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Association between translation efficiency and horizontal gene transfer within microbial communities.

Tuller T, Girshovich Y, Sella Y, Kreimer A, Freilich S, Kupiec M, Gophna U, Ruppin E - Nucleic Acids Res. (2011)

Bottom Line: These results remain significant after controlling for diverse ecological and evolutionary parameters.Our analysis demonstrates that there are bi-directional associations between the similarity in the tRNA pools of organisms and the number of HGT events occurring between them.Our results also suggest that frequent HGT may be a homogenizing force that increases the similarity in the tRNA pools of organisms within the same community.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Mathematics and Computer Science, Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Blavatnik School of Computer Science, School of Medicine, Tel Aviv University, Ramat Aviv 69978, Israel.

ABSTRACT
Horizontal gene transfer (HGT) is a major force in microbial evolution. Previous studies have suggested that a variety of factors, including restricted recombination and toxicity of foreign gene products, may act as barriers to the successful integration of horizontally transferred genes. This study identifies an additional central barrier to HGT-the lack of co-adaptation between the codon usage of the transferred gene and the tRNA pool of the recipient organism. Analyzing the genomic sequences of more than 190 microorganisms and the HGT events that have occurred between them, we show that the number of genes that were horizontally transferred between organisms is positively correlated with the similarity between their tRNA pools. Those genes that are better adapted to the tRNA pools of the target genomes tend to undergo more frequent HGT. At the community (or environment) level, organisms that share a common ecological niche tend to have similar tRNA pools. These results remain significant after controlling for diverse ecological and evolutionary parameters. Our analysis demonstrates that there are bi-directional associations between the similarity in the tRNA pools of organisms and the number of HGT events occurring between them. Similar tRNA pools between a donor and a host tend to increase the probability that a horizontally acquired gene will become fixed in its new genome. Our results also suggest that frequent HGT may be a homogenizing force that increases the similarity in the tRNA pools of organisms within the same community.

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(A) The tRs of organisms that live in the same community [(12), left] are higher than the tRs of organisms from different communities (right). The y-axis is the mean tRs of the organisms in each group; we used the Kolmogorov–Smirnov (KS)-test for computing P-values. (B) Non-parametric correlations of several variables with niche-sharing, when controlling for all the other variables. p denotes asymptotic P-value, pe denotes empirical P-value (‘Materials and Methods’ section). (C) Correlation given increasing number of factors (A) sum genome of sizes, (B) phylogenetic distance, (C) similarity in the amino acid usage, (D) selection for translation efficiency, (E) similarity in the GC content, (F) similarity in the growth rates and (G) similarity in genome sizes.
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Figure 3: (A) The tRs of organisms that live in the same community [(12), left] are higher than the tRs of organisms from different communities (right). The y-axis is the mean tRs of the organisms in each group; we used the Kolmogorov–Smirnov (KS)-test for computing P-values. (B) Non-parametric correlations of several variables with niche-sharing, when controlling for all the other variables. p denotes asymptotic P-value, pe denotes empirical P-value (‘Materials and Methods’ section). (C) Correlation given increasing number of factors (A) sum genome of sizes, (B) phylogenetic distance, (C) similarity in the amino acid usage, (D) selection for translation efficiency, (E) similarity in the GC content, (F) similarity in the growth rates and (G) similarity in genome sizes.

Mentions: In the previous sections, we showed that there is an association between HGT and similarity in tRNA pool measured by the tRs. It is known that organisms that share the same environment are involved in more HGT (for example, the correlation between community co-membership and the number of shared genes when controlling for all the other variables defined in the pervious section is r = 0.23, P = 2.4 × 10−10, pe < 0.001). Thus, we aimed to compare the similarity in the tRNA pools, measured by the tRs, within and between communities, using the environmental partitioning established by Freilich et al. (12). Indeed, microorganisms that occupy similar niches have significantly higher tRs than those that live in different ones (P = 2 × 10−30; Figure 3A).Figure 3.


