Microbial Genomics & Bioprocessing Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, Illinois
Correspondence: E-mail: rooney{at}ncaur.usda.gov.
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Abstract |
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Key Words: birth-and-death purifying selection multigene family rRNA
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Introduction |
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Regardless of the organizational pattern, rRNA genes are usually repeated a few to several hundred times and are presumed by most researchers to be highly homogenized, owing to their concerted evolution. Under the concerted evolution model, mutations that arise in one member of a multigene family can spread to all other members through some sort of homogenization process other than purifying selection, such as gene conversion or unequal crossover (Brown, Wensink, and Jordan 1972; Zimmer et al. 1980; Dover and Coen 1981; Arnheim 1983; Li 1997; Ohta 1989, 2000). As a result, the members of the multigene family do not evolve independently. The notion that all rRNA genes (with the exception of those in organellar genomes) evolve in a concerted manner has in effect become dogma (Dover and Coen 1981; Hillis and Dixon 1991; Ohta 2000). Nevertheless, there are cases in which departures from the rRNA concerted evolution model have been identified. For example, there are two distinct repeat families of 18S rRNA genes in dugesiid flatworms (Carranza et al. 1996; Carranza, Baguñà, and Riutort 1999) and two distinct repeat families of 16S rRNA genes in certain actinomycetous bacteria (Wang, Zhang, and Ramanan 1997; Ueda et al. 1999). Similarly, many species of the microbial eukaryotic phylum Apicomplexa possess distinct rRNA gene "types."
In apicomplexans, the structure and function of rRNA genes has been best studied in Plasmodium. Species within this genus possess functionally distinct rRNA "types" believed to be maintained in response to developmental constraints imposed by a multihost life cycle (Gunderson et al. 1987, McCutchan et al. 1988; Zhu et al. 1990; Rogers et al. 1996; Li et al. 1997; Gardner et al. 2002; Mercereau-Puijalon, Barale, and Bischoff 2002). Specifically, a certain rRNA type is expressed only during a particular growth stage of the organism, whereas another type is expressed at a different stage (Gunderson et al. 1987; Le Blancq et al. 1997; Mercereau-Puijalon, Barale, and Bischoff 2002). An important question that remains unanswered is how rRNA functional heterogeneity evolved and subsequently has been maintained over millions of years of apicomplexan evolutionary history. This is an important question to answer, because the "rule" in all other eukaryotes is that rRNA genes are homogeneous (Coen, Strachan, and Dover 1982; Nei 1987; Li 1997; Graur and Li 2000). As such, the exception of apicomplexan rRNA genes to this "rule" indicates that they must undergo unique mechanisms of multigene family evolution. The purpose of this study is to examine these mechanisms in more detail by studying the evolutionary patterns of 18S rRNA gene diversification in representative apicomplexan species.
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Materials and Methods |
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Multigene Family Models
In this study, patterns of apicomplexan 18S gene evolution are reconciled with either the concerted evolution (Brown, Wensink, and Jordan 1972; Zimmer et al. 1980; Arnheim 1983) or birth-and-death evolution models (Hughes and Nei 1989; Ota and Nei 1994; Nei, Gu, and Sitnikova 1997; Gu and Nei 1999; Rooney, Piontkivska, and Nei 2002). In the latter model, gene duplication gives rise to new genes, some of which persist in the genome for long periods, whereas others are lost through deletion events or degenerate into pseudogenes. Accordingly, multigene family members evolve more or less independently and do not show high levels of nucleotide sequence homogeneity under this model, except in the case of recently duplicated genes. Thus, in a phylogenetic analysis of genes from several closely related taxa, sequences will not show a within-species clustering pattern, except in the case of recent gene duplicates (fig. 1).
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Results |
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An examination of Kimura (1980) nucleotide distances (d) between P. falciparum genes shows that the 18S coding regions of chromosomes 11 and 13 genes differ by only one nucleotide (d = 0.001) and that these coding regions in turn differ from the chromosome 1 coding region by only five (d = 0.002) and six nucleotides (d = 0.003), respectively. All three of these coding regions are highly divergent (between 199 [d = 0.104] and 130 [d = 0.105] nucleotide differences) from the coding regions of the chromosome five and seven genes, which show 25 nucleotide sequence differences (d = 0.018) from each other. Thus, certain pairs of 18S genes appear to be homogenized. The question raised by this information is whether the apparent homogeniza-tion is the result of recombination or if it actually represents sequence conservation resulting from purifying selection.
