Integrating horizontal gene transfer and common descent to depict evolution and contrast it with "common design"

Abstract

Horizontal gene transfer (HGT) and common descent interact in space and time. Because events of HGT co-occur with phylogenetic evolution, it is difficult to depict evolutionary patterns graphically. Tree-like representations of life's diversification are useful, but they ignore the significance of HGT in evolutionary history, particularly of unicellular organisms, ancestors of multicellular life. Here we integrate the reticulated-tree model, ring of life, symbiogenesis whole-organism model, and eliminative pattern pluralism to represent evolution. Using Entamoeba histolytica alcohol dehydrogenase 2 (EhADH2), a bifunctional enzyme in the glycolytic pathway of amoeba, we illustrate how EhADH2 could be the product of both horizontally acquired features from ancestral prokaryotes (i.e. aldehyde dehydrogenase [ALDH] and alcohol dehydrogenase [ADH]), and subsequent functional integration of these enzymes into EhADH2, which is now inherited by amoeba via common descent. Natural selection has driven the evolution of EhADH2 active sites, which require specific amino acids (cysteine 252 in the ALDH domain; histidine 754 in the ADH domain), iron- and NAD(+) as cofactors, and the substrates acetyl-CoA for ALDH and acetaldehyde for ADH. Alternative views invoking "common design" (i.e. the non-naturalistic emergence of major taxa independent from ancestry) to explain the interaction between horizontal and vertical evolution are unfounded.

Fig. 1–4

Significant depictions of life’s evolutionary history. 1. “Reticulated tree” or net representing frequent lateral transfer of genetic material among the ancestors of bacteria, Eukarya, and Archaea (after Doolittle 1999; with permission from Science Magazine). 2. The “ring of life” connects all unicellular life by horizontal gene transfer and depicts major ancestral groups by tiny circles on the ring (Rivera and Lake 2004); bacteria (three left arrows) generate an “operational eukaryotic ancestor,” while archaea (two right arrows) generate an “informational eukaryotic ancestor,” both merge at the root of the eukaryotes (with permission from Nature Publishing Group). 3. The “symbiogenetic whole-organism reconstruction” of the evolution of early life (Margulis 2009; illustration modified from original drawing by K. Delisle) depicts life emerging from a last universal common ancestor (LUCA), the origin of eukaryotes after a series of symbiotic fusions of ancestral archaebacteria and eubacteria, which led to the emergence of the last eukaryotic common ancestor (LECA); three significant genome “anastomoses” are represented by the merging of archaebacteria and a “swimming” bacteria, eukaryotes and “oxygen-breathing” bacteria, and eukaryotes and “photosynthetic” bacteria; the ulterior origin of animals, fungi, and plants is also depicted (with permission from Springer Science and Business Media). 4. The “pattern pluralism scheme” (Bapteste and Boucher 2009; Doolittle and Bapteste 2007) is depicted as three overlapping circles, within a larger circle, representing “family resemblance” among taxa, a well-known concept among taxonomists; the tree in the middle shows a classic phylogeny, where six taxa belong to three identifiable groups (α-, β-, and γ-proteobacteria); the “interactive data base” (bottom) is structured by keywords that highlight overlapping features of the six taxa, which can appear grouped in different taxonomic units because they share common properties in specific dimensions, i.e. anoxygenic photosynthesis, nitrification, nitrogen fixation (with permission from Springer Science and Business Media).

Fig. 5–6

Integrative model of lateral and vertical evolution. 5. Reticulated patterns of unicellular life (RPUL), connected by both horizontal gene transfer and common descent (arrows), emerged from a last universal common ancestor (LUCA) and diverged into clusters of archaeal (CATU, overlapping circles) or bacterial (CBTU, overlapping squares) taxonomic units; the last eukaryotic common ancestor (LECA) probably originated from symbiogenetic junction of archaeal and bacterial cells; overlapping pentagons represent clusters of eukaryotic taxonomic units (CETU); the “ring of life” depicted in the background emphasizes ongoing HGT. 6. A tree-like representation of relatedness among multicellular organisms coalesces to a RPUL, note how modern archaea and bacteria also coalesce to RPUL; “anastomosis” between eukaryotes with oxygen-breathing bacteria probably gave origin to mitochondria (mt, white arrow; a much earlier event is also possible: gray-dashed arrow with question mark on top), and between oxygen-breathing eukaryotes with photosynthetic bacteria led to chloroplast evolution (cp white arrow); hybridization (lateral exchange of genetic material via recombination) is probably more frequent in plants, algae or fungi than in animals (black horizontal arrows); a bifurcation pattern of diversification (white branching lines) is probably real among multicellular organisms because they acquire genetic material mostly via common descent. Note that only Amoebozoa are shown to account for the discussion on the origin of Entamoeba’s alcohol dehydrogenase (see text); however, other unicellular Eukaryotes—Excavata, Chromalveolata, and Rhizaria—(Andersson 2008, 2009) likely emerged from early CETU.

Fig. 7

Schematic diagram of Entamoeba histolytica alcohol dehydrogenase 2 (EhADH2). The enzymatic activities reside in two separate, interacting domains: N-terminal aldehyde dehydrogenase (ALDH) and C-terminal alcohol dehydrogenase (ADH) (catalytic residues: Cys252 and His754, respectively). Conserved amino acids essential for each domain’s function are shown; the iron-binding region in ADH is crucial for Eh-ADH2 activity and interaction between domains (Espinosa et al. 2001, 2009).