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Common ancestry of eukaryotes and Asgardarchaeota: Three, two or more cellular domains of life?
Journal of Theoretical Biology 486 (2020) 110083
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Common ancestry of eukaryotes and Asgardarchaeota: Three, two or more cellular domains of life? Massimo Di Giulio a,b,∗ a b
The Ionian School, Genetic Code and tRNA Origin Laboratory, Via Roma 19, 67030 Alfedena (L’Aquila), Italy Early Evolution of Life Laboratory, Institute of Biosciences and Bioresources, CNR, Via P. Castellino, 111, 80131 Naples, Italy
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Article history: Received 22 February 2019 Revised 8 August 2019 Accepted 15 November 2019 Available online 16 November 2019 Keywords: Progenote Evolutionary transitions Eukaryogenesis Cellular membrane timing appearance Subdomains of life Eukaryotic taxonomic rank
a b s t r a c t There is much evidence that eukaryotes have many traits in common with archaea and in phylogenetic analyses they are closely linked. In particular, it has been suggested that Asgardarchaeota would be part of the same clade of eukaryotes. If so - and being the difference between Asgardarchaeota and eukaryotes very large - then all this would imply that their common ancestor was a progenote, i.e. a protocell in which the relationship between genotype and phenotype was still evolving. This, in turn, would imply that true cells would appear on the tree of life only later, that is to say, only when the ancestor of Asgardarchaeota and the one of eukaryotes appeared. However, this way of seeing would define these ancestors as primary fundamental cells, namely, as cellular domains of life because it would be in this evolutionary stage that true cells would appear for the first time. Finally, the Asgardarchaeota-eukaryote transition is discussed, that is, some aspects of eukaryogenesis and the taxonomic rank of eukaryotes are analyzed. © 2019 Elsevier Ltd. All rights reserved.
1. Introduction The classification that brings together organisms in three domains of life - Bacteria, Archaea and Eucaryota (Woese and Fox, 1977b; Woese et al., 1990) - might require updates in light of new findings (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Castelle and Banfield, 2018). Indeed, already Lake et al. (1984) found that the ribosome structure of eocytes (i.e., Crenarchaeota) was more closely related to that of eukaryotes than to other archaea. This was also confirmed by Rivera and Lake (1992) who, analysing the elongation factors, revealed evidence that eukaryotes and eocytes were in a close phylogenetic relationship, narrower than that to other archaea (Lake, 1986). More recently, Gribaldo et al. (2010) summarized the evidence in favour of hypothesis that eukaryotes are either originated within archaea (hypothesis of two domains of life) (see also Fig. 2) or that they have a common ancestor with archaea (hypothesis of three domains of life) (see also Fig. 1), although they did not success to define which of two hypotheses is the most corroborated (Gribaldo et al., 2010). Instead, Williams et al. (2013) found evidence above all in favour of hypothesis of two domains of life, ∗
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https://doi.org/10.1016/j.jtbi.2019.110083 0022-5193/© 2019 Elsevier Ltd. All rights reserved.
constructing evolutionary trees with new methods which place the core of eukaryotic genes within archaeal domain (Williams et al., 2013; Fig. 2). Moreover, with the discovery of Asgardarchaeota, the hypothesis of two domains of life seems to have taken a more consistent form (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fig. 2). Asgardarchaeota is a group of organisms that possess different genetic and physiological characteristics of an archaeal type but that in molecular phylogenies are more closely related to eukaryotes (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017). Moreover, they possess eukaryote signature proteins that would reinforce the hypothesis that they have a closer affinity with eukaryotes than to other archaea (Dey et al., 2016; Eme et al., 2017; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018). In fact, since Asgardarchaeota and eukaryotes share derived characters that are not present in other phyla of archaea, this led Fournier and Poole (2018) to suggest that Asgardarchaeota could be better interpreted if they were the early and divergent members of a larger group of organisms that also included eukaryotes. That is to say, Fournier and Poole (2018) support the fascinating hypothesis that Asgardarchaeota and eukaryotes are part of a single clade for which they propose the name Eukaryomorpha (Fig. 1 and Fig. 2). All this raises some wonderful and intriguing questions to which I try to give some answers here.
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Fig. 1. The representation - of a part - of the tree of life consistent with a three domain topology. The image was taken by Fournier and Poole (2018) but has been modified. The domain of bacteria is not represented. See Fournier and Poole (2018) for comments and further information. Only the general topology makes sense while the length of branches and their number are completely arbitrary. See text for implications and discussion.
Fig. 2. The representation - of a part - of the tree of life consistent with a two domain topology. The image was taken by Fournier and Poole (2018) but has been modified. The domain of bacteria is not represented. See Fournier and Poole (2018) for comments and further information. Only the general topology makes sense while the length of branches and their number are completely arbitrary. See text for implications and discussion.
