Horizontal gene transfer in evolution

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A three-domain tree of life showing the separation of Bacteria, Archaea, and Eukaryote domains. See Microorganisms article for further explanation. Phylogenetic tree.svg
A three-domain tree of life showing the separation of Bacteria, Archaea, and Eukaryote domains. See Microorganisms article for further explanation.

Horizontal gene transfer (HGT) refers to the transfer of genes between distant branches on the tree of life. In evolution, it can scramble the information needed to reconstruct the phylogeny of organisms, how they are related to one another.

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HGT can also help scientists to reconstruct and date the tree of life, as a gene transfer can be used as a phylogenetic marker, or as the proof of contemporaneity of the donor and recipient organisms, and as a trace of extinct biodiversity.

HGT happens very infrequently – at the individual organism level, it is highly improbable for any such event to take place. However, on the grander scale of evolutionary history, these events occur with some regularity. On one hand, this forces biologists to abandon the use of individual genes as good markers for the history of life. On the other hand, this provides an almost unexploited large source of information about the past.

Three domains of life

The three main early branches of the tree of life have been intensively studied by microbiologists because the first organisms were microorganisms. Microbiologists (led by Carl Woese) have introduced the term domain for the three main branches of this tree, where domain is a phylogenetic term similar in meaning to biological kingdom. To reconstruct this tree of life, the gene sequence encoding the small subunit of ribosomal RNA (SSU rRNA, 16s rRNA) has proven useful, and the tree (as shown in the picture) relies heavily on information from this single gene.

These three domains of life represent the main evolutionary lineages of early cellular life and currently include Bacteria, Archaea (single-celled organisms superficially similar to bacteria), and Eukarya. Eukarya includes only organisms having a well-defined nucleus, such as fungi, protists, and all organisms in the plant and animals kingdoms (see figure).

The gene most commonly used for constructing phylogenetic relationships in microorganisms is the small subunit ribosomal RNA gene, as its sequences tend to be conserved among members with close phylogenetic distances, yet variable enough that differences can be measured. [1] The SSU rRNA as a measure of evolutionary distances was pioneered by Carl Woese when formulating the first modern "tree of life", and his results led him to propose the Archaea as a third domain of life. However, recently it has been argued that SSU rRNA genes can also be horizontally transferred. [2] Although this may be rare, this possibility is forcing scrutiny of the validity of phylogenetic trees based on SSU rRNAs.

Recent discoveries of "rampant" HGT in microorganisms, and the detection of horizontal movement of even genes for the small subunit of ribosomal RNA, have forced biologists to question the accuracy of at least the early branches in the tree, and even question the validity of trees as useful models of how early evolution occurs. [3] In fact, early evolution is considered to have occurred starting from a community of progenotes, able to exchange large molecules when HGT was the standard. This lateral gene transfer occurred also beyond the Darwinian threshold, after heredity or vertical gene transfer was established. [4] [5]
"Sequence comparisons suggest recent horizontal transfer of many genes among diverse species including across the boundaries of phylogenetic "domains". Thus determining the phylogenetic history of a species can not be done conclusively by determining evolutionary trees for single genes." [6] HGT is thus a potential confounding factor in inferring phylogenetic trees from the sequence of one gene. For example, if two distantly related bacteria have exchanged a gene, a phylogenetic tree including those species will show them to be closely related even though most other genes have diverged substantially. For this reason it is important to use other information to infer phylogenies, such as the presence or absence of genes, or, more commonly, to include as wide a range of genes for analysis as possible. [6]

Earlier HGTs are thought to have happened. The first universal common ancestor (FUCA), earliest ancestor of the last common ancestor to all life (LUCA), is thought to have had other descendants that had their own lineages. [7] [8] These now-extinct sister lineages of LUCA descending from FUCA are thought to have horizontally transferred some of their genes into the genome of early descendants of LUCA. [8]

Choice of metaphor: tree, net, cobweb, or ring

In his article Uprooting the Tree of Life, W. Ford Doolittle discusses the Last Universal Common Ancestor – the root of the Tree of Life – and the problems with that concept posed by HGT. [9] He describes the microorganism Archaeoglobus fulgidus as an anomaly with respect to a phylogenetic tree based upon the code for the enzyme HMGCoA reductase – the organism is definitely an archaean, with all the cell lipids and transcription machinery expected of an archaean, but its HMGCoA genes are of bacterial origin. In the article, Doolittle says that while it is now widely accepted that mitochondria in eukaryotes derived from alpha-proteobacterial cells and that chloroplasts came from ingested cyanobacteria, [9]

".. it is no longer safe to assume that those were the only lateral gene transfers that occurred after the first eukaryotes arose. Only in later, multicellular eukaryotes do we know of definite restrictions on horizontal gene exchange, such as the advent of separated (and protected) germ cells...

