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Comparative genomics brought the shocking realization that bacterial and archaeal genomes were literally shaped by HGT. These are striking examples of extensive gene exchange between the most distant prokaryotes that is stimulated by cohabitation. Not unexpectedly, the extent of gene exchange is far greater between more closely related organisms, even if often more difficult to detect Abby et al. Nevertheless, phylogenomic analysis of a variety of bacteria and archaea clearly reveals their mosaic origins: different genes affiliate with homologs from different organisms Koonin et al.

These findings have been encapsulated in the concept of the Rhizome of Life under which the history of any given genome can be represented as a rhizome, with diverse sources and evolutionary histories for different genes Raoult, ; Merhej et al. Recent, detailed studies indicate that at least in tight microbial communities, such as for instance the human gut microbiota, gene exchange is constant and rampant Smillie et al.

Otherwise, all genetic exchanges would be equal, and the only adequate depiction of evolution would be an undirected network graph. Thus, the validity of the tree representation of evolution and the very existence of HGT are inextricably linked. Nevertheless, these genes appear to comprise a single, co-evolving ensemble, in at least general agreement with the so-called complexity hypothesis Jain et al.

Under the complexity hypothesis, HGT of genes encoding subunits of macromolecular complexes is largely suppressed because of the deleterious effect caused by disruption of interactions refined by a long time of co-evolution. Indeed, a recent analysis has shown that it is the involvement in complex formation that shows a strong negative correlation with the rate of HGT, rather than any specific biological function Cohen et al.

Thus, genes encoding many translation system components probably coevolve and accordingly are rarely horizontally transferred because they are preferentially involved in large complexes above all, the ribosome itself rather than owing to their special biological importance or any other peculiarities of their biological function. Other genes show a much weaker but also significant phylogenetic coherence with the nearly universal genes for translation system components, perhaps also reflecting the involvement in complex formation.

The same series of phylogenomic studies that demonstrated the validity of the statistical tree of life quantified the contributions of tree-like vertical and web-like horizontal gene transmission to the relationships between bacterial and archaeal genomes Puigbo et al. Figure 3. Tree-like vertical and web-like horizontal contributions in the evolution of nearly universal genes and the entire phylogenetic forest. The two heat maps schematically depict comparison of bacterial and archaeal genomes as described previously Puigbo et al.

The extensive HGT that permeates the prokaryote world is the source of gene gain by bacterial and archaeal genomes. The opposite trend, gene loss, is at least as prominent as gene gain via HGT Snel et al. A prime example is evolution of intracellular parasites and symbionts, for example, Buchnera , a close relative of E. The balance between gene gain and gene loss translates into a distinct shape of the distribution of gene occurrence in prokaryote pangenomes at all levels, from closely related bacteria e.

This universal distribution has an asymmetric U-shape and can be approximated by three exponential functions Figure 4. The dynamic, fluid character of the prokaryote genomes yields a distinct, fractal-like structure of the gene universe O'Malley and Koonin, Figure 4. The universal distribution of gene commonality in the microbial genomic universe: a generalized schematic. The three broken lines represent three exponential functions that fit the core on the right , the shell in the middle and the cloud on the left of prokaryotic genes O'Malley and Koonin, Figure 5.

The core, shell, and cloud of microbial genes. A generalized schematic showing the approximate contributions of the core, shell, and cloud to the pangenomes of prokaryotes and individual genomes. Darwin himself actually saw species more as an arbitrary category in the continuum of varying life forms than a fundamental unit of life. In the twentieth century the species concept received its biological interpretation, primarily in the work of Ernst Mayr who famously defined a species as a system of panmictic populations that are genetically isolated from other such systems Mayr, This concept indeed captures a key feature of the biology of organisms with regular, obligatory sexual reproduction such as, above all, animals and to a lesser extent plants.

