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Molecular Plant Pathology Laboratory, USDA-Agriculture Research Service, BARC-West, 10300 Baltimore Avenue, Beltsville, MD 20705, USA
Correspondence
Yan Zhao
zhaoy{at}ba.ars.usda.gov
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 10 June 2005 as DOI 10.1099/ijs.0.63655-0.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Davis et al., 1972; Lee et al., 2000). These phytopathogenic agents are restricted, in plants, to sieve cells of phloem tissue and are transmitted from diseased to healthy plants by insect vectors, mainly leafhoppers and psyllids. Spiroplasmas and phytoplasmas belong to the class Mollicutes and have been thought to be derived from ancestral low-G+C Gram-positive bacteria, possibly some ancient members of the Bacillus–Clostridium group, through retrogressive evolution and massive genome reduction (Razin et al., 1998). Since phytopathogenic mollicutes parasitize both plant hosts and insect vectors, knowledge of the evolution of these agents could be helpful in understanding their biology.
Genetic relatedness or evolutionary relationships among micro-organisms, including mollicutes, have often been proposed based on analyses of 16S rRNA genes (Gasparich et al., 2004; Gundersen et al., 1994; Olsen & Woese, 1993; Stackebrandt & Goebel, 1994; Stackebrandt et al., 1997; Weisburg et al., 1989; Woese, 1987), mainly because 16S rRNA gene sequences are ubiquitous and well-conserved across the spectrum of prokaryotes, and are known for many bacterial species. However, the highly conserved nature of the 16S rRNA gene tends to limit its power to resolve closely related organisms that diverged at almost the same time (Fox et al., 1992; Woese, 1987). Individual, conserved protein-encoding genes have also been analysed to build phylogenetic trees of prokaryotes. Nevertheless, the topologies of such protein-based phylogenetic trees do not always agree with that of a 16S rRNA gene tree (Brown & Doolittle, 1997; Golding & Gupta, 1995). This can be attributed to either extensive lateral gene transfer or degradation of phylogenetic signals caused by saturation of amino acid substitutions during the evolution of organisms (Brochier et al., 2000; Brown et al., 2001; Doolittle, 1999; Forterre & Philippe, 1999). The recent availability of multiple complete genome sequences from diverse bacterial taxa creates unprecedented opportunities to explore new phylogenetic approaches based on comparative analysis of full gene complements or large subsets thereof (Brown et al., 2001; Daubin et al., 2002; Wolf et al., 2001). One such new approach involves the use of large combined or concatenated orthologous proteins to construct a universal tree; the concatenated protein data lead to significant amplification of phylogenetic signals and increased resolving power (Brown et al., 2001; Wolf et al., 2001). Another novel approach involves comparison of topologies of individual gene trees and focuses on congruence of tree topologies, which permits identification of a core of genes that share a common history and have undergone fewer lateral transfers (Daubin et al., 2002). In the present study, by combining the above two approaches, we constructed a hypothetical phylogenetic tree to propose the evolutionary positions of phytopathogenic mollicutes. Analyses of 61 core housekeeping proteins from 41 bacterial species suggested a consensus phylogeny: phytopathogenic spiroplasmas and phytoplasmas clustered with other mollicutes, forming a monophyletic clade. Phytoplasmas diverged from spiroplasmas and mycoplasmas at an early stage in the evolution of the class Mollicutes.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) were extracted from the annotated genome data deposited in GenBank, DDBJ and EMBL. Incomplete genome sequences of Spiroplasma kunkelii strain CR2-3x and ‘Candidatus Phytoplasma asteris’-related strain AY-WB were retrieved from the University of Oklahoma's Advanced Center for Genome Technology Internet web site at http://www.genome.ou.edu/spiro.html and the Ohio State University's phytoplasma genome sequencing web site at http://www.oardc.ohio-state.edu/phytoplasma/genome.htm respectively, as assembled contigs. The individual contigs were analysed by using the heuristic models of GeneMark and GeneMark.hmm programs (Besemer & Borodovsky, 1999) for identifying potential open reading frames. The predicted protein-encoding genes were annotated following a search of the National Center for Biotechnology Information (NCBI)'s non-redundant protein database using the position-specific iterated and pattern-hit iterated BLAST programs (Altschul et al., 1997), and a search of the Clusters of Orthologous Groups (COG) database using the program COGnitor (Tatusov et al., 2001).
