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Journal of Cosmology, 2010, Vol 10, 3418-3445. JournalofCosmology.com, August, 2010 Archae, Bacteria, Viruses and Horizontal Gene Transfer Rhawn Joseph, Ph.D.
1. ORIGINS OF LIFE When life first took root on Earth is unknown. Because of the incessant astral bombardment from space during the first several hundred million years, surface features including rocks, were pulverised erasing any and all evidence of life. And yet, when rocks first began to reform 4.2 billion years ago (bya), there is evidence of biological activity (Nemchin et al. 2008; O'Neil et al. 2008), demonstrated, for example, by very high concentrations of carbon 12, or "light carbon" which is typically associated with microbial life (Nemchin et al. 2008). How did these early Earthly life forms arise? And did they include archae, bacteria, and eukaryotes? Joseph and colleagues (Joseph 2009a; Joseph and Schild 2010ab; Joseph and Wickramasinghe 2010) have detailed and reviewed a large volume of evidence suggesting life arrived here encased in the debris which formed the surface of this planet. By contrast, Russell and colleagues (Milner-White and Russell 2010; Nitschke and Russell 2010; Russell and Kanik 2010) have presented an impressive body of data indicating Earthly life (and even extraterrestrial life) may have been fashioned by the fortuitous mixture of the necessary chemicals within a watery thermal environment. Certainly early Earth was hot. Likewise, evidence of the earliest life was left in rocky formations bathed in water, i.e. banded iron formations consisting of alternating magnetite and quartz dated to 4.28 bya (O'Neil et al, 2008). More definitive evidence of life has been dated from 3.8 to 3.9 bya, and includes carbon-isotopes discovered in quartz-pyroxene rocks on Akilia, West Greenland dated to 3.8 BY, and within a phosphate mineral, apatite, which includes tiny grains of calcium and high levels of organic carbon; the residue of photosynthesis, oxygen secretion, and thus biological activity (Manning et al. 2006; Mojzsis et al. 1996). In addition, microfossils resembling yeast cells and fungi were discovered in 3.8 billion year old quartz, recovered from Isua, S. W. Greenland (Pflug 1978). Evidence of biological activity including photosynthesis was also discovered in this area dated from the same time period (Rosing 1999, Rosing and Frei 2004). It appears that Earthly life had begun to proliferate on the surface of this planet between 4.2 to 3.8 bya. Further, it can be deduced that these first Earthly creatures included archae, bacteria, and possibly (by 3.8 bya) single celled eukaryotes, all of which may have been accompanied by viruses (Joseph 2009a; Joseph and Schild 2010a,b). Viruses are found in association with and outnumber archae and bacteria on ratios ranging from 1 to 10, and 1 to 100, and are sources of genes and DNA which directly benefit or improve the functioning of the recipient (Sullivan et al., 2006; Williamson et al., 2008). Presumably, in the chain of life, eukaryotes emerged last, after viruses, archae and bacteria. Certainly life did not spring to life as a fully formed cell. Woese (2004) has proposed that initial proto cells may have lived together and repeatedly swapped and shared genes via horizontal gene transfer (HGT). "Eventually this collection of eclectic and changeable cells coalesced into the three basic domains known today" (Woese, 2004). According to this proposal, bacteria, archaea and eukaryotes may have been established at around the same time and differentiated from a diverse collection of proto-cellular ancestors. However, it also seems reasonable to assume there were stages of development leading from chemicals to proto-cells, to single celled life, and then to multi-cellularity and increasing complexity. Therefore it is possible this prebiotic process resulted in the eventual establishment of viruses, archae and bacteria, prior to the evolution of a more complex cell represented by the first eukaryote. This assumption is also supported by genetics (Joseph 2009b). Battistuzzi and Hedges (2009), based on a genomic analysis, concluded that both bacteria and archae were present on this planet over 4 billion years ago. Therefore prokaryotes and viruses may have been present between 4.2 to 4 bya, thus 400 to 200 million years before singled celled eukaryotes (i.e. yeast cells and fungi discovered by Pflug (1978) in 3.8 billion year old quartz). It is possible that eukaryotes emerged from the same diverse pool of proto cells which produced the first prokaryotes and their DNA. However, this does not mean they all appeared at the same time. Instead, based on genetics, it appears that viral and prokaryote genes preceded and may have triggered the creation of the eukaryote genome (Joseph 2009b). As detailed in this paper, the first eukaryote may have been fashioned when certain archae, bacteria, and viruses exchanged and shared genes and formed symbiotic/parasitic relationships, thus creating a combined genome within a single cell (the first proto-eukaryote) which later came to be comprised of compartments consisting of the remains of stripped down prokaryotes (Joseph 2009b; Joseph and Schild 2010b). As some single celled eukaryotes acquired additional symbiotic partners and genes donated by archae, bacteria, and viruses, they became multi-cellular. However, many prokaryotic genes, once donated, were not replaced, thus insuring that eukaryotes and not prokaryotes would evolve (Joseph 2009b). 2. EUKARYOGENESIS AND HORIZONTAL GENE TRANSFER Bacteria, archae, and viruses serve as genetic messengers and are ideally suited for acquiring and making copies of genes, transferring these genes to other species, as well as accepting foreign genes, and then later donating and transferring these genes, including their own genes, to yet other organisms (Forterre 2006; Hotopp et al., 2007; Iyer et al., 2006; Nikoh et al., 2008). Genomic analysis has demonstrated that genes are commonly shared between bacteria and archaea (Aravind et al, 1998; Nelson et al., 1999; Koonin 2009a,b), between prokaryotes and eukaryotes (Hotopp et al., 2007; Nikoh et al., 2008; Martin et., al., 2002; Nikoh et al., 2008), and between viruses and prokaryotes (Lindell et al., 2004; Sullivan et al., 2006), and viruses and eukaryotes (Conley et al., 1998; López-Sánchez et al., 2005; Romano et al., 2007). This is accomplished via horizontal gene transfer (HGT). Even introns, ribosomal proteins and RNA polymerase subunits are subject to HGT (Brochier et al., 2000; Iyer et al., 2004) and the same is true of regulatory genes, many of which have been inserted into the prokaryotic and eukaryotic genome by viruses. For example, group II introns and ribozymes which are derived from viruses are found in the genomes of archae, bacteria, and eukaryotes (Dai and Zimmerly 2003; Dai et al., 2003). 