Most of the prokaryotes do not engage in regular sex but instead exchange genes via HGT with diverse other microbes that they happen to cohabitate with. In general, in the prokaryote world, there are indeed no discrete, genetically isolated systems of panmictic populations but rather complex webs of gene exchange Dagan et al. Thus, the very notion of species as a distinct biological category does not apply even though traditionally bacteria and archaea are still denoted by Linnaean species names e.

However, the modes of evolution substantially differ across the diversity of prokaryotes, spanning the entire continuum from fully sexual to fully clonal populations Smith et al. Some bacteria, especially parasites such as for example Neisseria gonorrhoeae , have been shown to form largely isolated communities that engage in regular conjugation, the bacterial equivalent of sex, resulting in extensive homologous recombination.

For these distinct organisms but not for the majority of bacteria and archaea, Mayr's biological definition of species might be a relevant concept. The irrelevance of the traditional species concept for most prokaryotes by no means implies non-existence of structure in the genome space. Indeed, bacteria and archaea that share common origin in phylogenetic trees of marker genes, such as rRNA, typically also possess similar gene content.

Interestingly, it has been shown that, among the processes that lead to the divergence of gene content between evolving lineages of prokaryotes, gene loss appears to occur stochastically and generally follows the divergence of marker genes whereas gene gain primarily, via HGT is more episodic Snel et al. This view does not imply any mysterious strive for perfection as imagined by some pre-Darwinian biologists including Lamarck or teleology of any kind.

Nevertheless, Darwin's position does suggest a trend of evolution from simple to complex forms which is indeed a highly intuitive notion that has some obvious support in well known facts of the history of life on earth. For example, the most organizationally complex organisms with the largest genomes, animals, and plants, appear only at relatively late stages of evolution. Thus, notwithstanding the numerous cases of reductive evolution, in particular among parasites and symbionts, the belief in a general complexification trend in the evolution of life appears to be common.

However, is complexification the prevailing modality of evolution? Phylogenomic reconstruction, at least for bacteria and Archaea, suggests otherwise. It is not surprising that differential gene loss dominates the evolution of commensal bacteria, such as Lactobacilli, from a complex free-living ancestor Makarova et al. However, a qualitatively similar pattern was detected in evolutionary reconstructions for all bacteria and archaea Snel et al. Strikingly, more recent reconstructions that were performed using larger genome sets and more sophisticated computational methods confidently indicate that the genome of the last common ancestor of all extant archaea apparently was at least as large and complex as that of typical modern organisms in this domain of cellular life Csuros and Miklos, Fully compatible reconstruction results have been reported for the expanded set of cyanobacterial genomes Larsson et al.

Thus, counter-intuitively, at least in prokaryotes, genome shrinkage that is sometimes called streamlining Lynch, and is attributed to increasing selective pressure in successful, large populations Lynch, ; Koonin, b , appears to be is no less and probably more common than genome growth and complexification. The Modern Synthesis of evolutionary biology emphasizes the randomness of mutations that provide the starting material for selection which engenders survival of the fittest under the given conditions and hence constitutes the adaptive, deterministic component of evolution.

The insistence on such strict separation between the stochastic and deterministic aspects of evolution departs from Darwin's view that included the Lamarckian inheritance, with adaptive mutations directly caused by environmental cues, as an important, even if ancillary mechanism of evolution Darwin, Recently, several genetic phenomena with a distinct Lamarckian flavor have been discovered Koonin and Wolf, a ; O'Malley and Koonin, The transcript of this unique spacer functions as a guide RNA that is incorporated into a specific complex of Cas proteins possessing DNAse activity and directs this complex to the cognate alien DNA or RNA molecules that are cleaved and accordingly inactivated.

Indeed, this system directly responds to an environmental cue in this case, foreign DNA by introducing a genetic change into the genome that is immediately adaptive with respect to that particular cue. Indeed, even if HGT cannot be viewed as being directly caused by a specific environmental factor, it certainly is the case that the repertoire of the acquired genes depends on the environment.

Genes common in a given environment will be acquired often and are likely to possess adaptive value. Stress-induced mutagenesis is triggered directly by environmental stress factors, e.

