Evolution of glutamate dehydrogenase genes: evidence for lateral gene transfer within and between prokaryotes and eukaryotes

Abstract

Background: Lateral gene transfer can introduce genes with novel functions into genomes or replace genes with functionally similar orthologs or paralogs. Here we present a study of the occurrence of the latter gene replacement phenomenon in the four gene families encoding different classes of glutamate dehydrogenase (GDH), to evaluate and compare the patterns and rates of lateral gene transfer (LGT) in prokaryotes and eukaryotes.

Results: We extend the taxon sampling of gdh genes with nine new eukaryotic sequences and examine the phylogenetic distribution pattern of the various GDH classes in combination with maximum likelihood phylogenetic analyses. The distribution pattern analyses indicate that LGT has played a significant role in the evolution of the four gdh gene families. Indeed, a number of gene transfer events are identified by phylogenetic analyses, including numerous prokaryotic intra-domain transfers, some prokaryotic inter-domain transfers and several inter-domain transfers between prokaryotes and microbial eukaryotes (protists).

Conclusion: LGT has apparently affected eukaryotes and prokaryotes to a similar extent within the gdh gene families. In the absence of indications that the evolution of the gdh gene families is radically different from other families, these results suggest that gene transfer might be an important evolutionary mechanism in microbial eukaryote genome evolution.

Figure 1

Maximum likelihood tree of GDH-1 The phylogenetic tree is based on 380 unambiguously aligned amino acid positions. The Γ shape parameter, α, was estimated to 0.76 with no invariable sites detected (P_inv = 0). The tree is arbitrarily rooted. Eukaryotes are labeled red and Eubacteria black. Potential inter-domain and intra-domain LGTs supported by a maximum likelihood bootstrap support value > 50% are indicated by red and green ovals, respectively. Protein maximum likelihood bootstrap values are shown above the branches and protein maximum likelihood distance bootstrap values are shown below the branches. Only values >50% for bipartitions are shown, except that maximum likelihood distance bootstrap values <50% are shown in parentheses at nodes where potential transfers are indicated.

Figure 2

Maximum likelihood tree of GDH-2 The phylogenetic tree is based on 305 unambiguously aligned amino acid positions. The Γ shape parameter, α, and the fraction of invariable sites, P_inv, were estimated to 1.10 and 0.08, respectively. The tree is arbitrarily rooted. Labeling as in Figure 1 with the addition that Archaea are labeled in blue.

Figure 3

Maximum likelihood trees of GDH-3 and GDH-4 (A) The phylogenetic tree is based on 457 unambiguously aligned amino acid positions of GDH-3. The Γ shape parameter, α, and the fraction of invariable sites, P_inv, were estimated to 1.07 and 0.06, respectively. (B) The phylogenetic tree is based on 1141 unambiguously aligned amino acid positions of GDH-4. The Γ shape parameter, α, and the fraction of invariable sites, P_inv, were estimated to 1.14 and 0.14, respectively. The trees are arbitrarily rooted. Labeling as in Figure 1.