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DOMAIN EUKARYA

EUKARYA
DOMAIN EUKARYA LINKS

Introduction

In the Era of Set

The Archezoa Hypothesis and Chaos

Supertrees and Supergroups

Domain Unikonta

Supergroup Excavata

Supergroup Chromalveolata

Supergroup Archaeplastida

Literature Cited

Eukarya (pronounced: u-KA-ree-a) is a combination of two Greek roots that mean “well or true” (eu -εὖ) and “nut” (karydi -καρύδι). The reference is to having cells with a nucleus (a nut).
INTRODUCTION TO THE DOMAIN EUKARYA

Determination of the evolutionary relationships between major eukaryotic groups has been the Holy Grail of phylogenetics since the demise of the Plant-Animal dichotomy of the old Aristotelian 2-Kingdom system. Through the latter half of the 20th Century, structural and ultrastructural evidences, together with growing support for the theory of the endosymbiotic origin of eukaryotes, brought about a general acceptance of the 5-Kingdom system, both of which were energetically championed by Lynn Margulis. The immediate results were the realizations that protozoa and algae were ecological concepts rather than taxonomic realities and occupied the Kingdom Protista (or Protochtista). Otherwise, early attempts to resolve eukaryotic relationships promised some successes but were slow to deliver.

Eukaryotes are clearly different from organisms in the bacterial domains. They have internal membrane-bound structures (including the nucleus, the minimal requirement for a eukaryote), microtubular cytoskeletons, and characteristic ribosomes. In addition, Roger (1999) summarizes synapomorphic characters that all Eukaryotes possess or once possessed and have lost through simplification (see Table 1). However, direct comparisons with bacterial domains are difficult. Compared to bacteria (prokaryotes), eukaryotes are chimeroid living structures because they have evolved through a variety of non-Darwinian means: endosymbiosis and fusion of cells (fusion of bacteria with nuclear host and the fusion of eukaryotes), to lateral gene transfer (Katz 1999). The resulting changes from such a mode of construction should have led to large steps or apparent saltations separating the resulting taxa, the largest of which is the transition from bacteria (likely an ancestor to the present day Archaea) to the Eukarya (or Eukaryota).

TABLE 1. Structural Features, Processes, and Genes/Proteins that are possessed by all eukaryotes or were possessed by their ancestors and lost through simplification. From Roger (1999).

STRUCTURAL FEATURES (Ultrastructure):

  • Nucleus
  • Nuclear pores
  • Endoplasmic reticulum
  • 9+2 flagellar apparatus
  • mitotic spindle
  • acidified vacuoles
  • golgi apparatus
  • multiple linear chromosomes

PROCESSES (Ultrastructure and physiology)

  • mitosis
  • meiotic sex
  • endocytosis
  • endosymbiosis
  • mitochondrial respiration

GENES/PROTEINS (Molecular biology and physiology)

  • alpha and beta tubulins
  • actin
  • dyneins
  • centrin
  • alpha actinin
  • tropomyosin
  • myosin
  • kinesins
  • annexins
  • RNA pol I, II, III
  • Alpha, delta, and epsilon DNA pol
  • Bip/cystosolic hsp70
  • Beta, epsilon, and nu Tcp-1 chaperonins
  • CDC2/28
  • PRP8
  • Calmodulin
  • Ubiquitin
  • Histones H3 and H4
  • Eukaryotic telomeres
IN THE ERA OF SET

Various theories have been proposed to account for the origin of eukaryotes. Perhaps, the most generally accepted one is the Serial Endosymbiosis Theory (SET) of Margulis (1967) and Taylor (1974). SET explains that eukayotes arose relatively quickly from bacterial ancestors as they came together in symbiotic communities, and their communal DNA coalesced as linear chromosomes within an internal membrane-bound nucleus. Organelles like the mitochondrion (an alpha proteobacterium) and chloroplast (a cyanobacterium) retained their bacterial identities. The origins of other eukaryotic structures are more problematic.

One of the earliest positive outcomes of SET was Taylor (1976; Figure 1), in which he created a phylogeny of flagellated eukaryotes based on ultrastructure within a 5-Kingdom paradigm. His phylogeny suffered from the assumption that non-flagellated taxa were primitive, and, therefore, rooted his tree on the red algae (also, they were photosynthetic with pigments and storage products very similar to those of the Cyanobacteria). Nevertheless, Taylor (1976) was one of the first to attempt such an analysis (in cladistic format) based on numerous ultrastructural and cytological characters. His tree made some very prescient statements such as the relationship between the ciliates and the dinoflagellates and the interrelationships between taxa of the chrysophyte complex (a group that later was called the stramenopiles or heterokonts).

