Chapter III. Original, non-Darwinian evolution of prokaryotes
p. 73-88
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1Living organisms cannot be fully understood outside their evolutionary context. Although it is difficult, often impossible, to distinguish between facts and hypotheses when dealing with what happened billions of years ago, it is generally agreed that the first form of life must have been a simple, prokaryotic-type assemblage of compatible elements and molecules. Prokaryotes seem to be direct descendants of this first ancestor, the earliest cell on Earth which was able to multiply by successive divisions giving rise to a viable, successful offspring. We propose a coherent scenario in which gradually, over about two billion years, the original evolution of this ancestor led to a structured, global System or superorganism whose disjunct cells collaborate easily in many different ways and support each other. In the early years, when life began, each cell was part of the growing, single global clone which started by settling the more favorable parts of the oceans. This ancestor clone on Earth was probably composed of identical cells for tens of thousand years. The assumption here is that the probability and the time lapse for a completely new gene developing were similar then to what they are today. This gave enough time for the first type of daughter cells to reach astronomical numbers, a most significant presence that marked the beginning of a strong and stable biologic influence in the global aquatic milieu.
1. Ways in which errors in the division of the earliest cells could be prevented or compensated for
2It is likely that multiplication by binary fission of the first ancestral cells did not always result in their perfect partitioning into two identical descendants. Here and there one of the progeny cells missed an enzyme normally encoded by a gene not transmitted at the time of the mother cell's division. A possible way to prevent or to correct this unequal distribution of the hereditary patrimony may have been to group all the early cells’ genes in several, rather small, self-replicating DNA-containing structures (replicons) each one present in multiple copies within a given cell. The presence of several copies of each gene would have reduced the probability for one daughter cell of not inheriting at least one unit of each parental gene. Very soon, however, selective pressure favoured cells that were small and not harboring gene duplicates.
3One can also envisage two other possible ways in which failure to distribute all the essential genes to each new descendant could be corrected. One is by a primitive form of transformation in which the missing gene would move from one cell (possibly dead and disintegrated) to another in which this essential gene was missing. Another way would be by resorting to complementary metabolism, one enzyme synthesized by one cell diffusing into the surrounding medium and temporarily serving the needs of other members of the community. Thus, early prokaryotic life probably resorted to and benefited from both gene exchange and association of metabolically complementary cells as mechanisms of reciprocal support and survival. These were progressively improved to today’s efficient level.
2. Variety and diversification inside the early global prokaryotic clone
4As millions of years went by, the prokaryotic cells slowly began to accumulate in their population an increasing number of entirely new, successful genes resulting from successive random mutations. Each of these new genes, when it happened to be a favorable addition to its host cell, helped it not only to survive but to outnumber the other members of the still rather uniform global clone. Each new type of gene added a small supplement to the clone’s patrimony which thus became progressively enriched. This worked as a positive force bringing to the elements of the global prokaryotic clone more diversity and complexity in its bio-energetic capacities. It also increased its ability to settle new environments. The prokaryotic way of life was, therefore, strongly reinforced by the appearance of new, improved and reciprocally supporting types of differently modified cells. It not only proved viable but it prospered and diversified the former homogeneous population. It probably was a climate of free for all constructive competition, and cells and genes changed their associations as needed. An abundant and complex bank of genes, possibly equivalent to the present one, was likely completed 1.5 B.Y. ago. During this long episode of evolution, the chances or the need for an entirely new and completely different type of cell able to compete and survive in these prevailing conditions were low. A mutation toward an entirely different trait meant fierce competition with a well-adapted and established clone. This also means that, for a long time, there was little future in major genetic adventures. Established bacterial communities in general discourage the development of newly arrived foreign strains. This has been shown by modem day experimentation on the normal prokaryotic population of the digestive tract of animals, which has proved over and over again that a strain could successfully colonize the gut of germ-free animals, but would often fail to develop when exposed to the competition offered by the well adapted and abundant resident flora of a holoxenic (normal) animal (Ducluzeau et Raibaud, 1984). The massive presence of a locally successful mixed microbial population would not allow easy multiplication of a dissimilar type. A new gene had a better chance to become integrated in a team if it increased the collaboration potential of the existing genes which had already united in forming or helping reciprocally supporting strains. On the other hand, once a newly formed gene became operative and successful within its host cell, chances were good that it would be transferred to other different type cells during the following years and centuries. From then on, this gene was no longer in danger of being lost and becoming extinct. This contributed to survival, resiliency and favoured “immmortality” of the successful genes and cells in the prokaryotic world.
