Paper: Genomics and the Irreducible Nature of Eukaryote Cells

Science 19 May 2006:
Vol. 312. no. 5776, pp. 1011 - 1014
DOI: 10.1126/science.1121674Prev | Table of Contents | Next

Review
Genomics and the Irreducible Nature of Eukaryote Cells
C. G. Kurland, L. J. Collins, D. Penny

Large-scale comparative genomics in harness with proteomics has
substantiated fundamental features of eukaryote cellular evolution. The
evolutionary trajectory of modern eukaryotes is distinct from that of
prokaryotes. Data from many sources give no direct evidence that eukaryotes
evolved by genome fusion between archaea and bacteria. Comparative genomics
shows that, under certain ecological settings, sequence loss and cellular
simplification are common modes of evolution. Subcellular architecture of
eukaryote cells is in part a physical-chemical consequence of molecular
crowding; subcellular compartmentation with specialized proteomes is
required for the efficient functioning of proteins.

Comparative genomics and proteomics have strengthened the view that modern
eukaryote and prokaryote cells have long followed separate evolutionary
trajectories. Because their cells appear simpler, prokaryotes have
traditionally been considered ancestors of eukaryotes (1-4). Nevertheless,
comparative genomics has confirmed a lesson from paleontology: Evolution
does not proceed monotonically from the simpler to the more complex (5-9).
Here, we review recent data from proteomics and genome sequences suggesting
that eukaryotes are a unique primordial lineage.

Mitochondria, mitosomes, and hydrogenosomes are a related family of
organelles that distinguish eukaryotes from all prokaryotes (10). Recent
analyses also suggest that early eukaryotes had many introns (11, 12), and
RNAs and proteins found in modern spliceosomes (13). Indeed, it seems that
life-history parameters affect intron numbers (14, 15). In addition,
"molecular crowding" is now recognized as an important physical-chemical
factor contributing to the compartmentation of even the earliest eukaryote
cells (16, 17).

Nuclei, nucleoli, Golgi apparatus, centrioles, and endoplasmic reticulum are
examples of cellular signature structures (CSSs) that distinguish eukaryote
cells from archaea and bacteria. Comparative genomics, aided by proteomics
of CSSs such as the mitochondria (18, 19), nucleoli (20, 21), and
spliceosomes (13, 22), reveals hundreds of proteins with no orthologs
evident in the genomes of prokaryotes; these are the eukaryotic signature
proteins (ESPs) (23, 24). The many ESPs within the subcellular structures of
eukaryote cells provide landmarks to track the trajectory of eukaryote
genomes from their origins. In contrast, hypotheses that attribute eukaryote
origins to genome fusion between archaea and bacteria (25-30) are
surprisingly uninformative about the emergence of the cellular and genomic
signatures of eukaryotes (CSSs and ESPs). The failure of genome fusion to
directly explain any characteristic feature of the eukaryote cell is a
critical starting point for studying eukaryote origins.

It is agreed that, whether using gene content, protein-fold families, or RNA
sequences (31-36), the unrooted tree of life divides into archaea, bacteria,
and eukaryotes (Fig. 1). On such unrooted trees, the three domains diverge
from a population that can be called the last universal common ancestor
(LUCA). However, LUCA (37) means different things to different people, so we
prefer to call it a common ancestor; in this case it is the hypothetical
node at which the three domains coalesce in unrooted trees.

There are links between comparative genomics and the ecology of organisms.
These include the aerobic/anaerobic states of the environment and the
adaptive fit of organelles such as mitochondria, hydrogenosomes, and
mitosomes (10, 18, 19, 38-41). In addition to the advantages from oxidative
metabolism and/or oxygen detoxification, other advantages must have accrued
from having a cellular compartment with dense proteomes (15, 38, 42).
Ecological specialization can account for the differences between prokaryote
and eukaryote cell architectures and genome sizes. Small prokaryote cells
with streamlined genomes may reflect adaptation to rapid growth and/or
minimal resource use by autotrophs, heterotrophs, and saprotrophs. Divergent
evolutionary paths may emerge with the adoption of a phagotrophic-feeding
mode in an ancestor of eukaryotes. This uniquely eukaryote feeding mode
requires a larger and more complex cell, consistent with earlier suggestions
that a unicellular raptor (predator), which acquired a bacterial
endosymbiont/mitochondria lineage, became the common ancestor of all modern
eukaryotes (3, 4, 43). Indeed, predator/prey relationships may provide the
ecological setting for the divergence of the distinctive cell types adopted
by eukaryotes, bacteria, and archaea.

Proteomics of Cell Compartments
Comparative genomics and proteomics reveal phylogenetic relationships
between proteins making up eukaryote subcellular features and those found in
prokaryotes. We distinguish three main phylogenetic classes; the first are
proteins that are unique to eukaryotes: the ESPs. The ESPs we place in three
subclasses: proteins arising de novo in eukaryotes; proteins so divergent to
homologs of other domains that their relationship is largely lost; or
finally, descendants of proteins that are lost from other domains, surviving
only as ESPs in eukaryotes.

The second class contains interdomain horizontal gene transfers; these are
proteins occurring in two domains with the lineage of one domain rooted
within their homologs in a second domain (44). The third class contains
homologs found in at least two domains, but the proteins of one domain are
not rooted within another domain(s); instead, the homologs appear to descend
from the common ancestor (Fig. 1). Most eukaryote proteins shared by
prokaryotes are distant, rather than close, relatives. Thus, proteins shared
between domains appear to be descendants of the common ancestor; few seem to
result from interdomain lateral gene transfer (31-35).

Although the genomes of mitochondria are clearly descendants
of -proteobacteria (45, 46), proteomics and comparative genomics identify
relatively few proteins in yeast and human mitochondria descended from the
ancestral bacterium (17, 18, 36, 47). Several hundred genes have been
transferred from the ancestral bacterium to the nuclear genome, but most
proteins from the original endosymbiont have been lost. For yeast, the
largest protein class contains more than 200 eukaryote proteins (ESPs)
targeted to the mitochondrion but encoded in the nucleus. In addition, the
yeast nucleus encodes 150 mitochondrial proteins not uniquely identifiable
with a single domain but apparently eukaryotic descendants from the common
ancestor. Accordingly, the yeast and human mitochondria proteomes emerge
largely as products of the eukaryotic nuclear genome (85%) and only to a
lesser degree (15%) as direct descendants of endosymbionts (17, 18, 36, 45).
The strong representation of ESPs in their proteomes means that mitochondria
and their descendants are usefully viewedas"honorary" CSSs.

There are substantial numbers of ESPs in the other CSSs. For the proteome of
the reduced anaerobic parasite Giardia lamblia (23), searches of 2136
proteins found in each of Saccharomyces cerevisiae, Drosophila melanogaster,
Caenorhabditis elegans, and Arabidopsis thaliana yielded 347 ESPs for G.
lamblia. This was reduced to roughly 300byrigorousscreening, with ESPs
distributed between nuclear and cytoplasmic compartments (Fig. 2) (48). The
ubiquity of the ESPs and the absence of archaeal descendants are not easily
explained by a prokaryote genome fusion model (49). The simplest
interpretation is that the host for the endosymbiont/mitochondrial lineage
was an ancestral eukaryote.

Full Text at Science
http://www.sciencemag.org/cgi/content/full/312/5776/1011

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