In 1988, Richard Lenski (of the University of Michigan) and colleagues founded 12 populations of the bacteria Escherichia coli from the same clone. Since then, the bacterial populations have been studied over thousands of generations to provide data relating to real-time experimental evolution. In 2008, Blount, Borland, and Lenski reported significant developments in the ability of E. Coli to metabolise citrate (see here). This was widely perceived as an evolutionary innovation because normal E. coli is unable to digest citrate in the presence of oxygen (although the bacterium can metabolize citrate in the absence of oxygen). In the intervening years, Blount and the research group have analyzed 29 genomes from different generations to find the mutational events that were involved in the observed changes. The research paper has now been published in the journal Nature, and the Editor's summary is as follows:
"It has been suggested that small evolutionary steps pave the way for more major evolutionary leaps - in a combination of Darwinian gradualism and saltationism - but mechanistic details have been hard to determine from natural history. Rich Lenski and colleagues have now combined full-genome sequencing and 'evolutionary replay' experiments to dissect the multi-step origin of one key innovation - the evolution of aerobic citrate-utilization in an experimental bacterial population - over more than 30,000 generations and two decades. The three-step process they unveil, in which potentiation makes a trait possible, actualization makes it manifest and refinement makes it effective, is likely to be typical of other biological revolutions such as the colonization of land by proto-tetrapods."
Zachary Blount, postdoctoral researcher in MSU's BEACON Center for the Study of Evolution in Action, led a team of researchers in documenting the step-by-step process in which organisms evolve new functions. (Credit: Courtesy of Brian Baer, source here)
The Press Release accompanying the paper suggests that it provides the key to understanding evolutionary innovation: "How Organisms Evolve New Functions: Evolution is as Complicated as 1-2-3". There are three steps, which are described as follows:
"The first stage was potentiation, when the E. coli accumulated at least two mutations that set the stage for later events. The second step, actualization, is when the bacteria first began eating citrate, but only just barely nibbling at it. The final stage, refinement, involved mutations that greatly improved the initially weak function. This allowed the citrate eaters to wolf down their new food source and to become dominant in the population.
"We were particularly excited about the actualization stage," Blount said. "The actual mutation involved is quite complex. It re-arranged part of the bacteria's DNA, making a new regulatory module that had not existed before. This new module causes the production of a protein that allows the bacteria to bring citrate into the cell when oxygen is present. That is a new trick for E. coli." " (Source here)
Probably few readers of these reports are aware that experimental evolution has provided evidence that fails to map well on to neodarwinian theory. Instead of mutations creating novel genes, they are typically degradative and sometimes essentially neutral. This was pointed out by Behe in an academic paper an in a recent blog:
"In a manuscript published a few years ago in the Quarterly Review of Biology (Behe 2010), I discussed laboratory evolution results from the past four decades up to that point, including Lenski's. His laboratory had shown clearly that random mutation and selection improved the bacterium with time, as measured by the number of progeny it could produce in a given time. He demonstrated without doubt that beneficial mutations exist and can spread quickly in a population of organisms. However, once Lenski's lab eventually identified the mutations at the DNA level (a difficult task), many of the beneficial mutations turned out to be, surprisingly, degradative ones. In other words, breaking or deleting some pre-existing genes or genetic regulatory elements so that they no longer worked actually helped the organism under the conditions in which it was grown. Other beneficial mutations altered pre-existing genes or regulatory elements somewhat."
It is of interest, consequently, to know whether a similar situation applies to the citrate-consuming E. coli. In Behe's blog, the reported mutations are considered in the light of his 2010 paper. Here is the comment on Actualisation:
"They divide the mutations conceptually into three categories: 1) potentiation; 2) actualization; and 3) refinement. "Actualization" is the name they give to the mutation that first confers a weak ability to transport citrate into the laboratory E. coli. (It turns out that the bacterium is lacking only a protein to transport citrate into the cell in the presence of oxygen; all other enzymes needed to further metabolize citrate are already present.) The gene for the citrate transporter, citT, that works in the absence of oxygen is directly upstream from the genes for two other proteins that have promoters that are active in the presence of oxygen. A duplication of a segment of this region serendipitously placed the citT gene next to one of these promoters, so the citT gene could then be expressed in the presence of oxygen. Gene duplication is a type of mutation that is known to be fairly common, so this result, although requiring a great deal of careful research to pin down, is unsurprising." "
So, in this case, the gene for citrate transportation and all other enzymes needed to metabolize citrate pre-exist. What is new is the mutation that puts the citT gene next to a suitable promoter. This was achieved via a gene duplication mutation. No new information was created, but the mutation was sufficient to activate this key gene. Blount et al. use the term "amplification mutation" to describe what happened: "Amplification mutations can alter the spatial relationship between structural genes and regulatory elements, potentially causing altered regulation and novel traits." Behe comments also refinement stage as follows:
"Further work showed this was due to multiple duplications of the mutant gene region, up to 3-9 copies. Again, gene duplication is a fairly common process, so again it is unsurprising. In another experiment Lenski and co-workers showed that increasing the concentration of the citrate transporter gene was sufficient in itself to account for the greater ability of E. coli to grow on citrate."