3. Prokaryotic cells evolved and progressed together towards both high specialization and easy complementarity
5The prokaryotic way of evolution made the diversity of the cells increase progressively toward reciprocal support, to the point that eventually there was less and less similarity between the bio-energetic reactions of different strains. These were becoming complementary and more specialized, and carried a minimum of bio-energetic genes essential to life and easy to combine in different associations. The cells kept and improved their basic characteristics needed for life in common, such as small size and minimal intracellular genome. In parallel, they improved the structures and mechanisms for easy horizontal gene exchange. The few basic shapes of the cells and particular properties of their outer membranes facilitated survival in various environments. The generalized mechanisms of horizontal gene transfer operated effectively due to cellular genomic organization involving two types of replicons: a large one for stable genes, and small ones for exchanges of visiting genes. The solidarity of the prokaryotic global entity was also helped by the creation of other cellular features: the competence operons allowing, today, transformation in possibly 50% of all the strains, cell surface receptors attracting temperate phages and present in all strains, and pili for the transfer of ST plasmids found in about half of the strains. The existence of these features has unified global prokaryotic populations and helped them perform complex functions. It has kept all the prokaryotic hereditary patrimony permanently available for strains. The origin and the evolution of the small replicons has been a most significant episode in the prokaryotes’ life, an essential step toward the status of global superorganism. Even if not all small replicons are necessarily contributing to the survival and daily life of all prokaryotic cells, at the global level, they can be viewed as a reliable insurance policy. Genes and cells which might not have survived in isolation did well as associates and collaborators in communities. Their potential is best realized when they are combined into dynamic, adaptable chimeras. An analogy can be made between their relationships and a computerized communication network (Sonea, 1988a, Sonea & Panisset, 1980). The information bank consists of all the prokaryotic genes. Selection takes place through permanent competition and amplification results from the higher multiplication of the right combination. Other mechanisms too favor the association of reciprocally supporting strains. For instance, prokaryotic cells have a good degree of tolerance among themselves, like the different cells of the same animal or plant. Associations and mixed communities of prokaryotic strains are the rule. So, on the basis of what is known about genetic exchange, metabolite and enzyme sharing, indications exist that for the overwhelming majority of prokaryotes the selective pressures have favored collaboration, not reciprocal or unilateral destruction. Prokaryotic evolution has been and still is non-Darwinian. Only eukaryotes have evolved as described by Darwin.
6We believe, therefore, that during two billion years of solitary evolution, because of its ability to retain and disseminate among its constituents favorable new genetic information, the prokaryotic clone constantly grew in collective complexity and in possibilities of local variations that made it able to colonize more and more different niches. In each of them, the continuons multiplication of prokaryotic cells adapted to prevailing conditions lead to positive and constructive competition first between rather similar cells and, much later, between increasingly diversified ones. It is also probable that the replicon containing the genes responsible for cell division progressively accumulated all the other genes essential for bio-energetic activity, possibly with the help of transposons. It became the stable replicon found today in each prokaryotic cell, the large replicon sometimes referred to as nucleoid (improperly called the chromosome). Non essential genes, for their part, seem to have progressively been grouped in much smaller replicons and therefore became more likely candidates for successful gene exchanges. The offspring of these autonomous small replicons had their own evolution and ended up as plasmids and prophages. They are fïtted to maintain in the host cells temporary genetic help made available to other types of strains as well.
