Impact Factor 4.076

The 3rd most cited journal in Microbiology

This article is part of the Research Topic

The quest for simple life

Perspective ARTICLE

Front. Microbiol., 19 October 2015 | https://doi.org/10.3389/fmicb.2015.01144

The evolution of early cellular systems viewed through the lens of biological interactions

  • 1Allan Wilson Centre for Molecular Ecology and Evolution, University of Canterbury, Christchurch, New Zealand
  • 2Biomolecular Interaction Centre, University of Canterbury, Christchurch, New Zealand
  • 3School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
  • 4Department of Biochemistry and Biophysics, Arrhenius Laboratories, Stockholm University, Stockholm, Sweden
  • 5Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, Kalmar, Sweden
  • 6Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA
  • 7Yale Systems Biology Institute, Yale University, New Haven, CT, USA

The minimal cell concept represents a pragmatic approach to the question of how few genes are required to run a cell. This is a helpful way to build a parts-list, and has been more successful than attempts to deduce a minimal gene set for life by inferring the gene repertoire of the last universal common ancestor, as few genes trace back to this hypothetical ancestral state. However, the study of minimal cellular systems is the study of biological outliers where, by practical necessity, coevolutionary interactions are minimized or ignored. In this paper, we consider the biological context from which minimal genomes have been removed. For instance, some of the most reduced genomes are from endosymbionts and are the result of coevolutionary interactions with a host; few such organisms are “free-living.” As few, if any, biological systems exist in complete isolation, we expect that, as with modern life, early biological systems were part of an ecosystem, replete with organismal interactions. We favor refocusing discussions of the evolution of cellular systems on processes rather than gene counts. We therefore draw a distinction between a pragmatic minimal cell (an interesting engineering problem), a distributed genome (a system resulting from an evolutionary transition involving more than one cell) and the looser coevolutionary interactions that are ubiquitous in ecosystems. Finally, we consider the distributed genome and coevolutionary interactions between genomic entities in the context of early evolution.

Introduction

The minimal genome concept is a theoretical idea that has been considered in two different arenas. One is synthetic biology, an area of biological engineering where there is interest in establishing the minimal machinery for a cell (Peterson and Fraser, 2001; Dewall and Cheng, 2011; Juhas et al., 2011; Acevedo-Rocha et al., 2013). The other is in cell origins, where there has been interest in establishing the nature of early cellular systems (Mushegian, 1999; Koonin, 2003). Synthetic biology has made strong technical advances, with key proof-of-principle results such as systematically screening for essential genes (Hutchison et al., 1999; Glass et al., 2006), synthetic genome assembly (Gibson et al., 2008), transformation of a cell with a chemical genome (Gibson et al., 2010), and the development of computational cellular models derived from genomic knowledge (Karr et al., 2012).

The synthetic biology approach to minimal cells is pragmatic, though of unclear value to evolutionary questions pertaining to cellular origins. As an engineering project it is very productive and has a straightforward definition: it is simply the microbe with the smallest genome that is able to grow in axenic culture. There may of course be numerous minimal genomes for growth media, and hence there need not be a definitive minimal genome (Smalley et al., 2003; Dewall and Cheng, 2011; Juhas et al., 2014). On the criterion of growth in axenic culture, an organism can be designated “free-living” if it can be cultured in the absence of other organisms. Through this criterion, Mycoplasma genitalium is a good candidate for a minimal genome (Hutchison et al., 1999), though growing it in this way has the effect of removing it completely from its natural context, where, as an obligate intracellular pathogen, it is not in the least bit free-living (Dewall and Cheng, 2011).

In contrast, the use of comparative genomics to reconstruct the hypothetical last universal common ancestor (LUCA) has been less successful. A range of studies indicate that few genes are common to all three domains of life (Bacteria, Archaea, and Eukaryotes), and fewer still can be said to have an evolutionary history consistent with placement in some hypothetical common ancestor (Harris et al., 2003; Koonin, 2003; Hoeppner et al., 2012; Goldman et al., 2013). Horizontal gene transfer (Koonin, 2003), secondary gene losses (Becerra et al., 1997), and loss of evolutionary signal (Penny and Poole, 1999; Penny and Zhong, 2014) all obscure or erase early evolutionary history. It is not clear how to establish which, if any, of the many processes for extracting a living from the environment is the most ancient (though opinions abound), and it seems there is little to be gained from revisiting this question with ever larger genomic datasets. Moreover, there is no reason to expect that the LUCA was in any way a minimal cell, and it is difficult to equate the two, other than to assess the core of processes common to known biological systems (Goldman et al., 2013). The common ground between these efforts is that both the LUCA and the minimal cell concept focus on the internal parts-list of the genome: the gene set.

