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The Biggest Evolutionary Jump: Restructuring of the Genome and Some Consequences © P 2010 ÖÈÒÎËÎÃÈß Òîì 52, ¹10 THE BIGGEST EVOLUTIONARY JUMP: RESTRUCTURING OF THE GENOME AND SOME CONSEQUENCES © P. Omodeo Dipartimento di Scienze Ambientali, Universita di Siena, Italy; e-mail: [email protected] Ï. Îìîäåî Âåëè÷àéøèé ýâîëþöèîííûé ñêà÷îê: ðåñòðóêòóðèçàöèÿ ãåíîìà In this paper, the evolution of the cell is investigated till the level of complexity obtained by protists. Part- icular attention is paid to the genomic compartment and to the question: why has the genome of prokaryotes re- mained so small over more than 3 billion years and more than 3 trillion generations? Constraints on their geno- me evolution may be attributed mainly to: 1) the fact that repetitions of nucleotide sequences longer than 12 to 15 bp are forbidden according to Thomas’ principle; 2) the high cost of the control of gene expression by means of regulatory proteins: this cost increases exponentially with chromosome elongation. The formation of chroma- tin, i. e. the wrapping of DNA around the nucleosomes, removed these constraints and allowed the increase of the genome and especially of the redundant sequences of DNA, whose role is discussed. The transformation and growth of the genome generated a trend towards separation of the various physiological functions and of their control. The formation of a nuclear envelope may have begun with the advent of mitosis, which replaced the simple but delicate device of pushing the newly formed DNA into the daughter prokaryotic cells. An increase of the O2 concentration in waters stimulated further evolution: the new cell established symbiosis with a bacterium capable of protecting against peroxides and performing aerobic respiration. The increased O2 concentration also led to the production of sterols, which became an important component of the cell membrane. The mutual adap- tation of cells belonging to different domains involved further modifications, leading to the birth of proto-euka- ryotic cells and facilitating the establishment of further symbioses with photosynthetic cyanobacteria. Pro- to-eukaryotic cells were devoid of motility and contractility, as are the cells of red algae, fungi and Zygnemata- les today. Both these faculties evolved when the protist eukaryotic cell acquired flagella, cytoplasmic contractility and sensors to govern them. K e y w o r d s: ñell evolution, genome evolution, constraints on genome growth, redundant DNA, pro- to-eukaryotes, protist motility and sensors. The prokaryotic genome and its duplication point of the wall; hence, the entire process determines some aspects of cell morphology, particularly its length. The pro- The bacterial genome typically consists of an annular or cess is the same in the archaean cell, but in species without a linear chromosome, usually 0.25—2.0 mm long, formed by cell wall or with a deformable wall the centres (or centre) of one-nine million base pairs (bp) (fig. 1). The average number DNA duplication can find stable support only in the structure of nucleotides per gene is usually higher than 1000. In bacte- of the cytoskeleton, and the lack of bilateral symmetry in ria that became endocellular parasites, the size of the chromo- some types of cells seems to make the process more preca- some is about an order of magnitude smaller, even in phyloge- rious. netically distant taxa. In procells with complex metabolic acti- The linear chromosomes of the procell divide in another vities and complicated shapes (cyanobacteria, streptomycetes manner because the DNA polymerase works in two different and others), the genome size can be up to 9 Mbp and beyond. ways on the two filaments of the double helix, which have op- Linear chromosomes are more common in such cases. posite polarity. Since the terminal tract of the nucleotide chain The genome of archaea differs significantly from that of cannot be duplicated entirely by the DNA polymerase, the li- bacteria: the nucleotide number is smaller by one third on ave- near chromosome would lose the terminal nucleotides and fa- rage; the number of nucleotides per gene is often less than tally shorten at each reproductive cycle. However, the enzyme 1000. It also differs in its relationships with histone molecu- telomerase adds a long appendix formed by repetitive les, which in some archaea form nucleosomes (Pereira et DNA sequences to the end of the chromosome. This appen- al., 1997), globular masses around which the DNA entwines, dix, called telomere,isnotentirely replicated by DNA po- plausibly for defence against heat denaturation. lymerase and is repaired by telomerase at each reproductive In the active procell, the chromosome duplicates continu- cycle. Thanks to this mechanism, the chromosomes are comp- ally and each new copy is apparently pushed by the replica- letely replicated without losing genetic information. In any ting apparatus to one of the two poles of the cell (which is a case, when the two new coils have reached separate centres in couple of mm long) without the thin filaments becoming en- the procell, cytodiaeresis takes place, involving the growth of tangled in the limited space. The operation proceeds in a surp- a diaphragm formed by the plasma membrane and cell wall (if risingly precise manner thanks to the activity of the two cent- it exists). During this process, mRNA transcription is not sus- res (or centre) of DNA polymerase (a multienzyme «replicati- pended, even though it must undergo momentary interrup- on machine») and to the fact that each centre is connected to a tions. 