Chapter 5: Major Biological Innovations in the History of Life on Earth

Abstract

All organisms living on Earth descended from a single, common ancestral population of cells, known as LUCA—the last universal common ancestor. Since its emergence, the diversity and complexity of life have increased dramatically. This chapter focuses on four key biological innovations throughout Earth's history that had a significant impact on the expansion of phylogenetic diversity, organismal complexity, and ecospace habitation. First is the emergence of the last universal common ancestor, LUCA, which laid the foundation for all life-forms on Earth. Second is the evolution of oxygenic photosynthesis, which resulted in global geochemical and biological transformations. Third is the appearance of a new type of cell—the eukaryotic cell—which led to the origin of a new domain of life and the basis for complex multicellularity. Fourth is the multiple independent origins of multicellularity, resulting in the emergence of a new level of complex individuality. A discussion of these four key events will improve our understanding of the intertwined history of our planet and its inhabitants and better inform the extent to which we can expect life at different degrees of diversity and complexity elsewhere.

As the only instance of known life, Earth life, and its evolutionary history, serves as the primary foundation for our predictions about possible life-forms elsewhere in the universe (see Chapter 8 and Chapter 9). Thus far, however, observations of life on this planet have yielded uncertain conclusions regarding the predictability of evolution. Evolutionary outcomes are frequently unpredictable because of contingencies relating to genetic background, environmental conditions, and ecological interactions (Blount et al., 2008). But these outcomes can be more repeatable due to constraints set by the physical and chemical properties of evolving systems and the deterministic force of natural selection, as in cases of convergent evolution. Exactly how contingency and determinism interact, especially over long periods of time, can strongly influence the predictability of evolution.

If life's history were nothing more than a series of idiosyncratic changes with no governing large-scale regularities, the task of making general predictions about life elsewhere in the universe would be in jeopardy. However, the apparent increases in diversity and average complexity of life over time give hope to the search for a common thread (see Chapter 2.5). To explain this pattern, it is necessary to understand, in relevant geological and ecological context, how life transitioned from prebiotic chemistry to the diversity of unicellular and multicellular organisms that exist today.

One of the most influential models to explain the increase in complexity over time was put forth by John Maynard Smith and Eörs Szathmáry (Maynard Smith and Szathmáry, 1995). They argued that the long-term trend in complexity was the result of a series of changes in the way that information is stored and transmitted, known as the “major transitions in evolution.” Although this model has drawn some criticism for combining different types of evolutionary processes into the same category (such as the evolution of the genetic code together with the evolution of sex and the evolution of language; McShea and Simpson, 2011; O'Malley and Powell, 2016), the remaining transitions (the origin of cells and chromosomes from groups of interacting replicators, the origin of the eukaryotic cell, the evolution of multicellularity, and the evolution of eusociality) share the common feature that smaller entities evolve to become specialized parts of new, “higher-level” entities. This idea set the foundation for subsequent works focused on transitions that involve a shift in the hierarchical complexity of organisms, termed major evolutionary transitions in individuality (Herron, 2021).

Although the theory of major transitions in individuality provides a comprehensive view of the evolution of hierarchical complexity, this framework falls short of capturing all the major evolutionary innovations that were pivotal to the history of life in several ways. For instance, it does not account for major biological innovations such as the evolution of oxygenic photosynthesis (O'Malley and Powell, 2016), an event of importance for the history of complex life on Earth but one that does not involve a transition in biological individuality (see Chapter 5.2). While this framework has been revolutionary for evolutionary theory, major evolutionary transitions in individuality may tell only part of the story of how life on Earth evolved greater complexity.

In addition to understanding evolutionary events that led to major biological innovations, the field of astrobiology seeks to discern whether life could exist in a particular environment, how life could impact the environments at a local or global scale, and how that environment, being modified by life, imparted new pressures that impacted the evolutionary trajectory of life. Single evolutionary events have been as important as the dynamic relationship between life and environment over time. Understanding these relationships might help us predict the probability that life could originate and the extent of biodiversity and complexity that could be expected to be found in an environment beyond Earth (see Chapter 7.1 and Chapter 8.3).

In this chapter we describe four major biological innovations in Earth's history that were key, directly or indirectly, to significant expansions in phylogenetic diversity and ecospace. Innovations covered in this chapter are (i) the origin of living systems from prebiotic chemistry and the emergence of life's last universal common ancestor (LUCA), (ii) the evolution of oxygenic photosynthesis, (iii) the evolution of the eukaryotic cell, and (iv) the evolution of multicellularity. This work is not intended to serve as an exhaustive list of the important events in life's history nor to present a conceptually unified synthesis of evolutionary theory. We considered the innovations chosen, arising within different domains of life, to be the most consequential in Earth's history due to their global impact, and thus the most relevant for and central to astrobiology (for more elaborated treatments, see Knoll and Bambach [2000], Ligrone [2019]).

5.1. When, Where, and How Did LUCA Emerge? Origins and Characteristics

All organisms on Earth can be traced back to a single common ancestor, the last universal common ancestor (LUCA). LUCA was most likely a self-replicating unit that harnessed many of the prebiotic chemical systems that were present on early Earth (see Chapter 4.2). To understand the evolutionary history of life and develop the capacity to predict whether a cellular system could emerge in another planet, it is essential to examine the transition from prebiotic chemistry to an enclosed cellular system that contained all the genes and metabolisms necessary for LUCA to evolve (see Chapter 4.4).

Genetic sequences shared universally among all modern bacteria and archaea were most likely present in LUCA and can provide some clues about LUCA's metabolism (Weiss et al., 2016). Analysis of a wide diversity of genomes from living organisms, looking for universally common genes, suggests that LUCA had a lipid membrane, a DNA-based genetic code, and 500–1000 protein-coding genes and was capable of RNA biosynthesis and translation to protein (Mushegian, 2008; Weiss et al., 2016).

Hypotheses about the origin of LUCA must therefore provide a plausible scenario that would facilitate the co-emergence of at least three components universal to all cells: (i) an informational aspect (how DNA and RNA became linked to metabolism, see Chapter 2.2.3.1 and Chapter 4.2.4.1), (ii) a catalytic aspect (how metabolism maintains the integrity of the cell and the generation of new cells, see Chapter 2.2.3.2 and Chapter 4.2.4.2), and (iii) a structural aspect (how metabolism was kept independent of the environment, see Chapter 2.2.3.3 and Chapter 4.2.4.4). It is also important to understand the identity, functionality, and ecology of LUCA and subsequent lineages. In other words, what organic molecules were available, and how did they assemble to eventually form LUCA and beyond?

