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Extensive horizontal transfer of core genome genes between two Lactobacillus species found in the gastrointestinal tract.

Nicolas P, Bessières P, Ehrlich SD, Maguin E, van de Guchte M - BMC Evol. Biol. (2007)

Bottom Line: Lowering the confidence threshold for trees to be taken into consideration does not significantly affect this ratio, and therefore suggests that gene transfer may have affected as much as 40% of the core genome genes.This case-study reports an unprecedented level of phylogenetic incongruence, presumably resulting from extensive horizontal gene transfer.The data give a first indication of the large extent of gene transfer that may take place in the gastrointestinal tract and its accumulated effect.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, Mathématique Informatique et Génome, UR1077, 78350 Jouy en Josas, France. pierre.nicolas@jouy.inra.fr

ABSTRACT

Background: While genes that are conserved between related bacterial species are usually thought to have evolved along with the species, phylogenetic trees reconstructed for individual genes may contradict this picture and indicate horizontal gene transfer. Individual trees are often not resolved with high confidence, however, and in that case alternative trees are generally not considered as contradicting the species tree, although not confirming it either. Here we conduct an in-depth analysis of 401 protein phylogenetic trees inferred with varying levels of confidence for three lactobacilli from the acidophilus complex. At present the relationship between these bacteria, isolated from environments as diverse as the gastrointestinal tract (Lactobacillus acidophilus and Lactobacillus johnsonii) and yogurt (Lactobacillus delbrueckii ssp. bulgaricus), is ambiguous due to contradictory phenotypical and 16S rRNA based classifications.

Results: Among the 401 phylogenetic trees, those that could be reconstructed with high confidence support the 16S-rRNA tree or one alternative topology in an astonishing 3:2 ratio, while the third possible topology is practically absent. Lowering the confidence threshold for trees to be taken into consideration does not significantly affect this ratio, and therefore suggests that gene transfer may have affected as much as 40% of the core genome genes. Gene function bias suggests that the 16S rRNA phylogeny of the acidophilus complex, which indicates that L. acidophilus and L. delbrueckii ssp. bulgaricus are the closest related of these three species, is correct. A novel approach of comparison of interspecies protein divergence data employed in this study allowed to determine that gene transfer most likely took place between the lineages of the two species found in the gastrointestinal tract.

Conclusion: This case-study reports an unprecedented level of phylogenetic incongruence, presumably resulting from extensive horizontal gene transfer. The data give a first indication of the large extent of gene transfer that may take place in the gastrointestinal tract and its accumulated effect. For future studies, our results should encourage a careful weighing of data on phylogenetic tree topology, confidence and distribution to conclude on the absence or presence and extent of horizontal gene transfer.

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Phylogenetic trees. a, phylogenetic tree based on 16S rRNA sequences by maximum likelihood; b, phylogenetic tree based on average distance from 480 single copy protein families; c, third possible tree topology for the acidophilus complex. Bootstrap support values for internal branches are indicated. Evolutionary distance scales for trees a and b are presented (expected number of substitutions per site). 16S rRNA tree reconstruction is based on a HKY model (expected transition/transversion ratio 1.68 and expected pyrimidine transition/purine transition ratio 0.62) with rate heterogeneity between sites modeled using a gamma distribution with coefficient of variation 2.64. Pairwise evolutionary distances for proteins are estimated with a JTT model and include separate gamma-corrections for each protein family (average coefficient of variation is 1.14).
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Figure 2: Phylogenetic trees. a, phylogenetic tree based on 16S rRNA sequences by maximum likelihood; b, phylogenetic tree based on average distance from 480 single copy protein families; c, third possible tree topology for the acidophilus complex. Bootstrap support values for internal branches are indicated. Evolutionary distance scales for trees a and b are presented (expected number of substitutions per site). 16S rRNA tree reconstruction is based on a HKY model (expected transition/transversion ratio 1.68 and expected pyrimidine transition/purine transition ratio 0.62) with rate heterogeneity between sites modeled using a gamma distribution with coefficient of variation 2.64. Pairwise evolutionary distances for proteins are estimated with a JTT model and include separate gamma-corrections for each protein family (average coefficient of variation is 1.14).

Mentions: The evolutionary tree inferred from 16S rRNA sequences is often considered authoritative in bacterial phylogeny reconstruction. In this tree, L. acidophilus and L. delbrueckii group together while the L. johnsonii lineage branches earlier (Fig. 2a). This result may seem surprising, since in apparent contradiction with both the difficulty to distinguish L. acidophilus and L. johnsonii on the basis of physiological and biochemical properties [16] and the results mentioned above where L. acidophilus and L. johnsonii look much more alike than L. acidophilus and L. delbrueckii.