2. The number of primary fundamental cells, i.e. the number of cellular domains, the taxonomic rank of eukaryotes, the evolutionary transition of Asgardarchaeota-eukaryotes and the nature of their ancestor If indeed Asgardarchaeota and eukaryotes were part of a single clade (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018) then we should also accept the following implications. It is certainly true that Asgardarchaeota share with eukaryotes a set of characteristics and that in molecular phylogenies they are closely linked (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018) and therefore they might be classifiable as eukaryotic organisms (Fournier and Poole, 2018), nevertheless it is also
true that Asgardarchaeota have been classified as prokaryotic organisms (Zaremba-Niedzwiedzka et al., 2017), i.e. as fundamentally dissimilar cells from eukaryotic ones (Mayr, 1998). All this - in my opinion - could not but should imply that the ancestor of Asgardarchaeota and eukaryotes was a progenote, that is to say a protocell in which the relationship between genotype and phenotype was not yet fully realized (Woese and Fox, 1977a; Woese, 1987; Doolittle and Brown, 1994; Di Giulio, 20 01, 20 06, 2011, 2015, 2017, 2018, 2019b). To illustrate this point, we consider a phylogenetically profound trait like the cell membrane. The cellular membrane of eukaryotes and that of archaea - and with the latter that of Asgardarchaeota (Hoshino and Gaucher, 2018) - are so different (Lombard and Moreira, 2011; Hoshino and Gaucher, 2018) that this led to suggest that
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the Last Universal Common Ancestor (LUCA) might have been acellular, that is to say, it was not surrounded by any kind of membrane (Koga et al., 1998), even if it had been referred, at that time, only to bacteria and archaea. However, the difference in cell membranes between eukaryotes and Asgardarchaeota seems to be so great (Hoshino and Gaucher, 2018) and such to imply that it was still segregating, namely still evolving at the evolutionary stage of the ancestor of these two groups of organisms. Therefore, such ancestor was a protocell, that is to say a progenote, and not a true and complete cell. This would seem to be an unavoidable conclusion because if a phylogenetically deep trait - like the cell membrane - was still in formation during such an evolutionary stage - that is, it was still in the progressive Darwinian evolutionary phase (Doolittle and Brown, 1994) - then it would mean that this trait would be originating for the first time. Evidently, this would define this evolutionary stage to belong to the stage of the progenote which is the stage in which the deep fundamental traits would have been formed (Woese and Fox, 1977a; Woese, 1987; Doolittle and Brown, 1994; Di Giulio, 20 01, 20 06, 2011, 2015, 2017, 2018, 2019b). It seems that one arrives in this way to define the ancestor of Asgardarchaeota and eukaryotes as a progenote and not instead as a completely realized cell. Since our classifications refer to cells and not to protocells (progenotes) (Di Giulio, 2018) and since we concluded that the ancestor of Asgardarchaeota and eukaryotes is instead a protocell and not a cell, then we should conclude that the first real cells appeared with the appearance of the ancestor of eukaryotes on the one hand and with that of the ancestor of Asgardarchaeota on the other, at least on this side of the tree of life. But this would indicate these cells as primary cells, that is to say, fundamental cells, i.e., as cellular domains of life because at these nodes it would have been ascertained - for the first time - the presence of the cellular state. This would lead to the conclusion that considering eukaryotes and Asgardarchaeota as phylogenetically closely related organisms (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018), would imply that these two groups of organisms actually have the highest taxonomic rank, namely, they are domains of life like Bacteria and Archaea. Therefore, the cellular domains of life would not be three or two but would be more (Di Giulio, 2014, 2018, 2019b). Similar arguments made on the ancestors of bacteria and archaea produced equivalent observations (Di Giulio, 2010, 2011, 2018, 2019b). As a general argument, it seems to me that it is expected that the number and type of cellular domains must depend on how the first "speciation" occurred from LUCA. In fact, for example, if the ancestor of eukaryotes and Asgardarchaeota had been a progenote - as I argue here - then the two different genotes that evolved from this same progenote should have been more similar than genotes that emerged from progenotes that gave rise to the lineage which led to bacteria and to that of archaea (Di Giulio, 2018). In other words, according to this way of seeing, the primary fundamental cells forming the different domains of life would be two by two more similar to each other, that is to say, they would form "subdomains" of life. For example, cells of eukaryotes and Asgardarchaeota would be more similar to each other than to cells of the two subdomains deriving from the progenote of the lineage of bacteria and that of archaea. In other words, this theory holds that the number and type of the domains of life depended on the kind of speciation that intervened during the formation of the deep nodes of the tree of life. Namely, if from a progenotic LUCA were immediately and directly derived fundamental primary cells (Di Giulio, 2001, 2011) – i.e. those that are normally called domains of life - then it would not be expected that beyond domains there were also subdomains. What instead awaited by the theory that I support here because the ancestor of bacteria, that of archaea and that of Asgardarchaeota+eukaryotes would have been
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of progenotes, but they would have also been different from each other (see also Di Giulio, 2018). So, being the appearance of true cells linked to subdomains this would be the most profound classification of the tree of life because going backwards from this evolutionary stage only populations of different progenotes would meet, as they would not, obviously, fall into the classification of cells. Thus the word domain should actually be used to refer to those that have been called subdomains here. It is thus clear that the deeper classification of organisms of the tree of life would provide cell types with different degrees of similarity in the sense that cells of all subdomains would be differently similar to each other; while domains would be identifiable only through subdomains, and they would not classify cells but only protocells and would therefore have a relative biological significance. Fournier and Poole (2018) argue that the Asgardarchaeota lineage should be considered as an early branch of the eukaryotic lineage and together represent a clade of an undetermined taxonomic rank dependant on the internal topology and the root of Archaea (Fournier and Poole, 2018). Obviously it is the position of the root in the archaeal domain to define the taxonomic rank of the clade of Asgardarchaeota+eukaryotes. However, it seems to me that the difference