5.1.1. The origin of LUCA's biological information system

All forms of life share the same genetic informational system: four nucleotides to store coding information about its proteins in RNA and the use of information in RNA as a blueprint to produce proteins (see Chapter 2.2.3.1). Proteins are built by the ribosome, a large biomolecule made of proteins and nucleic acids, that bridges two major functions required by living organisms: catalysis (which is the role of many proteins) and inheritance of information (which depends on nucleic acids). The association of the two ribosomal subunits allows separation of information transmission from catalysis reactions by using two different types of molecules. The ribosome is also present in all living cells. The nucleotide-based system of codification and the ribosomal system for translation into proteins is thus assumed to have been operating in LUCA. The only other known way for living cells to inherit functional information is with self-replicating ribozymes that operate catalysis and information transmission simultaneously. These ribozymes were likely present during the prebiotic period (Johnston et al., 2001).

The ribosome is the oldest RNA-protein complex in biological systems and produces proteins from information encoded in RNA. Ribosomes from all domains of life contain a structurally conserved common core, primarily composed of 2800 nucleotides and 28 ribosomal proteins (Bernier et al., 2018). The common core is composed of a large subunit (LSU) with a peptidyl transferase center (PTC) that synthesizes proteins via amide bond formation and peptide elongation, and a small subunit (SSU) with a decoding center (DCC) that selects the amino acid that corresponds to the appropriate nucleic acid sequence given by the mRNA that is being translated (Schmeing and Ramakrishnan, 2009). The informational and catalytic subunits of the ribosome are associated and highly conserved in three-dimensional structure in all organisms.

Archaea and bacteria (prokaryotes) share a common ribosomal core but have expanded segments beyond the common core with diverging ribosomal proteins and rRNA expansion segments. Eukaryotic ribosomes are generally larger than prokaryotic ones (Penev et al., 2020). This difference is due to expansions that emerge from a small number of conserved sites on the common core and are excluded from regions of essential ribosomal function until recently only observed in eukaryotes (Bernier et al., 2018).

The large and small ribosomal subunits appear to have formed independently and, only later, merged together (Fig. 5.1) (Petrov et al., 2015; Bowman et al., 2020). This association also marked the beginning of a transition from systems that replicated without coding ability to the one which was able to code. Early phases of rRNA evolution involved the functions of peptide bond catalysis and bridging of the two subunits. Later phases of rRNA evolution involved regions handling ribosomal fidelity, energetic requirements, and membrane localization (Petrov et al., 2015; Bowman et al., 2020). The modern ribosome appears to be a reasonable approximation of the rRNA in LUCA, although it is uncertain whether the two subunits had already assembled or operated separately.

FIG. 1.

The coevolution of LSU rRNA, SSU rRNA, tRNA, and proteins. Six phases of the accretion model led to the LUCA ribosome. In phase 1, RNAs form stem-loops and minihelices that begin to accrete. In phase 2, the peptidyl transferase center is formed and catalyzes condensation in the absence of coding. The SSU may have a single-stranded RNA binding function. In phase 3, the subunits gain mass. At the end of phase 3, the interface is acquired and the subunits associate, mediated by the expansion of tRNA from a minihelix to the modern L-shape. LSU and SSU evolution is independent and uncorrelated during phases 1 − 3. In phase 4, evolution of the subunits is correlated. The ribosome is a noncoding diffusive ribozyme in which proto-mRNA and the SSU act as positioning cofactors. In phase 5, the ribosome expands to an energy-driven, translocating, decoding machine. In phase 6, the ribosome matures, marking completion of the common core with a proteinized surface (the proteins are omitted for clarity). The colors of the rRNA and rProtein phases are blue-blue green and orange, respectively. mRNA is shown in light green. The A-site tRNA is magenta, the P-site tRNA is cyan, and the E-site tRNA is dark green. Adapted with permission from Bowman et al. (2020).

The only element of the ribosome that continually evolved throughout all phases of evolution is the exit tunnel (Yonath et al., 1987). The exit tunnel is where every coded protein leaves the ribosome and thus has a significant implication for the types of proteins that could be—and were—produced.

More details on the molecular mechanism of ribosomal evolution can be found in the supplementary material.

5.1.2. The origin of LUCA's cellular membrane

All cells are encapsulated by a semipermeable bilayer lipid membrane that controls the transport of biomolecules and maintains the internal physicochemical requirements for intracellular reactions (a capability termed “homeostasis”; see Chapter 2.2.3.4 and Chapter 4.2.4.4). A simple primordial membrane would have only required molecules with a nonpolar hydrocarbon moiety and a polar head group (i.e., an amphiphilic molecule; see Chapter 2.2.3.3). Under the right conditions, such as terrestrial water pools, hydrothermal vents, or in meteorites, these molecules can self-assemble into structures such as micelles or vesicles. Nascent membranes could have been composed of single-chain amphiphiles such as fatty acids, which could have formed via Fischer–Tropsch type reactions (see Chapter 4.2.3.5). Single-chain lipids such as fatty acids, once present at millimolar concentrations, spontaneously assemble into bilayers under high pH (Deamer, 2017). Stable vesicles are even more likely to form in mixtures of fatty acids and alcohols (Sarkar et al., 2020).

The prebiotic synthesis of peptide-based ion channels and pores may have been an important component of LUCA's membrane (Domagal-Goldman et al., 2016). Since water-soluble substrates cannot diffuse through the fatty-acid-based membrane as freely as small molecules like water, oxygen, and carbon dioxide, the evolution of channels and pores would have helped cells form a dynamic equilibrium between the interior and exterior environment (Dibrova et al., 2015; Domagal-Goldman et al., 2016). In addition, the nonpolar membrane prevents the free diffusion of monovalent cations, maintains ion gradients across the cellular membrane, and generates an electrochemical energy source that can be used for nutrient transport and other functions (Deamer, 2017).

5.1.3. The evolution of LUCA's metabolism

LUCA could have incorporated abiotic chemical cycles to generate energy for its maintenance and reproduction (Weiss et al., 2016). Metabolic cycles can transform carbon-containing molecules into cellular components. In the Archean, the atmosphere was anoxic (Lyons et al., 2014) and would have contained a variety of gases (H₂, CH₄, and CO₂), serving as a source of electrons or carbon (see Chapter 4.1.4). To build organic carbon, energy is required to transform inorganic carbon into longer and more complex molecules, a process called carbon fixation. Genomic analyses suggest that LUCA obtained energy and fixed carbon anaerobically from inorganic sources, consistent with the availability of inorganic components on early Earth. Furthermore, recent analyses examining an expanded pool of genes in modern genomes show that LUCA's predicted genome is similar to the genomes of microbes living in hydrothermal vents, generating energy from hydrogen through anaerobic metabolism (Weiss et al., 2016).

