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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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Support for alternative tree topologies. The number of single copy protein families supporting each of the three possible tree topologies for the acidophilus group is indicated as a function of the confidence (by AU test) threshold applied in tree reconstruction for individual families. Only the 401 protein families that strongly support the grouping of the three lactobacilli of the acidophilus complex are represented.
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Figure 3: Support for alternative tree topologies. The number of single copy protein families supporting each of the three possible tree topologies for the acidophilus group is indicated as a function of the confidence (by AU test) threshold applied in tree reconstruction for individual families. Only the 401 protein families that strongly support the grouping of the three lactobacilli of the acidophilus complex are represented.

Mentions: A similar distribution is observed for ML trees at different thresholds of confidence (Fig. 3). Of 181 trees reconstructed with ≥ 80% confidence, 104 correspond to topology Ta, 75 to topology Tb, and 2 to topology Tc. When the confidence threshold is lowered to 50%, 209 proteins are found to support Ta, 141 Tb and 22 Tc. These results are essentially the same as those obtained when only using trees with a confidence level ≥ 95%: a 3:2 ratio between topologies Ta and Tb, and (near) absence of topology Tc. Thus, although individual trees have a slightly higher chance of being erroneous, the overall informational content remains the same. Therefore, proteins with tree confidence levels <95% can be exploited for further analysis, offering the advantages linked to the use of larger datasets.


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)

Support for alternative tree topologies. The number of single copy protein families supporting each of the three possible tree topologies for the acidophilus group is indicated as a function of the confidence (by AU test) threshold applied in tree reconstruction for individual families. Only the 401 protein families that strongly support the grouping of the three lactobacilli of the acidophilus complex are represented.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Support for alternative tree topologies. The number of single copy protein families supporting each of the three possible tree topologies for the acidophilus group is indicated as a function of the confidence (by AU test) threshold applied in tree reconstruction for individual families. Only the 401 protein families that strongly support the grouping of the three lactobacilli of the acidophilus complex are represented.
Mentions: A similar distribution is observed for ML trees at different thresholds of confidence (Fig. 3). Of 181 trees reconstructed with ≥ 80% confidence, 104 correspond to topology Ta, 75 to topology Tb, and 2 to topology Tc. When the confidence threshold is lowered to 50%, 209 proteins are found to support Ta, 141 Tb and 22 Tc. These results are essentially the same as those obtained when only using trees with a confidence level ≥ 95%: a 3:2 ratio between topologies Ta and Tb, and (near) absence of topology Tc. Thus, although individual trees have a slightly higher chance of being erroneous, the overall informational content remains the same. Therefore, proteins with tree confidence levels <95% can be exploited for further analysis, offering the advantages linked to the use of larger datasets.

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