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The mutations are not specific to the biologically relevant loci but the activity of the molecular machineries of stress-induced mutagenesis [the best characterized of which is the SOS repair-mutagenesis system in bacteria Sutton et al. More generally, recent empirical and theoretical studies of diverse processes of stochastic and deterministic change in genomes make it clear that evolution is not limited to the basic Darwinian scheme of random variation that is subject to selection.

Evolution can be more adequately depicted as a continuum of processes from completely random ones, under the Wrightean modality defined by random variation and random fixation of changes via genetic drift; to the Darwinian modality with random changes fixed by the deterministic process of selection; to the Lamarckian mode in which both variation and fixation are deterministic Figure 6 Koonin and Wolf, a ; O'Malley and Koonin, Figure 6.

The continuum of evolutionary processes, from stochasticity to determinism. All organisms possess a certain degree of evolvability, i. At the most basic level, evolvability stems from the theoretical impossibility of error-free replication. Genomic variation in evolving organisms is created by a combination of intrinsic replication errors, recombination and mutations induced external agents mutagens. An intriguing, fundamental question in evolutionary biology is whether or not evolvability itself can evolve under selection, or put another way, whether there are dedicated mechanisms of evolution Kirschner and Gerhart, ; Poole et al.

The prevailing wisdom among biologists seems to be that evolvability is not selectable but is simply maintained at a sufficient level by inevitable errors at all levels of biological information processing. Under this view, selection is always directed at minimization of the error rate but the ability to attain perfection is limited by genetic drift resulting in sufficient evolvability Lynch, The very existence of complex molecular systems for stress-induced mutagenesis error-prone repair the activity of which is exquisitely regulated in response to stress implies that mechanisms enhancing variation when variation is needed for survival have evolved Galhardo et al.

Another remarkable mechanism that appears to have specifically evolved to generate variation involves the Diversity Generating Retroelements DGR Medhekar and Miller, Strikingly, the DGR are found both in bacteriophages where they generate diversity in cell attachment surface proteins via reverse transcription-mediated mutagenesis, resulting in host tropism switching Doulatov et al. The analogy between the activity of DGR and hypermutagenesis in animal immune systems is obvious except that the variation generated by the DGR is inherited. Many bacteria and some archaea possess the natural transformation ability that was used in the Avery experiment that requires specialized, complex pumps recently denoted transformosomes that internalize DNA from the environment Claverys et al.

The transformation machinery potentially could be viewed as a device that evolved under selective pressure to enhance HGT Johnsborg and Havarstein, However, one could argue that the enhancement of HGT is only a side effect of the evolution of the transformation system, its actual raison d'etre being the utilization of DNA as a rich source of replication substrates or simply food.

This argument hardly can hold with regard to the type 4 secretion systems T4SS that specialize in secretion of DNA from bacterial cells Hamilton et al. The GTAs are a distinct type of defective bacteriophages that package in the capsid not the phage genome which remains integrated in the host chromosome but rather apparently random pieces of the host chromosome. The GTAs have been discovered in diverse bacteria and archaea and have been shown to infect and transfer their genetic content to a broad range of cohabitating prokaryotes McDaniel et al.

This seemingly altruistic behavior can be explained in terms of group selection whereby the object of selection is an ensemble of organisms that jointly benefit from adaptive mutations rather than a single organism. Group selection is a controversial subject in evolutionary biology Maynard Smith, ; Borrello, ; Leigh et al. However, the case for the evolution of mechanisms for evolution seems to be much more general O'Malley and Koonin, Population genetic theory holds that under a broad range of conditions a clonal population is generally doomed to collapse through the action of Muller's ratchet, the irreversible accumulation of deleterious mutations leading to gradual decline in fitness Leigh et al.

The effect of Muller's ratchet that has been directly demonstrated in controlled evolutionary experiments on RNA viruses Chao, ; Duarte et al. The principal way to escape Muller's ratchet is to enhance recombination via sex in the form of meiotic crossing over in eukaryotes and in the form of conjugation in prokaryotes or HGT. Just as sex is generally viewed as a mechanism that evolved to counteract the ratchet, HGT may be best understood as a more general variation-generating process that is supported by various evolved mechanisms.