between eukaryotes and Asgardarchaeota is so great that it implies either that they are not part of the same clade or, on the contrary, if phylogenetically closely related (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018), then belong to two completely different cellular domains because the differences in their phylogenetically profound characters - such as, for example, the cell membrane, the size of the cell - would be so large and such as to justify progenotic states for their ancestor, as corroborated above. However, the unclear taxonomic rank of the clade of Asgardarchaeota+eukaryotes does not seem to be less clear than that of archaea and bacteria. Indeed, assuming that archaea and bacteria are domains of life, then also the clade of Asgardarchaeota+eukaryotes should have a taxonomic rank at least equal to that because the molecular variability in phylogenetically profound traits of the clade of Asgardarchaeota+eukaryotes should be larger than that detectable within the domain of bacteria and in that of archaea. [Here I assume that the high molecular variability in phylogenetically profound traits is an expression of where or near where the root of the tree of life can be located, or that it indicates ancestrality for that clade (Di Giulio, 2019a).] More clearly, there might be no doubt that in the clade of Asgardarchaeota+eukaryotes the molecular variability in phylogenetically profound traits is, or should be, much larger than the one observable in bacteria or archaea because this clade is formed by both prokaryotic and eukaryotic organisms, while the others are more similar to each other. This would seem to imply that if the molecular variability (understood as uniformity, singularity and heterogeneity of characters) in phylogenetically profound traits of archaea and bacteria determined a taxonomic rank equal to that of domain of life, then the greater molecular variability - that is to say, the minor uniformity and the more accentuated singularity and heterogeneity - in phylogenetically profound traits of the clade of Asgardarchaeota+eukaryotes it should imply that the taxonomic rank of the clade of Asgardarchaeota+eukaryotes is at least equal to that of domain of life. Even if it would seem to be greater than that of domain of life, namely, to be a deeper taxonomic unity than that of domain of life, that is to say, to be the root of the tree of life. This is because greater molecular variability in phylogenetically profound traits - that is, the absence of uniformity in at least some phylogenetically profound traits, together with the presence of a more pronounced singularity (greater heterogeneity) in these traits - would imply a taxonomic rank at least equal to that of bacteria and archaea. Indeed, being less uniform and more singular in phylogenetically profound traits - and yet belonging to the same
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clade – would mean to have had evolutionary histories in these traits at least as complex and evolutionary precocious precisely because different uniformity, singularity and heterogeneity of these traits would be the direct expression of different levels of evolutionary maturation of cellular stages. For example, a lower uniformity would imply that a certain trait was set earlier because at the time of its formation more forms of the same character could have been present increasing the non-uniformity (Di Giulio, 2019a). Thus, it would come to the conclusion that nodes of the tree of life might have the same taxonomic rank even if they refer to completely different distances from the LUCA node. This conclusion is not easy to accept, so I try to discuss some of its solutions below. One way to make this conclusion acceptable is to consider the hypothesis of three domains of life as true (Fig. 1). In fact, this hypothesis would approach the node of the ancestor of Asgardarchaeota+eukaryotes at the LUCA node and therefore bring the greater molecular variability of this ancestor close to that of the other nodes of ancestors of archaea and bacteria, making this conclusion more likely. However, even under this condition the molecular variability of the clade of Asgardarchaeota+eukaryotes might be the highest - something, however, not easy to evaluate (see Di Giulio, 2019a) - and could therefore imply that the root of the tree of life might be in this clade (Forterre and Philippe, 1999). This should be evaluated (see Di Giulio, 2014, 2018, 2019b). While, the hypothesis of two domains of life (Fig. 2) would lead to the opposite result because it would remove the node of the ancestor of the clade of Asgardarchaeota+eukaryotes from the LUCA node, and therefore its high molecular variability would no longer be easily explained, because it would be detected on less deep nodes of the tree of life (compare Fig. 2 to Fig. 1). It would therefore be curious that the hypothesis of two domains of life (Fig. 2) despite being empirically favoured in studies concerning the emergence of eukaryotes from within archaea (Zaremba-Niedzwiedzka et al., 2017), nevertheless these same observations can be used against the hypothesis of two domains and in favour of that of three domains of life because the high molecular variability of the node of the ancestor of the clade of Asgardarchaeota+eukaryotes would be not easily justifiable - in the hypothesis of two domains of life compared to that of three domains - precisely because it is too much far from the node of LUCA. Then, accepting the hypothesis of two domains of life (Fig. 2) would also partially contribute to accepting the hypothesis that nodes differentially distant from the LUCA node could nevertheless have the same taxonomic rank. A very fascinating thing that might be justified if the distance amongst the nodes is not too big otherwise it would generate difficulties. However, it may also have occurred that nodes with different distances from the LUCA node might have undergone particular evolutionary histories that could have resulted in an equivalent taxonomic rank. What still remains to be understood. Fournier and Poole (2018) argue that eukaryotes emerging from within archaea, they should not be considered a domain of the same primacy as that of Archaea. But how is it possible to affirm that the taxonomic rank of the clade of Asgardarchaeota+eukaryotes is different and inferior to that of archaea when the molecular variability of this clade would seem to be much higher than that of the domain of archaea? That is to say, how is it possible to affirm that the clade of Asgardarchaeota+eukaryotes has a lower taxonomic rank or at least different from that of archaea, when this clade, unlike archaea, contains organisms classified as both prokaryotes and eukaryotes? It would seem true the opposite, namely that the clade of Asgardarchaeota+eukaryotes has a higher (deep) taxonomic rank than that of archaea precisely because it contains within it so different organisms! And therefore perhaps forming the root of the tree of life (Di Giulio, 2019a, see also above). Finally, there is the possibility that the eukaryotic cell deriving from a multitude