3. VIRUSES AND HGT As summed up by Koonin (2009b) "in prokaryotes, the interaction between bacterial and archaeal chromosomes and selfish replicons is so intensive, and the distinction between chromosomes and megaplasmids is blurred to such an extent that chromosomes are, probably, best viewed as islands of relative stability in the turbulent sea of mobile elements." However, prokaryotes also obtained genes from viruses, which in turn may have been transferred to and inserted into the genomes of eukaryotes by viruses and prokaryotes. Similar transfer mechanisms played a role in eukaryogenesis and the evolution of multi-cellular life. For example, viruses have acted as a store-house for genes which code for photosynthesis (Lindell et al., 2004; Sullivan et al., 2005, 2006) including photoadaptation and the conversion of light to energy (Williamson et al., 2008). Some of these viruses (e.g., cyanophages) provide cynobacteria with genes which augment the host photosynthetic machinery during periods of stress, insufficient nutrients, or reduced sunlight (Sullivan et al., 2006). When the excess genes are no longer necessary, they are transferred from the bacteria genome back to the virus genome for storage (Lindell et al., 2004; Sullivan et al., 2005, 2006). However, as cyanobacteria have also provided genes to the eukaryotic genome, including those coding for photosynthesis, it is likely that some of these donated genes may have originated in viruses. Viruses maintain a large reservoir of excess genes, and viral bacteriophages commonly invade bacteria and transfer genes which improve the functioning of the host (Sullivan et al., 2006; Williamson et al., 2008). These enhancements include carbon metabolism during the dark cycle of host cells (Sullivan et al., 2005), and effect a variety of cellular processes such as vitamin B12 biosynthesis (cobS), host stress response (small heat shock proteins), antibiotic resistance (prnA) nitrogen fixation (nifU) and carbon metabolism (Williamson et al., 2008). Therefore, viruses may directly participate in nitrogen fixation and the carbon cycle (Evans et al., 2009). Yet others provide genes to eukaryotes (López-Sánchez et al., 2005; Romano et al., 2007), and these genes also confer advantages to the host species and appear to have played a major role in evolutionary transitions. The eukaryotic genome, including that of humans, not only contains DNA inserted by prokaryotes, but genes inserted by viruses (Conley et al., 1998; López-Sánchez et al., 2005; Romano et al., 2007). In fact 8% of the human genome consists of around 200,000 endogenous retroviruses (IHGSC 2001; Medstrand et al., 2002), and 3 million retro elements (Medstrand et al., 2002), and some of these retroviruses are still active (Conley et al., 1998; Medstrand and Mager, 1998). There has been extensive HGT between viruses, prokaryotes, and eukaryotes over the evolutionary history of this planet. Presumably, HGT was also a fact of life prior to, and after life took root on Earth 4.2 bya (Joseph 2009b; Joseph and Schild 2010a,b; Joseph and Wickramasinghe 2010). 4. ARCHAE, BACTERIA, VIRUSES AND UNICELLULAR EUKARYOGENESIS Based on genomic analysis, it appears the first Earthly unicellular eukaryotes were fashioned when genes from archae, bacteria, and viruses were exchanged via HGT and then combined thereby inducing eukaryogenesis and giving rise to the eukaryote genome (Feng et al., 1997; Hedges, 2002; Hedges et al. 2001; Martin and Muller, 1998; Rivera and Lake 2004). These genes subsequently underwent repeated single gene and whole genome duplications, perhaps in response to environmental triggers and regulatory genes inserted by viruses, thereby expanding the genome and leading to evolutionary innovation and increased complexity (Joseph 2009b). Thus, following HGT into a pre-eukaryotic host, unicellular eukaryotes were fashioned, and following additional HGT episodes they became multicellular and then increasingly complex and intelligent. The alternative explanation is that these genes were transferred into the genome of unicellular eukaryotes which had evolved from an interacting colony of proto cells as envisioned by Woese (2004). More specifically, there is genetic evidence supporting the possibility that an ancient photosynthetic archaea, or possibly a methanogenic archae that feasted on methane, may have fused with a photosynthetic Cyanobacteria (Joseph 2009c; Rivera and Lake 2004), or some other species of bacteria, thereby producing a combined genome and triggering eukaryogenesis (Hedges et al., 2001; Martin and Koonin 2006; Martin and Muller, 1998). If correct, this could account for the simplified eukaryotic microfossils dated to 3.8 bya (Pflug 1984), and which presumably evolved 400 million years after prokaryotic life became established on this planet 4.2 bya. Presumably bacterial ancestors extracted hydrogen from water, released oxygen as a waste product (Davidson 2001), and supplied hydrogen to a methane-eating archae (Martin and Muller, 1998; Rivera and Lake 2004). These first Earthly Methanogens may have reacted H2 with CO2 to obtain energy and make organic matter. As oxygen levels were negligible at best, these creatures may have engaged in anoxygenic photosynthesis, using H2 in lieu of an oxygen ‘acceptor’ (Olson 2006; Sleep and Bird 2008). Yet other microbes may have produced, incorporated and then employed sulphides and ferrous as oxygen acceptors (Olson 2006; Sleep and Bird 2008); hence, the presence of iron banded formations dated to 4.28 bya, and which appear to be associated with biological activity (O'Neil et al. (2008). Therefore, the first Earthly eukaryotes which acquired these prokaryotic genes via HGT, were able to survive on hydrogen and methane, or iron and sulphides, despite the initial lack of free oxygen. Hence, the first Earthly eukaryotic cells may have emerged as a result of HGT and a symbiosis between the genomes of methane or sulphide eating archaeon and a hydrogen or iron eating bacterium.