At the risk of being provocative, sex indeed can be legitimately regarded as a specialized form of HGT. Clearly, evolution maintains HGT within the optimal range rather than at the maximum possible level because the latter would eliminate genome stability and wreak havoc into selected high-fitness ensembles of genes O'Malley and Koonin, At a different level, an apparent mechanism of evolution involves unusual, stable phenotype modifications that are widespread in bacteria and lead to coexistence of two distinct phenotypes in a clonal population, the so-called bistability regimes Dubnau and Losick, ; Veening et al.

For instance, under limited nutrient supply, Bacillus subtilis will form two subpopulations of which only the smaller one has the capacity to sporulate and thus yields the only survivors when the conditions become incompatible with cell growth and division Veening et al. The coexistence is epigenetically inherited across many bacterial generations, hence this phenomenon has become known as bistability.

Darwin In the Genome: Molecular Strategies in Biological Evolution

The cost of maintaining this subpopulation is more than compensated by the benefit of survival under adverse conditions. Thus, the evolution of the regulatory circuitry that supports bistability appears to be not just a case of evolution of an evolutionary mechanism but more specifically evolution of a kin selection mechanism or evolution of altruism in bacteria. The evolution of kin selection demonstrated by bet hedging is paralleled by the mechanism of altruistic suicide that virus-infected bacteria and archaea commit using the toxin-antitoxin or abortive infection defense systems Makarova et al.

In this case, by killing themselves early, before the virus has a chance to replicate, the microbes save their kin from infection. The reality of kin selection, just as that of group selection, is often hotly debated by evolutionary biologists Nowak et al. In parallel with experimental studies, several theoretical models have been developed that characterize evolvability as a selectable trait in fluctuating environments Earl and Deem, ; Jones et al.

Thus, on the whole, and general theoretical doubts notwithstanding, evolution of evolvability appears to be an intrinsic and fundamental, if still poorly understood, aspect of the evolutionary process. Viruses are no part of the modern synthesis or more generally the traditional narrative of evolutionary biology. Until very recently, viruses have been viewed primarily as pathogens of animals, plants, and bacteria. Several lines of recent discovery have radically changed this view and promoted viruses to a central position on the stage of evolution.

This change in the evolutionary status of viruses and related selfish genetic elements has been discussed in detail elsewhere Claverie, ; Koonin et al. Here we quickly recapitulate several key points, with a focus on the importance of viruses for evolutionary biology in general. Metagenomic and ecological genomics studies have shown that, astonishingly, viruses are the most common biological entities on earth Edwards and Rohwer, ; Suttle, , Even the genomes of some unicellular eukaryotes, such as Trichomonas vaginalis , consist mostly of inactivated transposons Carlton et al.

Recruitment of mobile element sequences for transcription regulation and other cellular functions such as microRNA formation is a common phenomenon the full extent of which is not yet fully appreciated Jordan et al. Although genomes of prokaryotes are not so overwhelmed by mobile elements, due to the intense purifying selection, nearly all of them encompass multiple prophages and mobile elements.

Notably, deletion of all prophages leads to a substantial drop of fitness in E.

In at least some common environments such as ocean water and soil, the number of virus particles exceeds the number of cells by factors of 10— Edwards and Rohwer, ; Suttle, ; Srinivasiah et al. Similarly, the genetic diversity of viruses, measured as the number of distinct genes, substantially exceeds the genetic diversity of cellular life forms.

Furthermore, viruses, in particular bacteriophages, are major biogeochemical agents. Periodical killing of microbes, in particular cyanobacteria, has been identified as a major contributor to sediment formation and major contributors to the nutrient cycles in the biosphere Suttle, ; Rohwer and Thurber, The same process obviously is a key determinant of the population dynamics of the hosts that shapes the selection-drift balance throughout the course of evolution Weinbauer and Rassoulzadegan, The very fact that viruses greatly outnumber bacteria in the environment implies that antivirus defense systems are central to the evolution of bacteria and archaea.

