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Cited by 25Fungal and yeast genetics researchBacterial Genetics and BiotechnologyChromosomal and Genetic Variations

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Trans-Kingdom Horizontal DNA Transfer from Bacteria to Yeast Is Highly Plastic Due to Natural Polymorphisms in Auxiliary Nonessential Recipient Genes

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Moriguchi, Kazuki, Yamamoto, Shinji, Tanaka, Katsuyuki, Kurata, Nori, Suzuki, Katsunori·2013·PLoS ONE
DOI 10.1371/journal.pone.0074590PMC PMC3772842
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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.

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Figure 1 Effect of mitochondrial functional integrity and SSD1 mutation on efficiency of DNA transfer from Escherichia coli HB101 to Saccharomyces cerevisiae strains (BY4742 in (A), (B) and (C); EGY48 in (D)) by trans-kingdom conjugation (TKC). Enhanced TKC efficiency was observed in (A) the pretreatment of the recipient yeast with a mitochondrial translational inhibitor, erythromycin; (B) the pretreatment of the recipient yeast with a mitochondrial respiration inhibitor, antimycin; (C) a rho0 strain, lacking mitochondrial genome; and (D) an SSD1-knock-out mutant. The vertical axis “Log (TKCeffi)” represents the value of TKC efficiency (no. of transconjugant colonies/no. of recipient cell) converted to Log10. Data are represented as mean ± SD (n = 9 in A, B and D, 17 in C). Asterisks indicate a statistically significant difference: ***p<0.001 (two-tailed t-test). HB101 (pRH210, pAY205) was used as the donor.
Figure 1 Effect of mitochondrial functional integrity and SSD1 mutation on efficiency of DNA transfer from Escherichia coli HB101 to Saccharomyces cerevisiae strains (BY4742 in (A), (B) and (C); EGY48 in (D)) by trans-kingdom conjugation (TKC). Enhanced TKC efficiency was observed in (A) the pretreatment of the recipient yeast with a mitochondrial translational inhibitor, erythromycin; (B) the pretreatment of the recipient yeast with a mitochondrial respiration inhibitor, antimycin; (C) a rho0 strain, lacking mitochondrial genome; and (D) an SSD1-knock-out mutant. The vertical axis “Log (TKCeffi)” represents the value of TKC efficiency (no. of transconjugant colonies/no. of recipient cell) converted to Log10. Data are represented as mean ± SD (n = 9 in A, B and D, 17 in C). Asterisks indicate a statistically significant difference: ***p<0.001 (two-tailed t-test). HB101 (pRH210, pAY205) was used as the donor.CC BY · PubMed Central
Figure 2 Functional complementation of SSD1 mutation rescues its temperature sensitivity as well as high TKC receptivity phenotype. Saccharomyces cerevisiae strains carrying a deletion (BY4742 ssd1Δ) or a strain spontaneously carrying the truncated SSD1 (W303-1B) was transformed with either the vector alone (vec), or vector carrying full length (SSD1-V) or vector carrying truncated (ssd1-d) genes. The growth phenotype on solid media at 37°C for 15 h followed by 42°C for 48 h with serial dilution (A) and (C); and the DNA transfer efficiency by the standard TKC procedure was measured (B) and (D). Complementation with the full length, functional SSD1, but not the truncated gene rescued the phenotypes tested. Data are represented as mean ± SD (n = 15 in B and 6 in D, respectively). Letters above the bars indicate significant differences at p<0.001 (Holm’s test). HB101 (pRH210, pAY205) was used as the donor.
Figure 2 Functional complementation of SSD1 mutation rescues its temperature sensitivity as well as high TKC receptivity phenotype. Saccharomyces cerevisiae strains carrying a deletion (BY4742 ssd1Δ) or a strain spontaneously carrying the truncated SSD1 (W303-1B) was transformed with either the vector alone (vec), or vector carrying full length (SSD1-V) or vector carrying truncated (ssd1-d) genes. The growth phenotype on solid media at 37°C for 15 h followed by 42°C for 48 h with serial dilution (A) and (C); and the DNA transfer efficiency by the standard TKC procedure was measured (B) and (D). Complementation with the full length, functional SSD1, but not the truncated gene rescued the phenotypes tested. Data are represented as mean ± SD (n = 15 in B and 6 in D, respectively). Letters above the bars indicate significant differences at p<0.001 (Holm’s test). HB101 (pRH210, pAY205) was used as the donor.CC BY · PubMed Central
Figure 3 Universality of high receptivity under various reaction conditions in high receptivity mutants. TKC efficiency was examined using SSD1 deletion mutant (ssd1Δ), and rho0 mutant in various reaction buffers (A) or under various temparature (B). Data are represented as mean ± SD (n = 3). In all reaction conditions examined, the high recepitivity mutants showed higher recepitivity comparing with parental strain, and they were statistically significant at p<0.05 except rho0 mutant at 16°C (two-tailed t-test). HB101 (pRH210, pAY205) was used as the donor.
Figure 3 Universality of high receptivity under various reaction conditions in high receptivity mutants. TKC efficiency was examined using SSD1 deletion mutant (ssd1Δ), and rho0 mutant in various reaction buffers (A) or under various temparature (B). Data are represented as mean ± SD (n = 3). In all reaction conditions examined, the high recepitivity mutants showed higher recepitivity comparing with parental strain, and they were statistically significant at p<0.05 except rho0 mutant at 16°C (two-tailed t-test). HB101 (pRH210, pAY205) was used as the donor.CC BY · PubMed Central