As noted, it is possible that archae, bacteria, and single celled eukaryotes may have arisen from colonies of diverse proto cells, and it was the subsequent invasion of unicellular eukaryotes by prokaryotes and viruses, which triggered multi-cellularity. For example, several species of unicellular eukaryotes, such as the microsporidians, metamonads, and archamoebae, possess mitosomes but not mitochondria (Bakatselou et al., 2003; Tovar et al., 1999; Williams et al., 2002). As will be detailed, mitochondria may be a genetically stripped down symbiotic bacteria which invaded eukaryotes when Earth became sufficiently oxygenated. Coupled with data based on rRNA analysis of phylogenetic trees, it seems plausible that unicellular eukaryotes appeared before this bacterial genetic invasion and the origin of mitochondria. In addition, because unicellular eukaryotes possess organelles of bacterial descent (Gray et al., 1999), this suggests that unicellular eukaryotes were not created by, but were invaded by and were the recipients of HGT from prokaryotes, and this is what led to multi-cellularity and the evolution of mitochondria. However, this scenario does not rule out the possibility that unicellular eukaryotes were first fashioned when prokaryotes and viruses combined genes; and this is because not all genes are activated but may remain suppressed for hundreds of thousands and hundreds of millions of years before being triggered by genes inserted by viruses or the changing environment (Joseph 2009b,c). This may also explain why some unicellular eukaryotes contain mitosomes which are genetically related to mitochondria. In other words, the combined genes which gave rise to the first eukaryotes may have contained the silent genetic instructions for the metamorphosis of mitochondria.
5. PROKARYOTIC AND VIRAL GENES AND EUKARYOGENESIS
The ancestral viral and prokaryotic genes and genetic elements which were combined and donated included regulatory genes, introns, transposable elements, and all the genetic machinery necessary for fashioning multicellular eukaryotes and their genomes and to enable their evolution. Further, prokaryotes and viral agents provided eukaryotes with the regulatory elements controlling gene expression and which duplicate individual genes and the entire genome thereby enabling the eukaryote gene pool to grow in size (Joseph 2009b).
Eukaryotes received from prokaryotes a variety of genes, proteins and transcription enzymes which have played a major role in genetic continuity, gene duplication, and synthesis and transcription of long DNA molecules, thus shaping and guiding what has been called evolution. These elements and genetic mechanisms, including RNA polymerase, replicative DNA polymerase, introns and transposable elements, enabled genes and entire genomes to be duplicated and to expand. Regulatory genes inserted by viruses and prokaryotes, also guaranteed genetic linkage between genes, and insured accurate replication and transmission of genetic information following gene or whole genome duplication (reviewed by Joseph 2009c).
Genome sequencing has revealed an extensive conservation of the same repertoire of genes coding for core cellular functions in the genomes of prokaryotes and eukaryotes (Koonin et al., 2004; Koonin and Wolf 2008). A core set of approximately 70 genes contributed by archae and bacteria have been identified. These have been conserved and passed down, without deletion, for billions of years, and make up around between 1% to 10% of the genes in the genomes of all multicellular life (Koonin 2003; Harris et al., 2003; Charlebois and Doolittle 2004; Koonin and Wolf, 2008).
These conserved genes, proteins, and gene sequences, include those governing translation, the core transcription systems, and several central metabolic pathways, such as those for purine and pyrimidine nucleotide biosynthesis. Moreover, protein sequence conservation extends from mammals to bacteria thus demonstrating their great antiquity (Dayhoff et al., 1974, 1983; Eck and Dayhoff 1966).
Between 2150 to 4137 orthologous gene sets are highly conserved and can be traced back to the last common ancestor for eukaryotes (Makarova et al., 2005). And often these orthologs express or perform the same function regardless of species. In the human genome, these ultraconserved elements often overlap introns or genes involved in the regulation of gene transcription and expression. The introns also have as their source, prokaryotes and viruses.
6. INTRONS AND EUKARYOGENESIS
Introns play a significant role in gene regulation, gene duplication, exon-splicing, and signal which stretches of nucleotides should or should not be expressed. If the first eukaryotes emerged when genes were combined, introns must have been part of the mix. Prokaryotes and viruses (Joseph 2009c) must have flooded the eukaryotic genome with introns and transposable elements at the earliest stages of eukaryogenosis (Cavalier-Smith 1991; Sharp 1991; Stoltzfus 1999), and then periodically thereafter as the first Earthly multi-cellular eukaryotes were fashioned (Martin and Koonin 2006; Rogozin et al., 2005). A massive initial influx of introns would also explain why ancient eukaryotes (Roy 2006) including the last common ancestors for eukaryotes, possessed high intron densities (Carmel et al., 2007; Csuros et al., 2008; Roy 2006). However, that common ancestor must have obtained these introns from viruses and prokaryotes.
All eukaryotes whose genomes have been sequenced, including parasitic protists, have been shown to possess introns (Nixon et al. 2002; Simpson et al. 2002; Vanacova et al. 2005). Even the simplest of eukaryotes contain introns as well as spliceosomal proteins within their genomes (Collins and Penny 2005). After the initial invasion, introns then continued to be donated or duplicated as eukaryotes evolved. It can be concluded that introns accompanied the massive influx of genes at the outset of eukaryogenesis and thus at the earliest stages of eukaryote evolution.
Specifically ribosomal introns and protein sequences which circulate in the cytoplasm appear to have originated in the archae genome, and were donated to eukaryotes via HGT, as there is a specific affinity between eukaryotic genes and their orthologs from archae (Lake et al. 1984; Lake 1988; 1998; Rivera and Lake 1992, 2004 Vishwanath et al. 2004). By contrast, mitochondrial ribosomes and a significant number of introns are considered to be of bacterial origin (Kenmochi et al., 2001); a product of endosymbiosis (Dyall et al., 2004; O'Brien 2002). Yet other introns were inserted by viruses. Even those inserted into the eukaryotic genome by bacteria and archae, may have been stored in and obtained from the viral genome.
Viruses act as gene depositories and can donate regulatory elements to prokaryotes who in turn may horizontally transfer these genetic elements to eukaryotes (reviewed by Joseph 2009b,c). Viruses can also directly insert regulatory elements into the eukaryotic genome, including the genome of humans. For example, group II introns and ribozymes which are derived from viruses are found in the genomes of archae, bacteria, and eukaryotes (Dai and Zimmerly 2003; Dai et al., 2003), and retroviruses have continually inserted genes and introns into the primate lineage leading to humans (IHGSC 2001; Loppez-Sanchez et al., 2005; Medstrand et al., 2002; Romano et al., 2007).
