Horizontal gene transfer in evolution
Encyclopedia
Horizontal gene transfer
Horizontal gene transfer , also lateral gene transfer , is any process in which an organism incorporates genetic material from another organism without being the offspring of that organism...
(HGT) effectively scrambles the information on which biologist are relying to reconstruct a phylogeny of organisms – that is their evolutionary history and relationships.
Furthermore, the challenges that are raised by HGT are most awkward for the ambitious reconstruction of the earliest events in evolution, that is the early branches of the tree of life
Tree of life
The concept of a tree of life, a many-branched tree illustrating the idea that all life on earth is related, has been used in science , religion, philosophy, mythology, and other areas...
, because over long time intervals and with large numbers of organisms many low probability HGT events are certain to have actually occurred.
The three domains of life
The three main early branches of the tree of life have been intensively studied by microbiologistsMicroorganism
A microorganism or microbe is a microscopic organism that comprises either a single cell , cell clusters, or no cell at all...
because the first organisms were microorganisms. Microbiologists (led by Carl Woese
Carl Woese
Carl Richard Woese is an American microbiologist and physicist. Woese is famous for defining the Archaea in 1977 by phylogenetic taxonomy of 16S ribosomal RNA, a technique pioneered by Woese and which is now standard practice. He was also the originator of the RNA world hypothesis in 1977,...
) have introduced the term domain for the three main branches of this tree, where domain is a phylogenetic term very similar in meaning to biological kingdom. To reconstruct this tree of life, the sequence of a particular genes encoding the small subunit of ribosomal
Ribosome
A ribosome is a component of cells that assembles the twenty specific amino acid molecules to form the particular protein molecule determined by the nucleotide sequence of an RNA molecule....
RNA
RNA
Ribonucleic acid , or RNA, is one of the three major macromolecules that are essential for all known forms of life....
(SSU rRNA, 16s rRNA) have proven very 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 lineages in evolution of early cellular life and currently represented by the Bacteria
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
, the Archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
(single celled organisms superficially similar to bacteria), and Eukarya
Eukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. Eukaryotes may more formally be referred to as the taxon Eukarya or Eukaryota. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear...
(eukaryote) domains. Eukaryotes are all organisms with a well defined nucleus, and this domain comprises protists, fungi, and all organisms in the animal and plant kingdoms, including humans (see figure).
The most common gene used for constructing phylogenetic relationships in microrganisms
Prokaryote
The prokaryotes are a group of organisms that lack a cell nucleus , or any other membrane-bound organelles. The organisms that have a cell nucleus are called eukaryotes. Most prokaryotes are unicellular, but a few such as myxobacteria have multicellular stages in their life cycles...
is the small subunit ribosomal RNA gene, as its sequences tend to be conserved among members with close phylogenetic distances, yet it is variable enough that differences can be measured.
The SSU rRNA as a measure of evolutionary distances was pioneered by Carl Woese
Carl Woese
Carl Richard Woese is an American microbiologist and physicist. Woese is famous for defining the Archaea in 1977 by phylogenetic taxonomy of 16S ribosomal RNA, a technique pioneered by Woese and which is now standard practice. He was also the originator of the RNA world hypothesis in 1977,...
when formulating the first modern "tree of life", and his results led him to propose the Archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
as a third domain of life
Life
Life is a characteristic that distinguishes objects that have signaling and self-sustaining processes from those that do not, either because such functions have ceased , or else because they lack such functions and are classified as inanimate...
.) However, recently it has been argued that SSU rRNA genes can also be horizontally transferred. 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.