The point of this piece is to begin thinking about early evolution against the backdrop of biological interactions. We think that this is helpful for several reasons. First, systems that exist in isolation are probably the exception rather than the rule. Second, evolutionary transitions theory has provided the means by which to understand the emergence of complex systems, from replicators to cells to eukaryote cells with organelles, and is prefaced on interactions.

As a way to navigate this topic, we briefly summarize three concepts:

1. The pragmatic minimal genome concept

2. The evolutionarily stable distributed genome

3. Coevolutionary ecosystem interactions

We will then consider how biological interactions may help inform our understanding of early evolution.

The Pragmatic Minimal Genome Concept

As mentioned above, the pragmatic minimal genome concept has a straightforward definition. It is part of the wider question in biology of establishing, for any system, what is essential and what is functionally critical. “Essential” and “functionally critical” sound identical, but are not. In transposon mutagenesis studies, the definition of essential derives from whether a gene can be knocked out. For instance, two paralogs may each be knocked out individually, such that global transposon mutagenesis (Hutchison et al., 1999) and related Tn-seq methods (Barquist et al., 2013) would designate each a non-essential gene. However, if knocking out both is lethal, then having at least one of these genes is functionally critical: without one of these genes, the function is not maintained. Hence the process is functionally critical, but the individual genes are not essential. It is this combinatorics problem (establishing how many genes can be knocked out simultaneously) that makes generating, rather than inferring, a minimal genome such a challenge.

From the point of view of a minimal cellular system, growth in axenic culture focuses enquiry on individual cells, in the context of a controlled environment. However, it has been pointed out that some model systems are neither naturally free-living nor autotrophic, so are clearly dependent on other organisms (Dewall and Cheng, 2011). In this view, free-living autotrophs would constitute a more appropriate system, because they can grow on a minimal medium composed of simple compounds that may have an abiotic origin. That said, it is clear that organismal and ecological interactions are not absent from candidate minimal species such as Prochlorococcus (Coleman and Chisholm, 2007; Lindell et al., 2007). Indeed, Prochlorococcus lacks catalase and has been shown to be dependent upon the hydrogen peroxide scavenging capacity of other microbes (Morris et al., 2011). More generally, genomic streamlining may drive loss of expensive, leaky traits as these can be derived through interactions (Morris, 2015). There may well be cellular entities that have few or no interactions with other biological systems—perhaps in deep subsurface communities where chemolithoautotrophs derive resources directly from mineral sources, there are few interactions because cell densities are low. A recent study estimates <1 cell/gram of sediment in samples from 2.5 km below the sea floor (Inagaki et al., 2015). Such extremes aside, it seems likely that most microbes do not exist in splendid isolation.

Against this backdrop of interactions, that genomes smaller than that of M. genitalium derive from bacterial endosymbionts indicates that, while genomes with fewer genes do exist, they do so not in isolation, but in close interaction. In comparison to the inferred minimal genome of M. genitalium, which carries an estimated 382 genes (Glass et al., 2006), the genome sequence of Carsonella, an endosymbiont of psyllids, is both smaller and carries fewer genes (160 kb, 182 open reading frames (ORFs); Nakabachi et al., 2006). However in this instance, it seems that this endosymbiont has too few genes to perform all the processes required for independent reproduction. Thus, endosymbionts such as Carsonella fall outside the pragmatic minimal genome concept. That said, if we ignore the biological context required for reproduction, replicating entities can carry much less genetic information than Carsonella. The logical, though absurd, endpoint is a minimal replicating element (Wegrzyn, 2001), which at its extreme is a single nucleotide [see (Dawkins, 1982) who noted this and labeled it “reductio ad absurdum,” and Griffiths and coworkers for subsequent discussion (Griffiths and Neumann-Held, 1999; Sterelny and Griffiths, 1999)].

The Evolutionarily Stable Distributed Genome

While the genome of Carsonella is a stunning example of a highly-reduced endosymbiont genome, the context of the endosymbiont is clearly key—it is only possible to understand the genome within the context of coevolution with its host. In a number of cases, it seems that the host and endosymbiont have become so tightly integrated that one cannot exist without the other.

Indeed, endosymbionts like Carsonella and Buchnera, the maternally-inherited obligate endosymbiont of aphids, may well be on their way to becoming organelles, owing to ongoing genome reduction (Andersson, 2000, 2006). Taken in this light, their genomes are much more intact than genomes resulting from much older endosymbiotic interactions, such as the mitochondrion and chloroplast, and diminutive nucleomorph genomes resulting from secondary endosymbiosis (Archibald, 2007). The logical genomic endpoint of reductive evolution is an organelle without genes. This is seen in hydrogenosomes, the majority of which now completely lack DNA [though some carry genomes larger than the human mitochondrial genome (de Graaf et al., 2011)]. In this instance, the process of genome integration is complete, as all genes have relocated to a single compartment (the nucleus). In most cases, this endpoint may not be possible: the redox regulation of gene expression may necessitate the retention of genes in both chloroplasts and mitochondria (Allen, 2015).