Group II introns are highly mobile retroelements (Belfort et al., 2002) and include retrotransposons, and are progenitors of nuclear spliceosomal introns (Cavalier-Smith 1991; Sharp 1991). Retroelements have as their source, retroviruses. These retroelements can splice together exons (Michel and Ferat 1995), thereby creating genes from genes. Spliceosomes and spliceosomal introns are responsible for splicing out introns and transposable elements, and insuring that the genetic sequences in introns are not translated into proteins. These introns regulate gene expression and help guarantee that only designated exons are translated and transcribed (Roy and Gilbert, 2006).
Archae, bacteria, and viruses, therefore, were a major source of introns and ribosomes, with viruses also contributing introns, transposable elements, and other regulatory genes. These genes interacted in networks, regulating gene expression and silencing, as well as gene duplication, the splicing together of new genes from old genes, and the production of specific protein products. Therefore, it can be deduced that bacteria, archae, and viruses contributed and combined genes with a proto-eukaryote, whereas viruses (and prokaryotes) inserted regulatory elements which duplicated and activated specific gene sequences thereby triggering eukaryogenesis.
Thus, following the initial donation of introns to eukaryotes, new genes were assembled from old genes (De Souza et al., 1996, 1998, 2003; Fedorov 2001, 2003; Long et al., 1995; Roy 2003; Roy et al., 1999, 2001, 2003), albeit in a highly regulated, coordinated, purposeful fashion, so as to produce specific protein products, thereby promoting eukaryogenesis, multi-cellularity, and evolutionary metamorphosis. The genome began to increase in size and complexity and genes expressed new, albeit precoded functions; which gave rise to new tissues, organs, and the evolution of new species (Duret 2001; Comeron and Krietman 2000; Joseph 2009b,c). Single celled eukaryotes, therefore, became multi-cellular, diversified, and evolved.
7. EUKARYOGENESIS: PROKARYOTIC OPERATIONAL AND INFORMATIONAL GENES
Broadly considered, the eukaryote genome contains two sets of functionally distinct prokaryotic genes: operational and informational; one set derived from archaea and the other from bacteria (Esser et al. 2004; Rivera and Lake 2004).
It is now well established that archae provided the eukaryote genome with genes for information processing and expression (translation, transcription, replication, and repair), whereas bacteria provided operational genes responsible for the membrane system, the cytoskeletal system, and metabolic activity. The combination of these two sets of genes, informational and operational, contributed significantly to eukaryogenesis and the evolution of eukaryotic complexity.
Specifically, highly conserved eukaryotic protein-coding genes, particularly those involved in translation, transcription, replication, repair, and thus information-processing systems, are derived from archaea. Informational genes interact with nongene products such as ions, small molecules (GTP, GDP, etc.), and numerous proteins. For example, during assembly a single informational subunit protein interacts with four to five other ribosomal gene products (Jain et al., 1999). An operational gene protein may interact with just one. In fact, over 350 eukaryotic genes have been identified that are of apparent archaeal origin and which were acquired via early horizontal gene transfer (Yutin et al., 2008).
Studies have shown that operational genes have been repeatedly and continuously horizontally transferred over the course of evolution (Jain et al., 1999). However, these same eukaryotic/archae genes are not found in the bacteria genome. Likewise, the key proteins involved in DNA replication are homologous in archaea and eukaryotes but are not related to the proteins employed by bacteria (Leipe et al. 1999). In fact, an analysis of introns, transposable elements, and especially ribosomal structure and ribosomal protein sequences indicates a specific affinity between eukaryotic genes and their orthologs from archae (Lake et al. 1984; Lake 1988; 1998; Rivera and Lake 1992; Rivera and Lake 2004; Vishwanath et al. 2004) as well as viruses (Conley et al., 1998; López-Sánchez et al., 2005; Romano et al., 2007). Thus, archae (along with viruses) provided numerous genes to the eukaryotic gene pool and likely did so at the onset of eukaryogenesis.
Conversely, hundreds of genes are homologous in eukaryotes and bacteria but are not found in archaea. These includes genes producing the principal enzymes of membrane biogenesis (Pereto et al. 2004). Bacteria also provided genes for the creation of the eukaryotic membrane system, the inner cytoskeleton, complex metabolic activity, metabolic enzymes, and which serve operational functions (Yutin et al., 2008; Esser et al. 2004; Rivera and Lake 2004). These donated genes and proteins directly influence metabolism and the ingestion and excretion of various waste products. Some of these waste products would eventually build up in the environment and act on gene selection, activating silent genes donated to the eukaryotic genome by prokaryotes and promoting evolutionary metamorphosis (Joseph 2009b, 2010).
Further, the transfer of these genes may have been made possible with the aid of viruses which selectively transferred regulatory genes into the eukaryotic genome (Joseph, 2009b,c, Joseph and Wickramasinghe 2010). Coupled with the fact that transferred genes were not replaced in the prokaryote genome, these donated viral/prokaryote genes, in combination, would have significantly affected the evolutionary development of eukaryotes including the transition from pre-eukaryotic cell to single cell to multi-cell, whereas in contrast, prokaryotes would not be subjected to the same genetic influences.
8. ARCHAE/BACTERIA SYMBIOSIS AND EUKARYOTIC COMPARTMENTALIZATION
Donation or combination of bacteria, archae, and viral genes to create the first Earthly multi-cellular eukaryote, resulted in approximately 60 major innovations (Cavalier-Smith, 2009; Joseph 2009b,c). These included the eukaryotic cytoskeleton and a complex internal endomembrane system where lipids and proteins are synthesized and which allow eukaryotes to engage in phagotrophy and digestion which provided additional energy and nutrition to the host. Thus after these genes were combined, eukaryotes began to increase in complexity whereas the expansion in size enabled them to form endosymbiotic relationships with smaller microbes.
Because the donation of these genes were from 3 separate sources which were combined in the eukaryotic genome, this ensured that the interactions of these genes, and subsequent evolutionary development, would be restricted to eukaryotes. For example, the eukaryotic cytoskeleton and endomembrane system was no longer compatible with the normal processes of bacterial division and reproduction. This led to the evolution of the nucleus and mitotic cycle and then the metamorphosis of mitochondria which originally may have been an endosymbiotic bacteria.
Initially, the first single celled eukaryotes, like prokaryotes, likely lacked a protective nucleus. In consequence, eukaryotes were able to easily incorporate bacterial and archael genes within the eukaryotic genome (Dyall et al., 2004; Margulis et al., 1997) such as when archae and bacteria were ingested. Eukaryotes and their genome, grew in size.
