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Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes.

Mirkin BG, Fenner TI, Galperin MY, Koonin EV - BMC Evol. Biol. (2003)

Bottom Line: Therefore different gain penalties were used and the resulting series of reconstructed gene sets for the last universal common ancestor (LUCA) of the extant life forms were analysed.Therefore, the results seem to be compatible with approximately equal likelihoods of HGT and gene loss in the evolution of prokaryotes.In reality, horizontal transfer might have contributed to the evolution of many other genes also, which makes it a dominant force in prokaryotic evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Information Systems and Computer Science, Birkbeck College, University of London, Malet Street, London, WC1E 7HX, UK. mirkin@dcs.bbk.ac.uk

ABSTRACT

Background: Comparative analysis of sequenced genomes reveals numerous instances of apparent horizontal gene transfer (HGT), at least in prokaryotes, and indicates that lineage-specific gene loss might have been even more common in evolution. This complicates the notion of a species tree, which needs to be re-interpreted as a prevailing evolutionary trend, rather than the full depiction of evolution, and makes reconstruction of ancestral genomes a non-trivial task.

Results: We addressed the problem of constructing parsimonious scenarios for individual sets of orthologous genes given a species tree. The orthologous sets were taken from the database of Clusters of Orthologous Groups of proteins (COGs). We show that the phyletic patterns (patterns of presence-absence in completely sequenced genomes) of almost 90% of the COGs are inconsistent with the hypothetical species tree. Algorithms were developed to reconcile the phyletic patterns with the species tree by postulating gene loss, COG emergence and HGT (the latter two classes of events were collectively treated as gene gains). We prove that each of these algorithms produces a parsimonious evolutionary scenario, which can be represented as mapping of loss and gain events on the species tree. The distribution of the evolutionary events among the tree nodes substantially depends on the underlying assumptions of the reconciliation algorithm, e.g. whether or not independent gene gains (gain after loss after gain) are permitted. Biological considerations suggest that, on average, gene loss might be a more likely event than gene gain. Therefore different gain penalties were used and the resulting series of reconstructed gene sets for the last universal common ancestor (LUCA) of the extant life forms were analysed. The number of genes in the reconstructed LUCA gene sets grows as the gain penalty increases. However, qualitative examination of the LUCA versions reconstructed with different gain penalties indicates that, even with a gain penalty of 1 (equal weights assigned to a gain and a loss), the set of 572 genes assigned to LUCA might be nearly sufficient to sustain a functioning organism. Under this gain penalty value, the numbers of horizontal gene transfer and gene loss events are nearly identical. This result holds true for two alternative topologies of the species tree and even under random shuffling of the tree. Therefore, the results seem to be compatible with approximately equal likelihoods of HGT and gene loss in the evolution of prokaryotes.

Conclusions: The notion that gene loss and HGT are major aspects of prokaryotic evolution was supported by quantitative analysis of the mapping of the phyletic patterns of COGs onto a hypothetical species tree. Algorithms were developed for constructing parsimonious evolutionary scenarios, which include gene loss and gain events, for orthologous gene sets, given a species tree. This analysis shows, contrary to expectations, that the number of predicted HGT events that occurred during the evolution of prokaryotes might be approximately the same as the number of gene losses. The approach to the reconstruction of evolutionary scenarios employed here is conservative with regard to the detection of HGT because only patterns of gene presence-absence in sequenced genomes are taken into account. In reality, horizontal transfer might have contributed to the evolution of many other genes also, which makes it a dominant force in prokaryotic evolution.

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Two evolutionary scenarios leading to pattern II of Figure 1. The black circle represents gene loss and the white circle represents emergence of the COG.
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Figure 2: Two evolutionary scenarios leading to pattern II of Figure 1. The black circle represents gene loss and the white circle represents emergence of the COG.

Mentions: Consider, for instance, the possible evolutionary histories of genes (COGs) whose phyletic patterns are represented by I, II and III in Figure 1, given the evolutionary tree shown in the figure. Gene I is present in all extant species (A, B, C, and D) and thus can be inferred to have evolved in the common ancestor of all four species, the tree root, and to have been inherited by all of them. Gene II can be thought of as being present in the last common ancestor of species B, C, and D and inherited by all its descendants (Fig. 2a). However, another possible scenario for pattern II could be the gene's presence in the root, with a subsequent loss in species A (Fig. 2b). The scenario in 2a is the parsimonious one because it includes only one event as opposed to two events in the scenario 2b.


Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes.