Thus, some endosymbiont genomes clearly derive from free-living lineages, but may be difficult or impossible to grow in axenic culture, as they are far too dependent upon their host. In these instances, they may be well on the way to becoming part of a distributed genome. By this, we mean that the set of essential genes are distributed across multiple genomes in the same cell (perhaps organism) and coevolve and operate as a single evolutionary unit. In this respect distributed genomes are an evolutionarily stable state deriving from what once were individual entities (Maynard Smith, 1991; Kiers and West, 2015; Szathmáry, 2015). The “minimal number” of genes retained in one compartment is clearly less informative than this broader evolutionary understanding of the process.

More generally, the distinction between the state immediately prior to the evolutionary transition and directly after may be difficult to assess, and, in terms of genetic events, a bit of a holy grail: it may be futile to try to state which genetic change—a specific instance of gene loss, compartmental transfer, or coevolutionary molecular interaction—was the point at which the transition occurred. There is nothing to say transitions require one specific discrete change, though, viewed as a spectrum from pre-transition to post-transition, there are states that are clearly one or the other. Considered as a process, whether there is an exact event becomes less important.

One final point requires us to return to the example of Mycoplasma, where, because it is an obligate intracellular parasite, there is an asymmetry to the dependency: the parasite can become highly specialized and dependent upon its host, while the host would be quite happy in the absence of the parasite, even if it may have coevolved in its presence. Note that this kind of “extended genome” is not an evolutionary unit, so does not fit the above definition of a distributed genome.

The Isolated Minimal Genome Versus Coevolutionary Systems

Distributed genomes are the product of an evolutionary transition, where none of the parties can revert to the ancestral, unintegrated state. Distributed genomes have clearly emerged in the evolution of the eukaryote cell (Szathmáry, 2015), and in secondary endosymbiosis (Curtis et al., 2012). This process has clearly been repeated multiple times in eukaryote evolution, and interactions between eukaryote hosts and their bacterial endosymbionts may represent early stages in this process (Poole and Penny, 2007). Thus, endosymbionts that are well on the spectrum to becoming organelles are not minimal genomes, but may be part of an emerging distributed genome, though it may be difficult in practice to determine the tipping point at which a set of closely interacting individuals becomes an evolutionarily stable, distributed genome.

As mentioned earlier, it seems difficult to imagine many biological systems that exist in total isolation. In that respect, most biological systems involve genome interactions at some level, and many of the species with the most minimal genomes show extensive genome-level dependencies. Consider the following thought experiment:

“Try to imagine a plant that can survive and reproduce in a real ecosystem without using, in addition to its nuclear genome, most of the following: a mitochondrial genome (to convert energy); a chloroplast genome (to regulate photosynthesis); one or more mycorrhizal fungal genomes (to improve nutrient and water uptake); the genomes of pollinators (to assist in reproduction); and the genomes of a few birds, mammals, or ants (to move seeds around the ecosystem).” (Thompson, 2006)

This illustration at once indicates that few, if any, genomes exist in genuine isolation from any other genome. In that respect, it may be tempting to state that the pragmatic minimal genome, by only requiring growth in axenic culture, utterly divorces the genome from its biology. In one respect, that is certainly the case: it is an extreme that follows from isolating the organism from its lifestyle, and which focuses on a very different research question than the ecological one raised above. However, this ecological idea could conceivably be taken to another extreme—that all life is a globally-distributed genome. Indeed, there has been some debate along these lines in ecological circles (Dagg, 2002, 2003). While few would subscribe to a “genomic Gaia,” this point is relevant because this type of model has been mooted in models of early cellular life, where the ideas of a planetary megaorganism (Mathieu and Sonea, 1995) or communal ancestor driven by global horizontal gene transfer (Woese, 2002; Goldenfeld and Woese, 2007) have become popular (Kim and Caetano-Anolles, 2011). There is every reason to expect horizontal gene transfer to have played an important role in early evolution, where it may have contributed to the emergence of the modern genetic code (Vetsigian et al., 2006). However, the difficulty for both some sort of genomic Gaia and microbial planetary megaorganisms is that they both rely on strong group selection and ignore the effect of selection at lower levels (Dawkins, 1982; Williams, 1992; Dagg, 2003; Poole, 2009; Szathmáry, 2015).