Earth life uses six different carbon fixation pathways, of which the Wood–Ljungdahl pathway (WLP) and the reverse tricarboxylic acid (rTCA) cycle are considered the most ancient (see Chapter 6.2.1; Berg, 2011). Extensive research has shown that the WLP and the rTCA cycle can occur abiotically if some naturally occurring organic precursors and inorganic catalysts are present, but there is no consensus as to which one would have appeared first or been produced in significant abundances for the cycle to persist (Martin and Russell, 2003).

The WLP was proposed previously to be the most ancient pathway (Fuchs, 2011), as this pathway is present in archaea and bacteria, and acetyl-coA synthase has a common root among all prokaryotes. Inferences from genomic analyses also suggest that LUCA used the WLP (Weiss et al., 2016). In contrast, the rTCA cycle is widespread among anaerobes or microaerobes but has not been found in archaea (Berg, 2011). Thus, it is possible that the rTCA cycle arose in bacteria after they diverged from LUCA. It has also been proposed that a complete or partial rTCA cycle may have once been linked to the WLP in an ancestral, possibly prebiotic, carbon fixation network (Braakman and Smith, 2012).

The reverse tricarboxylic acid (rTCA) cycle is a central anabolic biochemical pathway that fixes CO₂ into 3- to 6-carbon intermediates, such as acetyl-CoA, which then can then be used in a variety of biosynthetic pathways (e.g., amino acids, fatty acids). Experimental evidence indicates that an rTCA cycle can be catalyzed by Zn²⁺, Cr³⁺, and Fe⁰ in an anoxic, acidic aqueous solution and that primitive anabolism could have occurred in an acidic, metal-rich reducing Archean environment (Muchowska et al., 2017). Recent evidence also suggests that the prebiotic molecules glyoxylate and pyruvate can react to make a range of compounds that include chemical analogs to all the intermediary products in the TCA cycle, except for citric acid, resulting in a linear pathway instead. The WLP, like the rTCA cycle, is extremely sensitive to oxygen (Ragsdale and Pierce, 2008), but unlike the rTCA cycle, it is a linear pathway in which two CO₂ molecules are fixed to form the acetyl group of the central molecule acetyl-CoA. Recent experiments have demonstrated that the different biochemical steps in the WLP can also occur abiotically from CO₂ in the presence of iron and nickel, conditions typical of hydrothermal vents (Martin and Russell, 2007; Varma et al., 2018).

5.2. The Emergence of Metabolisms Producing and Consuming Oxygen

5.2.1. Energy and biosynthesis in an oxygen-starved early Earth

Geochemical evidence combined with genomic reconstructions of deeply rooted microorganisms (e.g., Archeoglobales, Thermotogales) suggests that the first metabolisms were anaerobic and fixed inorganic carbon. These metabolisms could have used CO₂, and H₂ or CH₄ (produced by methanogenesis from CO₂ and H₂) and reduced species of Fe and S as potential sources of energy (i.e., chemolithoautotrophy; see Chapter 6.2.1 and Table 6.1). Many enzymes involved in these anaerobic metabolisms contain Fe-S clusters or iron as cofactors (Chapter 4.2.6), suggesting a strong relationship between the evolution of metabolism and environmental conditions of the Hadean. Numerous microbes use anaerobic metabolisms today, which are based on redox reactions between compounds that needed to co-occur (Falkowski et al., 2008).

5.2.2. The evolution of light-driven metabolisms

The energetic limits of life dependent on chemoautotrophy were expanded by the biochemical innovation of using light to power chemical reactions (Overmann and Garcia-Pichel, 2006). The ability to use light to fix carbon is called photosynthesis. Photosynthesis employs a variety of biochemical complexes in coordination to extract electrons from an electron donor using light. Incoming photons change the redox potential of the electrons donated from an inorganic source (water, Fe²⁺, or several reduced forms of S) which are then transferred across a membrane to generate adenosine triphosphate (ATP; see Chapter 6.1.3). The by-products of the extractions of electrons from reduced iron or sulfur are their oxidized counterparts, and the by-product generated from water is oxygen.

Because light is widespread on Earth's surface and subsurface, photosynthesis expanded potential niches for microbial life. This allowed organisms that can utilize this metabolism—or its metabolic by-products like oxygen—to colonize and expand into new habitats (Lalonde and Konhauser, 2015; Camacho et al., 2017).

When life originated, the oxygen concentration in the ocean-atmosphere system was essentially zero (<0.001% of the present atmospheric oxygen level; Liu et al., 2019). However, by ∼2.4 Ga (billion years ago), oxygen had increased to about 1% of present atmospheric levels (Planavsky et al., 2014). This early increase in Earth's oxygen level was termed the Great Oxidation Event (GOE). For oxygen to have accumulated to inferred abundances on a timescale of a few million years, it must have been produced at a rate and quantity that outpaced its reduction by redox-active abiotic scavengers (such as reduced forms of Fe and S; see Chapter 4.1.2). Oxygen production at this rate likely resulted from biological catalysts, that is, microorganisms (Des Marais et al., 2002), which initially produced oxygen from photosynthesis as a metabolic by-product. Events that would have decreased O₂ reduction (thus facilitating accumulation) include geochemical events such as continental breakup and increased carbon burial (see Chapter 3.4.3.3).

Despite the significance of the GOE, oxygen in the ocean-atmosphere system stayed relatively low during the mid-Proterozoic (1.6–0.8 Ga)—although estimates vary, it was ∼1% of present levels (Planavsky et al., 2014). The partial pressure of O₂ could reach to modern-day levels only after two major oxygenation events: the first rise occurred between 800 million and 540 million years ago, and the second rise occurred between 450 million and 400 years ago (Alcott et al., 2019).

The evolution of photosynthesis is a highly debated topic (Hohmann-Marriott and Blankenship, 2011). Cyanobacteria are the most ancient and only prokaryotic lineage with the machinery for oxygen-producing photosynthesis and thus are thought to have produced the bulk of the oxygen that led to the GOE.

One model to explain the emergence of oxygenic photosynthesis argues that this metabolism arose from anoxygenic phototrophs, organisms that used iron or sulfur as electron donors for phototrophy and therefore did not produce oxygen (Blankenship and Hartman, 1998; Martin et al., 2018). Other models, which are based on comparisons of core reaction center proteins, suggest that oxygenic and anoxygenic phototrophy trace back to a common ancestor, implying that they evolved simultaneously (Sánchez-Baracaldo and Cardona, 2020). In either case, the widespread availability of sunlight and water, along with the high energetic yield of their photosystem, allowed phototrophs like cyanobacteria to outcompete their neighbors (Burnetti and Ratcliff, 2020). Their success was aided by the generation of oxygen, which was toxic to organisms relying on the rTCA cycle, the WLP, and similar pathways.

