Evolution of Intracellular Compartmentalization

Biochem. J. (2013) 449, 319–331 (Printed in Great Britain) doi:10.
1042/BJ20120957 319
REVIEW ARTICLE
Evolution of intracellular compartmentalization
Yoan DIEKMANN*† and José B. PEREIRA-LEAL*1
*Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal, and †Programa de Doutoramento em Biologia Computational (PDBC), Instituto Gulbenkian de
Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal
Cells compartmentalize their biochemical functions in a variety compartments from each of these three categories, membrane-
of ways, notably by creating physical barriers that separate based, endosymbiotic and protein-based, in both prokaryotes and
a compartment via membranes or proteins. Eukaryotes have a eukaryotes. We review their diversity and the current theories and
wide diversity of membrane-based compartments, many that controversies regarding the evolutionary origins. Furthermore,
are lineage- or tissue-specific. In recent years, it has become we discuss the evolutionary processes acting on the genetic
increasingly evident that membrane-based compartmentalization basis of intracellular compartments and how those differ across
of the cytosolic space is observed in multiple prokaryotic lineages, the domains of life. We conclude that the distinction between
giving rise to several types of distinct prokaryotic organelles. eukaryotes and prokaryotes no longer lies in the existence of a
Endosymbionts, previously believed to be a hallmark of compartmentalized cell plan, but rather in its complexity.
eukaryotes, have been described in several bacteria. Protein-based
compartments, frequent in bacteria, are also found in eukaryotes. Key words: endosymbiont, intracellular compartmentalization,
In the present review, we focus on selected intracellular organelle.
“Nothing epitomizes the mystery of life more than the Organelles are important cellular structures that perform
spatial organization and dynamics of the cytoplasm.” many essential functions. They allow multiple biochemical
Tim Mitchison [1] environments to coexist in the cell and to be adapted independently
INTRODUCTION [10]. For example, proteins can be translated and degraded
at the same time without undesired cross-talk [11]. Moreover,
Elaborate and dynamic spatial organization is a ubiquitous spatial confinement of toxic metabolites limits the propagation of
property of living matter and the key to life’s distinct condition potential damage.
[2]. Spatial structure is most apparent in the form of separate In the present paper, we consider the evolution of organelles
compartments or compartmentalization, a phenomenon studied and physical compartmentalization. Our main aim is to discuss
in its abstraction as ‘modularity’ in diverse fields ranging from how new organelles are formed and new organellar functions
psychology to engineering, from arts to biology [3]. evolve. To do so, we illustrate the broad diversity of organelles
In biology, modular or compartmentalized systems are found and contrast the various mechanisms of compartmentalization
across all scales. The separation of functions inherent to in prokaryotes and eukaryotes (Figure 1). We review current
compartmentalization results in robust [4] yet evolvable [5] theories about the origins and evolution of different types of
systems, which may explain the prevalence and evolutionary organelles. Finally, we briefly discuss the genetic basis of different
success of this organizational paradigm: ecological networks are compartments, i.e. the pathways for assembly, maintenance,
compartmentalized, individuals are composed of multiple parts inheritance, transport from/to and across the physical barriers,
such as organs, organs are composed of multiple cell types, and the evolutionary mechanisms shaping those genetic
cells themselves are subdivided into compartments, proteins are systems.
composed of domains, and so on. The tremendous diversity of organelles precludes an exhaustive
Among these entities, the cell plays a special role in biology and enumeration, as well as an in-depth discussion of each one in
has for long time been understood as the basic unit from which all particular. Instead, we chose to focus on selected compartments
living beings are built (the ‘Cell Theory’; see [6] for a historical which illustrate distinct aspects, and point the reader to recent
perspective). The cell compartmentalizes processes in multiple reviews for deeper exploration of this fascinating topic.
ways, e.g. by using gradients [7], via lateral diffusion barriers such
as the septins in membranes [8], by bringing multiple reactions
together via protein–protein interactions as for example in EVOLUTION OF ORGANELLES: PICTURES, REACTIONS AND GENES
metabolic channelling [9], or by using membranes and proteins to
physically separate distinct areas within the cell. Hereinafter, we How many types of organelles are there? How do they arise?
loosely refer to physically delimited compartments as organelles, These are old and surprisingly difficult questions, tightly linked
the focus of the present review. to the emergence of cell biology itself.