Difficulties with the communal ancestor model in light of levels of selection has been discussed in detail elsewhere (Poole, 2009), but one general difficulty with this class of model is that it is susceptible to parasites. Indeed, some simple systems such as hypercycles (where each gene in the cycle replicates itself and the next gene in the cycle) can be crashed by a parasite (an element that prefers to replicate instead of the next gene in the cycle; Maynard Smith, 1979). Such cycles are stable where there are barriers to interaction (Boerlijst and Hogeweg, 1991), which moves us away from a communal ancestor, where transfer barriers do not exist and are in fact selected against (Woese, 1998). Moreover, cellular membranes would in themselves represent a natural barrier to gene transfer (thus requiring the evolution of active transfer processes; Poole, 2009), suggesting a system where gene transfer was dominant and vertical inheritance insignificant would be difficult to explain on biophysical grounds. Finally, mobile elements that spread effectively through horizontal gene transfer have evolved to exclude competitors. A good example of these are toxin-antitoxin systems, which, when coded on a plasmid, will exclude other elements via a process of post-segregational killing (Cooper and Heinemann, 2000, 2005). In this process, competitor plasmids cannot invade the population because loss of the incumbent—toxin-antitoxin bearing—plasmid leads to cell death (because the toxin is longer-lived than the antitoxin, so loss of both genes leads to toxin-induced death). As a result, any displacement events are ultimately futile. One class of toxin-antitoxin system that has a broader effect on transfer are restriction-modification systems, which consist of a modification methylase, that marks DNA at specific palindromic motifs, and a restriction endonuclease, which cleaves at those same motifs, but only if they are not methylated. This leads to the cleavage of any DNA that comes into the cell from a foreign source (viruses, plasmids and cells lacking the restriction-modification system; Naito et al., 1995, 1998), so is a form of molecular patch-protection by a horizontally-transmitted parasite. The net effect is thus that all transfer events are reduced. Thus, we conclude that all three of these effects (unhindered parasitic spread, biophysical barriers, and reduction in transfer levels by horizontal replicators) all speak against a communal ancestor model.

In summary, the simple answer to why a globally-distributed genome is not viable in the forms presented thus far is that they confuse interactions between entities (be they mobile genes interacting via co-occupancy of compartments or organisms interacting in an ecosystem) and levels of selection (Poole, 2009). The theoretical tools to resolve this are well developed—this is the theory of evolutionary transitions (Szathmáry, 2015).

Implications for Early Evolution

It is our view that the pragmatic approach to minimal genomes works completely adequately for synthetic biology. Though the combinatoric problem of shaving genes from the parts list may be difficult in practice, an approximate answer can be arrived at and incrementally improved. A completely different approach is building a cell completely from scratch, as per Gánti’s chemoton model (Gánti, 2003). Though at present a theoretical conception, it has value for both origins and as an alternative approach to the genome design question owing to its generalization of the problem. The area where we think that the minimal genome concept is less pragmatic, and more in need of discussion, is with regard to early evolution. We therefore end with a brief consideration of the three concepts described in this paper: pragmatic minimal, distributed genome, and coevolutionary interaction.

In the case of the pragmatic minimal genome, the genome is studied in complete isolation. Under a model where cells emerge from an abiotic environment, minimal cellular systems would be autotrophs of some kind with a minimal set of environmental interactions. This is possible, but ignores how cells evolved in the first place. It is clear that early pre-cellular systems are the product of gene-level interactions. The emergence of entities such as chromosomes and cells are still best understood in terms of evolutionary transitions following on from interactions between individual entities (Szathmáry, 2015), and there is emerging experimental support for cooperative behavior as a feature of RNA-based systems (Vaidya et al., 2012; Higgs and Lehman, 2015). Second, it suggests that our view of LUCA has been far too skewed toward a parts-list, and removes the cell from its surrounds. In that regard, the ideas of Forterre, who has championed coevolutionary interactions between viruses and cells as an important feature of early evolution (Forterre, 2006; Forterre and Prangishvili, 2009), help us in appreciating that cells probably never existed in isolation. As nicely explained by Gogarten and colleagues (Fullmer et al., 2015), both Black Queen evolution, where interdependencies emerge following loss from some individuals of a leaky common good gene (it is leaky because producers cannot monopolize the product), and horizontal transfer of pan-genome genes between individuals both involve coevolutionary interactions.

We also need to be careful not to overextend the reach of biological interactions. As discussed above, this has been done repeatedly in other areas of biology, mostly because of a misunderstanding of which levels selection operates. In this regard, a communal ancestor or megaorganism model is problematic because, from the perspective of levels of selection, the megaorganism is no different from the unworkable Gaia hypothesis. In its form of a single, interconnected communal system, it can only work if there are multiple communal ancestors interacting and competing for a common resource. This point is no different from the point Dawkins made in regard to Gaia requiring earth-like planets in competition for the same resource (Dawkins, 1982). The important point here is that, theoretically, both can work—Gaia works if multiple planets are competing(!), and a communal ancestor/megaorganism only if multiple separate communal ancestors are in direct competition. That seems difficult, and, importantly, is unnecessary, if the main point of the communal ancestor is to highlight the potential for horizontal gene transfer to contribute to early evolution: it is possible to have gene transfer without invoking this extreme. Thus, the lesson of past errors of interpretation is clear: in refocusing on interactions, we need to keep levels of selection front and centre.