5.2.3. How oxygen dramatically changed the biosphere

The evolution of oxygenic photosynthesis was a milestone in the history of life because it resulted in a significant increase of oxygen in the atmosphere, consequently leading to an unprecedented expansion in the diversity and complexity of life. To begin with, the accumulation of O₂ led to the development of an ozone (O₃) layer that shields land-based life from UV damage (Kasting and Donahue, 1980). Photosynthesis also indirectly increased the rate of carbon cycling by orders of magnitude and increased the cycling rate of many inorganic compounds (Schlesinger, 2005). Organisms consuming CO₂ generated a positive feedback loop that depleted the excess CO₂ on Earth, lowering global temperatures. On the other hand, the emergence of organisms that produce CO₂ (from aerobic and anaerobic respiration) positively contributed to carbon levels. The balance between production and consumption eventually stabilized the global climate and is believed to have led to climatic recovery from low-temperature periods in Earth's history, referred to as “Snowball Earth” (Hoffman and Schrag, 2002).

In addition to impacting the availability of carbon and oxygen, the increase of O₂ in the atmosphere also affected the bioavailability of the other building blocks of life, such as nitrogen, phosphorus, and sulfur (see Chapter 2.2). Among these elements, nitrogen must be converted into the chemically active forms of ammonium and nitrate to participate in biochemical reactions. This is primarily achieved by bacteria and archaea that convert nitrogen to ammonium, allowing its usage as a building block or energy source. Anaerobic ammonia oxidation produces N₂, but with O₂, aerobic ammonia oxidation produces nitrite or nitrate. These nitrogen oxides can directly serve as electron acceptors for anaerobic respiration (Falkowski and Godfrey, 2008).

The primary abiotic source of reactive phosphorus (P) is weathering of highly insoluble calcium phosphate minerals (such as apatite) from rocks or in more reduced phases, such as schreibersite found in meteorites (Schlesinger, 2005; Pasek, 2017). It is possible that small continental land masses in the Hadean and early Archean limited the flux of P to early oceans (Bjerrum and Canfield, 2002), although lakes or ponds may have been able to accumulate significant concentrations of dissolved species (Toner and Catling, 2020). The bioavailability of P is typically the limiting nutrient in marine and continental photosynthesis over geological timescales (Planavsky et al., 2010; Guilbaud et al., 2020). Reduced P species might have reacted with prebiotic molecules on early Earth (Pasek et al., 2013). Additionally, P uptake could have played a role in the GOE around 2.4 Ga, potentially providing a significant nutrient source for oxygenic photosynthesis. This might have increased biological productivity and greater burial of reduced organic carbon (Domagal-Goldman et al., 2016).

Regarding sulfur (S), geological evidence shows that sulfate (SO₄^2-) levels increased from a few micromolar to millimolar levels at the same time as O₂ accumulated in the atmosphere. This is now an essential source of sulfur to all aerobic organisms, which cannot assimilate reduced forms (Shen and Buick, 2004). Oxygen would have catalyzed sulfur oxidation abiotically or biologically. In addition, SO₄^2- can be used by some anaerobic microbes as an electron acceptor to oxidize organic carbon (in anaerobic respiration) with the concomitant production of sulfide (H₂S) (Canfield, 1998).

5.3. Eukaryogenesis: The Emergence of the Eukaryotic Cell

The emergence of the eukaryotic cell is a major transition event in evolution: two lower-level units, an archaeal host, and a bacterial endosymbiont, merged and coevolved, forming a novel cell type (Maynard Smith and Szathmáry, 1995). This higher-level individual, classified as the third domain of cellular life, differs remarkably from the other two domains, that is, archaea and bacteria (Table 5.1). For instance, compared to bacteria and archaea, eukaryotic cells are much larger, biophysically elastic, and have a nucleus surrounded by a membrane envelope (Heim et al., 2017). These traits have enabled the evolution of motility and predation in various eukaryotic lineages. One key feature of eukaryotic cells is the presence of an organelle called the mitochondria. The mitochondrion has its own genome, and its reproduction is not tightly coupled to the host cell's reproduction. The inner mitochondrial membrane has an expanded surface area retaining proteins that transfer high-energy electrons to oxygen, significantly increasing the host cell's energy production efficiency (Brand, 1994; Lane, 2014).

Table 5.1.

Comparison of Notable Phenotypic Differences Among the Three Domains of Life

Characteristic	Bacteria	Archaea	Eukarya
Membrane-enclosed nucleus	No	No	Yes
Closed circular chromosome	Yes	Yes	No
Histones present	No	Yes	Yes
Peptidoglycan	Yes	No	No
Lipid linkage	Ester	Ether	Ester
Ribosomes	70S	70S	80S
Initiator tRNA	Formylmethionine	Methionine	Methionine
Introns in tRNA	No	Yes	Yes
RNA polymerase	One	Several	Three

This section discusses eukaryogenesis, the emergence of this new cell type, by tracking a few critical evolutionary events that occurred between the first eukaryotic common ancestor (FECA) and the last eukaryotic common ancestor (LECA) (see Fig. 5.2). According to the definitions in the literature, FECA refers to the ancestral proto-eukaryotic lineage, or the host, that branched off from within the archaeal domain of life (Hug et al., 2016). LECA, on the other hand, is a fully developed complex cell that possesses all canonical features of modern-day eukaryotes, including the fully integrated endosymbiont, the mitochondrion (Eme et al., 2017). Since the eukaryotic cell originated from two distinct cellular partners, this examination of eukaryogenesis focuses on the endosymbiont and host separately.

FIG. 2.

Evolution of life on Earth. (A) Phylogenetic ToL showing the diversity between bacterial and archaeal phyla and eukaryotic supergroups. Last common ancestors are shown on the main stem of the tree using colored circles. Phyla and supergroups containing aggregative and/or clonal multicellularity are shown across the tree with pink or blue circles, respectively. Tree is not precisely scaled to show actual evolutionary divergence and is only meant to be an informative model. Modified from Hug et al. (2016) with permission. (B) Timeline showing major geological and evolutionary events in Earth's history (for approximated dates, see references within). LUCA = last universal common ancestor; LBCA = last bacterial common ancestor; LACA = last archaeal common ancestor; FECA = first eukaryotic common ancestor; LECA = last eukaryotic common ancestor; NOE = Neoproterozoic oxygenation event.

