MBE Advance Access originally published online on May 30, 2003
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Mol. Biol. Evol. 20(8):1188-1194. 2003
DOI: 10.1093/molbev/msg138
© 2003 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038
Loss of DNA Recombinational Repair Enzymes in the Initial Stages of Genome Degeneration
* Department of Biochemistry and Molecular Biophysics
Department of Ecology and Evolutionary Biology, University of Arizona
E-mail: dalecol{at}auburn.edu.
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Abstract |
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Many obligate intracellular pathogens and symbionts undergo genome degeneration during long-term association with eukaryotic hosts; however, very little is known about genome changes that occur in the initial stages of such intracellular associations. By focusing on a clade of bacteria that have recently established symbiotic associations with insect hosts, we have identified events that may contribute to the reduction and degeneration of symbiont genomes. Unlike virtually all other bacteria, the obligate symbionts of maize and rice weevils each display substantial sequence divergence between multiple copies of their rDNA genes, resulting from a reduction in the efficacy of recombinational gene conversion, coincident with the inactivation of the recombinational repair gene recF in the common ancestor of both symbionts. The maize weevil endosymbiont also lacks a functional recA, resulting in further reduction in the efficacy of gene conversion between paralogous rDNAs and in a novel IS-mediated deletion in a 23S rDNA gene. Similar events may be pervasive during the evolution of symbiosis because symbiont genomes typically lack recombinational repair genes and have reduced numbers of ribosomal operons.
Key Words: recombinational repair • endosymbiont • genome degeneration • symbiosis • ribosomal RNA
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsLiterature Cited |
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In comparison with free-living relatives, bacteria that form permanent, obligate, intracellular associations with eukaryotic hosts often have small genomes, high A + T content, elevated mutation rates, and reduced numbers of 16S–23S rDNA operons (Andersson and Andersson 1999; Moran and Wernegreen 2000; Itoh, Martin, and Nei 2002). Moreover, these small genomes typically lack genes that are otherwise universally distributed among bacteria (Moran 2002). For example, Buchnera aphidicola, the obligate intracellular symbiont of aphids, has a massively reduced genome containing only 20% of ancestral genes (Moran and Mira 2001) and lacking many excision, mismatch and recombinational repair genes, including recA, recF, and the entire uvr operon (Shigenobu et al. 2000; Tamas et al. 2002).
When bacteria switch from an autonomous, free-living state to a permanent intracellular existence, there is relaxed selection on the maintenance of genes that are not required for intracellular survival. In addition, changes in population structure lead to an increased fixation of deleterious mutations arising from genetic drift (Moran 1996; Andersson and Kurland 1998). Comparative studies indicate that most gene loss occurs early in the evolution of an intracellular association; for example, in B. aphidicola, which has maintained a 250 Myr association with its insect host, genomes have been highly reduced and static for at least 50 million years (Tamas et al. 2002). For this reason, there is little information on genome changes occurring early in the evolution of an intracellular association, when the majority of gene loss occurs.
To investigate changes accompanying the initial stages of genome degeneration, we have focused on a clade of bacterial symbionts which, according to molecular evolutionary data, established symbiotic associations with their insect hosts some 50 to 100 MYA (Heddi et al. 1998; Dale et al. 2002). The facultative endosymbiont, Sodalis glossinidius, resides in a range of tissues within its tsetse fly host (Aksoy, Chen, and Hypsa 1997; Dale and Maudlin 1999), whereas closely related endosymbionts found in the maize and rice weevils (Sitophilus zeamais and Si. oryzae) are mutualists that only inhabit specialized organelles (bacteriomes) within their weevil hosts (Heddi et al. 1999). There is evidence of recent horizontal transmission of So. glossinidius between different tsetse species (Aksoy, Chen, and Hypsa, 1997), whereas the weevil endosymbionts have followed a strict pattern of exclusive maternal transmission within their hosts (Heddi et al. 1998). Both So. glossinidius and the weevil endosymbionts maintain genes homologous to those of the type III secretion systems found in enteric pathogens, indicative of a recent switch from parasitism to commensalism or mutualism (Dale et al. 2001, 2002). The weevil endosymbionts have not been cultured in vitro, have no official nomenclature, and are described as the Sitophilus zeamais primary endosymbiont (SZPE) and Sitophilus oryzae primary endosymbiont (SOPE).
