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| (A) Phylogenetic tree for one exemplar bdelloid transcript (contig 13848) encoding an acetyl-CoA synthetase. Branch colours represent different taxa: metazoa, black; eubacteria, blue; archaea, light blue; fungi, pink; protists, grey; plants, green. Numbers on nodes represent aLRT support. (B) Physical linkage of foreign genes to neighbouring genes in the genome: eight different Sanger sequenced and assembled genomic regions, with arrows showing gene length and orientation (metazoa, black; eubacteria, blue; fungi, pink; protists, grey); introns are indicated as interruptions. Bdelloid genes previously identified in A. vaga are marked with an asterisk. In both the first and fourth genomic regions shown, the two foreign genes belong to different taxa (fungi and bacteria). Scale, bp. See also Figure S2 and Table S1. |
Author Summary
Bdelloid rotifers are tiny invertebrates with unusual characteristics: they withstand stresses, such as desiccation and high levels of ionising radiation, that kill other animals, and they have survived over millions of years without sexual reproduction, which contradicts theories on the evolutionary advantages of sex. In this study, we investigate another bizarre feature of bdelloids, namely their ability to acquire genes from other organisms in a process known as horizontal gene transfer (HGT). We show that HGT happens on an unprecedented scale in bdelloids: approximately 10% of active genes are “foreign,” mostly originating from bacteria and other simple organisms like fungi and algae, but now functioning as bdelloid genes. About 80% of foreign genes code for enzymes, and these make a major contribution to bdelloid biochemistry: 39% of enzyme activities have a foreign contribution, and in 23% of cases the activity in question is uniquely specified by a foreign gene. This indicates biochemistry, such as toxin degradation and antioxidant generation, that is unknown in other animals and that is expected to improve the “robustness” of the bdelloid. It also represents a possible mechanism for survival without sex, by diversification of functional capacity and even replacement of defective genes by foreign counterparts.
Citation: Boschetti C, Carr A, Crisp A, Eyres I, Wang-Koh Y, et al. (2012) Biochemical Diversification through Foreign Gene Expression in Bdelloid Rotifers. PLoS Genet 8(11): e1003035. doi:10.1371/journal.pgen.1003035
From the Discussion
The method for assessing HGT in the bdelloid transcriptome is novel, but follows principles currently recognised as the most rigorous, where sequence matching is coupled with phylogenetics [14]. There have been relatively few such global analyses among the Metazoa that test for expression of horizontally acquired sequences, one example being in Hydra magnipapillata, where seventy-one “gene models” apparently derive from bacteria, 70% of which were shown to be transcribed [28].
...The complexity of foreign gene expression observed in the bdelloid rotifer A. ricciae is comparable to that in prokaryotes [31] and is far greater than in other animals where relatively few genes are involved [14], [25], [28]. For example, while in Hydra perhaps 50 foreign genes are active [28], in Drosophila ananassae, which has acquired most of the genome of its endosymbiont, Wolbachia, by HGT, only 28 genes are transcribed; the model fly, D. melanogaster, has not acquired the Wolbachia genome [32], [33]. In pea aphids, red body colour results from the expression of carotenoid genes acquired and diversified from fungal counterparts [34], [35]. In the sea slug, Elysia chlorotica, HGT and expression of the algal psbO gene allows photosynthesis in plastids also acquired from the alga [36]. However, there is a need for more animal studies at the whole transcriptome level. It is surprising, for example, that there are no comprehensive global studies of HGT in C. elegans in the literature [37], as our analysis suggests there are approximately 200 foreign transcripts in the model nematode. The software pipeline developed for this study has the potential to be used more widely where expression data are available to gain a more complete picture of HGT in metazoans.
Nevertheless, the scale of HGT in the bdelloid seems to be unusual among animals and it would be interesting to address the importance of asexuality and desiccation tolerance in this phenomenon. For example, transcriptome data from the nematode Panagrolaimus superbus, which is anhydrobiotic, but gonochoristic (i.e. reproduces only sexually), has recently been published [38]. The authors highlighted one foreign sequence in the P. superbus transcriptome, but did not perform a global analysis for HGT. If this nematode contains low numbers of foreign sequences, it would rule out that desiccation tolerance per se, without asexuality, is associated with extensive HGT. Another characteristic of HGT in A. ricciae is that the source organisms are extremely diverse and include examples that are unlikely to be symbionts or even in the bdelloid's immediate habitat, such as the trypanosome relative from which trypanothione biosynthesis genes derive. Therefore, bdelloids are likely able to readily scavenge and incorporate DNA from the environment, and desiccation, which could lead to both leakiness in cell membranes and double-strand breaks in rotifer chromosomes, might facilitate this.
Citation: Boschetti C, Carr A, Crisp A, Eyres I, Wang-Koh Y, et al. (2012) Biochemical Diversification through Foreign Gene Expression in Bdelloid Rotifers. PLoS Genet 8(11): e1003035. doi:10.1371/journal.pgen.1003035
From the Discussion
The method for assessing HGT in the bdelloid transcriptome is novel, but follows principles currently recognised as the most rigorous, where sequence matching is coupled with phylogenetics [14]. There have been relatively few such global analyses among the Metazoa that test for expression of horizontally acquired sequences, one example being in Hydra magnipapillata, where seventy-one “gene models” apparently derive from bacteria, 70% of which were shown to be transcribed [28].
...The complexity of foreign gene expression observed in the bdelloid rotifer A. ricciae is comparable to that in prokaryotes [31] and is far greater than in other animals where relatively few genes are involved [14], [25], [28]. For example, while in Hydra perhaps 50 foreign genes are active [28], in Drosophila ananassae, which has acquired most of the genome of its endosymbiont, Wolbachia, by HGT, only 28 genes are transcribed; the model fly, D. melanogaster, has not acquired the Wolbachia genome [32], [33]. In pea aphids, red body colour results from the expression of carotenoid genes acquired and diversified from fungal counterparts [34], [35]. In the sea slug, Elysia chlorotica, HGT and expression of the algal psbO gene allows photosynthesis in plastids also acquired from the alga [36]. However, there is a need for more animal studies at the whole transcriptome level. It is surprising, for example, that there are no comprehensive global studies of HGT in C. elegans in the literature [37], as our analysis suggests there are approximately 200 foreign transcripts in the model nematode. The software pipeline developed for this study has the potential to be used more widely where expression data are available to gain a more complete picture of HGT in metazoans.
Nevertheless, the scale of HGT in the bdelloid seems to be unusual among animals and it would be interesting to address the importance of asexuality and desiccation tolerance in this phenomenon. For example, transcriptome data from the nematode Panagrolaimus superbus, which is anhydrobiotic, but gonochoristic (i.e. reproduces only sexually), has recently been published [38]. The authors highlighted one foreign sequence in the P. superbus transcriptome, but did not perform a global analysis for HGT. If this nematode contains low numbers of foreign sequences, it would rule out that desiccation tolerance per se, without asexuality, is associated with extensive HGT. Another characteristic of HGT in A. ricciae is that the source organisms are extremely diverse and include examples that are unlikely to be symbionts or even in the bdelloid's immediate habitat, such as the trypanosome relative from which trypanothione biosynthesis genes derive. Therefore, bdelloids are likely able to readily scavenge and incorporate DNA from the environment, and desiccation, which could lead to both leakiness in cell membranes and double-strand breaks in rotifer chromosomes, might facilitate this.
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