of symbioses (Margulis, 1981; López-García et al., 2017) is actually a "super-cell" that should not be classified with the "normal-cells". This could then explain the anomalous taxonomic rank that one might be forced to commit to eukaryotes. In other words, the taxonomic rank of eukaryotes would be a consequence of symbioses of the eukaryotic cell that circumventing the normal phylogenetic pathways would have determined these anomalies. Evidently, this way of seeing would fall under the category of two domains of life as there would only exist two domains - bacteria and archaea because the presumed eukaryotes would not be classifiable with these two because of a completely different origin. This would be a real conjecture that should be taken into consideration in discussions like this. It seems to me that the derivation of eukaryotes from archaea (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018) is equivalent to the transition from a gram-positive to an archaeon suggested by Valas and Bourne (2011) that is a subject of strong criticism (Woese, 20 0 0; Forterre, 2011; Staley, 2017; Di Giulio, 2001, 2006, 2011, 2018). It is good to say explicitly the transition between domains of life that is to say, the transition between fundamental types of primary cells - should not and could not happen because it would be strongly hampered by having to modify - at the same time or in sequence - many fundamental and phylogenetically profound characters, which would strongly influence all molecular aspects of these cells preventing the evolutionary transition between cells belonging to different domains of life (Woese, 20 0 0; Di Giulio, 2001, 2006, 2010, 2011, 2018; Forterre, 2011; Staley, 2017). Therefore, I do not consider it absolutely probable that there has been a transition between Asgardarchaeota - understood as a complete archaeal cell - and eukaryotes, contrary to what other authors support (Koonin, 2015; Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018). Namely, if Asgardarchaeota and eukaryotes were really part of the same clade then they would be derived from a same progenotic stage - but not genotic stage as claimed by the latter authors - and would form two different domains of life though more closely related to each other (subdomains) than to the domains (subdomains) of bacteria and archaea, as maintained above. Finally, I do not think that eukaryogenesis could have been triggered by the acquisition of the bacterium that led to the mitochondrion - as claimed by other authors (Koonin, 2015; Martin et al., 2015) - because if this bacterium was either an alpha-proteobacteria (Gray et al., 1999) or in the lineage of proteobacteria (Martijn et al., 2018), then this would already testify the presence of completely evolved cells and not of protocells at this evolutionary stage. Hence, eukaryogenesis had to be already in place because the presence of completely realized cells - although prokaryotic cells - should imply an evolutionary stage of genotes and not more than progenotes. Indeed, the presence of true cells (genotes) would have supplanted all populations of protocells (progenotes) because the first having reached an optimal relationship between genotype and phenotype would have been quickly selected for this huge selective advantage, not possessed by populations of progenotes. Thus, the origin of the eukaryotic cell should have been in a very advanced stage - when symbiosis with the proteobacterium began - precisely because the stage of the progenote had already been exceeded, thus indicating the presence of only cells and not protocells at this evolutionary stage and, therefore also the presence of the eukaryotic cell although evidently still devoid of mitochondria. This conjecture is in agreement with theories that foresee a late acquisition of the mitochondrion during eukaryogenesis (Martijn and Ettema, 2013; Poole and Gribaldo, 2014; López-García et al., 2017). Moreover, this way of looking would seem to be able to explain why the eukaryotic membrane - which is of the same type as that of bacteria - cannot
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be derived from the membrane of the bacterium that would become the mitochondrion. In fact, the presence of the cellular state at this evolutionary stage would seem to make improbable the derivation of the eukaryotic membrane from the membrane of the bacterium - ancestor of the mitochondrion - precisely because the reached cellular stage would not favour for itself such transition as would be that of the progenote - because this would represent a huge change with great pleiotropic effects that would have been strongly selected against. 3. Conclusion Taking also into account other analyses (Di Giulio, 2018), we come to the conclusion that the ancestor of bacteria, that of archaea and that of eukaryotes would have been of progenotes. If so, then the number of cellular domains would be more than three, since we classify cells and not protocells (Di Giulio, 2018). That is to say, the first true cells would originate from these progenotes. Thus, the so-called cellular domains would be only protocellular domains and the true cellular domains would be those derived from them. Namely, they would be represented by those who were called cellular subdomains here. References Castelle, C.J., Banfield, J.F., 2018. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197. Dey, G., Thattai, M., Baum, B., 2016. On the archaeal origins of eukaryotes and the challenges of inferring phenotype from genotype. Trends Cell. Biol. 26, 476–485. Di Giulio, M., 2001. The non-universality of the genetic code: the universal ancestor was a progenote. J. Theor. Biol. 209, 345–349. Di Giulio, M., 2006. The non-monophyletic origin of the tRNA molecule and the origin of genes only after the evolutionary stage of the Last Universal Common Ancestor (LUCA). J. Theor. Biol. 240, 343–352. Di Giulio, M., 2010. Biological evidence against the panspermia. J. Theor. Biol 266, 569–572. Di Giulio, M., 2011. The Last Universal Common ancestor (LUCA) and the ancestors of archaea and bacteria were progenotes. J. Mol. Evol. 72, 119–126. Di Giulio, M., 2014. On how many fundamental kinds of cells are present on Earth: looking for phylogenetic traits that would allow the identification of the primary lines of descent. J. Mol. Evol. 78, 313–320. Di Giulio, M., 2015. The non-biological meaning of the term "prokaryote" and its implications. J. Mol. Evol. 80, 98–101. Di Giulio, M., 2017. The indefinable term ‘prokaryote’ and the polyphyletic origin of genes. J. Genet. 96, 393–397. Di Giulio, M., 2018. On Earth, there would be a number of fundamental kinds of primary cells — cellular domains — greater than or equal to four. J. Theor. Biol. 443, 10–17. Di Giulio, M., 2019a. A qualitative criterion for identifying the root of the tree of life. J. Theor. Biol. 464, 126–131. Di Giulio, M., 2019b. The universal ancestor, the deeper nodes of the tree of life, and the fundamental types of primary cells (cellular domains). J. Theor. Biol. 460, 142–143. Doolittle, W.F., Brown, J.R., 1994. Tempo, mode, the progenote, and the universal root. Proc. Natl. Acad. Sci. USA 91, 6721–6728. Eme, L., Spang, A., Lombard, J., Stairs, C.W., Ettema, T.J.G., 2017. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723.