Thus, in the world before eukaryote cells, which were the first entities with distributed genomes (an evolutionary transition), interactions between cells were effectively a set of ecological interactions (akin to the mycorrhizal fungi, pollinators and seed dispersers in the scenario quoted from Thompson, above). The real difficulty is that metabolic interactions between early cells are completely invisible to us. It may therefore be most productive to study processes such as the emergence and evolutionary stability of ecological interactions (Foster and Wenseleers, 2006; Morris et al., 2014; Oliveira et al., 2014; Morris, 2015) rather than searching for historical interactions. In that regard, it is worth noting that simple ecological interactions can be described as hypercycles (Maynard Smith and Szathmáry, 1995). More practically, minimal ecosystems (Guerrero et al., 2002), modeling (Oliveira et al., 2014), and experimental study of Black Queen evolution (Morris et al., 2014) and syntrophic interactions (Mee et al., 2014) all suggest a productive way forward for the study of the evolution of early cellular life, as these place both genome and organism in a biological context.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

AP is supported by a Rutherford Discovery Fellowship from the Royal Society of New Zealand (RDF-11-UOC-013). Past support to AP from the Royal Swedish Academy of Sciences and the Swedish Research Council during the inception of this work is gratefully acknowledged.

References

Acevedo-Rocha, C. G., Fang, G., Schmidt, M., Ussery, D. W., and Danchin, A. (2013). From essential to persistent genes: a functional approach to constructing synthetic life. Trends Genet. 29, 273–279. doi: 10.1016/j.tig.2012.11.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Allen, J. F. (2015). Why chloroplasts and mitochondria retain their own genomes and genetic systems: colocation for redox regulation of gene expression. Proc. Natl. Acad. Sci. U.S.A. 112, 10231–10238. doi: 10.1073/pnas.1500012112

PubMed Abstract | CrossRef Full Text | Google Scholar

Andersson, J. O. (2000). Evolutionary genomics: is Buchnera a bacterium or an organelle? Curr. Biol. 10, R866–R868. doi: 10.1016/s0960-9822(00)00816-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Andersson, S. G. (2006). Genetics. The bacterial world gets smaller. Science 314, 259–260. doi: 10.1126/science.1133739

PubMed Abstract | CrossRef Full Text | Google Scholar

Archibald, J. M. (2007). Nucleomorph genomes: structure, function, origin and evolution. Bioessays 29, 392–402. doi: 10.1002/bies.20551

PubMed Abstract | CrossRef Full Text | Google Scholar

Barquist, L., Boinett, C. J., and Cain, A. K. (2013). Approaches to querying bacterial genomes with transposon-insertion sequencing. RNA Biol. 10, 1161–1169. doi: 10.4161/rna.24765

PubMed Abstract | CrossRef Full Text | Google Scholar

Becerra, A., Islas, S., Leguina, J. I., Silva, E., and Lazcano, A. (1997). Polyphyletic gene losses can bias backtrack characterizations of the cenancestor. J. Mol. Evol. 45, 115–118. doi: 10.1007/PL00006209

PubMed Abstract | CrossRef Full Text | Google Scholar

Boerlijst, M. C., and Hogeweg, P. (1991). Spiral wave structure in pre-biotic evolution: hypercycles stable against parasites. Physica D 48, 17–28. doi: 10.1016/0167-2789(91)90049-F

CrossRef Full Text | Google Scholar

Coleman, M. L., and Chisholm, S. W. (2007). Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol. 15, 398–407. doi: 10.1016/j.tim.2007.07.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Cooper, T. F., and Heinemann, J. A. (2000). Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc. Natl. Acad. Sci. U.S.A. 97, 12643–12648. doi: 10.1073/pnas.220077897

PubMed Abstract | CrossRef Full Text | Google Scholar

Cooper, T. F., and Heinemann, J. A. (2005). Selection for plasmid post-segregational killing depends on multiple infection: evidence for the selection of more virulent parasites through parasite-level competition. Proc. Biol. Sci. 272, 403–410. doi: 10.1098/rspb.2004.2921

PubMed Abstract | CrossRef Full Text | Google Scholar

Curtis, B. A., Tanifuji, G., Burki, F., Gruber, A., Irimia, M., Maruyama, S., et al. (2012). Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492, 59–65. doi: 10.1038/nature11681

PubMed Abstract | CrossRef Full Text | Google Scholar

Dagg, J. L. (2002). Unconventional bed mates: gaia and the selfish gene. Oikos 96, 182–186. doi: 10.1034/j.1600-0706.2002.960120.x

CrossRef Full Text | Google Scholar

Dagg, J. L. (2003). Ecosystem organization as side-effects of replicator and interactor activities. Biol. Philos. 18, 491–492. doi: 10.1023/A:1024128115666

CrossRef Full Text | Google Scholar

Dawkins, R. (1982). The Extended Phenotype: The Long Reach of the Gene. Oxford: Oxford University Press.

