Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions, and prokaryote-to-eukaryote lateral gene transfers

Abstract

Lateral gene transfer has been identified as an important mode of genome evolution within prokaryotes. Except for the special case of gene transfer from organelle genomes to the eukaryotic nucleus, only a few cases of lateral gene transfer involving eukaryotes have been described. Here we present phylogenetic and gene order analyses on the small subunit of glutamate synthase (encoded by gltD) and its homologues, including the large subunit of sulfide dehydrogenase (encoded by sudA). The scattered distribution of the sudA and sudB gene pair and the phylogenetic analysis strongly suggest that lateral gene transfer was involved in the propagation of the genes in the three domains of life. One of these transfers most likely occurred between a prokaryote and an ancestor of diplomonad protists. Furthermore, phylogenetic analyses indicate that the gene for the small subunit of glutamate synthase was transferred from a low-GC gram-positive bacterium to a common ancestor of animals, fungi, and plants. Interestingly, in both examples, the eukaryotes encode a single gene that corresponds to a conserved operon structure in prokaryotes. Our analyses, together with several recent publications, show that lateral gene transfers from prokaryotes to unicellular eukaryotes occur with appreciable frequency. In the case of the genes for sulfide dehydrogenase, the transfer affected only a limited group of eukaryotes--the diplomonads--while the transfer of the glutamate synthase gene probably happened earlier in evolution and affected a wider range of eukaryotes.

FIG. 1.

The ML tree of the inferred amino acid sequence of gltD, sudA, and gltD-like genes and their gene arrangements. See Materials and Methods for gene nomenclature. The different typefaces of the species names indicate whether the species belongs to the eukaryotes (all capitals), Archaea (lowercase, normal), or Bacteria (lowercase italic). Three main parts of the tree are indicated with large boxes, as follows: a clade with mostly gltD genes (A); a clade with only sudA genes (B); and a paraphyletic group with different gltD-like genes (C). The tree was arbitrarily rooted between the gltD clade and the paraphyletic group of gltD-like genes. Black boxes represent the homologous part of the gltD, gltD-like, and sudA sequences (used in analysis), open boxes represent gltB genes, gray boxes represent sudB genes, and boxes with dotted borders represent unique N- or C-terminal extensions of the gltD-like genes. Note that there is no detectable sequence homology between the extensions represented by dotted boxes. A thin line between two boxes indicates neighboring genes on the chromosome. Two boxes attached to each other indicate fusion of the genes. Protein ML-distance bootstrap values >50% for bipartitions are shown.

FIG. 2.

Amino acid alignment of the iron-cluster binding motifs in sulfide dehydrogenase, proposed by Hagen et al. (15). The numbers above the alignments refer to the amino acid position in the P. furiosus SudB (cluster I) and SudA (cluster II and III) proteins. The proposed ligands are indicated by shadowed boxes. Note that cluster I has been proposed to have a novel Asp(Cys)₃ binding motif (15).

FIG. 3.

Phylogeny of concatenated sudA and sudB protein sequences. Protein ML bootstrap and ML distance bootstrap support values are shown above and below the branches, respectively. Only support values >50% for bipartitions are shown.