"Sequence comparisons suggest recent horizontal transfer of many gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
s among diverse species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
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." HGT is thus a potential confounding factor
Lurking variable
In statistics, a confounding variable is an extraneous variable in a statistical model that correlates with both the dependent variable and the independent variable...
in inferring phylogenetic tree
Phylogenetic tree
A phylogenetic tree or evolutionary tree is a branching diagram or "tree" showing the inferred evolutionary relationships among various biological species or other entities based upon similarities and differences in their physical and/or genetic characteristics...
s from the sequence
Sequence
In mathematics, a sequence is an ordered list of objects . Like a set, it contains members , and the number of terms is called the length of the sequence. Unlike a set, order matters, and exactly the same elements can appear multiple times at different positions in the sequence...
of one gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
. For example, if two distantly related bacteria have exchanged a gene, a phylogenetic tree
Phylogenetic tree
A phylogenetic tree or evolutionary tree is a branching diagram or "tree" showing the inferred evolutionary relationships among various biological species or other entities based upon similarities and differences in their physical and/or genetic characteristics...
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.
Which metaphor: tree, a net, cobweb, or ring?
In his article Uprooting the Tree of Life, W. Ford DoolittleFord Doolittle
Dr. W. Ford Doolittle is a biochemist., he is a professor at Dalhousie University in Halifax, Nova Scotia. He received his BA in Biochemical Sciences from Harvard University in 1963 and his PhD from Stanford University in 1967.Since joining the biochemistry department at Dalhousie in 1971, Dr...
discusses the Last Universal Common Ancestor
Last universal ancestor
The last universal ancestor , also called the last universal common ancestor , or the cenancestor, is the most recent organism from which all organisms now living on Earth descend. Thus it is the most recent common ancestor of all current life on Earth...
– the root of the Tree of Life – and the problems with that concept posed by HGT. He describes the microorganism Archaeoglobus fulgidus as an anomaly with respect to a phylogenetic tree based upon the code for the enzyme
Enzyme
Enzymes are proteins that catalyze chemical reactions. In enzymatic reactions, the molecules at the beginning of the process, called substrates, are converted into different molecules, called products. Almost all chemical reactions in a biological cell need enzymes in order to occur at rates...
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 chloroplast
Chloroplast
Chloroplasts are organelles found in plant cells and other eukaryotic organisms that conduct photosynthesis. Chloroplasts capture light energy to conserve free energy in the form of ATP and reduce NADP to NADPH through a complex set of processes called photosynthesis.Chloroplasts are green...
s came from ingested cyanobacteria,
".. 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 cell
Germ cellA germ cell is any biological cell that gives rise to the gametes of an organism that reproduces sexually. In many animals, the germ cells originate near the gut of an embryo and migrate to the developing gonads. There, they undergo cell division of two types, mitosis and meiosis, followed by...
s...
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..."
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 gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
s freely. Eventually, from these eclectic cells came the three domains of life as we know them today: bacteria
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
, archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
and eukaryote
Eukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. Eukaryotes may more formally be referred to as the taxon Eukarya or Eukaryota. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear...
. 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."
Resolution of uncertainty with Phylogenomics
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. One such approach, sometimes called 'multi-locus typing', has been used to deduce phylogenic trees for organisms that exchange genes, such as meningitis bacteria.Jonathan Eisen
Jonathan Eisen
Jonathan A. Eisen is an American evolutionary biologist, currently working at University of California, Davis. His academic research is in the fields of evolutionary biology, genomics and microbiology and he is the academic editor-in-chief of the open-access journal PLoS Biology.In 2011 Eisen was...
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"
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. 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.
Interestingly, such a fusion of organisms hypothesis
Hypothesis
A hypothesis is a proposed explanation for a phenomenon. The term derives from the Greek, ὑποτιθέναι – hypotithenai meaning "to put under" or "to suppose". For a hypothesis to be put forward as a scientific hypothesis, the scientific method requires that one can test it...
for the origin of complex nucleated cells has been put forward by Lynn Margulis
Lynn Margulis
Lynn Margulis was an American biologist and University Professor in the Department of Geosciences at the University of Massachusetts Amherst. She is best known for her theory on the origin of eukaryotic organelles, and her contributions to the endosymbiotic theory, which is now generally accepted...
using quite different reasoning about symbiosis
Symbiosis
Symbiosis is close and often long-term interaction between different biological species. In 1877 Bennett used the word symbiosis to describe the mutualistic relationship in lichens...
between a bacterium and an archaen arising in an ancient consortium of microbes.