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Common ancestry of eukaryotes and Asgardarchaeota: Three, two or more cellular domains of life? Massimo Di Giulio a,b,∗ a b
The Ionian School, Genetic Code and tRNA Origin Laboratory, Via Roma 19, 67030 Alfedena (L’Aquila), Italy Early Evolution of Life Laboratory, Institute of Biosciences and Bioresources, CNR, Via P. Castellino, 111, 80131 Naples, Italy
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Article history: Received 22 February 2019 Revised 8 August 2019 Accepted 15 November 2019 Available online 16 November 2019 Keywords: Progenote Evolutionary transitions Eukaryogenesis Cellular membrane timing appearance Subdomains of life Eukaryotic taxonomic rank
a b s t r a c t There is much evidence that eukaryotes have many traits in common with archaea and in phylogenetic analyses they are closely linked. In particular, it has been suggested that Asgardarchaeota would be part of the same clade of eukaryotes. If so - and being the difference between Asgardarchaeota and eukaryotes very large - then all this would imply that their common ancestor was a progenote, i.e. a protocell in which the relationship between genotype and phenotype was still evolving. This, in turn, would imply that true cells would appear on the tree of life only later, that is to say, only when the ancestor of Asgardarchaeota and the one of eukaryotes appeared. However, this way of seeing would define these ancestors as primary fundamental cells, namely, as cellular domains of life because it would be in this evolutionary stage that true cells would appear for the first time. Finally, the Asgardarchaeota-eukaryote transition is discussed, that is, some aspects of eukaryogenesis and the taxonomic rank of eukaryotes are analyzed. © 2019 Elsevier Ltd. All rights reserved.
1. Introduction The classification that brings together organisms in three domains of life - Bacteria, Archaea and Eucaryota (Woese and Fox, 1977b; Woese et al., 1990) - might require updates in light of new findings (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Castelle and Banfield, 2018). Indeed, already Lake et al. (1984) found that the ribosome structure of eocytes (i.e., Crenarchaeota) was more closely related to that of eukaryotes than to other archaea. This was also confirmed by Rivera and Lake (1992) who, analysing the elongation factors, revealed evidence that eukaryotes and eocytes were in a close phylogenetic relationship, narrower than that to other archaea (Lake, 1986). More recently, Gribaldo et al. (2010) summarized the evidence in favour of hypothesis that eukaryotes are either originated within archaea (hypothesis of two domains of life) (see also Fig. 2) or that they have a common ancestor with archaea (hypothesis of three domains of life) (see also Fig. 1), although they did not success to define which of two hypotheses is the most corroborated (Gribaldo et al., 2010). Instead, Williams et al. (2013) found evidence above all in favour of hypothesis of two domains of life, ∗
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constructing evolutionary trees with new methods which place the core of eukaryotic genes within archaeal domain (Williams et al., 2013; Fig. 2). Moreover, with the discovery of Asgardarchaeota, the hypothesis of two domains of life seems to have taken a more consistent form (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fig. 2). Asgardarchaeota is a group of organisms that possess different genetic and physiological characteristics of an archaeal type but that in molecular phylogenies are more closely related to eukaryotes (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017). Moreover, they possess eukaryote signature proteins that would reinforce the hypothesis that they have a closer affinity with eukaryotes than to other archaea (Dey et al., 2016; Eme et al., 2017; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018). In fact, since Asgardarchaeota and eukaryotes share derived characters that are not present in other phyla of archaea, this led Fournier and Poole (2018) to suggest that Asgardarchaeota could be better interpreted if they were the early and divergent members of a larger group of organisms that also included eukaryotes. That is to say, Fournier and Poole (2018) support the fascinating hypothesis that Asgardarchaeota and eukaryotes are part of a single clade for which they propose the name Eukaryomorpha (Fig. 1 and Fig. 2). All this raises some wonderful and intriguing questions to which I try to give some answers here.
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Fig. 1. The representation - of a part - of the tree of life consistent with a three domain topology. The image was taken by Fournier and Poole (2018) but has been modified. The domain of bacteria is not represented. See Fournier and Poole (2018) for comments and further information. Only the general topology makes sense while the length of branches and their number are completely arbitrary. See text for implications and discussion.
Fig. 2. The representation - of a part - of the tree of life consistent with a two domain topology. The image was taken by Fournier and Poole (2018) but has been modified. The domain of bacteria is not represented. See Fournier and Poole (2018) for comments and further information. Only the general topology makes sense while the length of branches and their number are completely arbitrary. See text for implications and discussion.