This is indeed the case as made evident by the remarkable proliferation of diverse antivirus systems including CRISPR-Cas discussed above as well as multiple restriction-modification, abortive infection, toxin-antitoxin and other, still poorly characterized defense systems that in different combinations and with different abundances are present in most prokaryotes Juhas et al. Taken together, these findings and theoretical considerations strongly support the view that the virus-host arms race is one of the principal processes in all evolution Forterre and Prangishvili, ; Stern and Sorek, These two categories of biological entities can be characterized as informational genetic parasites, i.

Mathematical modeling indicates that genetic parasites inevitably emerge in any replicator system Szathmary and Maynard Smith, ; Takeuchi and Hogeweg, This conclusion is certainly intuitively plausible: one expects that cheaters will appear in any system with limited resources—in particular, in any system of replicators, such parasites will attempt to utilize the replication machinery without making it Koonin and Martin, Also, the notion that virus-like selfish elements are an intrinsic part of life since its inception [which can be reasonably considered to coincide with the origin of replication O'Malley and Koonin, ] is compatible with the ubiquity of these elements in nature.

In mathematical modeling, the outcome of the virus-host interaction depends on the specific parameters of the adapted model. In homogeneous models, virus-like parasites tend to cause collapse of the entire systems but in models with compartmentalization, which are most relevant for the actual evolution of life, stable host-parasite coexistence is possible Takeuchi and Hogeweg, Moreover, the destructive effect of genetic parasites on the host is mitigated when a dedicated genetic information storage medium evolves, which could be one of the driving forces behind the evolution of DNA in the primordial RNA world Takeuchi et al.

Figure 7. Indeed, while cellular life forms all use a uniform replication-expression strategy based on double-stranded ds DNA replication, transcription of genes into mRNA or non-coding RNA, and translation of mRNA into protein, viral genome can be represented by all known forms of nucleic acids, and alternative replication processes such as RNA replication and reverse transcription are widely used Figure 7 Koonin et al.

Finally, although viral genomes are generally small compared to the genomes of cellular life forms viruses being the ultimate genetic parasites , the range of genomic complexity is remarkable, from only about nucleotides and no genes in the simplest virus-like parasites, the viroids, to over a megabase and more than genes genomes that are more complex than those of many bacterial parasites and symbionts in the giant mimiviruses Raoult et al. Overall, the conclusion is inescapable that the entire history of life is a story of perennial interplay between genetic parasites and their hosts that is a major driver of evolution for both biological empires.

Prokaryotes bacteria and archaea and viruses entered the realm of evolution with the advent of genomics. Has the comparative study of these relatively simple compared to eukaryotes organisms radically changed the core tenets of evolutionary biology that were first envisaged by Darwin and were augmented with the genetic foundation in the Modern Synthesis? In terms of Kuhn's concept of the development of science Kuhn, , did the study of microbial evolution engender a paradigm shift?

It is not easy to answer this question definitively, possibly because the paradigm shift model does not adequately describe the evolution of biology regardless of whether or not it fits the evolution of physics. Probably, a more appropriate epistemological framework is that of integration, i. This model of the evolution of science was recognized by Kuhn himself in his later work Kuhn, and was recently examined by O'Malley in the context of biology O'Malley, ; O'Malley and Soyer, The phylogenomic study of microbes and viruses uncovered new biological realms which Darwin and even the authors of the Modern Synthesis could not possibly fathom.

The modes of evolution of these relatively simple organisms that, as we now realize, have dominated the biosphere since its beginning about 4 billion years ago to this day and into any conceivable future are different from the evolutionary regimes of animals and plants, the traditional objects of evolutionary biology. The study of microbial evolution has shattered the classic idea of a single, all-encompassing tree of life by demonstrating that the evolutionary histories of individual genes are generally different.