If there had never been any lateral gene transfer, all these individual gene trees would have the same topology (the same branching order), and the ancestral genes at the root of each tree would have all been present in the last universal common ancestor, a single ancient cell. But extensive transfer means that neither is the case: gene trees will differ (although many will have regions of similar topology) and there would never have been a single cell that could be called the last universal common ancestor..." [9]

Doolittle suggested that the universal common ancestor cannot have been one particular organism, but must have been a loose, diverse conglomeration of primitive cells that evolved together. These early cells, each with relatively few genes, differed in many ways, and swapped their genes freely. Eventually, from these eclectic cells came the three domains of life as we know them today: bacteria, archaea and eukaryote. These domains are now recognizably distinct because much of the gene transfer that still occurs is within these domains, rather than between them. Biologist Peter Gogarten reinforced these arguments, and suggested that the metaphor of a tree does not fit the data from recent genome research, and that biologists should instead use "the metaphor of a mosaic to describe the different histories combined in individual genomes and use [the] metaphor of a net to visualize the rich exchange and cooperative effects of HGT among microbes." [10]

Resolution of uncertainty with phylogenomics

Tree Based on the Median Tree Algorithm. Branches with bootstrap (statistical) scores less than 50% were collapsed. The three domains of life are (A) archaea, (B-J) bacteria, and (K) eukaryote. Species are labeled with different colors based on their inferred HGT rates: red, >4%; yellow, 3-4%; pink, 2-3%; blue, 1-2%; green, <1%. Taxonomy labels are (A) Euryarchaea, (B) Proteobacteria, (C) Chlamydiae, (D) Spirochaetes, (E) Thermotogae, (F) Aquificae, (G) Actinobacteria, (H) Deinococcus, (I) Cyanobacteria, (J) Firmicutes, and (K) Fungi. Tree microbialgenomes nocobwebs.jpg
Tree Based on the Median Tree Algorithm. Branches with bootstrap (statistical) scores less than 50% were collapsed. The three domains of life are (A) archaea, (B–J) bacteria, and (K) eukaryote. Species are labeled with different colors based on their inferred HGT rates: red, >4%; yellow, 3–4%; pink, 2–3%; blue, 1–2%; green, <1%. Taxonomy labels are (A) Euryarchaea, (B) Proteobacteria, (C) Chlamydiae, (D) Spirochaetes, (E) Thermotogae, (F) Aquificae, (G) Actinobacteria, (H) Deinococcus, (I) Cyanobacteria, (J) Firmicutes, and (K) Fungi.

Despite the uncertainties in reconstructing phylogenies back to the beginnings of life, progress is being made in reconstructing the tree of life in the face of uncertainties raised by HGT. The uncertainty of any inferred phylogenetic tree based on a single gene can be resolved by using several common genes or even evidence from whole genomes. [12] One such approach, sometimes called 'multi-locus typing', has been used to deduce phylogenic trees for organisms that exchange genes, such as meningitis bacteria. [13]

Jonathan Eisen and Claire Fraser have pointed out that:

"In building the tree of life, analysis of whole genomes has begun to supplement, and in some cases to improve upon, studies previously done with one or a few genes. For example, recent studies of complete bacterial genomes have suggested that the hyperthermophilic species are not deeply branching; if this is true, it casts doubt on the idea that the first forms of life were thermophiles. Analysis of the genome of the eukaryotic parasite Encephalitozoon cuniculi supports suggestions that the group Microsporidia are not deep branching protists but are in fact members of the fungal kingdom. Genome analysis can even help resolve relationships within species, such as by providing new genetic markers for population genetics studies in the bacteria causing anthrax or tuberculosis. In all these studies, it is the additional data provided by a complete genome sequence that allows one to separate the phylogenetic signal from the noise. This is not to say the tree of life is now resolved – we only have sampled a smattering of genomes, and many groups are not yet touched" [14]

These approaches are enabling estimates of the relative frequency of HGT; the relatively low values that have been observed suggests that the 'tree' is still a valid metaphor for evolution – but the tree is adorned with 'cobwebs' of horizontally transferred genes. This is the main conclusion of a 2005 study of more than 40 complete microbial genomic sequences by Fan Ge, Li-San Wang, and Junhyong Kim. They estimate the frequency of HGT events at about 2% of core genes per genome. [15] Similar whole genome approaches to assessing evolution are also enabling progress in identifying very early events in the tree of life, such as a proposal that eukaryotes arose by fusion of two complete but very diverse prokaryote genomes: one from a bacterium and one from an archaeal cell. [3]

Such a fusion of organisms hypothesis for the origin of complex nucleated cells has been put forward by Lynn Margulis using quite different reasoning about symbiosis between a bacterium and an archaen arising in an ancient consortium of microbes. [16]

Use in evolutionary studies

While HGT is often seen as a challenge for the reconstruction of the tree of life, an alternative view is that oppositely it provides additional valuable information for its reconstruction.