2. The number of primary fundamental cells, i.e. the number of cellular domains, the taxonomic rank of eukaryotes, the evolutionary transition of Asgardarchaeota-eukaryotes and the nature of their ancestor If indeed Asgardarchaeota and eukaryotes were part of a single clade (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018) then we should also accept the following implications. It is certainly true that Asgardarchaeota share with eukaryotes a set of characteristics and that in molecular phylogenies they are closely linked (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018) and therefore they might be classifiable as eukaryotic organisms (Fournier and Poole, 2018), nevertheless it is also
true that Asgardarchaeota have been classified as prokaryotic organisms (Zaremba-Niedzwiedzka et al., 2017), i.e. as fundamentally dissimilar cells from eukaryotic ones (Mayr, 1998). All this - in my opinion - could not but should imply that the ancestor of Asgardarchaeota and eukaryotes was a progenote, that is to say a protocell in which the relationship between genotype and phenotype was not yet fully realized (Woese and Fox, 1977a; Woese, 1987; Doolittle and Brown, 1994; Di Giulio, 20 01, 20 06, 2011, 2015, 2017, 2018, 2019b). To illustrate this point, we consider a phylogenetically profound trait like the cell membrane. The cellular membrane of eukaryotes and that of archaea - and with the latter that of Asgardarchaeota (Hoshino and Gaucher, 2018) - are so different (Lombard and Moreira, 2011; Hoshino and Gaucher, 2018) that this led to suggest that
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the Last Universal Common Ancestor (LUCA) might have been acellular, that is to say, it was not surrounded by any kind of membrane (Koga et al., 1998), even if it had been referred, at that time, only to bacteria and archaea. However, the difference in cell membranes between eukaryotes and Asgardarchaeota seems to be so great (Hoshino and Gaucher, 2018) and such to imply that it was still segregating, namely still evolving at the evolutionary stage of the ancestor of these two groups of organisms. Therefore, such ancestor was a protocell, that is to say a progenote, and not a true and complete cell. This would seem to be an unavoidable conclusion because if a phylogenetically deep trait - like the cell membrane - was still in formation during such an evolutionary stage - that is, it was still in the progressive Darwinian evolutionary phase (Doolittle and Brown, 1994) - then it would mean that this trait would be originating for the first time. Evidently, this would define this evolutionary stage to belong to the stage of the progenote which is the stage in which the deep fundamental traits would have been formed (Woese and Fox, 1977a; Woese, 1987; Doolittle and Brown, 1994; Di Giulio, 20 01, 20 06, 2011, 2015, 2017, 2018, 2019b). It seems that one arrives in this way to define the ancestor of Asgardarchaeota and eukaryotes as a progenote and not instead as a completely realized cell. Since our classifications refer to cells and not to protocells (progenotes) (Di Giulio, 2018) and since we concluded that the ancestor of Asgardarchaeota and eukaryotes is instead a protocell and not a cell, then we should conclude that the first real cells appeared with the appearance of the ancestor of eukaryotes on the one hand and with that of the ancestor of Asgardarchaeota on the other, at least on this side of the tree of life. But this would indicate these cells as primary cells, that is to say, fundamental cells, i.e., as cellular domains of life because at these nodes it would have been ascertained - for the first time - the presence of the cellular state. This would lead to the conclusion that considering eukaryotes and Asgardarchaeota as phylogenetically closely related organisms (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018), would imply that these two groups of organisms actually have the highest taxonomic rank, namely, they are domains of life like Bacteria and Archaea. Therefore, the cellular domains of life would not be three or two but would be more (Di Giulio, 2014, 2018, 2019b). Similar arguments made on the ancestors of bacteria and archaea produced equivalent observations (Di Giulio, 2010, 2011, 2018, 2019b). As a general argument, it seems to me that it is expected that the number and type of cellular domains must depend on how the first "speciation" occurred from LUCA. In fact, for example, if the ancestor of eukaryotes and Asgardarchaeota had been a progenote - as I argue here - then the two different genotes that evolved from this same progenote should have been more similar than genotes that emerged from progenotes that gave rise to the lineage which led to bacteria and to that of archaea (Di Giulio, 2018). In other words, according to this way of seeing, the primary fundamental cells forming the different domains of life would be two by two more similar to each other, that is to say, they would form "subdomains" of life. For example, cells of eukaryotes and Asgardarchaeota would be more similar to each other than to cells of the two subdomains deriving from the progenote of the lineage of bacteria and that of archaea. In other words, this theory holds that the number and type of the domains of life depended on the kind of speciation that intervened during the formation of the deep nodes of the tree of life. Namely, if from a progenotic LUCA were immediately and directly derived fundamental primary cells (Di Giulio, 2001, 2011) – i.e. those that are normally called domains of life - then it would not be expected that beyond domains there were also subdomains. What instead awaited by the theory that I support here because the ancestor of bacteria, that of archaea and that of Asgardarchaeota+eukaryotes would have been
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of progenotes, but they would have also been different from each other (see also Di Giulio, 2018). So, being the appearance of true cells linked to subdomains this would be the most profound classification of the tree of life because going backwards from this evolutionary stage only populations of different progenotes would meet, as they would not, obviously, fall into the classification of cells. Thus the word domain should actually be used to refer to those that have been called subdomains here. It is thus clear that the deeper classification of organisms of the tree of life would provide cell types with different degrees of similarity in the sense that cells of all subdomains would be differently similar to each other; while domains would be identifiable only through subdomains, and they would not classify cells but only protocells and would therefore have a relative biological significance. Fournier and Poole (2018) argue that the Asgardarchaeota lineage should be considered as an early branch of the eukaryotic lineage and together represent a clade of an undetermined taxonomic rank dependant on the internal topology and the root of Archaea (Fournier and Poole, 2018). Obviously it is the position of the root in the archaeal domain to define the taxonomic rank of the clade of Asgardarchaeota+eukaryotes. However, it seems to me that the difference between eukaryotes and Asgardarchaeota