Elsevier

Biosystems

Volumes 193–194, June 2020, 104131
Biosystems

Shuffling type of biological evolution based on horizontal gene transfer and the biosphere gene pool hypothesis

https://doi.org/10.1016/j.biosystems.2020.104131Get rights and content

Abstract

Widespread horizontal gene transfer (HGT) may appear a significant factor that accelerates biological evolution. Here we look at HGT primarily from the point of view of prokaryote clones, which we take as the descendants of a single cell, all of whom have exactly the same nucleotide sequence. Any novelty that emerges as a random mutation, creating a new clone, could either disappear before its first HGT, or survive for a period and be transferred to another clone. Due to the chain character of HGT, each gene with an adaptive mutation is thus spread among numerous existing clones, creating further new clones in the process. This makes propagation far faster than elimination, and such genes become practically immortal and form a kind of “biosphere gene pool” (BGP). Not all of these genes exist in every clone, and moreover not all of them are expressed. A significant fraction of the BGP includes of genes repressed by regulatory genes. However, these genes express often enough to be subject to natural selection. In a changing environment, both repressed and expressed genes, after transferring to another clone, may prove useful in an alternative environment, and this will give rise to new clones. This mechanism for testing repressed genes for adaptability can be thought as a “shuffle of a deck of genes” by analogy with shuffling a deck of cards. In the Archean and Proterozoic eons, both BGP and the operational part of each genome were rather poor, and the probability of incorporation of randomly expressed genes into the operational part of each genome was very small. Accordingly, biological evolution during these eons was slow due to rare adaptive mutations. This explains why the realm of prokaryotes as the sole organisms on Earth lasted so long. However, over about 3.5 billion years before the Phanerozoic eon, the BGP gradually accumulated a huge number of genes. Each of them was useful in a certain environment of past eras. We suggest that multicellular eukaryotes that appeared at the end of the Proterozoic eon could shuffle these genes accumulated in BGP via HGT from prokaryotes that live in these multicellular organisms. Perhaps this was the cause of the “Cambrian explosion” and the high (and increasing) rate of evolution in the Phanerozoic eon compared with the Archean and Proterozoic.

Introduction

The theory of biological evolution traditionally rests on three concepts: heredity, variability and natural selection. Heredity provides transfer of genetic information from one generation to the next. Variability in the form of random mutations provides the emergence of novelties. Natural selection chooses amongst those novelties and their precursor genomes. Natural selection discards novelties that have proved lethal or simply harmful to the existence of the clone, but also allows novelties representing improvements add to the genome resulting in a new clone.

This process is slow because of the tiny probability of useful mutations. Note that mutations can vary from point mutations of the nucleotides to additions, deletions, or rearrangements of parts of genes to whole chromosomes, plus aneuploidy and polyploidy events. For example, if the mutation is of a single transcribed gene that yields a protein, its probability is a result of multiplication of the following small probabilities: probability of mutation itself; probability that the mutated gene synthesizes an RNA molecule that, in turn, synthesizes a stable protein molecule; probability of incorporation of the synthesized protein molecule into a cell's metabolic network; and finally – the probability of usefulness of the incorporated protein. It is obvious that the resulting product of probabilities is small and this notion corresponds well to the slow rate of biological evolution in the Archean and Proterozoic eons (Gordon and Mikhailovsky, 2019; Mikhailovsky, 2018b; Mikhailovsky and Gordon, 2017).

We can argue as follows that this process is stationary if not slowing down. Heredity, confined here to exact reproduction of a genome, then corresponds in an ideal case to zero variability. It works against variability and preserves genetic traits rather than changes them. Generally heredity improves its mechanisms over time which leads to slower evolution. Variability, on the contrary, accelerates biological evolution, but is based on mutagenic factors that do not increase significantly, except for short periods of the Earth's magnetic field flip-flops (Sagnotti et al., 2014; Witze, 2019). Finally, natural selection neither accelerates nor decelerates evolution. More accurately, stronger selection self-evidently implies faster mutation-driven evolution. But on the other hand, stronger selection can imply slower evolution if genetic variation is primarily supplied by recombination (Ueda et al., 2017). Because natural selection pressure in both cases influences evolution in opposite directions, its rate remains on average the same. Thus, we could expect that during the last 4 billion years of life on Earth, the rate of evolution fluctuated around some average value or gradually decreased.