Dodge (1973; Figure 2) produced an analysis of the same groups of taxa as Taylor (1976). However, Dodge (1973) was predicated on the assumption that the dinoflagellates were the most primitive of the algae because of their presumed primitive nucleus which had numerous condensed chromosomes that lacked histones (a condition that he called mesokaryotic). He compared all of the photosynthetic eukaryotic microbial groups on the basis of cell covering, flagella, storage products, chlorophylls, etc. (many of the same characters that Taylor used later). His numerical taxonomic study confirmed the primitive nature of dinoflagellates (the initial assumption of the analysis), but was otherwise an uninformative jumble of taxa.

Round (1980) cautioned that the endosymbiotic theory would make any search for the relationships between higher taxa of eukaryotes very difficult especially if all major organelles (mitochondria, chloroplasts, etc.) were acquired through uptake of the appropriate symbionts. Thus, he concluded that the distinct nature of major eukaryotic groups was a consequence of non-Darwinian mix-and-match endosymbiotic events around the time of the origin of eukaryotes, which eliminated any solid evidence of lateral relationships and made the concept of Protista unusable (Figure 3). He concluded, therefore, that we should just return to the Plant-Animal dichotomy.

The Theory of Serial Endosymbiosis (SET; Margulis 1967 and Taylor 1974), that eukaryotes evolved from a singular line of nuclear taxa, which then acquired mitochondrial endosymbiotes of several different types (those with tubular, flattened, or discoid cristae) seemed to respond to the warnings of those like Round (1980). Ultrastructural work confirmed that such groups of eukaryotes existed and helped to define major groups of eukaryotic protists based on mitochondrial types as platycristate, discicristate, tubulocristate, and amitochondrial. Margulis (Margulis and Schwartz 1982, 1988, 1998, 2001) further defined lines of eukaryotes based on the occurrences of flagella and their orientations. She interpreted the flagellum as a spirochete that entered into an endosymbiotic relationship with a nuclear host, and, thus, the lines of eukaryotic evolution could be defined as having anteriorly-directed, posteriorly-directed, or no flagella. That the clusters of major groups with particular types of flagella also had similar kinds of mitochondria tended to confirm her position. However, for her, the flagellum (she called the eukaryotic flagellum an undulapodium) loomed as the single most important defining character for any major line of eukaryotes (e.g. Margulis and Schwartz, 1982, 1988, 1998, 2001; and Margulis et al. 1990). Indeed, Margulis (1990) presents a modified version of SET in which a spirochaete symbiosis not only gave rise to flagella (undulapodia), but also to basal bodies, centrioles, and the cytoskeleton. Even without the spirochaete modification of SET, the origin of the eukaryotes is difficult to infer from current microbial eukaryotes.

FIGURE 1.  This is Figure 7 from Taylor (1976).  Max Taylor considered the phylogeny of flagellated protists in a cladistic paradigm.  The categories of characters (all ultrastructural and cytological) were: mitotic mechanisms, flagella, chloroplast structure, and mitochondria.  The tree that he produced was remarkably modern in many ways by suggesting connections between the ciliates and dinoflagellates, between the kinetoplastids and the euglenoids, between the phragmoplastic and phycoplastic plants, and between the hypermastigids-trichomonads-diplomonads-retortomonads. 

FIGURE 2.  This is Figure 14.3 from Dodge (1973).  John Dodge considered the major groups of eukaryotic algae and compared them through numerical taxonomic methods.  He compared them on the basis of: cell covering,  nucleus, flagella, and ejectile organelles (all characters in which the dinoflagellates (DIN) were very different from the other taxa.  Except for the similarity between the xanthophytes (XAN) and phaeophytes (PHAE), the diagram has almost no meaning in current thinking.  Compare this analysis (numerical taxonomy) with that of Taylor (1976; phylogenetic taxonomy).

FIGURE 3. This is Figure 2 from Round (1980).  Frank Round considered concept of Protista.  He argued that the earliest lines of eukaryotes were heterotrophic and became autotrophic by endosymbiosis.  Then, he said that although some of the autotrophic lines lost their photosynthetic abilities, they could still be divided into Plants and Animals.  Thus, he considered the concept of Protista as a failed idea that needed to be relegated to the history of Biology.