Abbreviations used: BMC, bacterial microcompartment; DCG, dense-core granule; EGT, endosymbiotic gene transfer; ER, endoplasmic reticulum; ES,
endomembrane system; IFT, intraflagellar transport; IMS, internal membrane system; LRO, lysosome-related organelle; MB, magnetotactic bacteria; MRO,
mitochondria-related organelle; NE, nuclear envelope; NPC, nuclear pore complex; TGN, trans -Golgi network; TIC, transporter of the inner chloroplast
membrane; TIM, transporter of the inner mitochondrial membrane; TOC, transporter of the outer chloroplast membrane; TOM, transporter of the outer
mitochondrial membrane.
1
To whom correspondence should be addressed (email [email protected]).

c The Authors Journal compilation
c 2013 Biochemical Society
320 Y. Diekmann and J. B. Pereira-Leal
Not surprisingly, comparative genomics has its own limitations.

The starting point for a comparative genomic study is always
a set of sequenced and annotated genomes. As sequencing is
biased towards organisms of biomedical or industrial interest,
many evolutionarily interesting taxa are not represented by
a single sequenced genome. The second step in comparative
genomics is the selection of genes that are informative about
a given organelle. As we will see below, a significant fraction
of organellar diversity is not associated to any molecular data
that can be mapped to a genome and, as a result, comparative
genomics is simply impossible. Having genomes to compare,
and representative genes selected, the homology between genes
need to be established. For closely related organisms, this is
a rather simple task. However, after hundreds of millions of
years, the evolutionary relationships may be less obvious. After
establishing homology, the potential gene content of ancestral
hypothetical species lying on the interior branching points of
the species tree can be reconstructed. This is mostly done using
parsimony, a straightforward application of Occam’s razor. In
brief, the ancestral state is chosen which requires the fewest
evolutionary events that alter its gene content (i.e. gene gains
and losses) to explain its descendants. However, there is no
Figure 1 Diversity of physically delimited compartments
intrinsic reason why evolution would have to always proceed
parsimoniously, i.e. in a minimal number of steps, and statistically
Examples of membranous and proteinaceous organelles in the prokaryotic and eukaryotic more sophisticated model-based approaches exist. Lastly, the
domain with their taxonomic distribution. Shown are the nucleus (IMS/Eukarya), bacterial interpretation of the results requires judging the cell-biological
thylakoids (inspired by the model presented in [74]) (IMS/Bacteria), a granule which has consistency of the comparative genomics predictions [17]. There
been proposed to represent an organelle homologous with acidocalcisomes (the broken-line
circles represent the cell wall and plasma membrane) [159] (IMS/Archaea), a mitochondrion
is no general recipe to do so, and any reasoning depends on what is
(Endosymbiotic/Eukarya), a Gammaproteobacterial endosymbiont of a Betaproteobacteria living known about the cell biology of the compartment. Reconstructing
in cells of the mealy bug (the outer broken-line circle represents the plasma membrane, and the evolution of organelles is thus a perilous adventure. However,
the inner broken-line circle represents the outer membrane of the mealy bug’s endosymbiotic as we discuss below, a series of general principles regarding the
compartment) [122] (Endosymbiotic/Bacteria), the eukaryotic vault protein complex [131,132] origins and evolution of intracellular compartments are emerging.
(Proteinaceous/Eukarya), a model for the shell of BMCs [77] (Proteinaceous/Bacteria), and For practical reasons, we divide the discussion into three types of
finally archaeal gas vesicles [127,163] (Proteinaceous/Archaea). To the best of our knowledge,
no endosymbiont living in an archaea has been described to date. Furthermore, the existence of a
organelles: IMSs (internal membrane systems), endosymbiotic
membrane delimiting the archaeal granule has to be confirmed (indicated by the question mark). and protein-based organelles.
The presence of vaults in Excavata is inferred from our own BLAST analysis retrieving putative
homologues of the major vault protein in Kinetoplastida; however, cell biological evidence is
required (again indicated by a question mark).
INTERNAL MEMBRANE SYSTEMS
As early as the 19th Century, light microscopy had shown The characteristic cellular architecture of eukaryotes is defined
the existence of the nucleus, ER (endoplasmic reticulum) or by extensive membrane-delimited compartments. In animals,
‘ergatoplast’, Golgi, mitochondria and chloroplasts [6]. Yet, approximately half of the volume of a eukaryotic cell is
the full extent of eukaryotic cellular complexity was only membrane-enclosed (see Table 12.1 in [18]), and in plants
revealed with the advent of electron microscopy in mid-20th the vacuole can make up to 95 % of the cellular volume.