However, real biological evolution was approximately stationary during only the first 3.5 billion years, i.e., in the Archean and Proterozoic eons, of respective durations of 1.5 and 1.96 billion years (Wikipedia, 2019b). A closer look, including the division of eons into epochs (Table 1) shows that such a slowdown manifested itself only at the beginning of the Proterozoic eon in the Paleoproterozoic era, that is, 2.5 to 1.6 billion years ago. From the middle of this eon (Mesoproterozoic era), biological evolution began to accelerate. This allows an approximation of the last six eras, i.e., the left six points in Fig. 1 based on data from Table 1, as an exponential curve y = a + ex where a = 4.5 and x = 7.0 (Fig. 2a). It agrees well with the exponential approximation of the increase in biological complexity by Alexei Sharov (2006).

At the same time, the right seven points of the curve in Fig. 1 from the very beginning of life (Eoarchean era) till the end of Proterozoic eon (Neoproterozoic era) could be interpreted as fluctuations around the average rate of the biological evolution that approximately equals to relative rate of Ri = 10. In this case, one could approximate as an exponential curve the last three points in Fig. 1 that relates to eras of the Phanerozoic eon. Such an exponential curve has the other values of its parameters: a = 3.2 and x = 2.8 (Fig. 2b). On the other hand, it is possible to approximate the dynamics of the rate of biological evolution throughout all its history, starting from 4 billion years ago, by combining the straight line (left) and the exponential curve (right). The best approximation of this kind (Fig. 3) shows that the switch from average constant (equals to 9.023) to exponential rate (with a = 6.3045 and x = 1.0) occurred during the Neoproterozoic era, the last one of the Proterozoic eon, simultaneously with the appearance of the first complex multicellular organisms (Table 1). In any case, at the beginning of the Phanerozoic eon the rate of evolution began to rise, obviously exponentially.

The Phanerozoic eon itself lasted only 541 million years. Of course, it is not complete yet, but mankind is changing the biosphere so radically and rapidly that the end of the current eon can be expected in the near future. (Some call the present era the Anthropocene (Wikipedia, 2019a). More important is that duration of the main milestones inside the Phanerozoic, i.e., Paleozoic, Mesozoic and Cenozoic eras, were 289, 187 and 65 million years, respectively (see Table 1). In other words, after the end of the Proterozoic eon, there is a clear acceleration of evolution, which cannot be explained by any of the three main concepts of evolution. This means that these three traditional concepts are not enough, and there is a need for a fourth concept to explain the increased evolutionary rate in the Phanerozoic eon. The purpose of this article is to formulate the fourth concept, which we call “shuffling evolution”, to be explained below.

It is not surprising that the sudden jump in the rate of evolution, dated by the very beginning of the Phanerozoic eon (the so-called “Cambrian explosion”) and the subsequent exponential evolution, still has no generally accepted explanation. The suggested options include an “ecological snowball” effect due to a series of knock-on ecological processes when environmental changes crossed critical thresholds (Zhang and Shu, 2014), increasing of bottom water oxygenation up to near modern oxygen levels (Chen et al., 2015; Zhang and Cui, 2016), sea level rise as a major factor (Smith and Harper, 2013), continental emergence (Lee et al., 2018), erosion enriching the ocean with nutrients (Maruyama et al., 2014; Santosh et al., 2014), global methane cycling (Kirschvink and Raub, 2003), extinction of the Ediacarian fauna (Darroch et al., 2018), predation (Bicknell and Paterson, 2018), interdependence between clones (Vannier, 2009), homeobox gene duplications (Holland, 2015), metamerism (Couso, 2009), head and appendage evolution (Chen, 2009), and several other options (Conway-Morris, 2003; Marshall, 2006; Zhang et al., 2014), from the impact of a life bearing comet seeding Earth with new cosmic-derived cellular organisms (Hoyle and Wickramasinghe, 1981a, 1981b; Steele et al., 2018) to divine intervention of intelligent design (Meyer, 2013). The most common point of view considers the Cambrian explosion as a result of a complex interaction of abiotic and biotic processes (Smith and Harper, 2013). It may have been due to the invention of “continuing differentiation” (Gordon, 1999; Gordon and Gordon, 2019), i.e., the ability to duplicate branches of an organism's differentiation tree (Alicea and Gordon, 2016; Gordon and Gordon, 2016; Gordon, 2013). The resulting explosive growth of the fractal tree of life (Gordon, 1992, 1999) would suggest that the Cambrian explosion is simply a mathematical consequence of the autocatalytic nature of the evolution of multicellular organisms with continuing differentiation (Gordon, 1999).