First, for the recipient organism, HGT is a DNA mutation like others, and as such, it can be modeled and used in tree reconstruction and rooting. [17]

Second, it is necessary that the recipient of a gene acquisition by HGT lives at the same time, or at an ulterior time, as the donor. [18] In consequence there is an information on the timing of diversification in HGT. [19] This is all the more remarkable since the principal usual source for dating in the living world, the fossil record, is absent precisely where HGT is abundant, in the microbial world.

Third, it provides information about the extinct biodiversity, because transfers are likely from extinct species. [20]

See also

Related Research Articles

<span class="mw-page-title-main">Carl Woese</span> American microbiologist (1928–2012)

Carl Woese was an American microbiologist and biophysicist. Woese is famous for defining the Archaea in 1977 through a pioneering phylogenetic taxonomy of 16S ribosomal RNA, a technique that has revolutionized microbiology. He also originated the RNA world hypothesis in 1967, although not by that name. Woese held the Stanley O. Ikenberry Chair and was professor of microbiology at the University of Illinois Urbana–Champaign.

In biology, a kingdom is the second highest taxonomic rank, just below domain. Kingdoms are divided into smaller groups called phyla.

In biological taxonomy, a domain, also dominion, superkingdom, realm, or empire, is the highest taxonomic rank of all organisms taken together. It was introduced in the three-domain system of taxonomy devised by Carl Woese, Otto Kandler and Mark Wheelis in 1990.

A phylogenetic tree, phylogeny or evolutionary tree is a graphical representation which shows the evolutionary history between a set of species or taxa during a specific time. In other words, it is a branching diagram or a tree showing the evolutionary relationships among various biological species or other entities based upon similarities and differences in their physical or genetic characteristics. In evolutionary biology, all life on Earth is theoretically part of a single phylogenetic tree, indicating common ancestry. Phylogenetics is the study of phylogenetic trees. The main challenge is to find a phylogenetic tree representing optimal evolutionary ancestry between a set of species or taxa. Computational phylogenetics focuses on the algorithms involved in finding optimal phylogenetic tree in the phylogenetic landscape.

<span class="mw-page-title-main">Three-domain system</span> Hypothesis for classification of life

The three-domain system is a taxonomic classification system that groups all cellular life into three domains, namely Archaea, Bacteria and Eukarya, introduced by Carl Woese, Otto Kandler and Mark Wheelis in 1990. The key difference from earlier classifications such as the two-empire system and the five-kingdom classification is the splitting of Archaea from Bacteria as completely different organisms. It has been challenged by the two-domain system that divides organisms into Bacteria and Archaea only, as Eukaryotes are considered as a clade of Archaea.

<span class="mw-page-title-main">Horizontal gene transfer</span> Type of nonhereditary genetic change

Horizontal gene transfer (HGT) or lateral gene transfer (LGT) is the movement of genetic material between organisms other than by the ("vertical") transmission of DNA from parent to offspring (reproduction). HGT is an important factor in the evolution of many organisms. HGT is influencing scientific understanding of higher-order evolution while more significantly shifting perspectives on bacterial evolution.

<span class="mw-page-title-main">Thermoproteota</span> Phylum of archaea

The Thermoproteota are prokaryotes that have been classified as a phylum of the Archaea domain. Initially, the Thermoproteota were thought to be sulfur-dependent extremophiles but recent studies have identified characteristic Thermoproteota environmental rRNA indicating the organisms may be the most abundant archaea in the marine environment. Originally, they were separated from the other archaea based on rRNA sequences; other physiological features, such as lack of histones, have supported this division, although some crenarchaea were found to have histones. Until recently all cultured Thermoproteota had been thermophilic or hyperthermophilic organisms, some of which have the ability to grow at up to 113°C. These organisms stain Gram negative and are morphologically diverse, having rod, cocci, filamentous and oddly-shaped cells.

<span class="mw-page-title-main">Last universal common ancestor</span> Most recent common ancestor of all current life on Earth

The last universal common ancestor (LUCA) is the hypothesized common ancestral cell from which the three domains of life, the Bacteria, the Archaea, and the Eukarya originated. It is suggested to have been a "cellular organism that had a lipid bilayer and used DNA, RNA, and protein". The LUCA has also been defined as "a hypothetical organism ancestral to all three domains". The LUCA is the point or stage at which the three domains of life diverged from preexisting forms of life. The nature of this point or stage of divergence remains a topic of research.

<span class="mw-page-title-main">Neomura</span>

Neomura is a proposed clade of biological life composed of the two domains Archaea and Eukaryota, coined by Thomas Cavalier-Smith in 2002. Its name reflects the hypothesis that both archaea and eukaryotes evolved out of the domain Bacteria, and one of the major changes was the replacement of the bacterial peptidoglycan cell walls with other glycoproteins.