Century [12]. In parallel, biochemical fractionation led to the Prokaryotes also have unique and diverse membranous organelles
discovery of other compartments such as the peroxisome and compartmentalizing the cytoplasmic space [19] (Figure 2).
the lysosome [13,14]. Most importantly, biochemical approaches
allowed the assignment of specific biochemical activities to
distinct organelles, establishing the notion of biochemical or
The eukaryotic ES (endomembrane system)
functional compartmentalization of the cell.
Microscopy showed very early on that similar compartments The eukaryotic ES is composed of numerous organelles, such
were present in many organisms. For example, the early Cell as the ER, the Golgi apparatus, lysosomes or vacuoles, and a
Theory postulated that all plants, and later also all animals, were trafficking machinery that links these compartments via vesicular
composed of nucleated cells (reviewed in [6,12]), and fuelled the intermediates. It is functionally organized mainly along two major
first debates about the origins and inheritance of an organelle pathways: the secretory/exocytic pathway that synthesizes, folds,
[15,16]. modifies and targets proteins and lipids to the plasma membrane
Besides morphological and functional similarity, comparative or the outside of the cell [20], and the endocytic pathway which
genomics has recently opened a new window that allows for operates in the opposite direction, taking proteins and material up
the comparison of the genetic basis of organelles. The steady from the surface in order to be either recycled or degraded [21].
growth of fully sequenced genomes and the accumulation of The ES probably evolved from inward budding of the plasma
data that map organellar functions to gene products allows us membrane in some ancestor of eukaryotes [22]. The main support
to ask whether two organelles are homologous, because they are for this hypothesis comes from the location of the protein
built from homologous gene products, or whether the apparent translocation machinery, a system to integrate or translocate
similarity is based on entirely different machineries, suggesting a proteins into or across lipid bilayers and which is a fundamental
functional and/or morphological analogy instead. requirement for all autonomous lifeforms. In prokaryotes, it is

Evolution of intracellular compartmentalization 321
found in the plasma membrane, whereas eukaryotes translocate As it is not implausible to think that eukaryogenesis involved
proteins through the membrane of the ER. major population bottlenecks, non-selective processes may also
Depending on the cellular complexity ascribed to the eukaryotic explain the evolution of some of the eukaryotic cellular structures.
ancestor, eukaryotes are an example either for an increase in As a consequence, although the emergence of complex features
compartmentalization or even for the de novo evolution of inspires us to think of selective drives, many of the features of
an ES in an ancestral cell previously lacking membranous the eukaryotic ES, and of the nucleus in particular, may have
compartments. This directly prompts an essential question: what started as non-adaptive events. These would have been fixed as a
are the evolutionary forces which can lead to autogenous evolution consequence of small population sizes, and only later gained the
of compartments? essential functions that ensured their conservation in eukaryotes.
The autogenous versus exogenous debate: peroxisomes

Evolving a compartmentalized cell plan: the nucleus
Compartments can evolve in different ways: autogenously, as we
In this section, we discuss possible evolutionary forces driving discuss above for the nucleus, or as a result of an endosymbiotic
organellogenesis. We illustrate the debate using the example event. For most organelles, both scenarios have been proposed, but
of the eukaryotic nucleus, which is the defining morphological in many cases the debate has settled: the community mostly agrees
feature shared by all eukaryotic cells and the organelle that has on an endosymbiotic origin of mitochondria and an autogenous,
spurred the most debate. The nucleus is a specialized compartment i.e. non-endosymbiotic, origin of the ES.
spatially confining the chromosomal DNA and consists of the However, for example, in the case of the peroxisome, deciding
double bilayered NE (nuclear envelope), a specialized part of between the two competing models of compartmental origin is not
the ER. Nuclear pores fenestrate the NE and are the sole sites straightforward, and owing to its hybrid characteristics, arguments
of material exchange, which are filled and stabilized by one of in favour of both modes of origin persist. Peroxisomes are
the largest macromolecular assemblies of the eukaryotic cell, the single-membrane-bound organelles characterized by the presence
NPC (nuclear pore complex). of hydrogen-peroxide-producing oxidases, and catalases that
The question of how the nucleus evolved has attracted break down hydrogen peroxide [33]. In animals, peroxisomes
much attention, as it has to be explained by any scenario for are involved in lipid metabolism and free radical detoxification
eukaryogenesis. Multiple models based on endosymbiosis, either [34], among other processes. In protists, the diversity and
of viral [23] or prokaryotic organisms [24], as well as autogenous specializations of their functions sometimes blurred their common
origins in the context of an evolving ES have been proposed and identity as peroxisomes, and motivated names such as glycosome,
extensively debated [17,25,26]. Although this debate surely is not glyoxysome or Woronin body [35].