Google Scholar

de Graaf, R. M., Ricard, G., Van Alen, T. A., Duarte, I., Dutilh, B. E., Burgtorf, C., et al. (2011). The organellar genome and metabolic potential of the hydrogen-producing mitochondrion of Nyctotherus ovalis. Mol. Biol. Evol. 28, 2379–2391. doi: 10.1093/molbev/msr059

PubMed Abstract | CrossRef Full Text | Google Scholar

Dewall, M. T., and Cheng, D. W. (2011). The minimal genome: a metabolic and environmental comparison. Brief. Funct. Genomics 10, 312–315. doi: 10.1093/bfgp/elr030

PubMed Abstract | CrossRef Full Text | Google Scholar

Forterre, P. (2006). The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16. doi: 10.1016/j.virusres.2006.01.010

PubMed Abstract | CrossRef Full Text | Google Scholar

Forterre, P., and Prangishvili, D. (2009). The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann. N. Y. Acad. Sci. 1178, 65–77. doi: 10.1111/j.1749-6632.2009.04993.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Foster, K. R., and Wenseleers, T. (2006). A general model for the evolution of mutualisms. J. Evol. Biol. 19, 1283–1293. doi: 10.1111/j.1420-9101.2005.01073.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Fullmer, M. S., Soucy, S. M., and Gogarten, J. P. (2015). The pan-genome as a shared genomic resource: mutual cheating, cooperation and the black queen hypothesis. Front. Microbiol. 6:728. doi: 10.3389/fmicb.2015.00728

PubMed Abstract | CrossRef Full Text | Google Scholar

Gánti, T. (2003). The Principles of Life. Oxford: Oxford University Press.

Google Scholar

Gibson, D. G., Benders, G. A., Andrews-Pfannkoch, C., Denisova, E. A., Baden-Tillson, H., Zaveri, J., et al. (2008). Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science 319, 1215–1220. doi: 10.1126/science.1151721

PubMed Abstract | CrossRef Full Text | Google Scholar

Gibson, D. G., Glass, J. I., Lartigue, C., Noskov, V. N., Chuang, R. Y., Algire, M. A., et al. (2010). Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329, 52–56. doi: 10.1126/science.1190719

PubMed Abstract | CrossRef Full Text | Google Scholar

Glass, J. I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M. R., Maruf, M., et al. (2006). Essential genes of a minimal bacterium. Proc. Natl. Acad. Sci. U.S.A. 103, 425–430. doi: 10.1073/pnas.0510013103

PubMed Abstract | CrossRef Full Text | Google Scholar

Goldenfeld, N., and Woese, C. (2007). Biology’s next revolution. Nature 445, 369. doi: 10.1038/445369a

PubMed Abstract | CrossRef Full Text | Google Scholar

Goldman, A. D., Bernhard, T. M., Dolzhenko, E., and Landweber, L. F. (2013). LUCApedia: a database for the study of ancient life. Nucleic Acids Res. 41, D1079–D1082. doi: 10.1093/nar/gks1217

PubMed Abstract | CrossRef Full Text | Google Scholar

Griffiths, P. E., and Neumann-Held, E. M. (1999). The many faces of the gene. Bioscience 49, 656–662. doi: 10.2307/1313441

CrossRef Full Text | Google Scholar

Guerrero, R., Piqueras, M., and Berlanga, M. (2002). Microbial mats and the search for minimal ecosystems. Int. Microbiol. 5, 177–188. doi: 10.1007/s10123-002-0094-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Harris, J. K., Kelley, S. T., Spiegelman, G. B., and Pace, N. R. (2003). The genetic core of the universal ancestor. Genome Res. 13, 407–412. doi: 10.1101/gr.652803

PubMed Abstract | CrossRef Full Text | Google Scholar

Higgs, P. G., and Lehman, N. (2015). The RNA World: molecular cooperation at the origins of life. Nat. Rev. Genet. 16, 7–17. doi: 10.1038/nrg3841

PubMed Abstract | CrossRef Full Text | Google Scholar

Hoeppner, M. P., Gardner, P. P., and Poole, A. M. (2012). Comparative analysis of RNA families reveals distinct repertoires for each domain of life. PLoS Comput. Biol. 8:e1002752. doi: 10.1371/journal.pcbi.1002752