is so great that it implies either that they are not part of the same clade or, on the contrary, if phylogenetically closely related (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018), then belong to two completely different cellular domains because the differences in their phylogenetically profound characters - such as, for example, the cell membrane, the size of the cell - would be so large and such as to justify progenotic states for their ancestor, as corroborated above. However, the unclear taxonomic rank of the clade of Asgardarchaeota+eukaryotes does not seem to be less clear than that of archaea and bacteria. Indeed, assuming that archaea and bacteria are domains of life, then also the clade of Asgardarchaeota+eukaryotes should have a taxonomic rank at least equal to that because the molecular variability in phylogenetically profound traits of the clade of Asgardarchaeota+eukaryotes should be larger than that detectable within the domain of bacteria and in that of archaea. [Here I assume that the high molecular variability in phylogenetically profound traits is an expression of where or near where the root of the tree of life can be located, or that it indicates ancestrality for that clade (Di Giulio, 2019a).] More clearly, there might be no doubt that in the clade of Asgardarchaeota+eukaryotes the molecular variability in phylogenetically profound traits is, or should be, much larger than the one observable in bacteria or archaea because this clade is formed by both prokaryotic and eukaryotic organisms, while the others are more similar to each other. This would seem to imply that if the molecular variability (understood as uniformity, singularity and heterogeneity of characters) in phylogenetically profound traits of archaea and bacteria determined a taxonomic rank equal to that of domain of life, then the greater molecular variability - that is to say, the minor uniformity and the more accentuated singularity and heterogeneity - in phylogenetically profound traits of the clade of Asgardarchaeota+eukaryotes it should imply that the taxonomic rank of the clade of Asgardarchaeota+eukaryotes is at least equal to that of domain of life. Even if it would seem to be greater than that of domain of life, namely, to be a deeper taxonomic unity than that of domain of life, that is to say, to be the root of the tree of life. This is because greater molecular variability in phylogenetically profound traits - that is, the absence of uniformity in at least some phylogenetically profound traits, together with the presence of a more pronounced singularity (greater heterogeneity) in these traits - would imply a taxonomic rank at least equal to that of bacteria and archaea. Indeed, being less uniform and more singular in phylogenetically profound traits - and yet belonging to the same
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clade – would mean to have had evolutionary histories in these traits at least as complex and evolutionary precocious precisely because different uniformity, singularity and heterogeneity of these traits would be the direct expression of different levels of evolutionary maturation of cellular stages. For example, a lower uniformity would imply that a certain trait was set earlier because at the time of its formation more forms of the same character could have been present increasing the non-uniformity (Di Giulio, 2019a). Thus, it would come to the conclusion that nodes of the tree of life might have the same taxonomic rank even if they refer to completely different distances from the LUCA node. This conclusion is not easy to accept, so I try to discuss some of its solutions below. One way to make this conclusion acceptable is to consider the hypothesis of three domains of life as true (Fig. 1). In fact, this hypothesis would approach the node of the ancestor of Asgardarchaeota+eukaryotes at the LUCA node and therefore bring the greater molecular variability of this ancestor close to that of the other nodes of ancestors of archaea and bacteria, making this conclusion more likely. However, even under this condition the molecular variability of the clade of Asgardarchaeota+eukaryotes might be the highest - something, however, not easy to evaluate (see Di Giulio, 2019a) - and could therefore imply that the root of the tree of life might be in this clade (Forterre and Philippe, 1999). This should be evaluated (see Di Giulio, 2014, 2018, 2019b). While, the hypothesis of two domains of life (Fig. 2) would lead to the opposite result because it would remove the node of the ancestor of the clade of Asgardarchaeota+eukaryotes from the LUCA node, and therefore its high molecular variability would no longer be easily explained, because it would be detected on less deep nodes of the tree of life (compare Fig. 2 to Fig. 1). It would therefore be curious that the hypothesis of two domains of life (Fig. 2) despite being empirically favoured in studies concerning the emergence of eukaryotes from within archaea (Zaremba-Niedzwiedzka et al., 2017), nevertheless these same observations can be used against the hypothesis of two domains and in favour of that of three domains of life because the high molecular variability of the node of the ancestor of the clade of Asgardarchaeota+eukaryotes would be not easily justifiable - in the hypothesis of two domains of life compared to that of three domains - precisely because it is too much far from the node of LUCA. Then, accepting the hypothesis of two domains of life (Fig. 2) would also partially contribute to accepting the hypothesis that nodes differentially distant from the LUCA node could nevertheless have the same taxonomic rank. A very fascinating thing that might be justified if the distance amongst the nodes is not too big otherwise it would generate difficulties. However, it may also have occurred that nodes with different distances from the LUCA node might have undergone particular evolutionary histories that could have resulted in an equivalent taxonomic rank. What still remains to be understood. Fournier and Poole (2018) argue that eukaryotes emerging from within archaea, they should not be considered a domain of the same primacy as that of Archaea. But how is it possible to affirm that the taxonomic rank of the clade of Asgardarchaeota+eukaryotes is different and inferior to that of archaea when the molecular variability of this clade would seem to be much higher than that of the domain of archaea? That is to say, how is it possible to affirm that the clade of Asgardarchaeota+eukaryotes has a lower taxonomic rank or at least different from that of archaea, when this clade, unlike archaea, contains organisms classified as both prokaryotes and eukaryotes? It would seem true the opposite, namely that the clade of Asgardarchaeota+eukaryotes has a higher (deep) taxonomic rank than that of archaea precisely because it contains within it so different organisms! And therefore perhaps forming the root of the tree of life (Di Giulio, 2019a, see also above). Finally, there is the possibility that the eukaryotic cell deriving from a multitude