over yet, recent evidence strongly supports an autogenous origin An endosymbiotic origin of peroxisomes is suggested by
(see [27] for a recent review). several lines of evidence. Peroxisomal membrane and matrix
In any case, the origin of the nucleus does not explain why it proteins are translated by free cytosolic ribosomes independently
evolved in the first place. In the following, we highlight some of the ER, and their import into the peroxisome is mediated
suggestions for an adaptive value early in the origin of the by short peroxisome-targeting signals [33], which are bound by
nucleus. Lopez-Garcia and Moreira [28] propose a scenario in cytosolic receptors. Such ER-independent protein translation and
which the formation of the nucleus is initially driven by the targeting mechanisms are also found in mitochondria and plastids,
need to separate the anabolic and catabolic pathways. Hence with which peroxisomes share certain metabolic pathways.
this hypothesis states that the enclosing of the genome is Peroxisomes normally arise from fission of existing peroxisomes,
a by-product of metabolic compartmentalization. In contrast, an inheritance strategy shared with endosymbiotic organelles.
other theories place the adaptive value on the informational However, this model has recently been challenged by
function of the nucleus. Cavalier-Smith [29] hypothesized that both genomic [36] and cell-biological [37] evidence. Comparative
as chromosomes became longer, the nucleus emerged to provide genomic analysis of peroxisomal proteomes revealed that
physical protection against chromosome shearing. Jékely [30] approximately half of the genes are of eukaryotic origin.
proposed that the nucleus allowed the cell to avoid the formation of Furthermore, mechanisms for the recruitment of entire
less efficient chimeric ribosomes resulting from mixing ribosomal mitochondrial pathways have been proposed [36,38], able to
subunits in the chimaeric proto-eukaryote. Another scenario account for the presence of the bacterial genes in the peroxisomal
argues for the separation between DNA transcription in the proteome. Particularly relevant is that the import machinery used
nucleus and RNA translation in the cytoplasm as a central by peroxisomes has been found to share similarities with the
driver for compartmentalizing the genetic material. Assuming an ER misfolded protein machinery. More generally, peroxisomal
early origin of mitochondria, such a separation would provide maintenance proteins were found to be homologous with the
a mechanism allowing for (slow) splicing to occur before ERAD (endoplasmic-reticulum-associated protein degradation)
translation, important to cope with an invasion of introns in the pathway [34,36], suggesting an evolutionary connection between
wake of the acquisition of mitochondria [31]. This latter view peroxisomes and the ER and hence to the ES. A second major line
is not inconsistent with the other scenarios, and has also been of evidence supporting an autogenous origin of the peroxisome
suggested as a later drive for nuclear evolution in [28]. Thus these relates to its inheritance. Besides fission, peroxisomes can be
three models argue that fidelity and efficiency of information formed de novo [34] from membranes and vesicles clearly
processing provided the basic selective drive to form an NE. originating from the ER [33]. Hence current evidence strongly
An alternative to the above is to view the nucleus as a ‘frozen supports an autogenous origin.
