies show a comparable diversity (Brown and Doolittle 1997
) raises the question of why this particular gene has been so successful in bacterial evolution. The existence of different functions, such as erythrose-4-phosphate dehydrogenase activity that was found for the E. coli GapB enzyme (affiliated with the Gap III subtree; Zhao et al. 1995
) or ADP-ribosylating activity on the outer membrane as determined for a GAPDH in group A streptococci (Pancholi and Fischetti 1993
), may in part explain why so many divergent GAPDH genes have been retained in eubacteria. This functional pleiotropism of an ancient and highly conserved component of primary metabolism is surprising. It culminates in mammalian cells where GAPDH proteins are implicated in a number of fundamental processes not related to energy metabolism, such as tRNA export from the nucleus, DNA repair, and protein phosphorylation (for review see Sirover 1999
).
Spirochetes, Donors of Eukaryotic GAPDH Genes
Recently, we showed that a Gap1 sequence from the syphilis-spirochete T. pallidum is very closely related to GapC sequences from Euglenozoa. The phylogenetic position of these GapC sequences made a mitochondrial and thus alpha-proteobacterial origin extremely unlikely, and therefore we invoked an additional gene transfer between T. pallidum and Euglenozoa (Figge et al. 1999
). We have now examined this close relationship in the context of other spirochetal Gap sequences determined in this study. We show that in addition to the T. pallidum Gap1 sequence, several other spirochetal Gap1 sequences are closely related to Euglenozoan GapC. This raises the question of whether the gene transfer postulated did specifically occur between T. pallidum and the Euglenozoa, as originally assumed. In figure 1
, GAPDH sequences from the spirochetes B. hyodysenteriae and S. murdochii seem to be more closely related to the Euglenozoan GAPDH sequences. However, figure 3A
clearly shows that in the absence of distant outgroup sequences, the Treponema sequences cluster with the Euglenozoa with high bootstrap support. The increase of distant outgroup sequences pulls the two Treponema sequences away from the Euglenozoa. Thus, in figure 1
long-branch attraction (LBA) (Felsenstein 1978
) influences the position of the Treponema Gap sequences and makes it difficult to discern which spirochete lineage was actually involved in the transfer. The fact that the GAPDH genes of Euglenozoan nuclei are nested within eubacterial sequences makes a transfer from eukaryotes to prokaryotes very unlikely. There are two further arguments in favor of a transfer in the spirochetes-to-Euglenozoa direction. First, Gap IB is a class I GAPDH and clearly not related to class II GAPDH of Archaea, as would be expected if the gene were inherited from the archaeal/eukaryotic host cell lineage (Hensel et al. 1989
; Cerff 1995
). It also seems possible that the host cell which engulfed the mitochondrial ancestor did not have a glycolytic pathway at all, and hence no authentic GAPDH gene (Martin and Müller 1998
; Liaud et al. 2000
). Therefore, it would be difficult to explain the origin of the euglenozoan gene under the assumption that the transfer occurred in the eukaryote-to-prokaryote direction. Second, very few mechanisms are known that account for a transfer from eukaryotes to prokaryotes (Doolittle 1998
), whereas many have been documented for gene transfer in the opposite direction (Martin 1999
). Therefore, our phylogenetic data together with parsimony clearly favor a scenario in which a spirochete donated a gene to the Euglenozoa.
Finally, it should be noted that the GAPDH tree indicates another, though loose, relationship between spirochetes of the genus Borrelia and protists belonging to the division Parabasalia. In addition to the common branch that was observed in the NJ and ProtML analyses performed, these organisms share a specific insertion (see fig. 2 ). These findings indicate that, similar to the case described above, the GAPDH gene in Parabasalia may have been acquired from a spirochete belonging to the genus Borrelia.
In conclusion, several eukaryotic genes seem to be of spirochetal descent (this study; Doolittle et al. 1999b
; Hannaert et al. 2000
), indicating that spirochetes may have played an important role in the evolution of the eukaryotic cell.
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Acknowledgements |
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Footnotes |
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Keywords: glyceraldehyde-3-phosphate dehydrogenase
gene diversity
spirochetes
lateral gene transfer
eukaryotic evolution
Address for correspondence and reprints: Department of Chemistry and Biochemistry, UCLA, 405 Hilgard Avenue, Los Angeles, California 90095-1569. rfigge{at}chem.ucla.edu
.
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