7Probably the major concentrations of cells (including many Archaean ancestors) during the earliest millions of years inhabited the oceanic regions, sites of frequent volcanic activity, under anaerobic conditions. However, genes for photosynthesis appeared relatively early. The cells benefiting from this new biochemical photosynthetic potential could grow and multiply at the surface, or in shallow waters where sunlight could reach them. Abundant stromatolite fossils are proof of the incredible numbers of photosynthetic prokaryotes already present in the first billion years of life on Earth (Margulis, 1993). This constant and progressively more abundant photosynthetic activity increased the concentration of O2 in the atmosphere and in the surface water expanses. Here again prokaryotes not only participated but were determinant in a capital evolutionary transition. The O2 produced by photosynthesis contributed to the formation of today’s type of atmosphere and favored aerobic respiration, an extremely efficient means of energy conversion.
8Prokaryotic cells kept increasing in number and variety but remained small as they still are today. Almost all their energetic and metabolic formulas needed for life in the different niches of our planet seem to have been present, spread among the cells of the ensemble 2 B.Y. years ago. Strains could function in different mixed communities in the mutualistic way of prokaryotic associations. There was neither a need for, nor real survival value in concentrating in large single cells more biochemical capabilities that were otherwise made available through associations, exchanges and sharing.
4. The appearance of the bacterial cell wall and of transformation
9Because of the almost certainly rigorous environmental conditions that prevailed and the fragile nature of the cell membrane, practically all prokaryotes ended up with genes for the synthesis of a stronger, protective supplementary envelope called the cell wall of which there are now only a few different basic types. These structures however are, in general, impervious to DNA molecules. The present type of transformation which has overcome the permeability problems posed by the cell wall seems to have appeared and spread at least about 2 B.Y. ago, implying a very early intracellular arrangement of the necessary genes in a “competence” operon. The fact that about half of today's prokaryotes may still benefit from transformation when more effective processes for horizontal gene exchanges (by small replicons) appeared in later periods highlights the important role played by transformation in the functioning and maintenance of genetic solidarity among prokaryotes.
5. Small replicons became the most efficient basic elements of a prokaryotic global communication System
10The small replicons appeared, presumably, before the branching into Archaea and Eubacteria, since they are present in both groups. These visiting genes are able to multiply in their temporary host cells and, when needed, make available to them a choice from a large variety of accessory genes. Their activity, added to that of transformation, keeps the horizontal gene transfer generalized and frequent. As already mentioned, the more complex, self-transmissible small replicons seem to have had a common origin and later they evolved into self-transmissible (ST) plasmids and prophages. A large proportion of horizontal gene transfer in prokaryotes is performed by these two types of ST small replicons. Added to the gene transfers effected by transformation and by NST small replicons, an impressive cumulative capacity of gene exchange was reached long ago at optimal frequency and kept to the present day when, presumably, all prokaryotes may exchange genes. For example, as the methodology for growing and studying the Archaea has developed enormously over the last two decades, it has become clear that cell to cell transfer of genetic information is not limited to eubacteria. Sulfolobus spp. are aerobic archaea that populate terrestrial hot springs; most grow optimally at about 80° C and pH 3. Various isolates have been found to contain prophages, transposable genetic elements and at least one self-transmissible conjugative plasmid. D.W. Grogan (1996) has shown that when two auxotrophic mutants of Sulfolobus acidocaldarius are mixed and grown on solid medium they form stable genetic recombinants which can be selected, enumerated and characterized. The results also indicate that, as in eubacteria, chromosomal mutations which arise in one cell lineage can be transferred to other lineages and this lateral gene flow provides, on the one hand, genetic diversity and evolutionary adaptability and possibly, on the other hand, genomic repair. It is also well documented that Archaea harbor phages of various kinds (Zillig et Arnold, 1999). Even the prokaryotic strains that are obligate parasites of eukaryotes contain small replicons and surface receptors. They exchange them with non-parasitic types, when needed. Prokaryote evolution benefited from and was accelerated and intensified by these exchanges of information (Anderson, 1966). Today, the same global communication System helps prokaryotes to solve problems without having to resort to newly synthesized genes. Heredity of prokaryotes is definitely non Mendelian. It is, instead, based on a global prokaryotic genome actively maintained available for any cell.