Increased eukaryotic size and phagocytosis also enabled microbes to easily form symbiotic relations with eukaryotes, and in so doing, donate their genes. The result was the formation of microbe-like compartments within the eukaryotic cell (Dyall et al., 2004). This symbiosis created a division of labor and freed eukaryotes of the necessity of synthesizing complex molecules, chemicals, and coenzymes that could be provided by prokaryotes and their genes. For example, after the first multi-cellular eukaryotes were fashioned, prokaryotes living inside eukaryotic cells provided these eukaryotes with nitrogen and engaged in denitrification from nitrate. Conversely, eukaryotes supplied various nutrients required by its prokaryotic symbiont (Margulis et al., 1997).
The phagocytosis of archae and bacteria and the subsequent donation of their genes to the eukaryotic host, resulted in the creation of subcompartments consisting of the ingested microbial body that had been stripped of most of its genes (Dyall et al., 2004). This led to the creation of organelles, each enclosed in their own lipid membranes, and which served a variety of functions including photosynthesis, oxidative phosphorylation, and the generation of energy in the form of ATP. Yet other compartments were specialized for the digestion of large molecules, the synthesis of minerals and large glycosylated and sulphated molecules, the expression of lipids and proteins, oxidation, energy storage, and waste removal (Margulis et al., 1997; Williams & Fraústo da Silva 1996, 2006).
Therefore, in contrast to single celled prokaryotes, the cells of eukaryotes contain several internal compartments, vesicles, organelles, internal filaments, including a separate nuclear compartment containing the cell's DNA. Eukaryotic cells are also protected by a flexible membrane consisting of lipids, steroids and cholesterol (Summons et al. 2006). However, all of this was made possible by prokaryotes and their genes.
9. THE EUKARYOTIC NUCLEUS
The establishment of compartments served a variety of purposes including protection. The DNA of multicellular eukaryotes is contained within the nucleus of every cell and the nucleus protects the genome. However, the nucleus, and the other compartments, may have originally consisted of symbiotic archae and bacteria which were subsequently stripped of their genes. Thus, the nucleus may be a derived endosymbiont, a descendant of an archaeon that invaded and was engulfed and phagotocyzed (Lake and Rivera 1994; Horiike et al. 2004). Likewise, organelles, as well as mitochondria, may have been created following engulfment and the donation of bacterial and archae genes to the eukaryotic host (Dyall et al., 2004; Embley and Martin, 2006; Margulis et al., 1997; Pace 2006; Woese 1994). The incorporation of these genes and the symbiotic relations which developed between eukaryotes and genetically-stripped down bacteria and archae, led to the creation of the nucleus and compartmentalization.
The nucleus and compartmentalization made it possible for predatory eukaryotes to ingest and phagotocize other creatures while minimizing the risk of random gene mixing and the unregulated incorporation of foreign DNA. Therefore, it appears the eukaryotic nucleus was fashioned first, thereby providing genomic protection, and this allowed other microbes to be safely ingested or incorporated thereby giving rise to additional compartments including the metamorphosis of mitochondria. These developments enabled eukaryotes to become more complex and conquer new environments which then acted on gene selection.
10. MITOCHONDRIA Almost two billion years after the first unicellular eukaryotes appeared on the surface of this planet, a mitochondria-like bacteria may have invaded or was engulfed by a eukaryote consisting of perhaps two cell types (Joseph 2009b). The bacteria and eukaryote formed a symbiotic relationship and the bacteria may have donated many of its genes and was transformed into a mitochondria (Margulis et al., 1997). Mitochondria now live inside every single cell of every multi-cellular organism, adjacent to the nucleus. The genomes of all extant multi-cellular creatures, in fact, contain genes which can be traced to ancestors that possessed a bacterial endosymbiont that gave rise to the mitochondria (van der Giezen and Tovar 2005; Embley 2006). Another possibility is that genes donated by a bacteria (or archae) to the eukaryotic genome soon after eukaryogenesis, was passed down, vertically, for hundreds of millions of years, and were then activated in response to increasing oxygen levels, thereby expressing mitochondria. Mitochondria, as a distinct entity within eukaryotic cells, did not arise until between 2.3 to 1.8 BYA (Mentel and Martin 2008). It was during this time that oxygen, produced by photosynthetic bacteria and Cyanobacteria, had begun to enrich the atmosphere (Barleya et al., 2005; Joseph 2009b, 2010). When the environment had become sufficiently oxygenated and enriched with sulphide and ferrous iron which served as oxygen acceptors (Sleep and Bird 2008) oxygen-dependent ATP-generating pathways replaced the less efficient oxygen-independent pathways and eukaryotic cells underwent a significant alteration and began breathing oxygen via the metamorphosis of mitochondria. Therefore, the slow build up of oxygen and the liberation of other essential elements, gasses and proteins, acted on gene expression. Silent genes were expressed, the next stage of evolutionary development unfolded, and eukaryotic cells became equipped with mitochondria.
The evolution or development of a mitochondria and/or the establishment of the symbiotic relationship which gave rise to mitochondria, most likely took place after eukaryotes became multi-cellular and large enough to host a genetically endowed symbiote; i.e. around 2 bya when the planet became sufficiently oxygenated. There was no eukaryotic need for mitochondria until oxygen levels became sufficient so as to make them useful.
Mitochondria, as a distinct entity within eukaryotic cells, did not arise until between 2.3 to 1.8 BYA (Mentel and Martin 2008). Prior to this epic event, eukaryotes may have consisted of less than 2 cell types (Hedges et al., 2004). It was during this time that oxygen, produced by photosynthetic bacteria (Cyanobacteria), had begun to enrich the atmosphere (Barleya et al., 2005). Because of this biological activity, oxygen levels increased, methane levels decreased, and the Earth became glaciated, fueled by oxygenic photosynthesis (Joseph 2010). This rise in oxygen has been referred to as the Paleoproterozoic "Great Oxidation Event" (~2.2 to 2.0 Ga), when atmospheric oxygen may have risen to >1% of modern levels, a byproduct of oxygenic photosynthesis (Buick 2008; Canfield 2005; Holland 2006; Nisbett and Nisbett 2008; Olson 2006).