THE ARCHEZOA HYPOTHESIS AND CHAOS

The Archaezoa Hypothesis of Cavalier-Smith (1983) suggested that the eukaryotes appeared prior to the endosymbiotic events that produced mitochondrial eukaryotes. According to Cavalier-Smith an archeal bacterium gave rise to a prenuclear protoeukaryote through the elaboration of a cytoskeleton. Then, fully eukaryotic organisms, the Archaezoa, appeared with the development of an internal membrane system that included the formation of a nucleus. The flagella in his theory evolved as external elaborations of the cytoskeleton, and so he began the search for living members of the Archezoa. Like Margulis, Cavalier-Smith used his theory to explain the diversity of eukaryotes at the highest level.

In its original form, the Archaezoa Hypothesis defined the Microsporidia, Metamonada, Parabasalia, and Archamoebae as extant members of the Archaezoa [see Figure 4 from Roger 1999]. The theory developed with what appeared to be a string of confirmations. Most notable was the basal and deep branching positions of amitochondriate motile taxa like Giardia on molecular phylogenetic trees. The development of the Archezoa Theory could be followed through a whole string of publications by Cavalier-Smith (1983, 1987a, 1987b, 1987c, 1987d, 1988, 1989, 1990b, 1991, 1992a, 1992b, 1993, 1997, 1998a, 1999, 2000a, 2002a, 2002b, 2004a) and Cavalier-Smith and Chao (1995, 1996, 1997, 2003a, 2003b, 2003c, 2004). The group seemed to be confirmed by defined mitochondrial lines that emerged from a premitochondrial archezoan ancestor [see Figure 5 from Gray et al. 1998]. This organization also can be seen in Margulis and Schwartz (1998).

In the mean time, molecular phylogenetics led to the discovery of the Archaea as a separate domain of life and promised to provide the key to the elucidation of eukaryotic diversity. The methods that molecular phylogenetics used compared presumably-conserved and universal biopolymers (e.g. small subunit rRNA, actin, etc.). The earliest molecular analyses tended to be too sparsely branched to provide adequate information on whole groups. After a time, however, enough sequences could be compared to generate a tree that had a few deeply branched taxa with a collection of well-defined groups at its crown. The deeply-branched taxa like Giardia, Pelomyxa, and Microsporidia seemed to fit well into the Archezoa Hypothesis because they were amitochondriate. Margulis (1982, 1988) also used the molecular tree to confirm her theory that a primitive eukaryote without flagella or mitochondria was at the root of the tree. Pelomyxa seemed to fit that requirement perfectly well.

Through the decade of the 1990’s more and more molecular analyses began to be used and uncover relationships that were poorly understood, especially among the crown eukaryotes. Thus, the Heterokonts, Alveolates, Discicristates, and the Opisthokonts (animals + fungi) came together confirmed by molecular evidence and ultrastructural synapomorphies. The same methods, however, began to dismember the tree that had grown. Molecular genetics and ultrastructural studies showed that all of the deeply branched “primitive” taxa had mitochondrial genes in their nuclear genomes. Almost all of the deeply branched taxa were either parasites or symbionts with concomitant structural and molecular simplifications. Furthermore, even Pelomyxa had an internal flagellum. So, both the Archaezoan Hypothesis and the Margulis version of SET were overturned. Rather than the creation of a definitive tree, the work of the 1990’s produced 71 separate sisterless taxa (Patterson, 1999), and, by the end of the decade, eukaryotic systematics at the highest level was in chaos. Evidence of such phylogenetic confusion could be seen in Tudge (2000) where single genera like Giardia and Entamoeba were given kingdom-level status!

Roger (1999) gave a nice history of the Archezoa Hypothesis and ended with some uncomfortable details that led to the collapse of the theory. For example, the apparent primitive nature of the archezoa was an artifact of molecular trees and of the the parasitic/symbiotic simplification that occurred in the amitochondrial taxa. Also, certain genetic sequences that must have come from the mitochondrion could be found in all of the archezoa, and taxa like the parabasalids had hydrogenosomes, anaerobic organelles that seem to have evolved from mitochondria. If all extant eukaryotes had mitochondrial genes in their nuclear DNA, the most parsimonious solution would be that all living eukaryotes evolved from mitochondrial ancestors. Thus, by 1999 the Archezoa Hypothesis was in trouble, and by 2002, it had died. Keeling (2002) finally wrote the eulogy for the Archezoa Hypothesis.