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). This set of 78 proteins was used as queries for BLAST2 searches against completely sequenced bacterial genomes, listed in Table 1
, at the DDBJ's Genome Information Broker web site (http://gib.genes.nig.ac.jp/). Among the 78 proteins, 61 are ubiquitously present in all the genomes and are well conserved. These 61 proteins are also present in the partially sequenced genomes of ‘Candidatus Phytoplasma asteris’-related strain AY-WB and Spiroplasma kunkelii, and therefore were selected for phylogenetic analysis. Orthologues of these selected proteins were retrieved from the 41 genomes, divided into five subsets according to their functional categories and concatenated head-to-tail (Table 2).
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; Thompson et al., 1997). Each output alignment was converted to NBRF/pir format and was trimmed using GBLOCKS (version 0.91b) to eliminate poorly aligned positions (Castresana, 2000). The trimmed alignment was converted to MEGA or PHYLIP format for phylogenetic analyses. Distance analyses were performed with the MEGA2 (version 2.1; Kumar et al., 2001) or CLUSTAL_X (version 1.81; Thompson et al., 1997) package using the neighbour-joining (NJ) method with Gamma-distance model for multiple substitutions at the same amino acid site. Parsimony analyses were conducted with PHYLIP (version 3.62; Felsenstein, 1989, 2004) using the Protein Parsimony algorithm (ProtPars). Maximum-likelihood (ML) analyses were performed with PHYLIP (version 3.62) using the Protein Maximum Likelihood program (ProtML) (Felsenstein & Churchill, 1996) with the Jones–Taylor–Thornton probability model option (Jones et al., 1992). The reliability of each phylogenetic analysis was subjected to a bootstrap test with 1000 replicates. The five best trees from the default output of each analysis were used as input for the CONSENSE program of the PHYLIP (version 3.62) package to generate a consensus tree. Phylogenetic trees were viewed using TreeExplorer of the MEGA2 package (Kumar et al., 2001) and the PhyloDraw program (Choi et al., 2000). |
RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Ribosomal protein tree
Ribosomal proteins are key protein components of the ribosome, a ubiquitous cellular apparatus that translates genetic information encoded in mRNA into proteins. Ribosomal proteins are conserved among bacterial species not only at individual gene/protein sequence levels but also at the gene organization level. Most ribosomal protein genes are clustered in several highly conserved operons, such as the S10-spc-alpha superoperon, which ensures coordinated expression of the genes. Although duplication and possible horizontal transfer of individual ribosomal protein genes have been described in some recent reports (Brochier et al., 2000; Makarova et al., 2001), such events are considered infrequent. Large-scale comparative genomics studies suggest that ribosomal protein genes are among a core of genes that share a common history (Daubin et al., 2002) and carry a strong phylogenetic signal (Wolf et al., 2001). The 44 ribosomal proteins used in the present study were concatenated head-to-tail and treated as a single protein sequence. The initial alignment of the concatenated protein sequences from 41 species contained 8622 columns. The removal of gaps and poorly aligned regions that might not be homologous or might have been saturated by multiple substitutions (Castresana, 2000) resulted in a final alignment of 4117 columns. Use of concatenated multiple ribosomal protein sequences allowed for amplification of phylogenetic signals and reduction of potential noise caused by possible lateral gene transfer events. Phylogenetic analysis using a distance method (NJ algorithm) resulted in the tree topology shown in Fig. 1(a). The tree topology was supported by high bootstrap values. Phylogenetic analyses using maximum-parsimony (MP) and ML algorithms generated ribosomal protein trees with nearly identical topologies (data not shown; see consensus phylogeny below).
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Congruence of the ribosomal protein tree with other protein trees
The other protein datasets used in this study included five key enzymes that are involved in glycolysis (Table 2). Glycolysis is a universal metabolic pathway that converts glucose into pyruvate with the concomitant production of a relatively small amount of ATP. This pathway probably developed before there was sufficient oxygen in the atmosphere to sustain more-effective methods of energy extraction (Barnett, 2003). When aerobic organisms evolved, a more-efficient energy-harvesting pathway, namely the tricarboxylic acid (TCA) cycle, developed; oxidative phosphorylation steps were added onto glycolysis (Barnett, 2003). Glycolytic enzymes are among the most highly conserved enzymes known. It was estimated that one of the key glycolytic enzymes, phosphoglycerate kinase (Pgk), has an evolutionary history of 40 million years (Ciccarese et al., 1989) and has been evolving at a linear rate of 4·8 accepted point mutations per 100 million years (Fothergill-Gilmore, 1986). The value of glycolysis enzymes as a phylogenetic marker has been extensively evaluated (Canback et al., 2002; Chattopadhyay & Chakrabarti, 2003). Recently, Pgk was used to reconstruct a phylogeny of ‘Firmicutes’ with special reference to Mycoplasma (Wolf et al., 2004). The role of glycolysis in mollicutes is especially critical, as these organisms lack a TCA cycle (Pollack et al., 1997). In the present study, the initial alignment and the trimmed alignment of the concatenated glycolytic enzymes contained 2798 and 1141 columns, respectively. Phylogenetic analysis of the trimmed alignment generated a phylogeny (Fig. 1b) with a tree topology that was almost identical to that inferred from combined ribosomal proteins. The only difference was that, in the ribosomal protein tree (Fig. 1a), the members of the hominis group (represented by Mycoplasma pulmonis and Mycoplasma mobile) formed a sister lineage with members of the pneumoniae group, whereas in the glycolytic enzyme tree (Fig. 1b), the hominis group formed a sister lineage with members of the mycoides group, although the bootstrap value for this sister lineage relationship was lower than that for the hominis group–pneumoniae group sister lineage relationship in the ribosomal protein tree.