In this study, we characterized the genome complement of 16S-23S rDNA operons in So. glossinidius, SOPE, and SZPE to determine the dynamics of genome reduction in these endosymbionts. We also analyzed the sequences of recombinational repair genes to understand how the inactivation of these genes might have affected recombinational gene conversion during the evolution of these closely related endosymbionts.
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Materials and Methods |
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Symbiont Isolation and DNA Purification
So. glossinidius was grown in liquid culture, as described previously (Dale and Maudlin 1999). Si. zeamais and Si. oryzae were maintained in maize and wheat, respectively, at 27.5°C and 70% humidity. Bacteriomes (containing SZPE or SOPE) were isolated from fifth-instar Si. zeamais larvae by dissection. DNA was prepared from cultured So. glossinidius and from weevil bacteriomes with the DNeasy tissue kit (Qiagen, Inc., Valencia, Calif.).
Amplification, Cloning, and Sequencing of 16S–23S rDNA
For this study, 5-kb fragments encompassing 16S rDNA, the intergenic spacer region (ISR) and 23S rDNA were amplified from purified symbiont DNA by polymerase chain reaction (PCR) using primers 16SF (5'-GCA CTG CAG GAT CCA GAG TTT GAT CAT GGC TCA GAT TG) and 23SR (5'-GCA GGT ACC GCG GCC GCG CTC GCG TAC CAC TTT AAA TGG CG) in a modified version of the PCR assay described by Thao et al. (2001). Polymerase chain reactions contained 5 ng of symbiont DNA, 2.5 mM MgCl2, 0.2 mM dNTPs, 1 pmol of each primer, 1 U of Taq DNA polymerase and 0.3 U Pfu DNA polymerase. Amplification proceeded with 30 cycles of denaturation (94°C for 30 s), annealing (55°C for 2 min), and extension (70°C for 6 min), followed by a final 10 min extension at 70°C to promote the A-tailing of PCR products. The amplified 16S–23S rDNA fragments were cloned into pTOPO-XL (Invitrogen, Carlsbad, Calif.) according to the manufacturer's instructions, utilizing the ccdB conditional lethal selection procedure. At least 10 recombinant clones were sequenced from each template, and to ensure that every 16S and 23S rDNA gene was represented, we generated libraries of 16S rDNA sequences from each symbiont by cloning 16S rDNA PCR products amplified according to the methods described by Unterman, Baumann, and McLean (1989). Additional sequencing primers were designed as sequence information became available. Candidate tRNAs within the ISR were identified with the tRNAscan-SE software (Lowe and Eddy 1997).
Amplification, Cloning, and Sequencing of the recA and recF Genes
Partial fragments of recA (560 bp) and recF (538 bp) were amplified from So. glossinidius, SOPE, and SZPE with the use of universal primers (recAF: 5'-TNG ARA THT AYG GIC CIG ART C, recAR: 5'-ACN ACY TTN ACI CGI GTY TCR CT, recFF: 5'-MGN GCI TTY YTI GAY TGG G, and recFR: 5'-TCN ARY TCI GAR GCR AAR TC) in reactions containing 5 ng of purified symbiont DNA, 2.5 mM MgCl2, 0.2 mM dNTPs, 1 pmol of each primer, 1 U of Taq DNA polymerase, and 0.3 U Pfu DNA polymerase. Amplification proceeded as described above, but with 1 min annealing and extension steps. Amplicons were cloned into pTOPO2.1 (Invitrogen) according to the manufacturer's instructions, and six recombinant clones were sequenced from each reaction. The 5' and 3' ends of recA and recF were amplified with oligonucleotide primers matching adjacent genes in alignments of the Escherichia coli K12 and Salmonella typhimurium LT2 genomes. The complete recA and recF genes were amplified with primers (recAF1: 5'-CGT ATC GGC TCG GTG AAA GAA GG; ygaDR: 5'-CCT TCT TTC ACC GAG CCG ATA CG; gyrBF: 5'-GCA ATT TTT GCC GGA GTT TCG CC; recFR1: 5'-TTG ATA CTG GAG GAG TCA TAA; recFF1: 5'-TTG CTC CAG GCG GTA AAG AAA; dnaNR: 5'-GGA ACA GGA AGA AGC GGA AGA). Polymerase chain reactions and cycling conditions were the same as those used for the amplification of the internal recA and recF fragments, with extension times adjusted to 1 min/kb for products >1 kb. All products were cloned and sequenced in pTOPO2.1 (Invitrogen) as above.