Taylor (1999) insisted that molecular inference must be confirmed by phenotypic evidence. He considered the proposal of Gray et al. (1998) in which eukaryotes were marked by 3 great lines of mitochondrial descent (as defined by mtDNA sequences, see Figure 5). Taylor showed how the hypothesis of Gray et al. (1998) was supported by ultrastructural evidence (see Figure 6). This view also suggested that the mitochondrial symbiosis was one of the most fundamental steps in the appearance of the eukaryote lineages that are defined by mitochondria with discoid cristae, flattened cristae, and tubular cristae.

This view is both beautifully simple and simply too good to be true. The mitochondrial monophyly theory is not consistent with the diversity of mitochondrial types in multicellular lineages. For example, metazoans have both flattened and tubular cristate mitochondria depending on the tissues involved. How can this be reconciled with the hypothesis of Gray et al. (1998)? The state of eukaryotic taxonomy at the higher taxonomic levels (particularly kingdoms) mirrored the changes in phylogeny. The taxonomy went from the appearance of stability at four in the five kingdom system of Whittaker and Margulis (1978) to anarchy when molecular phylogenies began to be used in the decade of the 1990’s.

FIGURE 4. The modification of Cavalier-Smith’s Archaezoa Hypothesis as given by Roger (1999). In this view all extant eukaryotes evolved from a mitochondrial ancestor. If the Archezoa ever existed, they are all extinct. Only the Pelobionts (including Pelomyxa) might be direct descendants of the Archezoa. From Roger (1999).

FIGURE 5. A diagram from Gray et al. (1998) that is based on mtDNA comparisons. Taylor (1999) compares this with trees based on ultrastructure and says that this supports the monophyletic nature of mitochondrial types in the eukaryotes.

FIGURE 6. A diagram from Taylor (1999) that summarizes ultrastructural data in a cladistic format for the eukayote lineages.

SUPERTREES AND SUPERGROUPS

Resolution to the taxonomic cacophony began to come quickly in the early years of the 21st century by use of molecular-structural data. Fortunately, a new powerful method called supertree analysis had been pioneered with bacteria (Daubin et al. 2002). According to Baldauf (2003a), supertrees employed:

– combined multigene datasets
– recognition of common patterns (consensus)
– a better understanding of long branch attraction, an artifact of molecular comparisons that tends to produce false relationships between quite disparate groups.

Soon, the same methods were applied to major groups of eukaryotes and served to mitigate the problems to which analyses of single molecular sequences were prone (particularly to that of long branch attraction). Quickly, the orphaned groups began to be assembled into larger groups. Simpson and Roger (2002) summarized the changes from 1993-2002 in which the Archaezoa disappeared and the tree of life changed from being tree-like with a crown of advanced taxa to a shrub of major clusters of taxa (see Figures 7 and 8).

Baldauf (2003a) reviewed the state of the literature relative to the Eukaryotic Tree and identified eight major lines or supergroups of eukaryotes. Her analysis, grounded both in molecular and morphological taxonomy (see Figure 9), confirmed that the Archezoa Hypothesis in its early forms (Gray et al. 1998 and Keeling 1998) likely was dead. In particular, she eliminated the concept of the “crown eukaryotes” as an artifact of single-gene comparisons. The summary analysis of Keeling (2004) simplifies the supergroups to 5 (see Figure 10), and helped to resolve the chaos as illustrated by Patterson (1999), and, at the same time, take into account the concerns of Taylor (1999) by identifying the defining synapomorphies of those groups. Stechmann and Cavalier-Smith (2004) attempted to resurrect the Archaezoa Hypothesis in a new form by providing evidence that the eukaryotes and the archaea evolved from a Gram + bacterium like the Actinomycetes. This will not be the last word in the argument about the Eukaryotic “Tree”; however, the approach of multiple ultrastructural characters coupled with and confirmed by molecular data is the only solution to untying the Gordian Knot of Eukaryotic lineages.

The power of supertree analysis allowed for the assembly of many of the orphaned or sisterless taxa into a previously unrecognized kingdom called the Cercozoae. Thus, supertree analysis gave new life to the tree of life, one of Darwin’s favorite metaphors. Curiously though, rather than adopting the appearance of a tree, the supertrees of Baldauf (2003a) and Keeling (2004) emerged as large clades from a common root, much like the petals of a flower. Perhaps a different botanical metaphor should be applied.