Extensive horizontal transfer of core genome genes between two Lactobacillus species found in the gastrointestinal tract.

Nicolas P, Bessières P, Ehrlich SD, Maguin E, van de Guchte M - BMC Evol. Biol. (2007)

Phylogenetic trees. a, phylogenetic tree based on 16S rRNA sequences by maximum likelihood; b, phylogenetic tree based on average distance from 480 single copy protein families; c, third possible tree topology for the acidophilus complex. Bootstrap support values for internal branches are indicated. Evolutionary distance scales for trees a and b are presented (expected number of substitutions per site). 16S rRNA tree reconstruction is based on a HKY model (expected transition/transversion ratio 1.68 and expected pyrimidine transition/purine transition ratio 0.62) with rate heterogeneity between sites modeled using a gamma distribution with coefficient of variation 2.64. Pairwise evolutionary distances for proteins are estimated with a JTT model and include separate gamma-corrections for each protein family (average coefficient of variation is 1.14).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1994166&req=5

Figure 2: Phylogenetic trees. a, phylogenetic tree based on 16S rRNA sequences by maximum likelihood; b, phylogenetic tree based on average distance from 480 single copy protein families; c, third possible tree topology for the acidophilus complex. Bootstrap support values for internal branches are indicated. Evolutionary distance scales for trees a and b are presented (expected number of substitutions per site). 16S rRNA tree reconstruction is based on a HKY model (expected transition/transversion ratio 1.68 and expected pyrimidine transition/purine transition ratio 0.62) with rate heterogeneity between sites modeled using a gamma distribution with coefficient of variation 2.64. Pairwise evolutionary distances for proteins are estimated with a JTT model and include separate gamma-corrections for each protein family (average coefficient of variation is 1.14).
Mentions: The evolutionary tree inferred from 16S rRNA sequences is often considered authoritative in bacterial phylogeny reconstruction. In this tree, L. acidophilus and L. delbrueckii group together while the L. johnsonii lineage branches earlier (Fig. 2a). This result may seem surprising, since in apparent contradiction with both the difficulty to distinguish L. acidophilus and L. johnsonii on the basis of physiological and biochemical properties [16] and the results mentioned above where L. acidophilus and L. johnsonii look much more alike than L. acidophilus and L. delbrueckii.

Bottom Line: Lowering the confidence threshold for trees to be taken into consideration does not significantly affect this ratio, and therefore suggests that gene transfer may have affected as much as 40% of the core genome genes.This case-study reports an unprecedented level of phylogenetic incongruence, presumably resulting from extensive horizontal gene transfer.The data give a first indication of the large extent of gene transfer that may take place in the gastrointestinal tract and its accumulated effect.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, Mathématique Informatique et Génome, UR1077, 78350 Jouy en Josas, France. pierre.nicolas@jouy.inra.fr

ABSTRACT

Background: While genes that are conserved between related bacterial species are usually thought to have evolved along with the species, phylogenetic trees reconstructed for individual genes may contradict this picture and indicate horizontal gene transfer. Individual trees are often not resolved with high confidence, however, and in that case alternative trees are generally not considered as contradicting the species tree, although not confirming it either. Here we conduct an in-depth analysis of 401 protein phylogenetic trees inferred with varying levels of confidence for three lactobacilli from the acidophilus complex. At present the relationship between these bacteria, isolated from environments as diverse as the gastrointestinal tract (Lactobacillus acidophilus and Lactobacillus johnsonii) and yogurt (Lactobacillus delbrueckii ssp. bulgaricus), is ambiguous due to contradictory phenotypical and 16S rRNA based classifications.

Results: Among the 401 phylogenetic trees, those that could be reconstructed with high confidence support the 16S-rRNA tree or one alternative topology in an astonishing 3:2 ratio, while the third possible topology is practically absent. Lowering the confidence threshold for trees to be taken into consideration does not significantly affect this ratio, and therefore suggests that gene transfer may have affected as much as 40% of the core genome genes. Gene function bias suggests that the 16S rRNA phylogeny of the acidophilus complex, which indicates that L. acidophilus and L. delbrueckii ssp. bulgaricus are the closest related of these three species, is correct. A novel approach of comparison of interspecies protein divergence data employed in this study allowed to determine that gene transfer most likely took place between the lineages of the two species found in the gastrointestinal tract.

Conclusion: This case-study reports an unprecedented level of phylogenetic incongruence, presumably resulting from extensive horizontal gene transfer. The data give a first indication of the large extent of gene transfer that may take place in the gastrointestinal tract and its accumulated effect. For future studies, our results should encourage a careful weighing of data on phylogenetic tree topology, confidence and distribution to conclude on the absence or presence and extent of horizontal gene transfer.

Show MeSH
Related in: MedlinePlus