DNA polymerase III alpha-subunit, excinuclease ABC subunits and DNA-dependent RNA polymerase subunits were also included in our datasets. These proteins are among the core components whose genes share a common history (Daubin et al., 2002) and are involved in genetic information storage, repair and transcription. They carry strong phylogenetic signals and have greater resolving power than 16S rRNA gene sequences (Klenk & Zillig, 1994; Mollet et al., 1997; Teeling et al., 2004). A phylogenetic tree constructed based on concatenated DNA polymerase III subunit alpha (DNApol) and excinuclease subunits A, B and C (UVR) exhibited a topology that was almost identical to that of the ribosomal protein tree (Fig. 1a), with only minor differences at a low taxonomic level within the Bacillales group (Fig. 1c) where the positions of Listeria species and Staphylococcus species were switched, and Mycoplasma pulmonis and Mycoplasma mobile were grouped with the mycoides clade. Furthermore, in the UVR–DNApol tree, Oceanobacillus iheyensis was clustered with Staphylococcus species and paraphyletic to Bacillus halodurans, whereas in the ribosomal protein tree O. iheyensis was clustered with B. halodurans and was paraphyletic to Staphylococcus species. The phylogeny inferred from the four combined DNA-dependent RNA polymerase subunits gave a tree topology (Fig. 1d) that was almost exactly the same as that of the ribosomal protein tree.
In bacteria, the secretion of proteins from the site of their synthesis to outside the cytoplasmic membrane is mediated by multiple protein translocation systems, among which the Sec-dependent protein translocation machinery is the most prominent and is ubiquitous to all bacteria. The Sec machinery consists of a heterotrimeric transmembrane channel, SecYEG, and a peripheral homodimeric ATPase, SecA (den Blaauwen & Driessen, 1996). Highly hydrophobic preproteins that are translocated via the Sec machinery may bypass the SecA component and use the signal recognition particle (SRP) pathway to approach the SecYEG channel (Tjalsma et al., 2000). Sequences of both Sec machinery components and SRP components are well conserved among bacteria. In the present study, SecA, SecY, SRP54 and SRPR sequences were selected for phylogenetic analysis. The phylogeny inferred from this set of combined data was slightly different from that suggested by the ribosomal protein data. In this protein translocation tree (Fig. 1e), the Clostridium clade clustered together with the Bacillales–‘Lactobacillales’ clade to form a monophyletic group, paraphyletic to the Mollicutes clade. However, when the SRP54 and SRPR sequences were removed from the alignment, the SecA–SecY phylogeny obtained (Fig. 1f) was in excellent agreement with the ribosomal protein phylogeny, although the bootstrap support for some branches was weak. It would be interesting to know whether or not lineage-specific lateral SRP54/SRPR gene transfer occurred after the divergence of the Clostridium group and the Bacillales–‘Lactobacillales’ group. Since genes encoding SRP54 and SRPR proteins are single copy genes in all bacterial species used in this study, additional orthology information may be helpful in resolving the topology difference caused by the SRP54 and SRPR proteins (Philippe & Forterre, 1999).