More recently, Baldauf (2008) reviewed the state of our knowledge of the eukaryote tree. The structure is about the same as it had been, but she fused Rhizaria with the Chromalveolata (called Alveolates + Stramenopiles) after Burki et al. (2007) and Hackett et al. (2007) into a group referenced as RAS. If this is the case and the Cryptomonads + Haptophytes are subsumed into the RAS group, then all of the Chlorophyll a and c containing taxa would be united. Furthermore, the association of the unikonts as a group distinct from the bikonts might reduce the number of eukaryote supergroups to two. Until there is strong support for that position, we will adopt a modification of the supertree of Keeling (2004) as the template for the following system (Table 2). Furthermore, we accept the difference between animals and fungi to be a kingdom-level difference. Thus, we interpret supergroups as superkingdoms, all of which contain more than one kingdom. In all, in this system, the eukaryotes occupy 11 kingdoms, only one of which (the Hacrobiae) likely is artificial although its monophyly is confirmed by Hackett et al. (2007). This is a working hypothesis for which the details of all of the kingdoms and the eukaryotic clades that they represent have yet to be ironed out.
TABLE 2. Higher-Level Classification of the Eukaryota, which includes the eukaryotic supergroups and their kingdoms with representative higher taxa. The structure of this system is based on Keeling (2004) and modified by Baldauf (2008)
SUPERGROUPKINGDOMREPRESENTATIVE TAXA
UNIKONTAANIMALIAMETAZOA, MYXOZOA, CHOANOZOA, NUCLEARIID AMOEBAE, ICHTHYOSPORIDS.
FUNGIFUNGI, CHYTRIDS, MICROSPORIDS.
AMOEBOZOAEPELOBIONTS, PROTOSTELID SLIME MOLDS, PLASMODIAL SLIME MOLDS, DICTYOSTELID SLIME MOLDS, LOBOSE AMOEBAS, APUSOZOA?
EXCAVATAEUEXCAVATAEDIPLOMONADS, PARABASALIDS, RETORTOMONADS, OXYMONADS, JAKOBODS?
DISCICRISTATAEEUGLENOIDS, TRYPANOSOMES + LEISHMANIAS, VAHLKAMPHID AMOEBAS, ACRASID SLIME MOLDS.
CHROMALVEOLATAHETEROKONTAEALL HETEROKONTAE (ALSO CALLED STRAMENOPILES), ACTINOPHRYDIAN HELIOZOANS.
HACROBIAEHAPTOMONADS, CRYPTOMONADS, CENTROHELID HELIOZOANS.
ALVEOLATAEDINOFLAGELLATES, CILIATES, APICOMPLEXANS.
RHIZARIAERADIOLARIANS, EUGLIPHID AMOEBAS, FORAMINIFERANS, CERCOMONADS, CHLORARACHNIOPHYTES, PLASMODIOPHORIDS, HAPLOSPORIDS.
ARCHAEPLASTIDAVIRIDIPLANTAEGREEN ALGAE, EMBRYOPHYTES
RHODOPHYTAERED ALGAE, GLAUCOPHYTES

FIGURE 7. This Figure from Simpson and Roger (2002) shows the evolution of the tree of life over the decade 1993-2002.  During that time the Archaezoa Hypothesis flourished and died.  The idea of a tree of life with a crown of derived taxa gave way to a more shrubby appearance, which was further developed by Palmer et al. (2004; Figure 8), Baldauf (2003; Figure 9), and Keeling (2004; Figure 10).

FIGURE 8.  These are Figures 1 (left) and 2 (right) from Palmer et al. (2004).  Figure 1 generally supports Keeling (2004) and indicates where secondary photosynthetic symbioses occurred in the various eukaryotic lines.  Note that they call the primary photobionts Primoplantae.  Figure 2 shows a post-2003 tree of the embryophytes.  Note that the fern clade includes the whisk ferns (psilophytes) and horsetails and that the gnetophytes emerge within the conifer taxa.  The bryophytes emerge as an ambiguous polytomy.  Note also the complex nature of the angiosperms.

FIGURE 9. An illustration from Baldauf (2003) that presents a consensus phylogeny of the eukaryotes. This diagram summarizes ultrastructural and molecular data. The dotted lines indicate ciPCR “taxa”. Asterisks indicate likely paraphyletic groups. This diagram suggests that the Archezoa Hypothesis, in all of its forms, likely is dead.

FIGURE 10. This is Figure 1 from Keeling (2004) that illustrates a consensus phylogeny of the eukaryotes in which he defines five supergroups. Like Figure 9, this diagram summarizes ultrastructural and molecular data. The focus of the diagram is to show the distribution of plastid-bearing taxa.

FURTHER READING:

DISCOVERY OF THE DOMAINS OF LIFE
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By Jack R. Holt. Last revised: 09/05/2016
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