Abstract
With the rapid accumulation of genomic information from various eukaryotes in the last decade, genes proposed to have been derived from recent horizontal gene transfer (HGT) events have been reported even in non-phagotrophic unicellular and multicellular organisms, but the molecular pathways underlying HGT remain to be explained. The development of in vitro HGT detection systems, which permit the molecular and genetic analyses of donor and recipient organisms and quantify HGT, are helpful in order to gain insight into mechanisms that may contribute to contemporary HGT events or may have contributed to past HGT events. We applied a horizontal DNA transfer system model based on conjugal gene transfer called trans-kingdom conjugation (TKC) from the prokaryote Escherichia coli to the eukaryote Saccharomyces cerevisiae, and assessed whether and to what extent genetic variations in the eukaryotic recipient affect its receptivity to TKC. Strains from a collection of 4,823 knock-out mutants of S. cerevisiae MAT-α haploids were tested for their individual TKC receptivity. Two types of mutants, an ssd1 mutant and respiratory mutants, which are also found in experimental strains and in nature widely, were identified as highly receptive mutants. The TKC efficiency for spontaneously accrued petite (rho −/0) mutants of the functional allele (SSD1-V) strain showed increased receptivity. The TKC efficiency of the ssd1Δ mutant was 36% for bacterial conjugation, while that of the petite/ssd1Δ double mutants was even higher (220% in average) compared to bacterial conjugation. This increased TKC receptivity was also observed when other conjugal transfer systems were applied and the donor bacterium was changed to Agrobacterium tumefaciens. These results support the idea that the genomes of certain eukaryotes have been exposed to exogenous DNA more frequently and continuously than previously thought.
Highlights
The transfer of genes beyond mating barriers, termed Horizontal Gene Transfer (HGT) or Lateral Gene Transfer (LGT), is widely recognized as an important factor in bacterial evolution [1,2]
All other yeast and bacterial strains used in this study are listed in Table 1, including those provided by the National Bio-Resource Project (NBRP) of MEXT, Japan
Our results reveal two important features regarding the contribution of HGT to eukaryotic evolution: (1) the receptivity of a recipient eukaryotic organism to DNA transfer from a bacterium may be altered drastically by the presence of different alleles of certain loci and by the polymorphisms in non-essential genes, which are not primarily coded for blocking HGT in the recipient eukaryote, and (2) T4SS-mediated trans-kingdom conjugation (TKC) may represent the mechanistic means behind HGT from bacteria to eukaryotes (Figure 6)
Summary
The transfer of genes beyond mating barriers, termed Horizontal Gene Transfer (HGT) or Lateral Gene Transfer (LGT), is widely recognized as an important factor in bacterial evolution [1,2]. With the rapid accumulation of genomic information from various organisms in the last decade, genes proposed to have been acquired from HGT events occurring after evolutional loss of phagotrophy have been reported even in nonphagotrophic unicellular and multicellular organisms, such as yeasts, diatoms, higher plants, and bdelloids [5,6,7,8]. In vitro HGT detection systems have been developed for molecular and genetic analyses of donor and recipient organisms and quantification of HGT. These systems are helpful in gaining insight on mechanisms that may contribute to HGT events, both contemporary and ancient
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