To answer this question, the 5' and 3' flanking regions from each P. falciparum were analyzed. The latter corresponds to the internal transcribed spacer 1 (ITS1) region, which lies between the 18S and 5.8S genes. The level of divergence displayed between the 5' and 3' flanking sequences greatly exceeds what is observed between the 18S coding sequences. The chromosome 11 and 13 sequences differ by 60 nucleotides (d = 0.109) in the 5' flanking region and by 3 nucleotides (d = 0.008) in the 3' flanking region. These genes differ from the chromosome 1 gene by 185 (d = 0.427) and 191 (d = 0.438) nucleotides, respectively, in the 5' flanking region and by 24 (d = 0.072) and 26 (d = 0.079) nucleotides, respectively, in the 3' flanking region. The three genes differ by an even greater nucleotide distance compared to those on chromosomes 5 and 7, in which the ranges lie between 234 (d = 0.624) and 268 (d = 0.712) differences in the 5' flanking region and between 53 (d = 0.186) and 62 (d = 0.224) in the 3' flanking region. The chromosome 5 and 7 genes show the smallest level of divergence in the coding region, yet they differ by 30 nucleotides (d = 0.052) in the 5' flanking region and by 16 nucleotides (d = 0.046) in the 3' flanking region. As a whole, these divergence data strongly suggest that recombination does not influence 18S genes in P. falciparum. Otherwise, the topologies of the trees reconstructed from the flanking and coding regions (fig. 4) would have been different from one another owing to the creation of a mosaic of distinct phylogenetic histories in these different regions. Yet, this did not occur. Thus, it is no surprise that Bayesian analyses of recombination conducted using the computer program TOPALi failed to find evidence in support of recombination on a concatenation of all thee regions or when each region was analyzed separately. In summary, these results suggest that recombination does not act on P. falciparum 18S genes, or, if it does, the degree of recombination is so negligible that it has little impact.
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Rapid Locus Turnover in C. parvum
In most cases, genes are shared for prolonged periods between species under the birth-and-death model (Nei, Sitnikova, and Gu 1997; Takahashi, Rooney, and Nei 2000). Yet, there are some exceptional cases in which rapid locus turnover occurs. The MHC class I genes of callitrichine New World monkeys (Cadavid et al. 1997) and the eosinophil-associated RNase genes of rodents (Zhang, Dyer, and Rosenberg 2000) are good examples of multigene families that experience rapid gene turnover due to birth-and-death evolution. In these cases, rapid gene turnover has led to the creation of species-specific gene clusters as a result of frequent gene duplication and loss. Consequently, few or no genes are shared between species.
The results from this study suggest that 18S genes in some apicomplexans may also undergo rapid birth-and-death evolution. This is best shown through an analysis of C. parvum sequences. It was possible to determine in several cases the host-species for the C. parvum strains that that produced the 18S sequences (fig. 3). The sequences that correspond to the human host-species are separable into two classes known as type I and type II. These types produce distinct schizonts that are distinguishable on the basis of how they function in reproduction. Essentially, type I schizonts are involved in asexual reproduction, whereas type II schizonts are involved in sexual reproduction (reviewed in Laurent et al. 1999). In addition, the former have been found only in human hosts, whereas the latter have been found in humans as well as in other animals (Gibbons et al. 1998).
The phylogeny in figure 3 shows that types I and II 18S sequences form two distinct clusters that in turn are distinct from the other C. parvum 18S sequences. These latter sequences come from strains that possess nonhuman host-species (listed in parentheses next to each taxon in fig. 3). This pattern of clustering on the basis of host-species is explainable by host-specific adaptation, which has been described for other kinds of C. parvum molecular and biochemical data (Xiao et al. 2002; Gibbons-Matthews and Prescott 2003). Accordingly, a specific molecular or biochemical genotype is associated solely with a unique host-species. The reasons for host-specific adaptation are unclear, but they may have to do with antigenic variation and evasion of the host immune system. At any rate, rapid birth-and-death evolution would certainly facilitate, if not enhance, the process of host-specific adaptation, regardless of the causes. Accordingly, rapid gene duplication and loss would aid the acquisition of a set of genes optimally adapted to a particular host-species and would eventually guarantee that genes particular to one C. parvum strain are not shared with other strains.