Once the environment became sufficiently oxygenated, the incorporated bacterium either underwent metamorphosis to become a mitochondria, and/or the genes it contributed were activated and gave rise to aerobic mitochondria via "endosymbiotic gene transfer." The activation of these genes, and the metamorphosis of mitochondria enabled eukaryotes to colonize emerging oxygenated environments; with the oxygen being produced biologically.
Mitochondria serve as the powerhouse of the cell and are located outside the nucleus. Mitochondria generate most of the cell's supply of adenosine triphosphate (ATP) which is used as a source of chemical energy. The production of ATP is accomplished by oxidizing the major products of glucose, pyruvate, and NADH, which are produced in the cytosol (Akao et al., 2001; Dahout-Gonzalez et al., 2006; Garlid et al., 2003; Herrmann and Neupert 2000).
Many cells have only a single mitochondrion, whereas others contain several thousand. Mitochondria have their own independent genomes and their DNA shows substantial similarity to bacterial genomes (Pace 2006; Woese 1994). Mitochondria are enclosed in their own inner and outer membrane, play a significant role in signaling, cellular differentiation, cell death, as well as the control of the cell cycle and cell growth (Anderson et al., 1981; Chipuk et al., 2006; Mannella 2006; Rappaport et al., 1998). Thus, mitochondria are essential to the functioning of the cell, providing these organisms with substantial energy, and enabled eukaryotes to grow larger in size and exploit the changing biologically engineered environments, which in turn acted on gene selection.
It is possible that instead of a late oxygen-fueled bacterial invasion, those bacterium genes which contained the DNA instructions for the metamorphosis of mitochondria had been inserted at the initial stages of eukaryogenesis and remained suppressed and were not activated, as the environment and atmosphere of Earth lacked oxygen and other chemicals such as NADH and other oxidases (Joseph 2009b,c). In the absence of an oxygen rich atmsophere, eurkaryotes had no need for a mitochondria, and instead use alternate energy sources such as hydrogen and methane. During the initial stages of an Earthly eukarogenesis an anaerobic hydrogen-breathing bacteria and a methanogenic archaeon either transferred their genes or were incorporated into a host. The bacteria supplied hydrogen to the eukaryotic host (Martin and Muller, 1998) which then engaged in anaerobic respiration to metabolize glycolytic products and turn them into energy; releasing oxygen as waste. The archaen enabled the eukaryote to breath methane.
The first eukaryotes probably did not posses mitochondria but mitosomes, as is also exemplified by many unicellular eukaryotes (Bakatselou et al., 2003; Tovar et al., 1999; Williams et al., 2002), especially those living in an anaerobic environment. However, when oxygen levels increased around 2bya, and mitochondria took up residence, eukaryotes rapidly evolved, and by 1.5 bya they had expanded from 2 to 10 cell types (Hedges et al. 2004). By 1.2 bya, a varied assemblage of complex multi-cellular eukaryotes had evolved and diverged into a variety of species such as green and red algae, dinoflagellates, ciliates, amoebae, and a wide array of unornamented organic-walled acritarchs (Butterfield 2000; Porter and Knoll 2000; Wang et al. 1999; Xiao and Knoll, 1999; Zhou et al. 2001). 11. THE MITOSOME AND EUKARYOGENESIS There is considerable evidence that mitochondria are stripped down bacteria which formed a symbiogenetic relationship with multi-cellular eukaryotes consisting initially of 2 cell types. Given the lack of oxygen on the early Earth, it can therefore be deduced that the first single celled eukaryotes did not contain mitochondria and that the mitochondria invasion took place almost 2 billion years after unicellular eukaryotes left their biological footprints in 3.8 billion year old Greenland quartz (Pflug 1978). This late invasion could explain why a few groups of unicellular eukaryotes lack mitochondria: the microsporidians, metamonads, and archamoebae. As based on phylogenetic trees constructed using rRNA information, unicellular eukaryotes appeared before the origin of mitochondria. Thus, the endosymbiont may have been incorporated only after larger, more complex multicellular eukaryotes evolved in response to the biologically engineered changes taking place on Earth. However, unicellular eukaryotes who are without mitochondria nevertheless, possess organelles of bacterial descent (Gray et al., 1999). This has led to the possibility that genes giving rise to mitochondria, organelles, and the nuclear compartment originated at the same time in the common ancestor of all extant eukaryotes rather than in separate, subsequent events (Gray et al., 1999). The mitosome, for example, is an organelle found in some unicellular eukaryotic organisms and is related to mitochondria (Bakatselou et al., 2003; Tovar et al., 1999; Williams et al., 2002). Like mitochondria, they have a double membrane. The mitosome, however, has been detected only in anaerobic or microaerophilic parasitic organisms that do not have mitochondria (Bakatselou et al., 2003; Mentel and Martin 2008; Tovar et al., 1999; Williams et al., 2002). Unicellular eukaryotes had lived on Earth for almost 2 billion years before the planet became sufficiently oxygenated. Hence, there was no need to possess a mitochondria, whereas a mitosome would have conferred significant advantages. However, after the great oxygenation event, mitosomes would have been largely useless to those organisms living in an aerobic environment. Unlike mitochondria, mitosomes do not have the capability of gaining energy from oxidative phosphorylation (Mentel and Martin 2008) and this may be due to the anaerobic environments in which they evolved (Tovar et al., 1999). Mitosomes therefore, may also be related to a bacteria which gave rise to mitochondria (Mentel and Martin 2008). For example, the organelles of most unicellular eukaryotes have also been shown to be of bacterial descent (Gray et al., 1999). Mitosomes may be mini-mitochondria albeit stripped of their genes, or mitochondria may be partially derived from mitosome genes. The existence of the mitosome in anaerobic unicellular eukaryotes, and the link to bacteria and mitochondria, may indicate that mitosomes and mitochondria are derived from the genes that were either donated to or which gave rise to the first eukaryotes. However, unlike mitochondria, mitosome genes are contained in the nuclear genome of the host (Bakatselou et al., 2003; Tovar et al., 1999) whereas mitochondria are located outside the nucleus. Therefore, mitosomes may have been jettisoned and the larger sized mitochondria took their place outside the nucleus in response to increased levels of oxygen, sulphur and ferrous iron, and other gasses, ions and minerals; a consequence of the genetically engineered environment acting on gene selection. 12. MITOCHONDRIA & ENDOSYMBIOTIC GENE TRANSFER The activity of photosynthesizing organisms and other prokaryotes altered the environment via the liberation, secretion, and synthesis of a variety of chemicals, enzymes, and gasses including oxygen and NADH (Buick 1992, 2008; Falkowski and Godfrey 2008; Holland 2006; Olson 2006; Williams and Fraústo da Silva 2006). The changed environment acted on gene selection, activating genes contributed by bacteria and archae, giving rise to new traits and new species perfectly adapted for a world that had been prepared for them. However, not just the eukaryotic genome was impacted, but the mitochondria genome. Mitchondria subsequently donated numerous genes which were integrated into the eukaryotic genome (Rogers et al., 2007) via a process Andersson (2005) refers to as “endosymbiotic gene transfer." These included genes coding for organelles and the endoplasmic reticulum, as well as genes contributing to the nucleus, and the bacterial-type plasma membrane that displaced the original archaeal membrane (Esser et al., 2004; Rivera andLake 2004).