<span class="mw-page-title-main">Gracilicutes</span> Infrakingdom of bacteria

Gracilicutes is a clade in bacterial phylogeny.

<span class="mw-page-title-main">Prokaryote</span> Unicellular organism lacking a membrane-bound nucleus

A prokaryote is a single-cell organism whose cell lacks a nucleus and other membrane-bound organelles. The word prokaryote comes from the Ancient Greek πρό 'before' and κάρυον 'nut, kernel'. In the two-empire system arising from the work of Édouard Chatton, prokaryotes were classified within the empire Prokaryota. But in the three-domain system, based upon molecular analysis, prokaryotes are divided into two domains: Bacteria and Archaea. Organisms with nuclei are placed in a third domain, Eukaryota.

<span class="mw-page-title-main">Archaea</span> Domain of single-celled organisms

Archaea is a domain of single-celled organisms. These microorganisms lack cell nuclei and are therefore prokaryotes. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

Evolution of cells refers to the evolutionary origin and subsequent evolutionary development of cells. Cells first emerged at least 3.8 billion years ago approximately 750 million years after Earth was formed.

<span class="mw-page-title-main">Eocyte hypothesis</span> Hypothesis in evolutionary biology

The eocyte hypothesis in evolutionary biology proposes that the eukaryotes originated from a group of prokaryotes called eocytes. After his team at the University of California, Los Angeles discovered eocytes in 1984, James A. Lake formulated the hypothesis as "eocyte tree" that proposed eukaryotes as part of archaea. Lake hypothesised the tree of life as having only two primary branches: prokaryotes, which include Bacteria and Archaea, and karyotes, that comprise Eukaryotes and eocytes. Parts of this early hypothesis were revived in a newer two-domain system of biological classification which named the primary domains as Archaea and Bacteria.

Microbial phylogenetics is the study of the manner in which various groups of microorganisms are genetically related. This helps to trace their evolution. To study these relationships biologists rely on comparative genomics, as physiology and comparative anatomy are not possible methods.

The Woeseian revolution was the progression of the phylogenetic tree of life concept from two main divisions, known as the Prokarya and Eukarya, into three domains now classified as Bacteria, Archaea, and Eukaryotes. The discovery of the new domain stemmed from the work of biophysicist Carl Woese in 1977 from a principle of evolutionary biology designated as Woese's dogma. It states that the evolution of ribosomal RNA (rRNA) was a necessary precursor to the evolution of modern life forms. Although the three-domain system has been widely accepted, the initial introduction of Woese’s discovery received criticism from the scientific community.

Horizontal or lateral gene transfer is the transmission of portions of genomic DNA between organisms through a process decoupled from vertical inheritance. In the presence of HGT events, different fragments of the genome are the result of different evolutionary histories. This can therefore complicate investigations of the evolutionary relatedness of lineages and species. Also, as HGT can bring into genomes radically different genotypes from distant lineages, or even new genes bearing new functions, it is a major source of phenotypic innovation and a mechanism of niche adaptation. For example, of particular relevance to human health is the lateral transfer of antibiotic resistance and pathogenicity determinants, leading to the emergence of pathogenic lineages.

<span class="mw-page-title-main">Darwinian threshold</span> Period during the evolution of the first cells

Darwinian threshold or Darwinian transition is a term introduced by Carl Woese to describe a transition period during the evolution of the first cells when genetic transmission moves from a predominantly horizontal mode to a vertical mode. The process starts when the ancestors of the Last Universal Common Ancestor become refractory to horizontal gene transfer (HGT) and become individual entities with vertical heredity upon which natural selection is effective. After this transition, life is characterized by genealogies that have a modern tree-like phylogeny.

<span class="mw-page-title-main">Phylogenetic reconciliation</span> Technique in evolutionary study

In phylogenetics, reconciliation is an approach to connect the history of two or more coevolving biological entities. The general idea of reconciliation is that a phylogenetic tree representing the evolution of an entity can be drawn within another phylogenetic tree representing an encompassing entity to reveal their interdependence and the evolutionary events that have marked their shared history. The development of reconciliation approaches started in the 1980s, mainly to depict the coevolution of a gene and a genome, and of a host and a symbiont, which can be mutualist, commensalist or parasitic. It has also been used for example to detect horizontal gene transfer, or understand the dynamics of genome evolution.

The first universal common ancestor (FUCA) is a proposed non-cellular entity that is the earliest ancestor of the last universal common ancestor (LUCA) and its descendants, including every modern cell. FUCA would also be the ancestor of ancient sister lineages of LUCA, none of which have modern descendants.

References

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Further reading