6. The global prokaryotic superorganism (or biologic System) as a unique type of clonal entity; there are no prokaryotic species
11Generally, the most complex entities displaying the highest capacities seem to be the clones which contain specialized cells practicing a well adapted division of labor to fulfill superior fonctions. Let us compare the single global and clonal superorganism of all prokaryotes and one superior animal which is another type of complex clone. Both organisms originated from a single cell which divided into two identical daughters which continued the pattern of division for numerous generations. During this period of multiplication, the cells of an animal, changed into more and more specialized sub-units as a result of the selective expression of their genes. In the old prokaryotic clone this is the result of billions of years of developing and synthesizing new genes, as well as of their opportunistic partitioning and redistributing by horizontal transfer among increasingly different strains. In an animal the initial cell (the fertilized egg) transmits to all its progeny cells the totality of its genes, most of which become permanently repressed depending on the type of differentiation, while only a small proportion (about 5%) are derepressed. There are as many combinations of derepressed genes in an adult animal as there are types of resulting specialized cells. The development from an egg into an adult is somewhat similar (on a much smaller scale and in an infinitesimal fraction of time) to the evolution of the prokaryotic clone into a global superorganism. The latter’s evolution is also its ontogenesis. Each of these two types of clones is therefore using its own genes very differently to give rise to specialized cells: in prokaryotes, this is the result of having different evolutions and adapting to new situations by gene exchanges and various cell associations. In an animal, variations on the choice of the genes to be derepressed leads to numerous types of “differentiated” somatic cells, a process that unfolds into adulthood. The global prokaryotic superorganism presumably reached its own type of adulthood about two B.Y. ago (Sonea and Panisset, 1976) in the sense that by then all the necessary and the occasionnally useful genetic blueprints were available for it. Members of the animal and plant kingdoms are mortal; the prokaryotic superorganism has been “immortal” for 3.5 B.Y. Its stability since the appearance of the eukaryotes is a surprising evolutionary fact. Instead of being taken over by the other, both eukaryotes and prokaryotes collaborated in many instances and this seems to have insured a longer and more successful life for both groups. This evolution of prokaryotes, however, was seriously limited in one way: it could not produce three-dimensional multicellular organisms with compact tissues. All their evolution had been in the direction of the smallest possible disjunct cells with a specialized and limited bio-energetic activity. They tended to remain physically separated in liquid or viscous surroundings. It is likely that for, possibly, the first 1 B Y. such was their condition of life. Later, one innovative evolutionary episode seems to have given birth to larger cells (predators on the more conventional type of prokaryotes). Surprisingly, these presumed predators do not seem to have had a profound impact as rivals or ennemies of the other prokaryotic type. Their number in natural habitats does not appear high nor significant. Predators are believed, however, to have participated in a fateful evolutionary event. Being the First prokaryotic large cells, they could accept and accomodate smaller, cooperating symbionts; this opened the door for a major transition, a type of evolution which had not been accessible to their ancestors.