5.3.1. The FECA-to-LECA transition I: The endosymbiont perspective

Phylogenomic data investigating the ancestry of mitochondria suggest a proteobacteria-related origin for the endosymbiont (Andersson et al., 1998; Wang and Wu, 2015). Specifically, most analyses support the view that the mitochondrial endosymbiont is more closely related to Rickettsiales (Wang and Wu, 2015), which are facultative intracellular parasitic microbes. This suggests that the initial phases of the partnership between the two entities might have been parasitic. However, it is also conceivable that the initial interaction could have been mutually beneficial rather than parasitic (Zachar and Boza, 2020).

Despite these uncertainties, it is clear that the engulfed proteobacterium underwent several evolutionary changes on its path to evolving into an interdependent organelle. Some of these changes include (i) the transfer of several mitochondrial genes into the nuclear (host) genome, (ii) the evolution of intracellular transport machinery that retargets genes encoded from the nuclear genome to mitochondria, (iii) the evolution of cristae structure (i.e., folded structures at the inner mitochondrial membrane), and (iv) the evolution of biochemical signaling pathways between the organelle and the host (Vafai and Mootha, 2012; Gray, 2014; Roger et al., 2017). Concurrently, the proto-mitochondria underwent a dramatic genome reduction event (Timmis et al., 2004). The ancestral proto-mitochondrial genome is estimated to have contained 1100–1300 protein-coding genes. In contrast, the mitochondrial genomes of modern-day eukaryotes contain only 2–66 protein-encoding genes. (Wang and Wu, 2014; Roger et al., 2017). Ultimately, mitochondria brought aerobic respiration into the partnership, using oxygen to release energy from carbohydrates efficiently. This energy could be stored as ATP and exported to the host cell. Mitochondria harbored other unique reactions as well, including the formation of iron-sulfur clusters, critical to multiple biochemical pathways in the host (Wang and Wu, 2014; Burki, 2016). There is substantial evidence that the evolution of all these mitochondrial traits was completed in LECA because all the modern-day eukaryotes share these features (Müller et al., 2012; Eme et al., 2017).

5.3.2. The FECA-to-LECA transition II: The host perspective

The origin of the host cell can be traced back to the archaeal domain of life (Iwabe et al., 1989). Phylogenetic studies indicate that the molecular machinery of eukaryotic cells performing DNA replication, transcription, and translation originated from the archaea (Rivera et al., 1998). However, there are significant differences in the cellular structures of extant eukaryotic cells and archaeal cells (Koonin, 2011), suggesting an extended period of evolutionary divergence between ancestral archaea and the proto-eukaryotic cell that captured the endosymbiont (Heimerl et al., 2017). While it is clear that the host cell originated within the archaeal domain of life, there is still a debate regarding the extent of independent evolution that the ancestral proto-eukaryotic lineage underwent before capturing its bacterial partner (Pittis and Gabaldón, 2016; Gabaldón, 2018). In other words, did the proto-eukaryotic cell that captured the bacteria already have a complex cellular structure, or did it possess a more primitive one?

This discussion revolves around two competing hypotheses: the “Mito-early” and “Mito-late” models (Fig. 5.3) (Archibald, 2015; Pittis and Gabaldón, 2016). The Mito-early model proposes that the archaeal host was a simple cell lacking complex eukaryotic features such as a nuclear envelope, an endomembrane structure, or a cytoskeleton, until the acquisition of the proto-mitochondria (or endosymbiont). Conversely, the Mito-late model posits the archaeal host had already evolved eukaryote-like features, notably a well-developed cytoskeleton that would allow for phagocytosis, well before the host captured its endosymbiont (Archibald, 2015).

FIG. 3.

The hypothesized origins of the eukaryotic cell. Eukaryotic cells contain defining cytological features, such as a nucleus and mitochondria, that are not found in bacteria or archaea. The origin of these organelles is hypothesized to have occurred when an alphaproteobacteria fused with an archaeal cell and formed a syntrophic relationship that gave rise to the eukaryotic cell. Models showing the order of events leading to the evolution of the eukaryotic cell are divided into three scenarios: “Mito-early,” “Mito-intermediate,” and “Mito-late.”

The discovery of a new lineage of archaea has opened a new chapter in the debate about the nature of the ancestral proto-eukaryotic host cell. In 2015, deep marine sediments at the Arctic Mid-Ocean Ridge (a locality with hydrothermal vents) revealed the existence of a phylum named Lokiarchaeota, after the Norse god Loki (Spang et al., 2015). Phylogenomic inferences suggest that Lokiarchaeota forms a deeply branching sister lineage to eukaryotes. Additionally, 175 Loki proteins display similarities to the so-called eukaryotic signature proteins (ESPs), which were thought to be unique to eukaryotic cells (Spang et al., 2015). Some of these ESPs show genetic similarities to proteins involved in cellular deformation, motility, or phagocytosis, and other processes.

The discovery of Lokiarchaeota was followed by metagenomic discoveries of four other phyla located in different anoxic environments worldwide. These phyla are named Thorarchaeota, Odinarchaeota, Heimdalarchaeota, and Helarchaeota—all grouped under a new superphylum called Asgardarchaeota, which is also referred to as Asgard archaea (Zaremba-Niedzwiedzka et al., 2017). Like Loki's genome, each of these metagenomes has been shown to contain ESPs. The presence of ESPs in Asgardarchaeota suggests that the proto-eukaryotic (archaeal) host had already evolved a few signature traits that define cellular complexity in eukaryotes, providing support for the Mito-late, or perhaps more accurately, Mito-intermediate model (Fig. 5.3). This implies an archaeal host that had partially evolved some of the novel cellular features suggested in the Mito-late model (Ettema, 2016).

Despite recent data from metagenomic studies, it remains to be seen whether Asgard archaea contain cellular features that resemble eukaryotes. Therefore, it is crucial to culture Asgard archaea and study their cellular and metabolic characteristics in the laboratory. To date, only one strain of Asgard archaea (belonging to the Lokiarchaeota phylum) has been successfully cultured (Imachi et al., 2020). This strain is only a half-micron in size and lacks endomembrane structures and organelles. Its metabolism is anaerobic, and its growth depends on metabolic by-products produced by surrounding microbes. Due to its small size and anaerobic metabolism, it is unlikely to meet the structural and physiological requirements necessary to engulf a bacterium. Strikingly, though, this isolate possesses membrane-originated protrusions that are 4–6 μm long and can potentially entangle microbes in its vicinity. The presence of these protrusions suggests that the initial physical interaction between the host and the endosymbiont may have occurred through extracellular entanglement (Baum and Baum, 2014).