Figure 4 Efficiency of DNA transfer by TKC between a bacterial strain and yeast can be comparable to that for conjugation between two bacterial strains. TKC reactions were set up between Escherichia coli HB101 and Saccharomyces cerevisiae parental strain BY4742, or its petite mutants (clones 4–9), or a SSD1 deletion mutant (ssd1Δ), or petite mutants of the SSD1 deletion mutant (clones 1–6). The DNA transfer efficiencies of the above TKC were compared with conjugation between the same strain of Escherichia coli HB101 and Agrobacterium tumefaciens C58C1. Data are represented as mean ± SD (n = 15 in BY4742, ssd1Δ and C58C1, n = 9 in others). Letters above the bars indicate significant differences at p<0.05 (Holm’s test). HB101 (pRH210, pAY205) was used as the donor.
Figure 4 Efficiency of DNA transfer by TKC between a bacterial strain and yeast can be comparable to that for conjugation between two bacterial strains. TKC reactions were set up between Escherichia coli HB101 and Saccharomyces cerevisiae parental strain BY4742, or its petite mutants (clones 4–9), or a SSD1 deletion mutant (ssd1Δ), or petite mutants of the SSD1 deletion mutant (clones 1–6). The DNA transfer efficiencies of the above TKC were compared with conjugation between the same strain of Escherichia coli HB101 and Agrobacterium tumefaciens C58C1. Data are represented as mean ± SD (n = 15 in BY4742, ssd1Δ and C58C1, n = 9 in others). Letters above the bars indicate significant differences at p<0.05 (Holm’s test). HB101 (pRH210, pAY205) was used as the donor.CC BY · PubMed Central
Figure 5 Universality of components comprising TKC between a bacterial strain and a high-DNA-receptivity yeast mutant strain. Efficiency if DNA transfer was measured in the parental yeast strain or its high-receptivity mutants, SSD1 deletion mutant (ssd1Δ), and rho0 mutant, after TKC with Escherichia coli HB101 (pRH220, pRS316::oriT P) carrying T4SS functions on IncP1α (A), or with Escherichia coli HB101 (pDPT51, pAY205) carrying T4SS functions on IncP1β plasmid (B), or with A. tumefaciens C58C1 (RP4, pYN402) (C). Data are represented as mean ± SD (n = 9 in A and C, n = 15 in B). Letters above the bars indicate significant differences at p<0.01 in A, 0.001 in B, and 0.001 in C (Holm’s test).
Figure 5 Universality of components comprising TKC between a bacterial strain and a high-DNA-receptivity yeast mutant strain. Efficiency if DNA transfer was measured in the parental yeast strain or its high-receptivity mutants, SSD1 deletion mutant (ssd1Δ), and rho0 mutant, after TKC with Escherichia coli HB101 (pRH220, pRS316::oriT P) carrying T4SS functions on IncP1α (A), or with Escherichia coli HB101 (pDPT51, pAY205) carrying T4SS functions on IncP1β plasmid (B), or with A. tumefaciens C58C1 (RP4, pYN402) (C). Data are represented as mean ± SD (n = 9 in A and C, n = 15 in B). Letters above the bars indicate significant differences at p<0.01 in A, 0.001 in B, and 0.001 in C (Holm’s test).CC BY · PubMed Central
Figure 6 A schematic diagram of the gene and plasmid flow from bacteria to eukaryotes by T4SS. In bacteria X and Y, genes are transferred from genomic DNA to various plasmids depicted as A, B, and C by using transposons or another method (i). A conjugative plasmid A (such as IncP plasmids) can move from bacterium X to another bacterium Y or to a eukaryote A by its own T4SS system, i.e., T4SS A (ii). A mobilizable plasmid B (such as IncQ plasmids) transfers from bacterium X to Y and eukaryote A with the help of its own mob genes and T4SS A (iii). The plasmids A and B can also transfer from bacterium Y to eukaryote A by T4SS A (ii and iii). The eukaryote A has a subpopulation that accepts exogenous DNA efficiently transferred by T4SS A. The transferred bacterial genes spread and are maintained in the entire population, if they take on available roles, for its survival. In bacterium Y, a plasmid C transfers to eukaryote B by T4SS C (such as vir genes in Ti and Ri plasmids; iv). The plasmid B is also able to transfer to eukaryote B by using mob genes and T4SS C (v).
Figure 6 A schematic diagram of the gene and plasmid flow from bacteria to eukaryotes by T4SS. In bacteria X and Y, genes are transferred from genomic DNA to various plasmids depicted as A, B, and C by using transposons or another method (i). A conjugative plasmid A (such as IncP plasmids) can move from bacterium X to another bacterium Y or to a eukaryote A by its own T4SS system, i.e., T4SS A (ii). A mobilizable plasmid B (such as IncQ plasmids) transfers from bacterium X to Y and eukaryote A with the help of its own mob genes and T4SS A (iii). The plasmids A and B can also transfer from bacterium Y to eukaryote A by T4SS A (ii and iii). The eukaryote A has a subpopulation that accepts exogenous DNA efficiently transferred by T4SS A. The transferred bacterial genes spread and are maintained in the entire population, if they take on available roles, for its survival. In bacterium Y, a plasmid C transfers to eukaryote B by T4SS C (such as vir genes in Ti and Ri plasmids; iv). The plasmid B is also able to transfer to eukaryote B by using mob genes and T4SS C (v).CC BY · PubMed Central