7. Role of prokaryotes in the origin and subsequent evolution of eukaryotes
12Eubacteria and Archaea are not the only offsprings of the ancestor prokaryotes. Eukaryotes also seem to have originated from at least three different types of prokaryotic cells (Margulis, 1970) which, when united together, formed an entirely new type of cell. It was an “illegitimate” origin which did not follow the previous 2 B.Y. old general hereditary ways of the ancestors. It also represented the first (and possibly the last) successful permanent endosymbiosis exclusively involving prokaryotic cells (Margulis, 1993). The large cell which participated in this endosymbiosis was probably an Archaea and a predator (Guerrero et al, 1986; de Duve, 1996). One often overlooked aspect of this major biological event is that each of these permanently joined symbionts had a long uninterrupted past of participation as a member of close associations of strains in dynamic prokaryotic communities. Their long adaptation to life together in different, successful associations made them good candidates for putting together compatible groups of genes which contributed to the success of the earliest eukaryotes. Organisation of the nucleus followed later, starting with the fusion of the large replicon of the predator cell with that of a spirochete and the inclusion of their small replicons (Sonea, 1972). Once the nucleus and its membrane were later completed, early eukaryotic cells had enough intracellular genes of their own and no immediate need for visiting small replicons. Therefore, their descendants lost their bacterial ancestors’ ability to obtain genes easily from the global prokaryotic genome (Sonea and Panisset, 1976; Sonea, 1983). Newly independent (eukaryotic) cells became full unicellular organisms whose offspring could evolve in many directions without being restricted by the rules of team life which applied to their physically separated prokaryotic ancestors. Eukaryotes no longer had to collaborate with the global prokaryotic superorganism. They followed a “centrifugal” path of evolution which included the creation of a new biological category: the species, which, strictly speaking, does not exist among prokaryotes (Sonea and Panisset, 1983; Sonea, 1991; Mathieu and Sonea, 1996). In eukaryotes, the genetic isolation resulting from the early loss of small replicons and of the mechanism of transformation has been compensated for, but only in part, by the capacity to synthesize entirely new genes by serial random mutations (which, probably, had lost importance in prokaryotes approximately 2 B.Y. ago), and by Mendelian sexuality. As already stated, the latter is absent in prokaryotes. For hundreds of millions years eukaryotes conceivably remained unicellular and dependent on prokaryotes for food (Sonea, 1992). Later, one very important but often overlooked source of new genes for the developing eukaryotic world appeared. It consisted of highly innovative symbioses with complementary types of prokaryotic cells. This happened much later, as a large number of prokaryotes joined, as symbionts, different eukaryotes, starting with the protoctists, continuing with the ancestors of animals and, later, those of plants (Margulis and Fester, 1991). Such associations became easier for the eukaryotic cells, which could often integrate the future symbionts into their increasingly larger cells. Since the eukaryotes have never “discovered” the genes for photosynthesis, probably the most important prokaryotic bio-energetic contributors as symbionts to our biosphere have been the cyanobacteria. They participated successively in the origin of new, essential photosynthesizing entities by association with protoctists, thus producing many new and successful forms of life, the best known being the unicellular (eukaryotic) green algae which populate oceans and lakes. Much later, multicellular algae, lichens and plants were the result of symbioses between cyanobacteria and multicellular eukaryotes (fungi)(Honneger, 1991). These new associations made life possible and abundant under sunlight at different levels in the ocean or on the surface of soil or rocks of the continents. Multicellular, tri-dimentional and large beings began to populate the earth. Bryophytes and tracheophytes produced branching roots that increase access to water and minerals from below the surface of the soils. These are carried through conduits to vertical stems. This plant tissue supports the exposure to sunlight of fronds, leaves or needles containing chloroplasts (undisputable descendants of former cyanobacteria). Over the same area, plants expose to sunlight a much larger surface than the previous, thin prokaryotic cover on the soil. Increasingly complex plants prospered and around 450 million years ago they covered much of the continents with abundant growth. Benefiting from this rich new biomass, soil bacteria and land-dwelling animal species also evolved. This put an end to the three billion years of practically lifeless history of the continents. Thus, a most fateful evolutionary innovation on the continents, and a giant evolutionary transition were the extension of photosynthetic cyanobacteria as symbionts to the third dimension by multicellular tissue. After this most important event in the development of energy capture and transfer, the symbiosis between nitrogen fixing bacteria (e.g. Azobacter aerogenes) and many types of plants, particularly the legumes, also contributed to increase the biomass on the continents. A large number of animal species also need prokaryotic symbionts (mostly ecto) to survive in oceans or on continents (Margulis and Fester, 1991). As already seen, the ruminants (cattle, sheep, deer, camels, etc.) use assimilable short chain hydrocarbons obtained in their rumen from cellulose by the concerted activity of a complex team of bacteria and ciliates. Termites use a similar arrangement and many insects and marine animals also depend on the metabolic versatility of symbiotic prokaryotes. A large proportion of all other animals which have no such special capacities are dependent on prokaryotic teams in their alimentary tract, without which they cannot live normally. Experimentally obtained germfree animals may present serious (often deadly) health problems during their abnormal life. The prokaryotic teams of all normal alimentary tracts exert a favorable influence, often a necessary one for the well-being and survival of animals (Raibaud and Ducluzeau, 1984). Many successful symbioses are also known between fungi and prokaryotes (Kendrick, 1991). In the course of their evolution prokaryotes have built genetic variation by countless synthesis of new genes covering practically all the possible ways of unicellular life on our planet. Thereafter, redistribution of the genes from that pool to different strains has led to a giant common global genome for all prokaryotes. The potentialities of this genome, as we mentioned, is also made partially accessible to eukaiyotes through associations and symbioses. Prokaryotes have been determinant in the evolution of all beings on our planet. Many eukaryotes survived and prospered because of associations with them. The formers’ option in favor of the Darwinian struggle for life lead to the successive extinction of numerous species, but the net result of their associations with prokaryotes proved decidedly positive.