797 798 Ï. Îìîäåî Fig. 1. Comparison of the genome size of archaea and bacteria. Why does the genome of prokaryotes remain The importance of Thomas’ principle becomes more evi- so small? dent when paraphrased in the following manner: in the proka- ryotic chromosome, the repetition of DNA lengths containing Why has the prokaryotic genome remained so small thro- 12 or more nucleotides is forbidden; otherwise, the chromoso- ughout 3.8 billion years and at least a thousandfold higher me becomes unstable and its functionality is compromised. number of generations? This question comes to the fore insis- The situation postulated by Thomas’ principle finds an analo- tently in the mind of the biologist concerned with comparative gy in what philologists call a «jump from like to like», or ho- cytology. Why has the procell remained so small and simple moteleut: when on a page to be copied, one or more words are in this long period of time? This question is also raised by tho- se concerned with evolution and who marvel that, in less than half that time and an incomparably smaller number of genera- tions, eukaryotes showed a flowering of taxa and immensely larger forms of life. An answer to these questions can be found in a paper by Thomas (1966) dealing with recombinant DNA. He used phy- sico-chemical and biological evidence to formulate the follo- wing principle: «If freely recombining DNA molecules conta- in repetitious recognition lengths, they will be unstable under recombination» (p. 329). With the aid of collaborators from different scientific fields (see his appendixes), Thomas estab- lished that the repetitious recognition lengths should contain «at least twelve nucleotides» (p. 326). That implies that the chromosome, folding up inside the cell, can bring the two re- peated sequences into contact; because they have complemen- tary structures, they will adhere closely and the tract between Fig. 2. If A—C sequence of 12—15 base pairs (or longer) is repea- the two equal sequences can become detached and lost or un- ted along a bacterial chromosome, these sequences may come into dergo an «inversion» that compromises its functionality contact and adhere, forming a ring that may become detached; the- (fig. 2). refore, the chromosome becomes unstable (from: Thomas, 1966). Âåëè÷àéøèé ýâîëþöèîííûé ñêà÷îê: ðåñòðóêòóðèçàöèÿ ãåíîìà 799 repeated not far from each other, the copyist omits the interve- synthetic apparatus are present in several grouped copies ning phrase (Omodeo, 1975). (Grossman et al., 1993; Kirby, 2004). At the time he wrote, Thomas had only one sure datum A third difficulty arises from data emerging from the se- concerning the instability of the chromosome of a mutant stra- quencing of prokaryotic genomes: in about 15 % of the cases, in of Escherichia coli in which a repetition had appeared. La- the nucleotide number exceeds the value considered compa- ter, other confirmatory cases came to light. Hansche (1975) tible with Thomas’ minimum length. reported: «However, duplicate genes that code for enzymes in It is possible that these exceptions have explanations that prokaryotes are generally unstable in the laboratory (Jackson, do not compromise Thomas’ principle. However, since we Yanofsky, 1973) and are unknown outside the laboratory now have about a thousand complete sequences of bacterial (Heyemen, Rosenberg, 1970)». genomes, it would be advisable to test the validity of the prin- If the prokaryotic chromosome cannot exceed this num- ciple and investigate if there are mechanisms that allow ex- ber of base pairs, we can say that — assuming there is propor- ceptions. tionality between the complexity of the organism and the size of its genome — prokaryotes cannot go further than the comp- lexity attainable with only 1—2 megabytes of genetic infor- Control of the distribution of genetic information mation. This notion explains why there is such economy of and its problems codification in the prokaryotic genome and implies, above all, that the appearance of more complex cells, such as eukaryo- Examination of the bacterial genome reveals other inte- tes, was only made possible by a profound restructuring of the resting facts that supplement and confirm those discussed ear- genome. Indeed, the facts bear this out. lier. At the same time, they provide interesting perspectives on the evolutionary innovations which — after two billion years of history — allowed the prokaryotic cell to evolve into Implications of the principle of non-repeatability the eukaryotic cell and initiate its subsequent tumultuous pro- of DNA sequences in prokaryotes gress.
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