Section snippets

Horizontal gene transfer

Such rich diversity of possible explanations suggests that Phanerozoic evolution may be based on another fundamental concept of biological evolution, which has not yet been invoked. We suggest that the main contender for this role is horizontal gene transfer (HGT), also known as lateral gene transfer (LGT). HGT is transmission of a DNA fragment from one organism to another and its incorporation into the genome of the recipient that can belong to a different clone or even higher taxa. In

Possible consequences of a random mutation

Based on the numerous works referenced in the previous section, HGT not only exists but plays an essential role in evolution. Let us start by listing the consequences of a mutation of a gene (which we designate a “novelty”) that appears in a prokaryotic clone and generates a new clone. There can be three and only three such consequences:

  • 1.

    The novelty is a pseudogene that generally (Xu and Zhang, 2016) does not have protein coding ability (Sisu et al., 2014) and can exist and be horizontally

HGT as a chain reaction and the immortality of adaptive genes

At the moment of the first horizontal transfer of a new gene, there is only one donor clone containing this gene. If the transferred gene turns out to be lethal or harmful for the recipient clone, it is eliminated rapidly. But if the gene has become useful, it can successfully incorporate into the genome of the recipient clone. Initially, this happens only in one individual of the recipient, establishing a new clone. The population of this new clone will increase almost immediately on the

The biosphere gene pool (BGP) as a kind of biosphere's memory

Although the spreading of a gene sends it into genomes of all the clones that can accept it (in other words, for which it is useful), this does not mean that the transferred gene will remain in all such genomes. Some or even a majority of them can lose the gene because the process of gene loss occurs frequently (Albalat and Canestro, 2016) and represents a source of genetic variation (Huang, 2013). On the other hand, the chain reaction of gene transfer is obviously not limited to several years

Biological evolution as “shuffling of the deck of genes”

The next question that arises: is there a process that “reads” this chronicle, uses this memory, “recalls” the entries in this BGP, or does all this information, accumulated by countless generations of evolutionary winners, remain unclaimed and lie in vain, diverting resources necessary for its duplication in every new generation? The second alternative looks strange, and it is not surprising that this is not the case. The process that “reads” the chronicle really exists and this, as was

Accumulation of genes in the BGP and their shuffling in the history of the biosphere

In the very beginning of life on the Earth, i.e. in the very end of Hadean eon or beginning of the Archean, the number of mutations accumulated in the BGP and even more so in the individual genomes was rather small. Fortunately, because HGT was apparently of higher frequency at that time (Andam and Gogarten, 2011), this small BGP was immediately available for practically almost all of the clones, and this essentially increased the rate of spreading of novelties. Nonetheless, their fast

Some final remarks

Even if the probability of eukaryotic HGT is several orders of magnitude less than prokaryotic, and its characteristic time, respectively, is several orders of magnitude greater, such time is still negligible on the evolutionary scale. In addition, the BGP of the Late Proterozoic biosphere, well after the formation of the first eukaryotes, became richer, along with increased richness of the eukaryotic genomes. Both of these changes should have sharply increased the number of successful HGTs. As

Conclusions

Any novelty (useful gene mutation) can have only three consequences:

  • 1.

    The gene appears to be pseudogene that does not have protein-coding ability and can exist and even be horizontally transferred but is invisible to natural selection and evolution, except for its burden on metabolism.

  • 2.

    The protein encoded by the gene appears to be harmful, all the descendants of mutant die before the first HGT (horizontal gene transfer), and the gene is eliminated.

  • 3.

    The protein encoded by the gene appears to be

Declaration of competing interest

The authors declare no conflicts of interest.

Acknowledgement

Thanks to Natalie K. Gordon for some critical comments.

References (128)

  • S. Maruyama et al.

    Initiation of leaking Earth: an ultimate trigger of the Cambrian explosion

    Gondwana Res.

    (2014)
  • R.E. Musso

    Analysis of relative reversion frequencies for IS2 insertion mutations in the regulatory region of the galOPETK operon of Escherichia coli

    Plasmid

    (1989)
  • J.R. Penádes et al.

    Bacteriophage-mediated spread of bacterial virulence genes

    Curr. Opin. Microbiol.

    (2015)
  • J.C. Perez et al.

    Evolution of transcriptional regulatory circuits in bacteria

    Cell

    (2009)
  • M. Santosh et al.

    The cambrian explosion: Plume-driven birth of the second ecosystem on Earth

    Gondwana Res.

    (2014)
  • K.B. Sieber et al.

    Lateral gene transfer between prokaryotes and eukaryotes

    Exp. Cell Res.

    (2017)
  • Airlinersnet

    Boeing 777 Fun Facts

    (2002)
  • T. Akiba et al.