of symbioses (Margulis, 1981; López-García et al., 2017) is actually a "super-cell" that should not be classified with the "normal-cells". This could then explain the anomalous taxonomic rank that one might be forced to commit to eukaryotes. In other words, the taxonomic rank of eukaryotes would be a consequence of symbioses of the eukaryotic cell that circumventing the normal phylogenetic pathways would have determined these anomalies. Evidently, this way of seeing would fall under the category of two domains of life as there would only exist two domains - bacteria and archaea because the presumed eukaryotes would not be classifiable with these two because of a completely different origin. This would be a real conjecture that should be taken into consideration in discussions like this. It seems to me that the derivation of eukaryotes from archaea (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Eme et al., 2017; Fournier and Poole, 2018) is equivalent to the transition from a gram-positive to an archaeon suggested by Valas and Bourne (2011) that is a subject of strong criticism (Woese, 20 0 0; Forterre, 2011; Staley, 2017; Di Giulio, 2001, 2006, 2011, 2018). It is good to say explicitly the transition between domains of life that is to say, the transition between fundamental types of primary cells - should not and could not happen because it would be strongly hampered by having to modify - at the same time or in sequence - many fundamental and phylogenetically profound characters, which would strongly influence all molecular aspects of these cells preventing the evolutionary transition between cells belonging to different domains of life (Woese, 20 0 0; Di Giulio, 2001, 2006, 2010, 2011, 2018; Forterre, 2011; Staley, 2017). Therefore, I do not consider it absolutely probable that there has been a transition between Asgardarchaeota - understood as a complete archaeal cell - and eukaryotes, contrary to what other authors support (Koonin, 2015; Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017; Fournier and Poole, 2018). Namely, if Asgardarchaeota and eukaryotes were really part of the same clade then they would be derived from a same progenotic stage - but not genotic stage as claimed by the latter authors - and would form two different domains of life though more closely related to each other (subdomains) than to the domains (subdomains) of bacteria and archaea, as maintained above. Finally, I do not think that eukaryogenesis could have been triggered by the acquisition of the bacterium that led to the mitochondrion - as claimed by other authors (Koonin, 2015; Martin et al., 2015) - because if this bacterium was either an alpha-proteobacteria (Gray et al., 1999) or in the lineage of proteobacteria (Martijn et al., 2018), then this would already testify the presence of completely evolved cells and not of protocells at this evolutionary stage. Hence, eukaryogenesis had to be already in place because the presence of completely realized cells - although prokaryotic cells - should imply an evolutionary stage of genotes and not more than progenotes. Indeed, the presence of true cells (genotes) would have supplanted all populations of protocells (progenotes) because the first having reached an optimal relationship between genotype and phenotype would have been quickly selected for this huge selective advantage, not possessed by populations of progenotes. Thus, the origin of the eukaryotic cell should have been in a very advanced stage - when symbiosis with the proteobacterium began - precisely because the stage of the progenote had already been exceeded, thus indicating the presence of only cells and not protocells at this evolutionary stage and, therefore also the presence of the eukaryotic cell although evidently still devoid of mitochondria. This conjecture is in agreement with theories that foresee a late acquisition of the mitochondrion during eukaryogenesis (Martijn and Ettema, 2013; Poole and Gribaldo, 2014; López-García et al., 2017). Moreover, this way of looking would seem to be able to explain why the eukaryotic membrane - which is of the same type as that of bacteria - cannot
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be derived from the membrane of the bacterium that would become the mitochondrion. In fact, the presence of the cellular state at this evolutionary stage would seem to make improbable the derivation of the eukaryotic membrane from the membrane of the bacterium - ancestor of the mitochondrion - precisely because the reached cellular stage would not favour for itself such transition as would be that of the progenote - because this would represent a huge change with great pleiotropic effects that would have been strongly selected against. 3. Conclusion Taking also into account other analyses (Di Giulio, 2018), we come to the conclusion that the ancestor of bacteria, that of archaea and that of eukaryotes would have been of progenotes. If so, then the number of cellular domains would be more than three, since we classify cells and not protocells (Di Giulio, 2018). That is to say, the first true cells would originate from these progenotes. Thus, the so-called cellular domains would be only protocellular domains and the true cellular domains would be those derived from them. Namely, they would be represented by those who were called cellular subdomains here. References Castelle, C.J., Banfield, J.F., 2018. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197. Dey, G., Thattai, M., Baum, B., 2016. On the archaeal origins of eukaryotes and the challenges of inferring phenotype from genotype. Trends Cell. Biol. 26, 476–485. Di Giulio, M., 2001. The non-universality of the genetic code: the universal ancestor was a progenote. J. Theor. Biol. 209, 345–349. Di Giulio, M., 2006. The non-monophyletic origin of the tRNA molecule and the origin of genes only after the evolutionary stage of the Last Universal Common Ancestor (LUCA). J. Theor. Biol. 240, 343–352. Di Giulio, M., 2010. Biological evidence against the panspermia. J. Theor. Biol 266, 569–572. Di Giulio, M., 2011. The Last Universal Common ancestor (LUCA) and the ancestors of archaea and bacteria were progenotes. J. Mol. Evol. 72, 119–126. Di Giulio, M., 2014. On how many fundamental kinds of cells are present on Earth: looking for phylogenetic traits that would allow the identification of the primary lines of descent. J. Mol. Evol. 78, 313–320. Di Giulio, M., 2015. The non-biological meaning of the term "prokaryote" and its implications. J. Mol. Evol. 80, 98–101. Di Giulio, M., 2017. The indefinable term ‘prokaryote’ and the polyphyletic origin of genes. J. Genet. 96, 393–397. Di Giulio, M., 2018. On Earth, there would be a number of fundamental kinds of primary cells — cellular domains — greater than or equal to four. J. Theor. Biol. 443, 10–17. Di Giulio, M., 2019a. A qualitative criterion for identifying the root of the tree of life. J. Theor. Biol. 464, 126–131. Di Giulio, M., 2019b. The universal ancestor, the deeper nodes of the tree of life, and the fundamental types of primary cells (cellular domains). J. Theor. Biol. 460, 142–143. Doolittle, W.F., Brown, J.R., 1994. Tempo, mode, the progenote, and the universal root. Proc. Natl. Acad. Sci. USA 91, 6721–6728. Eme, L., Spang, A., Lombard, J., Stairs, C.W., Ettema, T.J.G., 2017. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723.
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