Phylogenetic Analysis
The 16S rDNA and 23S rDNA coding regions from the different operons of So. glossinidius, SZPE, and SOPE were aligned with the sequences from E. coli rrnH (NC_00913) using PILEUP (Genetics Computer Group package, Madison, Wis). For each of the two genes, individual sequence changes were examined on a phylogenetic tree using MacClade 4.02 (Maddison and Maddison 1992) with the "Trace All Changes" option.
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Results |
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The rDNA Operons of So. glossinidius, SOPE, and SZPE
We identified two distinct 16S–23S rDNA operons in So. glossinidius and three distinct 16S–23S rDNA operons in each of the weevil symbionts, SOPE and SZPE. No additional 16S rDNA genes were detected during comparisons of the operon sequences or during screening of libraries of polymorphic 16S rDNA sequences.
In prokaryotes, the rDNA genes are normally organized in tandem in a single operon in the order 16S–23S–5S. There is an intergenic spacer between 16S and 23S rDNA encoding tRNAs, usually either tRNAGlu alone or tRNAIle and tRNAAla. The rDNA genes are often multicopy, and rDNA operon copy numbers are associated with genome size (Gurtler and Stanisich 1996; Gurtler 1999). The 16S–23S rDNA operons of SOPE, SZPE, and So. glossinidius each have two different ISRs encoding either tRNAGlu alone (ISR1) or both tRNAIle and tRNAAla (ISR2; fig. 1). So. glossinidius maintains two distinct 16S–23S rDNA operons, one with ISR1 and another with ISR2, and each of the weevil endosymbionts (SOPE and SZPE) has three distinct 16S–23S rDNA operons, one with ISR1 and two with ISR2 (fig. 1B). Regardless of ISR type, the sizes of corresponding ISRs are larger in both SOPE and SZPE than in So. glossinidius. In addition, SOPE and SZPE have 243-bp and 189-bp regions of noncoding sequence adjacent to the 23S ends of ISR type 1 and 2 (respectively) that are deleted from So. glossinidius.
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An IS256-Like Element Located Within a 23S rDNA of SZPE
The maize weevil endosymbiont SZPE has a 1.33-kb insertion sequence (IS) element located within the coding sequence of 23S rDNA in the 16S–23S rDNA operon harboring ISR1 (fig. 1C). This element has an intact transposase open reading frame flanked by two inverted imperfect repeats (IIRL and IIRR) and is located 244-bp from the 3'-end of 23S rDNA. Based on the positions of conserved amino acids within the transposase and the length and sequence of the imperfect inverted repeats, this IS element is a member of the IS256 family (Mahillon and Chandler 1998), and we propose the name ISSZPE1. The closest matching IS element in the GenBank database is the IS1414 element of enteropathogenic E. coli (McVeigh et al. 2000).