This hypothesis can be tested through a phylogenetic analysis of 18S genes from the recently completed genome of a C. parvum type II strain (Abrahamsen et al. 2004) in conjunction with the sequences of other strains. There are five 18S rRNA genes in C. parvum (LeBlanq et al. 1997), and five genes were reported in the published type II genome. Unfortunately, only a small fragment (approximately 125 bp) of one of those genes (cgd7_5535) was sequenced, while another (cgd2_1375) appears to have been misidentified as an 18S gene. Regarding the latter, there are short stretches of sequence similarity between that gene and the other C. parvum sequences analyzed in this study, but the sequence is so divergent from the other 18S sequences that it cannot be aligned with any reliability. Furthermore, when the sequence was searched against GenBank using Blast, the closest matches were human oncogenes. Thus, only three of the 18S genes from the complete type II genome are useful for our purposes. In so far as that is concerned, the C. parvum genome sequences cluster with other type II sequences (fig. 3) but separately from the type I sequences, indicating that the genes originated subsequent to the divergence of the respective strains from which they came. These results indicate that types I and II genes undergo rapid turnover (i.e., rapid duplication and loss). It should be noted, however, that the support for distinct type I and type II clades is not very high (bootstrap values of 66% and 60%, respectively). Yet, this is not unexpected if the two groups were recently separated. It should also be pointed out that, until the remaining two genes from the type II genome become available for analysis, it cannot be said that all genes from the type II genome cluster apart from the type I sequences. Clearly, more studies are needed to investigate this problem. Nevertheless, the previously described results clearly indicate that 18S genes in C. parvum undergo rapid duplication and loss.
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Discussion |
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This study shows that apicomplexan 18S rRNA genes evolve according to a birth-and-death model under strong purifying selection. The action of purifying selection guarantees that rRNA gene copies maintain their functional integrity in spite of their independent evolution from one another. The differential rates of duplication and loss produced under the birth-and-death model explain why some rRNA genes are shared between species and are maintained for long periods of evolutionary time, while others appear to be recent gene duplicates or to have been lost from the genomes of other species (figs. 2 and 3). This explains why any one 18S gene copy does not exist in all species of apicomplexans, as there is a distinct process of gene turnover owing to repeated duplication and loss. Yet, how rapid is the process of gene turnover among apicomplexan 18S rRNA genes?
The results presented here indicate that there is a fairly rapid degree of 18S gene turnover in C. parvum and that this is probably tied to host-specific adaptation. It has been known for some time that there must be an underlying reason for the production of distinct C. parvum molecular and biochemical genotypes that have led to their classification as type I or type II (Gibbons-Matthews and Prescott 2003). What is unclear is whether type I and type II genotypes reflect that the cells from which the sequences come are distinct strains. The results from this study indicate that they indeed represent distinct strains, on the basis of our phylogenetic analyses (fig. 3). Given that type I has been found only in humans, whereas type II has been found in both humans and nonhuman species, it likely that type I represents a uniquely human-adapted strain. This information should prove useful in epidemiological studies of both human and veterinary cryptosporidiosis.
The results concerning rapid gene turnover in C. parvum are particularly interesting in light of the observation that T. gondii 18S rRNA genes do not form species-specific clusters (fig. 3) despite the fact that they are organized in a tandem array (Gagnon, Bourbeau, and Levesque 1996). This presents itself as an unusual situation that warrants further study, because concerted evolution is supposed to be the rule among multigene family members arranged in tandem arrays (Nei 1987; Li 1997; Graur and Li 2000). Although it cannot be shown with the currently available data, perhaps this result is also indicative of rapid locus turnover in different strains of this species. Thus, it will be interesting to examine T. gondii 18S genes more thoroughly after the completion of this species' genome sequencing project, provided that the rRNA gene cluster is sequenced.
Unfortunately, rRNA genes are not sequenced in their entirety in most genome projects if they are organized in large clusters. One reason for this is the practical difficulty of sequencing through a cluster of highly similar genes without having inadvertently sequenced any individual gene repeatedly. Another reason is the general presumption that all rRNA genes are identical (or nearly so) in a given genome, which leads many to believe that there is no need to sequence through rRNA clusters because they are uninteresting in terms of their molecular or genomic evolution. Thus, a large effort need not be expended upon them. Nevertheless, this study and others (Carranza et al. 1996; Carranza, Baguñà, and Riutort 1999) show that the evolutionary genomics of rRNA genes is more complex than what we currently assume in many different species. For instance, the 5S rRNA genes of many eukaryotes are organized in a tandem array, but in some species of fungi they are dispersed across the genome (e.g., Wood et al. 2002). In many of these species, the 5S genes appear to be divergent from one another (unpublished data), suggesting that they might also undergo birth-and-death evolution. Clearly, these observations and the findings of this study indicate that the evolutionary genomics of rRNA genes deserves a higher level of scrutiny than what it is currently afforded.
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Acknowledgements |
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Footnotes |
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