Although the phylogenetic relationship between Lokiarchaeota and modern eukaryotes is not yet definitive, evidence suggests that they are sister lineages. By discovering additional strains and analyzing their cellular and biochemical characteristics in the laboratory, we may partially unravel the puzzle of the proto-eukaryotic host and potentially reach a conclusion on the two-competing hypothesis (Liu et al., 2021). Indeed, a recent study reveals the presence of a complex cytoskeleton composed of actin protein in a newly cultured Asgard microbe, showcasing the ongoing pace of scientific discovery in this field (Rodrigues-Oliveira et al., 2023).

5.3.3. Tempo and mode of eukaryogenesis

The earliest microfossils resembling eukaryotes were found in rocks from 1.9–1.6 billion years ago, but more compelling evidence comes from microfossils discovered in rocks 1.6–1.2 billion years old (Butterfield, 2000; Knoll, 2014; Adam et al., 2017). By calibrating phylogenomic and molecular-clock data with information derived from fossil records of red algae, it is suggested that Asgardarchaeota and proto-eukaryotic lineages diverged 2.7–2.2 billion years ago, and LECA arose 1.86–1.67 billion years ago (Betts et al., 2018). However, there is still no consensus on these phylogenomics-based estimations, and some studies present differing views (Pittis and Gabaldón, 2016; Strassert et al., 2019).

While the exact timing of eukaryogenesis is uncertain, LECA displayed key features of contemporary eukaryotes and was a facultative anaerobic organism (Müller et al., 2012). As outlined in Bourke's framework for major transitions in evolution, the transition from FECA to LECA follows three phases: group formation, group maintenance, and group transformation (Bourke, 2011). Group formation between independent prokaryotic cells has been observed in nature, suggesting this initial step is not particularly unusual (von Dohlen et al., 2001; Yamaguchi et al., 2012). Once the group is formed, conflicts will inevitably arise between the proto-eukaryotic host and proto-mitochondrial endosymbiont.

During the group maintenance and transformation stages, conflict mediation and cooperation are decisive for a major transition event in individuality (Bourke, 2011). Because the host and endosymbiont belong to highly distinct biological taxa, the evolution of cooperation could have been challenging due to a higher likelihood of conflicts. This may partly explain why all lineages that diverged between the transition period from FECA and LECA have gone extinct. In one of these lineages, the host and endosymbiont established cooperation through the evolution of novel traits specific to the new cellular unit, such as nucleus/cytosol compartmentalization, gene transfer from endosymbiont to the host genome, and biochemical interactions between the host and the endosymbiont (Blackstone, 2013). Furthermore, compartmentalization between the nuclear and mitochondrial genomes reduced intra-genomic conflicts. Gene transfer from proto-mitochondria to host genome increased mutual dependence. Signaling pathways between the host and mitochondrial genome boosted cooperation. Cooperative energy metabolism increased the fitness of the collective.

5.3.4. Open questions

The evolution of eukaryotes unlocked the potential for further complexity in life on Earth, as complex multicellularity has only arisen from within eukaryotes (Knoll, 2011). Therefore, understanding why complex cells evolved only once and why complex multicellular life has evolved only within eukaryotes is central to astrobiology. To gain a theoretical understanding of such overarching questions, we need to study the cellular traits that proto-eukaryotic host cells possessed at the origin of their interaction with the endosymbiont. How did the interaction between the host and endosymbiont evolve on a spectrum from parasitism to mutualism? How were potential conflicts mediated between the evolutionary partners? How crucial were mitochondrial energetics for the evolution of complex cellular features? How long did the transition from FECA to LECA take? How did horizontal gene transfer events from other prokaryotes shape eukaryogenesis? Furthermore, how did the changes in Earth's ecology, such as oxygenation, shape eukaryogenesis? While it may not be possible to gather all the pieces required for a complete picture of eukaryogenesis, future discoveries will improve our understanding of this major transition event, which was central to the complexification of life on our planet.

5.4. The Origin(s) and History of Multicellularity on Earth

The transition to multicellularity involves solitary cells forming groups that can evolve multicellular traits though Darwinian adaptation. This results in the emergence of a novel, higher-level individual (Buss, 1987; Maynard Smith and Szathmáry, 1995). This transition has given rise to a remarkable diversity of multicellular forms, ranging from filament-forming bacteria with only two cell types to plant and animal species with large bodies and numerous cell types organized into complex networks of tissues and organs. Moreover, the transition to multicellularity has frequently led to significant increases in organismal size, spanning multiple orders of magnitude compared to their unicellular counterparts (Heim et al., 2017).

The transition from single cells into multicellular organisms can occur through the formation of groups by coming together (i.e., aggregative multicellularity) or by remaining together after cell division (i.e., clonal multicellularity) (Brunet and King, 2017). Aggregative multicellularity has independently arisen in bacteria and eukaryotes over ten times with hundreds of known species, such as slime molds and myxobacteria (Sebé-Pedrós et al., 2017). Clonal multicellularity has evolved even more commonly across the Tree of Life, with at least 25 known independent origins (Sebé-Pedrós et al., 2017). For example, animals and plants are the product of clonal multicellularity. Several examples of clonal multicellularity also exist within the domain of Bacteria, including Anabaena cylindrica, a filamentous cyanobacterium species, and Candidatus Magnetoglobus multicellularis, an obligate multicellular species of magnetotactic bacteria (Lyons and Kolter, 2015). Methanosarcina acetivorans, an archaeal species, also exhibits clonal multicellularity (Sowers et al., 1984).

5.4.1. Complex multicellularity

Despite the continuous diversity of organismal forms, we can categorize multicellularity as simple or complex (Nagy et al., 2018). From an evolutionary transition in individuality perspective, complex multicellularity marks an irreversible departure from the ancestral solitary state, making a reversion to self-sustaining unicellularity unlikely (Bourke, 2011). From a developmental biology perspective, which studies growth, cellular differentiation, and remodeling of cells in multicellular organisms to produce the adult form, complex multicellularity indicates the evolution of organisms with a precisely organized, three-dimensional body (Knoll, 2011; Nagy et al., 2018).

The definitions provided above for complex multicellularity reveal that only lineages with clonal multicellularity could have evolved into complex multicellular organisms, including plants, animals, fungi, red algae, and brown algae. The question that arises is why clonal multicellularity leads to a higher level of biological complexity compared to aggregative multicellularity. One critical factor is that genetic relatedness in clonal groups can facilitate the development of altruistic interactions and conflict resolution among lower-level parts (cells that form the multicellular group) more effectively than genetically diverse aggregative groups (Gilbert et al., 2007). Additionally, since aggregative organisms spend most of their life cycle as individual cells, there is little incentive for them to evolve complex multicellular traits (Márquez-Zacarías et al., 2021).