Because transposition normally occurs through a "cut-and-paste" process, it is surprising that one of the inverted repeat sequences flanking ISSZPE1 is partially duplicated (fig. 1C). Bacterial IS elements typically produce short, perfect, direct repeats of target DNA after transposase-mediated repair of the staggered dsDNA breaks generated during insertion. For the IS256 family of IS elements, the expected size of these direct repeats is 8-bp in length (Guedon et al. 1995; Picardeau, Bull, and Vincent 1997); however, no direct repeats are found adjacent to the imperfect inverted repeats flanking ISSZPE1 (5'-GGC TTT GAA and 5'-CAT AAG CTA).
Both replicative and nonreplicative IS-mediated rearrangements are predicted to occur at a higher frequency when two elements are located in close proximity (Weinert, Schaus, and Grindley 1983; Mahillon and Chandler 1998). Often, these events are deletogenic, resulting in the reciprocal deletion of an IS element and an adjoining piece of DNA. By aligning the sequences of two SZPE 23S rDNA genes (including one harboring ISSPZE1), we identified a 198-bp deletion in 23S rDNA adjacent to ISSZPE1. Combined with the fact that ISSZPE1 has a duplicated imperfect inverted repeat and no direct repeats, these results suggest that ISSZPE1 is a hybrid molecule, generated from the deletogenic rearrangement of two identical IS elements (fig. 2).
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Loss of the rec Genes in the Weevil Endosymbionts
Although the organization of the recA, recF and flanking genes in So. glossinidius, SOPE, and SZPE is essentially the same as that described for Escherichia coli and Salmonella spp. (fig. 3), both of the weevil endosymbionts have an identical 14-bp frameshift deletion located in the coding sequence of recF. Given that this deletion occurs in SOPE and SZPE, but not in So. glossinidius, it likely occurred in the last common ancestor of the weevil endosymbionts, after they split from So. glossinidius.
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The complete coding sequence of recA was obtained by amplifying the region corresponding to alaS–recX–recA–ygaD in Sa. typhimurium. Neither So. glossinidius, SOPE, nor SZPE harbors a full-length recX gene. In some bacterial species, the RecX protein plays a role in regulating RecA activity by potentiating RecA-driven homologous recombination and allowing high-level expression of RecA (Stohl and Seifert 2001; Sukchawalit et al. 2001).
Whereas both So. glossinidius and SOPE maintain full-length and intact recA genes, the coding sequence of recA in SZPE contains a nonsense mutation at position 235 (fig. 3A). Because the recA mutation is restricted to the maize weevil endosymbiont, it occurred after the divergence of the maize and rice weevils and, thus, after the acquisition of the 14-bp frameshift deletion in recF.
Evolution of the rDNA Operons in So. glossinidius, SOPE, and SZPE
Pairwise nucleotide sequence comparisons indicate that SOPE and SZPE each have unusually high levels of interoperon divergence between paralogous copies of 16S and 23S rDNA (table 1). To trace the evolutionary history of the 16S and 23S rDNA sequences in So. glossinidius, SOPE, and SZPE, we examined this sequence variation in a phylogenetic context. Initially, phylogenetic trees were constrained to reflect the divergence between SOPE and SZPE preceding any additional divergence between sequences of different operons within these symbionts. This would be anticipated if the rDNA coding sequences from different operons were being homogenized by gene conversion. After mapping base changes onto branches of the trees, we identified eight nucleotide substitutions that were maintained only in the rDNA coding sequences of operons harboring tRNAGlu in both SOPE and SZPE, indicating that rDNA coding sequences in SOPE and SZPE began diverging before speciation of the weevil symbionts.
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To take account of this pattern of evolution, we constructed phylogenetic trees assuming that divergence of the individual operons began before the split between SOPE and SZPE (fig. 4). The resulting trees show that So. glossinidius diverged from a common ancestor of the weevil symbionts before the onset of any interoperon divergence between rDNA sequences in SOPE and SZPE. Like most bacteria, So. glossinidius maintains paralogous 16S and 23S rDNA genes with near identical sequences. In contrast, SOPE and SZPE have paralogous 16S and 23S rDNA sequences that display an unusually high level of divergence (table 1). Because it is known that gene conversion drives the concerted evolution of genic sequences within the rDNA operons in bacteria (Liao 2000), our results indicate that there are differences in the efficacy of gene conversion in So. glossinidius, SOPE, and SZPE.