Mirkin BG, Fenner TI, Galperin MY, Koonin EV - BMC Evol. Biol. (2003)

Two evolutionary scenarios leading to pattern II of Figure 1. The black circle represents gene loss and the white circle represents emergence of the COG.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC149225&req=5

Figure 2: Two evolutionary scenarios leading to pattern II of Figure 1. The black circle represents gene loss and the white circle represents emergence of the COG.
Mentions: Consider, for instance, the possible evolutionary histories of genes (COGs) whose phyletic patterns are represented by I, II and III in Figure 1, given the evolutionary tree shown in the figure. Gene I is present in all extant species (A, B, C, and D) and thus can be inferred to have evolved in the common ancestor of all four species, the tree root, and to have been inherited by all of them. Gene II can be thought of as being present in the last common ancestor of species B, C, and D and inherited by all its descendants (Fig. 2a). However, another possible scenario for pattern II could be the gene's presence in the root, with a subsequent loss in species A (Fig. 2b). The scenario in 2a is the parsimonious one because it includes only one event as opposed to two events in the scenario 2b.

Bottom Line: Therefore different gain penalties were used and the resulting series of reconstructed gene sets for the last universal common ancestor (LUCA) of the extant life forms were analysed.Therefore, the results seem to be compatible with approximately equal likelihoods of HGT and gene loss in the evolution of prokaryotes.In reality, horizontal transfer might have contributed to the evolution of many other genes also, which makes it a dominant force in prokaryotic evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Information Systems and Computer Science, Birkbeck College, University of London, Malet Street, London, WC1E 7HX, UK. mirkin@dcs.bbk.ac.uk

ABSTRACT

Background: Comparative analysis of sequenced genomes reveals numerous instances of apparent horizontal gene transfer (HGT), at least in prokaryotes, and indicates that lineage-specific gene loss might have been even more common in evolution. This complicates the notion of a species tree, which needs to be re-interpreted as a prevailing evolutionary trend, rather than the full depiction of evolution, and makes reconstruction of ancestral genomes a non-trivial task.

Results: We addressed the problem of constructing parsimonious scenarios for individual sets of orthologous genes given a species tree. The orthologous sets were taken from the database of Clusters of Orthologous Groups of proteins (COGs). We show that the phyletic patterns (patterns of presence-absence in completely sequenced genomes) of almost 90% of the COGs are inconsistent with the hypothetical species tree. Algorithms were developed to reconcile the phyletic patterns with the species tree by postulating gene loss, COG emergence and HGT (the latter two classes of events were collectively treated as gene gains). We prove that each of these algorithms produces a parsimonious evolutionary scenario, which can be represented as mapping of loss and gain events on the species tree. The distribution of the evolutionary events among the tree nodes substantially depends on the underlying assumptions of the reconciliation algorithm, e.g. whether or not independent gene gains (gain after loss after gain) are permitted. Biological considerations suggest that, on average, gene loss might be a more likely event than gene gain. Therefore different gain penalties were used and the resulting series of reconstructed gene sets for the last universal common ancestor (LUCA) of the extant life forms were analysed. The number of genes in the reconstructed LUCA gene sets grows as the gain penalty increases. However, qualitative examination of the LUCA versions reconstructed with different gain penalties indicates that, even with a gain penalty of 1 (equal weights assigned to a gain and a loss), the set of 572 genes assigned to LUCA might be nearly sufficient to sustain a functioning organism. Under this gain penalty value, the numbers of horizontal gene transfer and gene loss events are nearly identical. This result holds true for two alternative topologies of the species tree and even under random shuffling of the tree. Therefore, the results seem to be compatible with approximately equal likelihoods of HGT and gene loss in the evolution of prokaryotes.

Conclusions: The notion that gene loss and HGT are major aspects of prokaryotic evolution was supported by quantitative analysis of the mapping of the phyletic patterns of COGs onto a hypothetical species tree. Algorithms were developed for constructing parsimonious evolutionary scenarios, which include gene loss and gain events, for orthologous gene sets, given a species tree. This analysis shows, contrary to expectations, that the number of predicted HGT events that occurred during the evolution of prokaryotes might be approximately the same as the number of gene losses. The approach to the reconstruction of evolutionary scenarios employed here is conservative with regard to the detection of HGT because only patterns of gene presence-absence in sequenced genomes are taken into account. In reality, horizontal transfer might have contributed to the evolution of many other genes also, which makes it a dominant force in prokaryotic evolution.

Show MeSH
Related in: MedlinePlus