5.4.2. The history of multicellularity on the planet

Simple clonal filamentous modes of multicellularity are nearly as old as the fossil record of life, and clear fossil evidence of multicellular organisms exists from at least ∼3.5 Ga (Chapter 4.1.5). These fossils are micrometer-scale segmented filaments, interpreted as bacterial or archaeal clonally multicellular organisms (Schopf, 1993; Schopf et al., 2018). Colonies of spheroidal as well as segmented filamentous cyanobacteria are well represented from the Paleoproterozoic era (<2.5 Ga) (Schopf, 1968; Butterfield et al., 1994). However, these examples do not give evidence of complex multicellularity—typically indicated by extensive cellular differentiation and interdependency—which is only known today in eukaryotic organisms (see Chapter 5.5.1).

The oldest multicellular fossil exhibiting complex multicellularity, Bangiomorpha, is dated to ∼1 Ga (Butterfield, 2000; Gibson et al., 2018) (Fig. 5.4). Thorough examination of several Bangiomorpha specimens has established a developmental history nearly identical to that known for modern red algae. Bangiomorpha is not only the oldest, most well-regarded multicellular organism in the fossil record, but it may also be among the oldest known eukaryotic fossils (see Chapter 5.4.3). Other potentially multicellular fossils have not been taxonomically resolved but hint at earlier origins of complex multicellularity. For example, macroscopic coiled filaments dated to ∼2.1 Ga, known as Grypania, are thought to represent the oldest known multicellular eukaryotes, a full ∼1 billion years older than Bangiomorpha (Han and Runnegar, 1992). Further examination of these and similar fossils may establish an earlier origin for complex multicellularity.

FIG. 4.

Optical micrograph of Bangiomorpha pubescens fossil from the Huntington Formation, Somerset Island, Canada, possibly the oldest definitive evidence of complex multicellularity (Butterfield, 2000). Figure modified from Yoon et al. (2010).

The available fossil evidence demonstrates that simple multicellularity evolved relatively quickly in both prokaryotes and eukaryotes. However, it is not clear why the evolution of complex multicellularity came so late, more than 2 billion years from the oldest fossil evidence of simple multicellularity (and life) (Schopf, 1993; Schopf et al., 2018), and why it never developed in prokaryotes (Butterfield, 2009b). The tempo of multicellular evolution has been linked to transitions in global environmental conditions. For example, the Neoproterozoic oxygenation event (800–540 million years ago; Fig. 5.2) changed the chemistry of the atmosphere and deep ocean and may have been an important driver in the early evolution of animals (Fike et al., 2006; Och and Shields-Zhou, 2012; Lyons et al., 2014; Alcott et al., 2019). The broad age correlation of earliest animal fossils (Droser and Gehling, 2015; Yin et al., 2015) and geochemical signatures of increased oxygenation potentially suggest that oxygen was a major limiting constraint in the evolution of macroscopic multicellularity (Fike et al., 2006; Bozdag et al., 2021).

It is reasonable to expect that an increase in oxygen during the Neoproterozoic would have paved the way for increasing multicellular complexity by satisfying metabolic requirements and expanding nutrient availability (Knoll, 2017) (see Chapter 5.3.3). However, research has not yet fully constrained the precise timing of this oxygenation history by geochemical means (Lyons et al., 2014), impeding a full understanding of the causal relationship between oxygen and multicellularity. The fact that complex multicellularity only arose in eukaryotes also challenges the notion of oxygen as a primary force in driving this increase in biological complexity. Butterfield (2009a) argues that eukaryotic gene regulation, rather than the availability of oxygen, was necessary for the evolution of large, complex multicellularity. For animals, modest (i.e., approximately 1% of present-day) levels of oxygen may have been a basic requirement. However, the evolution of animal multicellularity was thus likely a result of an interaction between multiple biological and environmental factors (Butterfield, 2009b; Erwin and Valentine, 2013). An interdisciplinary approach will be necessary to reach a comprehensive understanding of the constraints and drivers of the origin of complex multicellular life (Wood et al., 2020; Bozdag et al., 2021).

5.4.3. Scientific approaches to the study of evolution of multicellularity

The evolution of multicellularity is studied using either the top-down approach, which involves comparing extant multicellular organisms to their modern-day unicellular relatives, or the bottom-up approach, which focuses on the initial phases of how solitary living cells can form and evolve as multicellular groups (for a through discussion of these approaches, see van Gestel and Tarnita, 2017).

In the top-down approach, comparative genomic studies have revealed that multicellular and unicellular organisms have similar protein and gene content, suggesting that the evolution of multicellularity does not require significant genetic innovations (Suga et al., 2013; Hanschen et al., 2016; Paps and Holland, 2018). In fungi, the emergence of novel multicellular traits mostly appears to result from co-option of and structural changes in existing genes (Kiss et al., 2019). For animals and plants, the evolution of complex multicellularity seems to be associated with changes in gene regulation (Hanschen et al., 2016; Sebé-Pedrós et al., 2016; Featherston et al., 2018). Once simple multicellular groups form, the next step is often the evolution of large body size, which is evidenced in volvocine green algae by an expansion of glycoprotein (pherophorins) and matrix metalloprotease (MMP) protein families (Prochnik et al., 2010; Hanschen et al., 2016). However, in most comparative studies, extant multicellular organisms and their unicellular relatives have undergone tens to hundreds of million years of independent evolution since their divergence, making it hard to disentangle novelties versus co-opted multicellular features, which underscores the challenges faced in the top-down framework in the study of multicellularity.

Taking a bottom-up approach, laboratory microbial evolution experiments allow for direct observation of phenotypic and genetic changes in real-time (van Gestel and Tarnita, 2017). Several experiments have shown that microbes can evolve simple, microscopic multicellularity when subjected to selection for increased organismal size (Boraas et al., 1998). In long-term evolution experiments, where constraints like limiting O₂ concentrations are lifted, these multicellular clusters can further evolve to sizes visible to the naked eye (Bozdag et al., 2023). While predation and abiotic stress have been suggested to be some of the selective pressures behind the evolution of large, multicellular organisms, the full range of mechanisms that explain the remarkably diverse forms of multicellular organisms on Earth today is only beginning to be uncovered (Tong et al., 2022). Little is known about how simple, undifferentiated groups of cells evolve into large, complex multicellular individuals—with differentiated cells, well-regulated developmental programs, intercellular communication, and division of labor. Exploring all these questions with studies based on similar bottom-up approaches presents an exciting research path ahead.