    On the mechanism of the development of multiple drug-resistant clones of Shigella

    Jpn. J. Microbiol.

    (1960)
  • R. Albalat et al.

    Evolution by gene loss

    Nat. Rev. Genet.

    (2016)
  • B. Alicea et al.

    Quantifying mosaic development: towards an evo-devo postmodern synthesis of the evolution of development via differentiation trees of embryos [invited]

  • C.P. Andam et al.

    Horizontal gene flow in managed ecosystems

  • C.P. Andam et al.

    Biased gene transfer in microbial evolution

    Nat. Rev. Microbiol.

    (2011)
  • A. Babić et al.

    Direct visualization of horizontal gene transfer

    Science

    (2008)
  • E.S. Balakirev et al.

    Pseudogenes: are they "Junk" or functional DNA?

    Annu. Rev. Genet.

    (2003)
  • Y.M. Bar-On et al.

    The biomass distribution on Earth

    Proc. Natl. Acad. Sci. U.S.A.

    (2018)
  • G. Bernardi

    The genomic code: a pervasive encoding/molding of chromatin structures and a solution of the “non-coding DNA” mystery

    Bioessays

    (2019 Dec)
  • R.D.C. Bicknell et al.

    Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian Explosion

    Biol. Rev.

    (2018)
  • D.H.S. Block et al.

    Regulatory consequences of gene translocation in bacteria

    Nucleic Acids Res.

    (2012)
  • E. Boon et al.

    Interactions in the microbiome: communities of organisms and communities of genes

    FEMS Microbiol. Rev.

    (2014)
  • L. Boto

    Horizontal gene transfer in evolution: facts and challenges

    Proc. R. Soc. B-Biol. Sci.

    (2010)
  • G. Bratbak et al.

    Bacterial dry matter content and biomass estimations

    Appl. Environ. Microbiol.

    (1984)
  • J.Y. Chen

    The sudden appearance of diverse animal body plans during the Cambrian explosion

    Int. J. Dev. Biol.

    (2009)
  • L. Chen et al.

    Cell differentiation and germ-soma separation in Ediacaran animal embryo-like fossils

    Nature

    (2014)
  • X. Chen et al.

    Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals

    Nat. Commun.

    (2015)
  • D.P. Clark et al.

    Molecular Biology

    (2013)
  • O. Cohen et al.

    Inference and characterization of horizontally transferred gene families using stochastic mapping

    Mol. Biol. Evol.

    (2010)
  • S. Conway-Morris

    The Cambrian "explosion" of metazoans and molecular biology: would Darwin be satisfied?

    Int. J. Dev. Biol.

    (2003)
  • E. Corel et al.

    Bipartite network analysis of gene sharings in the microbial world

    Mol. Biol. Evol.

    (2018)
  • J.P. Couso

    Segmentation, metamerism and the Cambrian explosion

    Int. J. Dev. Biol.

    (2009)
  • C. Cronkite

    Determination of lac operon functionality of two strains of E. coli by comparing β-galactosidase activity

  • J. Daley

    Behold LUCA, the Last Universal Common Ancestor of Life on Earth: New Discoveries Suggest Life Likely Descends from the Inhospitable Environment of Deep Sea Vents

    (2016)
  • E.G.J. Danchin

    Lateral gene transfer in eukaryotes: Tip of the iceberg or of the ice cube?

    BMC Biol.

    (2016)
  • C.J. Dommar et al.

    Coevolutionary motion and swarming in a niche space model of ecological species interactions

    Eur. Phys. J. Spec. Top.

    (2008)
  • D.E. Dykhuizen

    Santa Rosalia revisited: why are there so many species of bacteria?

    Antonie Van Leeuwenhoek

    (1998)
  • D.H. Erwin

    A public goods approach to major evolutionary innovations

    Geobiology

    (2015)
  • D.H. Erwin

    Prospects for a general theory of evolutionary novelty

    J. Comput. Biol.

    (2019)
  • I. Ferro et al.

    Competition for amino acid flux among translation, growth and detoxification in bacteria

    RNA Biol.

    (2018)
  • M. Fondi et al.

    Every gene is everywhere but the environment selects": global geolocalization of gene sharing in environmental samples through network analysis

    Genome Biol. Evol.

    (2016)
  • V. Freeman

    Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae

    J. Bacteriol.

    (1951)
  • J. Fröhlich-Nowoisky et al.

    Diversity and seasonal dynamics of airborne archaea

    Biogeosciences

    (2014)
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