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To determine if there has been any recent gene conversion between paralogous rDNA sequences within SOPE and SZPE, we mapped base changes onto branches of the 16S and 23S rDNA trees and searched for regions of shared homology within paralogous sequences. We failed to identify any evidence of recent gene conversion in SZPE but found several sequence tracts in two of the three paralogous rDNA genes of SOPE that share identical consecutive nucleotide substitutions. Thus, in comparison with So. glossinidius and other bacteria, there is a reduced frequency of gene conversion in SOPE, insufficient to drive concerted evolution of the rDNA sequences. Furthermore, our results indicate that there is no ongoing gene conversion between rDNA sequences in SZPE.
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Discussion |
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Most obligate intracellular pathogens and symbionts studied to date are in the advanced stages of genome degeneration, as evidenced by their vastly reduced genome sizes, high A + T contents, and elevated rates of polypeptide evolution. In contrast, the genomes of So. glossinidius, SOPE, and SZPE provide insights into the early stages of the degenerative evolutionary processes following the transition from free-living to an intracellular lifestyle. In this study, we identified a link between the inactivation of two DNA recombinational repair enzymes (RecF and RecA) and the loss of recombinational gene conversion, occurring early in the evolution of mutualistic associations.
Several additional lines of evidence indicate that degenerative evolution is at an early stage in So. glossinidius, SOPE, and SZPE. First, the genome sizes of So. glossinidius and SOPE, estimated at 2 mb and 3 mb, respectively (Charles et al. 1997; Akman et al. 2001), are smaller than those of related free-living bacteria like E. coli (4.5–5.3 mb) but substantially larger than those of many other insect endosymbionts such as B. aphidicola (0.45–0.65 mb; Charles and Ishikawa 1999; Gil et al. 2002), Wigglesworthia glossinidia (0.75 mb; Akman and Aksoy 2001), Blochmannia spp. (0.8-mb; Wernegreen, Lazarus, and Degnan 2002) and Wolbachia spp. (0.95–1.66 mb; Sun et al. 2001). Second, the genomic base compositions of So. glossinidius, SOPE, and SZPE have been estimated to be equitable with those of free-living bacteria, and there is no evidence of an A + T bias in sequenced genes (Heddi et al. 1998; Dale and Maudlin 1999). Finally, the relative rates of synonymous and nonsynonymous nucleotide substitution in So. glossinidius and SZPE are similar to those observed for free-living bacteria (Dale et al. 2002).
Comparative evolutionary analyses of protein-coding genes indicate that So. glossinidius, SOPE, and SZPE shared a common ancestor about 100 MYA (Dale et al. 2002). After diverging from So. glossinidius, the last common ancestor of SOPE and SZPE established an obligate symbiosis with weevils (Heddi et al. 1998). Prior to the speciation of the rice and maize weevils (Si. oryzae and Si. zeamais), there was a 14-bp frameshift deletion in the recF of the ancestor of SOPE and SZPE, and subsequent to the divergence of the rice and maize weevils, SZPE acquired a nonsense mutation in recA. Thus, So. glossinidius retains intact copies of both recF and recA, whereas SOPE lacks a functional recF (but retains recA), and SZPE lacks functional copies of both recF and recA. In E. coli, recombinational repair is mediated by two pathways involving either the RecBCD or RecFOR protein complexes, both of which require RecA (Kowalczykowski 2000). In E. coli, experimental evidence indicates that the RecBCD pathway is more important than is the RecFOR pathway in conjugal recombination and transduction. However, in replication fork repair and in other major recombination functions, the RecBCD and RecFOR pathways both play critical roles (Galitski and Roth 1997; Lovett et al. 2002).