A consensus phylogeny
To resolve the minor differences that were present in the phylogenetic trees derived from the five sets of concatenated proteins, two approaches were taken towards building a consensus phylogeny. In the first approach, five output tree files resulting from each phylogenetic analysis method (NJ, MP or ML) were used as input files for computing consensus trees according to the majority rules set by the CONSENSE program of the PHYLIP software suite (Felsenstein, 1989). As shown in Fig. 2(a–c), the consensus trees based on the data from three different phylogenetic analysis methods are in close mutual agreement. The second approach involved further concatenation of the five sets of concatenated proteins into a single superprotein set and subsequent phylogenetic analysis of the superprotein set. The NJ phylogeny inferred by the superprotein (Fig. 3) was identical to the consensus NJ phylogeny computed using the CONSENSE program (Fig. 2a). In the consensus phylogeny, all mollicutes, including plant-pathogenic spiroplasmas and phytoplasmas, appear to be monophyletic and to share a common Clostridium-like ancestor. Within the Mollicutes clade, phytoplasmas diverged from the rest of the Mollicutes at an early stage in the evolution of mollicutes. The divergence between phytoplasmas and the other mollicutes is also indicated by the differences between the genetic code systems used by the phytoplasmas and the rest of the mollicutes examined in this study. Whereas phytoplasmas and acholeplasmas use the standard genetic code system, spiroplasmas and other mollicutes use an uncommon genetic code system, in which the triplet TGA encodes a tryptophan rather than being a translation termination codon (Citti et al., 1992). The plant-pathogenic species Spiroplasma kunkelii, together with its non-helical siblings, which include the animal-pathogenic species Mycoplasma mycoides and the non-pathogenic species Mesoplasma florum, formed the mycoides clade. The mycoides clade also branched off relatively early from the other human- and animal-pathogenic mollicutes. The remaining mollicutes were clustered into two major groups, namely the hominis group and the pneumoniae group. This multiple-protein consensus phylogeny coincided well with the phylogeny inferred from ribosomal 16S rRNA genes (Fig. 4). However, one problem with all the phylogenetic trees in this study is that they are all based on limited available sequences and mostly originate from taxa that are only distantly related (except the two ‘Candidatus Phytoplasma asteris’-related species). Thus, there is a risk that long-branch attraction can result in topologies that do not reflect the true phylogenies. Because of the lack of more-extensive sequence data, it is difficult to perform a more-extensive study at this time. Nevertheless, the multiple-protein sequence-based tree has branch lengths that are almost twice as long as those of the 16S rRNA gene tree. Therefore, the multiple-protein approach appears to offer a greater resolving power than the 16S rRNA gene approach, and should be helpful in determining phylogenetic positions of closely related species.
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Conclusion
The class Mollicutes consists of a group of genetically heterogeneous wall-less prokaryotes. Until recently, their taxonomy has been based on biochemical and phenotypic criteria (Razin et al., 1998) that are inaccessible for uncultured prokaryotes. The molecular technology developed during the past two decades has advanced the systematics of mollicutes, especially uncultured plant-pathogenic phytoplasmas. Phylogenetic analyses based on conserved 16S rRNA gene sequences made it possible to envision the molecular genetic relatedness among diverse mollicutes and their evolutionary relationships with walled prokaryotes (Gasparich et al., 2004; Gundersen et al., 1994; Lee et al., 2000; Weisburg et al., 1989; Woese, 1987). Several members of the class Mollicutes have been reclassified based on phylogenies inferred by 16S rRNA gene sequence analyses. To date, the class Mollicutes consists of four orders and eight formal genera. Moreover, 16S rRNA gene-based phylogenies have begun to reveal the evolutionary history of mollicutes; although they loosely formed a monophyletic group, mollicutes appeared to be comprised of several phylogenetic clusters that were deeply divergent from one another, as indicated by long branch lengths on phylogenetic trees. One deeply divergent cluster is comprised of phytoplasmas together with Acholeplasma species and Anaeroplasma species forming a monophyletic group (Gundersen et al., 1994; Lee et al., 2000).
In the present study, a consensus phylogeny inferred by multiple sets of concatenated housekeeping proteins clearly delineated phylogenetic relationships among 41 representative walled bacteria and wall-less mollicutes, reinforcing the notion that phytoplasmas represent a distinct lineage evolving in parallel with mycoplasmas. The divergence between phytoplasmas and the other mollicutes is also indicated by the difference in the genetic code systems used by the phytoplasmas and the other mollicutes examined in this study.
The phylogenetic trees reconstructed from the five sets of concatenated housekeeping proteins imply similar degrees of conservation among the five sets of proteins analysed. The phylogenies inferred by these proteins, whose sequences are less conserved than those of 16S rRNA genes, clearly amplify the resolving power for delineating phylogenetic relationships among the prokaryotes studied. Thus, these housekeeping proteins should provide a more discriminating tool for phylogenetic analysis than the 16S rRNA gene.
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ACKNOWLEDGEMENTS |
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