PubMed Abstract | CrossRef Full Text | Google Scholar

Hutchison, C. A., Peterson, S. N., Gill, S. R., Cline, R. T., White, O., Fraser, C. M., et al. (1999). Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165–2169. doi: 10.1126/science.286.5447.2165

PubMed Abstract | CrossRef Full Text | Google Scholar

Inagaki, F., Hinrichs, K. U., Kubo, Y., Bowles, M. W., Heuer, V. B., Hong, W. L., et al. (2015). DEEP BIOSPHERE. Exploring deep microbial life in coal-bearing sediment down to ∼2.5 km below the ocean floor. Science 349, 420–424. doi: 10.1126/science.aaa6882

PubMed Abstract | CrossRef Full Text | Google Scholar

Juhas, M., Eberl, L., and Glass, J. I. (2011). Essence of life: essential genes of minimal genomes. Trends Cell Biol. 21, 562–568. doi: 10.1016/j.tcb.2011.07.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Juhas, M., Reuss, D. R., Zhu, B., and Commichau, F. M. (2014). Bacillus subtilis and Escherichia coli essential genes and minimal cell factories after one decade of genome engineering. Microbiology 160, 2341–2351. doi: 10.1099/mic.0.079376-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Karr, J. R., Sanghvi, J. C., Macklin, D. N., Gutschow, M. V., Jacobs, J. M., Bolival, B., et al. (2012). A whole-cell computational model predicts phenotype from genotype. Cell 150, 389–401. doi: 10.1016/j.cell.2012.05.044

PubMed Abstract | CrossRef Full Text | Google Scholar

Kiers, E. T., and West, S. A. (2015). Evolutionary biology. Evolving new organisms via symbiosis. Science 348, 392–394. doi: 10.1126/science.aaa9605

PubMed Abstract | CrossRef Full Text | Google Scholar

Kim, K. M., and Caetano-Anolles, G. (2011). The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol. Biol. 11:140. doi: 10.1186/1471-2148-11-140

PubMed Abstract | CrossRef Full Text | Google Scholar

Koonin, E. V. (2003). Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat. Rev. Microbiol. 1, 127–136. doi: 10.1038/nrmicro751

PubMed Abstract | CrossRef Full Text | Google Scholar

Lindell, D., Jaffe, J. D., Coleman, M. L., Futschik, M. E., Axmann, I. M., Rector, T., et al. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86. doi: 10.1038/nature06130

PubMed Abstract | CrossRef Full Text | Google Scholar

Mathieu, L. G., and Sonea, S. (1995). A powerful bacterial world. Endeavour 19, 112–117. doi: 10.1016/0160-9327(95)97496-U

PubMed Abstract | CrossRef Full Text | Google Scholar

Maynard Smith, J. (1979). Hypercycles and the origin of life. Nature 280, 445–446. doi: 10.1038/280445a0

PubMed Abstract | CrossRef Full Text | Google Scholar

Maynard Smith, J. (1991). “A Darwinian view of symbiosis,” in Symbiosis as a Source of Evolutionary Innovation, eds L. Margulis and R. Fester (Cambridge, MA: MIT Press), 26–39.

Google Scholar

Maynard Smith, J., and Szathmáry, E. (1995). The Major Transitions in Evolution. Oxford: W. H. Freeman/Spektrum.

Google Scholar

Mee, M. T., Collins, J. J., Church, G. M., and Wang, H. H. (2014). Syntrophic exchange in synthetic microbial communities. Proc. Natl. Acad. Sci. U.S.A. 111, E2149–E2156. doi: 10.1073/pnas.1405641111

PubMed Abstract | CrossRef Full Text | Google Scholar

Morris, J. J. (2015). Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet. 31, 475–482. doi: 10.1016/j.tig.2015.05.004

PubMed Abstract | CrossRef Full Text | Google Scholar

Morris, J. J., Johnson, Z. I., Szul, M. J., Keller, M., and Zinser, E. R. (2011). Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean’s surface. PLoS ONE 6:e16805. doi: 10.1371/journal.pone.0016805

PubMed Abstract | CrossRef Full Text | Google Scholar

Morris, J. J., Papoulis, S. E., and Lenski, R. E. (2014). Coexistence of evolving bacteria stabilized by a shared Black Queen function. Evolution 68, 2960–2971. doi: 10.1111/evo.12485

PubMed Abstract | CrossRef Full Text | Google Scholar

Mushegian, A. (1999). The minimal genome concept. Curr. Opin. Genet. Dev. 9, 709–714. doi: 10.1016/S0959-437X(99)00023-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Naito, T., Kusano, K., and Kobayashi, I. (1995). Selfish behavior of restriction-modification systems. Science 267, 897–899. doi: 10.1126/science.7846533