5.5. The Tree of Life

5.5.1. What is the Tree of Life?

The evolution of all living organisms, from LUCA to the present, took 3.8 billion to 3.5 billion years to occur. During this period, a very particular set of environmental and chemical conditions drove the evolution and diversification of LUCA into bacteria and archaea, which in turn gave rise to eukaryotes and the transition to complex multicellular life. Despite the vast complexity and diversity of evolutionary paths, the history of life on Earth can be reduced to a single image, referred to as the “Tree of Life” (ToL) (Fig. 5.2; see also Chapter 2.3).

The ToL summarizes the complete set of relationships among all life on Earth in a graphical representation. Most diagrams reflect one (of many) phylogenetic models of evolution. The utility of using a tree is its ability to visually represent the history and evolution of species in a diagrammatic manner that is easy to understand. The tree provides an easily understood diagram that connects extant species (or individuals or lineages at the tips of branches) by evolutionary history. As trees trace this history backward, branches can converge from information at the present moment, forming a node. That node represents the ancestral population from which the two species emerged. Together, the branches and nodes represent the evolutionary history of life; they show the relative order in which different species appeared, evolved, and left descendants.

In the ToL, LUCA lies just before the first branching of the tree, the first speciation event. All other species evolved from this common ancestor, with each newly evolved population represented as a new branch (corresponding to a point in the past), and the very tips of the branches representing still-living species. The stem beneath LUCA represents LUCA's ancestors (i.e., the first universal common ancestor, FUCA). This stem could also have had branches of divergent organisms that could have gone extinct and left no descendants. If life were found elsewhere in the universe, undergoing Darwinian evolution, a similar systematic classification of organisms (i.e., a phylogenetic approach) could be used to classify that life.

More details on how phylogenetic trees are generated are given in the supplementary material.

5.5.2. Viruses and the Tree of Life

Determining the origin of viruses and their relation to the rest of life is challenging due to their broad genetic diversity, rapid rate of evolution, and lack of a single common ancestor (see Chapter 2.4). Viral genomes are less conserved than cellular genomes, making them difficult to connect to the ToL. They can be DNA or RNA, double-stranded or single-stranded. They do not rely on conserved ribosomal genes, which could serve as a molecular clock. They display abundant horizontal transfer with host genomes, on which they depend for reproduction, and their reduced size can lead to convergence with other independently evolved lineages (Brüssow, 2009; Koonin et al., 2015; Al-Shayeb et al., 2020). It has been proposed that two (or maybe more) connected natural worlds have evolved in parallel from LUCA: the three cellular life domains on one side, and viruses on the other, forming three distinct parallel domains depending on which cellular life domain they are associated with (i.e., infect) (Raoult and Forterre, 2008; Brüssow, 2009; Brandes and Linial, 2019). This framework of viral domain independence arose because viruses have unique sequences absent from all cells and that originated from a common ancestral protein unique to viruses, such as those forming a double-jelly-roll fold.

Some scientists have suggested that a universal ToL might be replaced by a network model of sets of gene and protein sequences to represent more complex evolutionary processes and include viruses (Doolittle and Bapteste, 2007). Recently, a new application using whole-genome gene-sharing profiles resulted in a near-identical replication of existing viral taxonomy assignments provided by the International Committee on Taxonomy of Viruses and confidently placed thousands of new viruses in an interconnected network (Jang et al., 2019). This represents a major step in connecting viruses across many clades but is currently limited to complete viral sequences and viruses of bacteria and archaea, though not eukaryotes (Simmonds et al., 2017). There is not yet a method that is able to place viruses and cellular life in one coherent network.

Further discussion of the origin of viruses is given in the supplementary material.

5.6. Conclusion

In our search for life on other planets, our inferences about whether a planet might be habitable depend on Earth's current and historical habitability. Every organism on Earth, whether unicellular or multicellular, phototrophic or reliant on organic carbon, descends from a primordial cell type. This cell possessed biochemical machinery so adept at survival and reproduction that it endured through eons.

It is important to remember, however, that these inferences about the history of life and its timing are all based on models built on our limited understanding of life, and such models might be missing important pieces. Furthermore, while we are aware of countless species inhabiting Earth, many more have gone extinct without our knowledge. This incomplete knowledge of Earth's past life may restrict our ability to infer implications for potential life elsewhere in the universe.

Finally, as we will see in Chapter 6, while most of the biomass on Earth is produced by macroscopic multicellular organisms (especially plants) (Bar-On et al., 2018), the organisms most successful at colonizing a more diverse set of conditions, particularly extreme conditions, are microbial prokaryotes (O'Malley, 2014). Although we present these transitions in a linear sequence, as they happened through time, we stress that the increases in complexity being described in this chapter are occurring for only a small subset of all the organisms that existed at each point in time. While the upper bound on organismal complexity has increased over time, shifting from simple chemical replicators to single-celled prokaryotes to eukaryotes to multicellular eukaryotes to eusocial colonies of multicellular eukaryotes, most of the diversity of life on Earth today remains microbial. This is important, as habitable environments outside of Earth likely fall within what we consider extreme limits for life (see Chapter 6.3), and thus the type of living organisms that we are likely to encounter might be similar to our microscopic neighbors.

Abbreviations Used

ATP

adenosine triphosphate

ESPs

eukaryotic signature proteins

FECA

first eukaryotic common ancestor

Ga

billion years ago

GOE

Great Oxidation Event

LECA

last eukaryotic common ancestor

LSU

large subunit

LUCA

last universal common ancestor

rTCA cycle

reductive tricarboxylic acid cycle

SSU

small subunit

ToL

Tree of Life

WLP

Wood–Ljungdahl pathway

Authors' Contributions

N.S. led the team, developed the chapter's structure, and co-authored sections on LUCA, oxygen-producing metabolism, ToL, and the conclusion. G.O.B. co-led the team, co-edited the chapter, developed the structure of the eukaryogenesis and multicellularity sections, authored the eukaryogenesis section, and co-authored the multicellularity section. P.L.C. developed and authored the introduction. G.A.S. co-authored the Tree of Life section, generated Figures 5.2 and 5.3. A.G. co-authored and edited the multicellularity section. K.C. co-authored the multicellularity section. S.M.F. and P.I.P. co-authored the subsection about the evolution of the ribosome within the section about LUCA's genetic system. G.T. authored the virus subsection.

Supplementary Material

Supplementary Information

Associate Editors: Sherry Cady and Christopher McKay