Analysis of the potentiation stage is different. Behe finds that degradation is the most likely mechanism for this:
"It turns out that the original E. coli they began with decades ago could not benefit from the gene duplication that brought together a citT gene with an oxygen-tolerant promoter. Before it could benefit, a preliminary mutation had to occur in the bacterium somewhere other than the region containing the citrate-metabolism genes. Exactly what that mutation was, Lenski and coworkers were not able to determine. However, they examined the bacterium for mutations that may contribute to potentiation, and speculated that "A mutation in arcB, which encodes a histidine kinase, is noteworthy because disabling that gene upregulates the tricarboxylic acid cycle." (They tried, but were unable to test this hypothesis.) In other words, the "potentiation" may involve degradation of an unrelated gene."
So, a the whole scenario involves the combination of an initial degradation mutation, making it possible for a gene duplication mutation to position the citrate transporter gene next to a promotor, followed by other gene duplication events to enhance the ability to metabolise citrate. These mechanisms do not go beyond the findings of Behe's 2010 paper - which suggests that whilst mutations can tinker with genetic systems, they cannot build them. There are no grounds here for the claim, made by the Editor of Nature, that the three-stage process documented by Blount et al. "is likely to be typical of other biological revolutions such as the colonization of land by proto-tetrapods". There is a great gulf between genetic tinkering and the engineering of complex functional systems. Neodarwinists (such as Hendrickson & Rainey, referenced below) would do well to reflect on Behe's Edge of Evolution concept and the concluding comment of his blog:
"In retrospect, the most surprising aspect of the oxygen-tolerant citT mutation was that it proved so difficult to achieve. If, before Lenski's work was done, someone had sketched for me a cartoon of the original duplication that produced the metabolic change, I would have assumed that would be sufficient - that a single step could achieve it. The fact that it was considerably more difficult than that goes to show that even skeptics like myself overestimate the power of the Darwinian mechanism."
Genomic analysis of a key innovation in an experimental Escherichia coli population
Zachary D. Blount, Jeffrey E. Barrick, Carla J. Davidson & Richard E. Lenski
Nature, 27 September 2012, 489, 513-518 | doi: 10.1038/nature11514 (pdf here)
Abstract: Evolutionary novelties have been important in the history of life, but their origins are usually difficult to examine in detail. We previously described the evolution of a novel trait, aerobic citrate utilization (Cit+), in an experimental population of Escherichia coli. Here we analyse genome sequences to investigate the history and genetic basis of this trait. At least three distinct clades coexisted for more than 10,000 generations before its emergence. The Cit+ trait originated in one clade by a tandem duplication that captured an aerobically expressed promoter for the expression of a previously silent citrate transporter. The clades varied in their propensity to evolve this novel trait, although genotypes able to do so existed in all three clades, implying that multiple potentiating mutations arose during the population's history. Our findings illustrate the importance of promoter capture and altered gene regulation in mediating the exaptation events that often underlie evolutionary innovations.
How the unicorn got its horn
Heather Hendrickson & Paul B. Rainey
Nature, 489, 504-505 (27 September 2012) | doi:10.1038/nature11487
An experiment studying bacterial populations over thousands of generations shows that a novel trait can evolve through rearrangement and amplification of a few pre-existing genes.
Rose-Colored Glasses: Lenski, Citrate, and BioLogos
Evolution News & Views (13 November 2012)
How Organisms Evolve New Functions: Evolution is as Complicated as 1-2-3, ScienceDaily (Sep. 19, 2012)
The Latest From Lenski's Lab, Uncommon Descent (8 October 2012)
Innovation or Renovation? by Ann Gauger, Biologic Institute (24 September 2012)
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