8. The prokaryotes were and remain the most influential biological factor in the development and maintenance of our biosphere
13The biosphere may be much better understood when the primordial and central role of the all pervading and stable prokaryotic world is given its true importance. It has evolved as a balanced, life-supportive, global entity which had, without other biological interference, a very long stretch of time to organize itself by trial and error, constantly correcting and adjusting by positive competition. During their long solitary evolution, the prokaryotes have succeeded in reaching a much greater variety of metabolic and energetic capacities which offered them wider opportunities in a large choice of niches. They “discovered” many types of energy channeling and liberating (respiration) reactions including that which the eukcaryotes have inherited from the prokaryotic ancestor of the mitochondria. The variety and richness of biochemical reactions and pathways in prokaryotes explain the abundance and success of the successive genetic innovations realized in eukaryotes following a variety of symbioses with complementary prokaryotes. Moreover, all along their 3.5 B.Y. of life on Earth, prokaryotes had a most influential and favorable ecological impact on our entire biosphere, keeping it a stable and life-promoting milieu just like a superior animal keeps its “milieu intérieur” stable during its entire life.
14The evolution of life on our planet, which previously seemed to biologists to be an entirely centrifugal phenomenon, has instead yielded a balanced blossoming of our biosphere, under the positive stabilizing influence of the global prokaryotic superorganism which also supports the eukaryotes (their profoundly modifïed offspring) and is reciprocally supported by them.
15From the origin of life on Earth, in the case of prokaryotes for a period of about 2 B.Y., evolution consisted mainly in enriching the clonal prokaryotic population and the homeostasis of the biosphere. The genes and strains that became lost and extinct during that period were probably few. When eukaryotes appeared as predator cells they started the Darwinian type of evolution at the cost of successive extinctions of different types, as a result of fierce competition. However, in parallel, innovative genetic improvements happened, presumably in most surviving eukaryotes through the agency of symbioses with complementing prokaryotic strains. This capital participation in eukaryotic evolution, a direct consequence of the prokaryotes’ ability to evolve and progress through associations, has been acknowledged and accepted belatedly, and only following major efforts, particularly those of Lynn Margulis to awaken scientific and public interest in this neglected aspect of evolution (Margulis and Fester, 1991).
16If, as we believe, a large proportion of the new genes were saved during the 3.5 B.Y. of prokaryotic evolution, it follows that a giant increment in the pool of useful genetic information, of time-tested bioenergetic formulas, took place. By allowing this rich collection of genes and strains to adjust and survive instead of becoming extinct, the prokaryotic System has accumulated and still keeps available for symbiotic associations a huge amount of hereditary information. It has also contributed to accelerate the speed of eukaryotic changes. In considering the development of our rich biosphere and the maintenance of its stability one must not forget two different and very important moments of prokaryotic evolution. The first was preparatory, built up stability, and was a purely prokaryotic episode. The second combined the continuity and the richness of the prokaryotes’ existence with the less secure Darwinian kind of life of eukaryotes. Collaboration, in a parallel non-Darwinian fashion, between the two domains (the prokaryotic global System and the eukaryotes) helped diversify, enrich and stabilize our present-day biosphere.
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