PubMed Abstract | CrossRef Full Text | Google Scholar

Naito, Y., Naito, T., and Kobayashi, I. (1998). Selfish restriction modification genes: resistance of a resident R/M plasmid to displacement by an incompatible plasmid mediated by host killing. Biol. Chem. 379, 429–436. doi: 10.1515/bchm.1998.379.4-5.429

PubMed Abstract | CrossRef Full Text | Google Scholar

Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H. E., Moran, N. A., et al. (2006). The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267. doi: 10.1126/science.1134196

PubMed Abstract | CrossRef Full Text | Google Scholar

Oliveira, N. M., Niehus, R., and Foster, K. R. (2014). Evolutionary limits to cooperation in microbial communities. Proc. Natl. Acad. Sci. U.S.A. 111, 17941–17946. doi: 10.1073/pnas.1412673111

PubMed Abstract | CrossRef Full Text | Google Scholar

Penny, D., and Poole, A. (1999). The nature of the last universal common ancestor. Curr. Opin. Genet. Dev. 9, 672–677. doi: 10.1016/S0959-437X(99)00020-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Penny, D., and Zhong, B. (2014). Two fundamental questions about protein evolution. Biochimie doi: 10.1016/j.biochi.2014.10.020 [Epub ahead of print].

PubMed Abstract | CrossRef Full Text | Google Scholar

Peterson, S. N., and Fraser, C. M. (2001). The complexity of simplicity. Genome Biol. 2, comment2002.1–comment2002.8.

PubMed Abstract | Google Scholar

Poole, A. M. (2009). Horizontal gene transfer and the earliest stages of the evolution of life. Res. Microbiol. 160, 473–480. doi: 10.1016/j.resmic.2009.07.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Poole, A. M., and Penny, D. (2007). Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84. doi: 10.1002/bies.20516

PubMed Abstract | CrossRef Full Text | Google Scholar

Smalley, D. J., Whiteley, M., and Conway, T. (2003). In search of the minimal Escherichia coli genome. Trends Microbiol. 11, 6–8. doi: 10.1016/S0966-842X(02)00008-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Sterelny, K., and Griffiths, P. E. (1999). Sex and Death: An Introduction to the Philosophy of Biology. Chicago: Chicago University Press.

Google Scholar

Szathmáry, E. (2015). Toward major evolutionary transitions theory 2.0. Proc. Natl. Acad. Sci. U.S.A. 112, 10104–10111. doi: 10.1073/pnas.1421398112

PubMed Abstract | CrossRef Full Text | Google Scholar

Thompson, J. N. (2006). Ecology. Mutualistic webs of species. Science 312, 372–373. doi: 10.1126/science.1126904

PubMed Abstract | CrossRef Full Text | Google Scholar

Vaidya, N., Manapat, M. L., Chen, I. A., Xulvi-Brunet, R., Hayden, E. J., and Lehman, N. (2012). Spontaneous network formation among cooperative RNA replicators. Nature 491, 72–77. doi: 10.1038/nature11549

PubMed Abstract | CrossRef Full Text | Google Scholar

Vetsigian, K., Woese, C., and Goldenfeld, N. (2006). Collective evolution and the genetic code. Proc. Natl. Acad. Sci. U.S.A. 103, 10696–10701. doi: 10.1073/pnas.0603780103

PubMed Abstract | CrossRef Full Text | Google Scholar

Wegrzyn, G. (2001). The minimal genome paradox. J. Appl. Genet. 42, 385–392.

PubMed Abstract | Google Scholar

Williams, G. C. (1992). Gaia, nature worship and biocentric fallacies. Q. Rev. Biol. 67, 479–486. doi: 10.1086/417796

CrossRef Full Text | Google Scholar

Woese, C. (1998). The universal ancestor. Proc. Natl. Acad. Sci. U.S.A. 95, 6854–6859. doi: 10.1073/pnas.95.12.6854

PubMed Abstract | CrossRef Full Text | Google Scholar

Woese, C. R. (2002). On the evolution of cells. Proc. Natl. Acad. Sci. U.S.A. 99, 8742–8747. doi: 10.1073/pnas.132266999

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: minimal genome, distributed genome, last universal common ancestor, coevolution, evolutionary transitions, communal ancestor, levels of selection

Citation: Poole AM, Lundin D and Rytkönen KT (2015) The evolution of early cellular systems viewed through the lens of biological interactions. Front. Microbiol. 6:1144. doi: 10.3389/fmicb.2015.01144

Received: 07 August 2015; Accepted: 05 October 2015;
Published: 19 October 2015.

Edited by:

Luis Delaye, Centro de Investigación y de Estudios Avanzados del IPN Unidad Irapuato, Mexico

Reviewed by:

Marc Strous, University of Calgary, Canada
Jeffrey Morris, University of Alabama at Birmingham, USA

Copyright © 2015 Poole, Lundin and Rytkönen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Anthony M. Poole, anthony.poole@canterbury.ac.nz