Association between translation efficiency and horizontal gene transfer within microbial communities.

Tuller T, Girshovich Y, Sella Y, Kreimer A, Freilich S, Kupiec M, Gophna U, Ruppin E - Nucleic Acids Res. (2011)

(A) The tRs of organisms that live in the same community [(12), left] are higher than the tRs of organisms from different communities (right). The y-axis is the mean tRs of the organisms in each group; we used the Kolmogorov–Smirnov (KS)-test for computing P-values. (B) Non-parametric correlations of several variables with niche-sharing, when controlling for all the other variables. p denotes asymptotic P-value, pe denotes empirical P-value (‘Materials and Methods’ section). (C) Correlation given increasing number of factors (A) sum genome of sizes, (B) phylogenetic distance, (C) similarity in the amino acid usage, (D) selection for translation efficiency, (E) similarity in the GC content, (F) similarity in the growth rates and (G) similarity in genome sizes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3113575&req=5

Figure 3: (A) The tRs of organisms that live in the same community [(12), left] are higher than the tRs of organisms from different communities (right). The y-axis is the mean tRs of the organisms in each group; we used the Kolmogorov–Smirnov (KS)-test for computing P-values. (B) Non-parametric correlations of several variables with niche-sharing, when controlling for all the other variables. p denotes asymptotic P-value, pe denotes empirical P-value (‘Materials and Methods’ section). (C) Correlation given increasing number of factors (A) sum genome of sizes, (B) phylogenetic distance, (C) similarity in the amino acid usage, (D) selection for translation efficiency, (E) similarity in the GC content, (F) similarity in the growth rates and (G) similarity in genome sizes.
Mentions: In the previous sections, we showed that there is an association between HGT and similarity in tRNA pool measured by the tRs. It is known that organisms that share the same environment are involved in more HGT (for example, the correlation between community co-membership and the number of shared genes when controlling for all the other variables defined in the pervious section is r = 0.23, P = 2.4 × 10−10, pe < 0.001). Thus, we aimed to compare the similarity in the tRNA pools, measured by the tRs, within and between communities, using the environmental partitioning established by Freilich et al. (12). Indeed, microorganisms that occupy similar niches have significantly higher tRs than those that live in different ones (P = 2 × 10−30; Figure 3A).Figure 3.

Bottom Line: These results remain significant after controlling for diverse ecological and evolutionary parameters.Our analysis demonstrates that there are bi-directional associations between the similarity in the tRNA pools of organisms and the number of HGT events occurring between them.Our results also suggest that frequent HGT may be a homogenizing force that increases the similarity in the tRNA pools of organisms within the same community.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Mathematics and Computer Science, Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Blavatnik School of Computer Science, School of Medicine, Tel Aviv University, Ramat Aviv 69978, Israel.

ABSTRACT
Horizontal gene transfer (HGT) is a major force in microbial evolution. Previous studies have suggested that a variety of factors, including restricted recombination and toxicity of foreign gene products, may act as barriers to the successful integration of horizontally transferred genes. This study identifies an additional central barrier to HGT-the lack of co-adaptation between the codon usage of the transferred gene and the tRNA pool of the recipient organism. Analyzing the genomic sequences of more than 190 microorganisms and the HGT events that have occurred between them, we show that the number of genes that were horizontally transferred between organisms is positively correlated with the similarity between their tRNA pools. Those genes that are better adapted to the tRNA pools of the target genomes tend to undergo more frequent HGT. At the community (or environment) level, organisms that share a common ecological niche tend to have similar tRNA pools. These results remain significant after controlling for diverse ecological and evolutionary parameters. Our analysis demonstrates that there are bi-directional associations between the similarity in the tRNA pools of organisms and the number of HGT events occurring between them. Similar tRNA pools between a donor and a host tend to increase the probability that a horizontally acquired gene will become fixed in its new genome. Our results also suggest that frequent HGT may be a homogenizing force that increases the similarity in the tRNA pools of organisms within the same community.

Show MeSH
Related in: MedlinePlus