Endosymbiotic gene transfers are a common and ongoing process in diverse eukaryotes (Bensasson et al. 2001; Leister 2003; Timmis et al. 2004). Endosymbiotic gene transfer from mitochondria may have facilitated the invasion of group II introns into host genes (Martin and Koonin, 2006) which served as the precursors of spliceosomal introns (Cavalier-Smith, 2009). These introns were most likely transferred into the eukaryotic genome through viral invasion and exerted a profound effect on the regulation of gene expression (e.g. Brietbart et al., 1985; Leff et al., 1986), the expansion and duplication of the eurkayotic genome, and the evolution and metamorphosis of increasingly complex creatures.
13. VIRUSES AND EUKARYOGENESIS
Viruses contain the genetic instructions necessary for duplicating individual genes, including those originally inserted into the eukaryotic genome by archae and bacteria. Viruses have provided elements which enabled nucleotides to be copied and expressed and may have played a significant role in stitching together the first replicating genes. Viruses, therefore, may have initially served as mobile "RNA Worlds" which acted on pre-biotic cells, splicing together and then duplicating nucleotides, thereby kicking starting DNA-based life capable of reproducing and making variable copies of itself.
The first eukaryotes could not have evolved or come into existence if not for viral RNA, DNA, introns, and other regulatory elements. It was viral elements, in conjunction with genes contributed by archae and bacteria, which contributed to the fashioning of unicellular eukaryotes and their evolutionary transition to multi-cellular eukaryote.
Eukaryotic evolution, in general, has been impacted by repeated episodes of viral invasion and the insertion of viral genes into the host genome and which have conferred functional advantages to the host. Tens of thousands of viral genes exert regulatory control over gene duplication, and mediate gene and genome rearrangement, transduction and the silencing vs activation of genes (Crombach and Hogeweg 2007; John and Miklos 1988). Once inserted, these viral genes can rapidly replicate and increase in number (Doolittle and Sapienza 1980; Tsitrone et al., 1999). They can also insert themselves into a variety of locations within the genome where they may promote gene expression or duplication; and this has been shown to be true even in the human genome. Endogenous retroviral (ERV) sequences, such as promoters, enhancers, and silencers determine when and which genes should be turned on or off and play important roles in the evolution of new species and in fetal and brain development.
Retroviruses, for example, do not merely attack host species in order to replicate, but intwine their genes with the host genome. These viruses manufacture enzymes (reverse transcriptase), to reverse transcribe the host's RNA to create a complementary viral DNA which then becomes an integral part of the host genome. Numerous copies of this viral DNA are then replicated and then transmitted via the germline through daughter cells, to subsequent generations. Moreover, eukaryotic RNA may have also been originally derived from viral elements (Joseph 2009c).
Autonomous retrotransposable elements make copies of themselves by releasing reverse transcriptase, which is an RNA-dependent DNA polymerase. This substance catalyzes reverse transcription of RNA transcripts into DNA, thus producing new copies of the retroelement and increasing their number by duplication. Retrotransposition is largely responsible for the proliferation of retroelements in many eukaryotic genomes.
After the RNA genome of an extracellular retrovirus is copied into DNA by virus-encoded reverse transcriptase it is then integrated into the nuclear DNA and thus the chromosome of the host cell via a viral enzyme integrase (Vogt 1997). Yet other retroviruses transpose via DNA excision and reintegration into the host genome. These are referred to as transposons. Integration is highly stable and, consequently, infection of germ line cells can lead to vertical transmission of retroviruses from parent to offspring as Mendelian alleles (Boeke and Stoye 1997). However, many of the viral-replicatory genes remain silent until their activation is triggered by specific genetic events and environmental signals. Yet other replicatory genes and proteins may be suppressed by these same signals. Via the turning on and off of genes, new species may be generated whereas others may become extinct (Joseph 2009b,c). Similar mechanism must have been at work when the first unicellular, then multi-cellular eukaryotes appeared.
Flurries of ERV activity, invasions, proliferation, deletions, and extinctions have corresponded to the divergence and metamorphosis of numerous species, and are associated with the Cambrian Explosion 540 million years ago, including the evolution of jawed vertebrates (Agrawal et al. 1998, Kapitonov and Jurka 2005), the subsequent split between fish and tetrapods 450 mya (Volff et al. 2003), the giant leap from teleost fish to amphibians 350 mya (Volff et al. 2001c), then reptiles (Hude et al., 2002) and leading up to birds, mammals (Herniou et al., 1998) then primates and humans (Hughes and Coffin 2001; Sverdlov 2000). For example, with the evolution of monkeys, 55 mya, ERVs formed numerous proviruses which became highly active and increased their activity until the divergence of Old World and New World primates (Lavie et al., 2004). However, there is no trace of ERV activity in prosimians. In addition, following the split between New and Old World monkeys 30 to 35 mya, new classes of ERVs flourished (Mayer and Meese 2002; Mayer et al., 1998; Medstrand and Mager 1998; Medstrand et al., 1997; Seifarth et al., 1998; Sverdlov 2000). During a period of ape-primate proliferation from 15 mya to 6 mya ERVs were again repeatedly mobilized (Lopez-Sanchez et al., 2005), with extensive traces being retained even in the human genome. There followed yet another period of ERV proliferation 8 to 6 MYA (Barbulescu et al., 1999; Johnson and Coffin 1999; Lopez-Sanchez et al., 2005) corresponding with the divergence between the common ancestors for chimps and humans, and then many of the ERV families became inactive and went extinct (Lopez-Sanchez et al., 2005).