In SOPE and SZPE, the sequential inactivation of both recF and recA affects rates of gene conversion, as evident from sequence analysis of multicopy rRNA genes within each endosymbiont genome. In virtually all bacterial species, there is little or no interoperon divergence between sequences of 16S and 23S rDNA, because paralogous gene copies are homogenized by ectopic recombination (Liao 2000). Coincident with the inactivation of the recF gene in a common ancestor of the weevil endosymbionts SOPE and SZPE, there was a substantial reduction in gene conversion between paralogous rDNA genes. Intragenomic divergence of the rDNA paralogs is substantially higher in SOPE and SZPE, which lack recF, than in So. glossinidius (table 1) as a result of the reduction in the frequency of recombinational gene conversion in the two weevil endosymbionts. The subsequent loss of recA in SZPE appears to have further reduced the frequency of gene conversion in this species, and there is no evidence of gene conversion between paralogous rDNA genes in SZPE.
In SZPE, the inactivation of both recF and recA is also linked to the presence of a novel IS-mediated deletion in one copy of the 23S rDNA gene, resulting from an intramolecular rearrangement between two adjacent, identical IS256-like elements. During random sequencing, we have identified an additional copy of the ISSZPE1 located on a 134-kbp extrachromosomal element maintained by SZPE (data not shown). This plasmid-borne copy of ISSZPE1 probably served as a donor for transposition of ISSZPE1 into the SZPE chromosome. In hosts lacking recA, IS elements are known to undergo duplicative intramolecular rearrangements, promoting deletion of adjacent IS elements and host DNA (Weinert, Schaus, and Grindley 1983). This mechanism could promote genome degeneration in chronic intracellular pathogens and symbionts that have lost components of their DNA recombinational repair machinery. The presence of a 1.33-kb IS element and the loss of almost 200 bp of coding sequence from the 23S rDNA gene likely prevents the correct folding and functioning of this rRNA subunit. In bacteria with active recombinational repair pathways, we would expect IS elements to be purged from multicopy rRNA genes during interoperon gene conversion.
Because it is known that many obligate intracellular pathogens and symbionts lose components of their DNA recombinational repair machinery, we might question whether such losses occur passively as a consequence of relaxed selection, or actively as part of an adaptive response toward life in the intracellular environment. The latter hypothesis suggests that loss of the DNA recombinational repair genes occurs as a result of a large-scale reduction in genome size. However, our results contradict this hypothesis, because the mutational inactivation of recF in the weevil endosymbionts occurred at an early stage in the evolution of the intracellular association, independent of massive gene loss. Furthermore, the recF pseudogene has been retained by SOPE and SZPE for at least 30 Myr, since the divergence of the maize and rice weevils.
Based on the available evidence, we conclude that the recA and recF genes were inactivated in the weevil endosymbionts as a consequence of relaxed selection, but it is interesting to note that this has not occurred in So. glossinidius. This could be attributed to differences in the nature of interactions between these endosymbionts and their hosts, especially given the fact that So. glossinidius is a facultative symbiont, residing both intra- and extracellularly in host tissues, whereas the weevil symbionts are exclusively intracellular. In free-living bacteria, the primary role of the recombinational repair machinery is the nonmutagenic restoration and repair of stalled replication forks (Lusetti and Cox 2002). As a result of the protective nature of their environment, obligate intracellular pathogens and symbionts are likely to experience a lower incidence of DNA damage, reducing their requirement for recombinational repair.
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Acknowledgements |
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The authors thank Alvin J. Clark and Ted Weinert for providing helpful comments. We also thank Serap Aksoy (Yale University) for providing So. glossinidius cultures and Jim Baker (USDA, Manhattan, Kans.) for providing Si. zeamais and Si. oryzae. This work was supported by National Institutes of Health grant GM56120 to H.O. and National Science Foundation grant DEB-9978518 to N.M.
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Footnotes |
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1 Present address: Auburn University.
Thomas Eickbush, Associate Editor
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