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Metadata

Authors
Moriguchi, K., Yamamoto, S., Tanaka, K., Kurata, N., & Suzuki, K.
Affiliations
  • Hiroshima University (JP)
  • National Institute of Genetics (JP)
Corresponding author
Moriguchi, Kazuki
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-09-13
Volume
8
Issue
9
Pages
e74590
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0074590
PMC
PMC3772842
OpenAlex
W2020206150
Cited by
25
References
1
Citations by year
2026: 1 · 2025: 3 · 2024: 1 · 2022: 1 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 4
FWCI
1.05
Type
journal article
Language
en
Update notices
correction (2015-04-13)
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • U.S. Department of Agriculture
  • Agricultural Research Service
  • Japan Society for the Promotion of Science (20570221, 21510209)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Keywords
Escherichia coli, Saccharomyces cerevisiae, Ssd1, petite mutants, rho- mutants, respiratory mutants, Agrobacterium tumefaciens, gene transfer efficiency
MeSH terms
Conjugation, Genetic, DNA, Bacterial, Escherichia coli, Genes, Bacterial, Genetic Complementation Test, Genetic Testing, Mitochondria, Models, Genetic, Mutation, Phenotype, Polymorphism, Genetic, Saccharomyces cerevisiae, Gene Transfer, Horizontal, Genetic Loci

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