Yet other ERV families have lived for tens of millions of years, continuing in the primate lineage leading to humans and displaying periodic bursts of activity which continued after the human-chimpanzee split (Costas 2001; Mayer et al., 1998; Medstrand and Mager 1998; Reus et al., 2001). However, hundreds of retrogenes were also formed in both the chimpanzee and human lineages after they split from a common ancestor (Chimpanzee Sequencing and Analysis Consortium 2005). Yet others are unique to humans and continue to show activity (Barbulescu et al., 1999; Buzdin et al., 2003; Medstrand and Mager 1998), and have contributed to human genetic diversity (Seleme et al. 2006) and the evolution of numerous species of Homo.
Human evolution, therefore, has been shaped by successive waves of viral invasion which have induced large-scale deletions, duplications and chromosome reshuffling in the human genome and have been a major source of genetic diversity. In fact, about one quarter of all analyzed human promoter regions harbor sequences derived from viral elements (Jordan et al. 2003).
Viruses, therefore, have played a decisive role in genomic and eukaryotic evolution and the transition to and emergence of new and increasingly complex species. It is thus reasonable to conclude that viruses played an identical role in the initial transition from pre-eukaryote to unicellular eukaryote, and again with the transition to multi-cellularity. Eukaryogenesis would not have been possible without viruses.
14. CONCLUSION
Despite the shuffling of genes and nucleotides and the repeated duplication of the ancestral genome, coupled with insertions, deletions and relocation of individual genes thereby erasing evidence of their ancestry, thousands of orthologous genes and hundreds of conserved genes and introns can still be traced back to the last common ancestor for eukaryotes (Snel et al., 2002; Mirkin et al., 2003; Kunin and Ouzounis 2003; Koonin 2003; Makarova et al., 2005; Mushegian 2008; Bejerano et al., 2004). And often these orthologs express or perform the same function regardless of species. These conserved genes, proteins, and gene sequences include those coding for core cellular functions and are found in the genomes of prokaryotes and eukaryotes (Koonin et al., 2004; Koonin and Wolf 2008). These conserved genes govern translation, the core transcription systems, and several central metabolic pathways, such as those for purine and pyrimidine nucleotide biosynthesis (Koonin 2003).
Although the genome has been repeatedly duplicated and rearranged, thereby obscuring the ancestral history of most genes, protein sequence conservation extends from mammals to bacteria thus demonstrating their great antiquity (Dayhoff et al., 1974; Eck and Dayhoff 1966; Dayhoff et al., 1983). Likewise, a large repertoire of core genes, including those involved in informational and operational functions, can be traced to prokaryotes which first donated these genes, via HGT, to the eukaryotic genome billions of years ago.
Moreover, introns, ribosomes, transposable elements, and other regulatory genes have been horizontally transferred from viruses and prokaryotes to eukaryotes. Introns have play a decisive and crucial role in regulating, copying, and duplicating genes which had also been transferred to the eukaryotic genome by prokaryotes and viruses. Moreover, they regulate the manufacture of new proteins and guide or influence the evolution of new tissues, organs, and species. These are not random events, but are under precise regulatory control (Joseph 2009b,c).
Massive numbers of regulatory genes have been transferred from viruses into the eukaryotic genome. The insertion of regulatory elements can prevent the transfer of additional genes, as well as turn gene sequences on or off giving rise to evolutionary change and the emergence of new species. In fact, the transfer of massive numbers of genes to the eukaryotic genome are directly related to evolutionary transitions (Joseph 2009b). Yet others may not be transferred and inserted until an appropriate host evolves or after the genome has been repeatedly duplicated.
Not all transferred genes are activated once they are acquired by a host. These inserted genes may not be expressed until passed on to later generations and later appearing species and only when exposed to specific environmental agents (Joseph 2009b). Thus many transferred genes, including those which are highly conserved, remain transcriptionally inactive, dormant and silent (Nicoh et al., 2008). Therefore, during the initial (and later) stages of eukaryogenesis, numerous genes may have been inserted but which remained silent and suppressed. These silent genes were passed down vertically from generation to generation, and transferred horizontally from species to species, for hundreds of millions, even billions of years waiting for an activating signal from the environment, or a regulatory gene which will induce transcription and evolutionary change. Many of these regulatory genes originated in viruses and prokaryotes and then acted on genes transferred to eukaryotic hosts by viruses and prokaryotes. These genes and regulatory elements, acting in concert, are responsible for evolutionary transitions including those leading to humans. It is thus only reasonable to conclude that these same genetic mechanisms were at work during the initial stages of eukaryogenesis and are responsible for the evolution of unicellular then multi-cellular eukaryotes.
Thus, it appears that after becoming established on Earth 4.2 bya, archae, bacteria, and viruses created the first Earthly eukaryotes by donating and transferring genes which became the eukaryotic genome and then regulated its expression. The other possibility is that archae, bacteria, and single celled eukaryotes share a common ancestor or independently evolved from a diverse colony of proto-cells.
If viruses also first emerged from this pool of proto-cells is unknown. It is possible that viruses simply serve as genetic warehouses for excess genes which are ejected from various hosts when not needed, and are then inserted into specific hosts on an as-needed-basis (Joseph 2009c, Joseph and Schild 2010b; Joseph and Wickramasinghe 2010). Viruses, however, also contain the genetic instructions necessary for duplicating individual genes, including those originally inserted by archae and bacteria into eukaryotic hosts. In fact, viruses have provided elements which enabled nucleotides to be copied, duplicated, and then expressed and may have played a significant role in jig sawing together the first replicating genes. Before life began, viruses may have served as mobile "RNA Worlds" which acted on pre-biotic cells, splicing together and then duplicating nucleotides, thereby kicking starting DNA-based life capable of replicating itself.
If viruses are the key to "how life began", or if they preceded or came after the emergence of archae and bacteria, is unknown. However, it is clear that prokaryotes and viruses transferred genes, introns, and regulatory elements into a pre-eukaryotic cell or unicellular eukaryote, perhaps around 4 bya, and are responsible for triggering multi-cellularity. Nearly 4 billion years later, the descendants of the first Earthly eukaryotes would give rise to humans.
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