Remarkably, however, these developments have not rendered trees irrelevant as a key metaphor of evolution O'Malley and Koonin, Tree-like evolution is a fundamental implication of the binary replication of the genetic material, so it served Darwin well to use a tree as the single illustration of his book. Without, obviously, knowing anything of DNA replication, Darwin grasped the central principle of the evolution of life, descent with modification, and the tree pattern followed naturally.

Microbiology yielded the first clear-cut case of Lamarckian evolution, the CRISPR-Cas system, and subsequent re-examination of other evolutionary phenomena in both prokaryotes and eukaryotes has strongly suggested that the quasi Lamarckian modality is common and important in all evolving organisms, completing the range of evolutionary phenomena from purely stochastic drift, Wrightean evolution to deterministic Lamarckian evolution. Again, these findings not so much overturned but rather expanded the vision of Darwin who seriously considered Lamarckian mechanisms as being ancillary to natural selection only the Modern synthesis banished Lamarck.

Crucially, the study of microbial evolution presented apparently undeniable cases of evolution of evolvability such as the GTAs and the DGRs. Moreover, the discovery of bet-hedging strategies and altruistic suicide in bacteria shows that kin selection a subject of considerable controversy in evolutionary biology is evolvable as well. Again, as in the case of Lamarckian mechanisms, these discoveries force one to re-examine many more phenomena and realize that evolution is not limited to fixation of random variation and survival of the fittest but rather is an active process with multiple feedback loops, and that dedicated mechanisms of evolution exist and themselves evolve.

This is a major generalization that substantially adds to the overall structure of evolutionary biology but one has to realize that the principle of descent with modification remains at the core of all these complex evolutionary phenomena. We now realize that evolution of life is to a large extent shaped by the interaction arms race but also cooperation between genetic parasites viruses and other selfish elements and their cellular hosts. Viruses and related elements, with their distinctive life strategy, informational parasitism, actually dominate the biosphere both physically and genetically, and represent one of the two principal forms of life that as intrinsic to the history of the biosphere as cells are.

This new dimension of evolution simply could not be perceived by Darwin or even the creators of the Modern Synthesis due to the lack of relevant data. Thus, we are inclined to view the change in evolutionary biology brought about by phylogenomics of microbes and viruses as a case of integration rather than an abrupt departure from the paradigm of the Modern Synthesis Figure 8. Darwin realized the importance of descent with modification and the tree pattern of evolution it implies whereas Fisher, Wright, and Haldane derived the laws of population genetics that still constitute the core of our understanding of evolution.

However, recent advances, in particular those of microbial phylogenomics, added multiple, new and interconnected layers of complexity Figure 8 such that the conceptual core is but a small part of the current big picture of evolutionary biology. Figure 8. The conceptual structure of evolutionary biology: the Darwinian core and the new levels of complexity.


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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Abby, S. Lateral gene transfer as a support for the tree of life. Andam, C. Biased gene transfer in microbial evolution.

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Human Genome and the Evolution of Medicine - Stylianos Antonarakis - TEDxThessaloniki

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Hamilton, H. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Hayes, F. Toxins-antitoxins: diversity, evolution and function. She talks about a feedback control as it relates to variation and selection in a loop. Genomes that generate variants that are more likely to survive are the genomes that would be more effective at adapting and would therefore tend to survive.

Caporale cites examples to support her thoughts, such as bacteria that have Coat proteins. As she states, bacteria can infect us, and our immune system can see the surface of the bacterium and mount an immune response, and Caporale explains what happens when the Coat mutates and how that affects the outcome. Additionally, she provides extensive information on adaptations and mutations within organisms. The biological scientist discusses human population in regard to the genome.

She outlines the three important concepts that relate to her studies: cooperation, diversity, and feedback control. Caporale talks about stress responses that produce specific variation in the genome, and explains how, miraculously, enzymes can move DNA around. Caporale talks about the many different theories in the building blocks of life and she provides more information on some of the unsettled issues that relate to life and how it is created.

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