accident’, using the words of Bill Martin [26]. The smaller the
population size, the weaker is the force of selection in relation
One organelle, many shapes: Golgi
to drift. This opens the possibility that characters which are not
advantageous in any way, or even slightly deleterious, can be fixed. Organelles of the ES mostly have complex shapes, with spherical,
It has been argued that this basic principle is able to account for flat or tubular regions, and the tendency of these shapes to be
much of the genomic architecture observed in eukaryotes [32]. conserved throughout evolution suggests that they are important

Figure 2 Ultrastructure of selected prokaryotic compartments

Illustrations of the structural and taxonomic diversity of prokaryotic intracellular compartments. 1, Archaeal gas vesicles. Taken from Springer, Complex Intracellular Structures in Prokaryotes ,
2006, 115–140, Gas vesicles of archaea and bacteria by Pfeifer, F., Figure 4(A), c 2006 Springer-Verlag, Berlin, with kind permission from Springer Science and Business Media. 2, An archaeal
granule which has been proposed to be homologous with acidocalcisomes (Acidocalcis., uncertainty indicated by question mark). The arrow indicates the electron-dense volutin granule. Reproduced
with permission from Seufferheld, M.J., Kim, K.M., Whitfield, J., Valerio, A. and Caetano-Anolles, G. (2011) Evolution of vacuolar proton pyrophosphatase domains and volutin granules: clues
into the early evolutionary origin of the acidocalcisome. Biol. Direct 6, 50. 3, Isolated chlorosomes (photosynthetic membranes) from Acidobacteria. From Bryant, D.A., Costas, A.M., Maresca,
J.A., Chew, A.G., Klatt, C.G. et al. (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317: 523–526. Reprinted with permission from AAAS.
4, Thylakoid membranes with perforations, as well as carboxysomes. Scale bar, 500 nm. Reprinted by permission from Macmillan Publishers Ltd: EMBO J., Nevo, R., Charuvi, D., Shimoni, E.,

for organelle function [39]. Yet, organelle structure can be very lysosomal membrane proteins delivered by endosomes coming
dynamic and vary across organisms and tissues. The Golgi from the TGN [49].
apparatus is an example of such a dynamic and morphologically The lysosome is a good example of an evolutionarily plastic
heterogeneous compartment. compartment which evolved additional functions. In fungi and
The Golgi is the central hub of the membrane-trafficking plants, the functional equivalent of the lysosome is the vacuole,
system and the site where the two major pathways, secretory which has adapted to many additional roles, e.g. in calcium
and endocytic, intersect. It receives secretory lipids and proteins homoeostasis and osmotic control, long-distance transport of
from the ER, which are post-translationally modified, sorted nutrients through the mycelial filaments, storage of organic and
and targeted to their final destination. Vesicles for constitutive inorganic nutrients, and in generating turgor pressure [50–52]. In
secretion are formed at a specialized subcompartment of the plants, at least three distinct vacuole types have been described,
Golgi, the TGN (trans-Golgi network). the lytic, protein storage and the senescence-associated vacuole
The Golgi is nearly ubiquitous in eukaryotic cells [40] that coexist in some cell types [53,54].
and performs essential functions. Yet, it shows great diversity In animals, the lysosome diversified into a whole family of
in biogenesis, morphology and inheritance. In mammals, it distinct compartments, the LROs (lysosome-related organelles)
consists of a series of flattened cisternal membrane structures [55]. Some LROs evolved to function as secretory compartments,
responsible for the Golgi’s large and regular structure. The yet without losing the ability to perform classic lysosomal
cisternae form Golgi stacks, which are interconnected by functions, as for example the lysosomes of cytotoxic T-
lateral tubules and organize into the Golgi ribbon [41]. At the lymphocytes. In contrast, other LROs have lost degradative
onset of mitosis, the Golgi loses its characteristic shape and capacity and coexist with lysosomes in one cell, e.g. melanosomes
fragments into tubulovesicular structures, which are partitioned and diverse types of granules. They are still formed from maturing
during cytokinesis and later reform the Golgi [42]. Interestingly, endosomes, and are therefore distinct compartments different
Drosophila cells usually lack a Golgi ribbon, but clearly have the from other organelles involved in regulated secretion such as
potential to form it, as is observed for example in spermatids secretory granules. LROs and lysosomes are biogenically related
[41]. In Saccharomyces cerevisiae, the Golgi does not have organelles [56], suggesting an ‘organelle paralogy’ that still awaits
the stacked morphology, but rather consists of single isolated confirmation at the genetic level. LROs are highly taxon- and
cisternae distributed throughout the cytoplasm [43]. However, tissue-specific, and with growing knowledge of the diversity of
this type of organization appears to be an exception, as most eukaryotic cell biology more of these organelles may be found.
fungi possess Golgi stacks [43,44]. Yet another shape is observed A candidate LRO is for example the apicomplexan rhoptry, an
in plants: their Golgi apparatus is made of hundreds of individual apical secretory organelle involved in host cell invasion [57].
motile stacks which are not disassembled during cell division
[45]. Most surprising for an organelle with essential functions,
the Golgi has been lost altogether on at least eight independent Homology versus analogy: granules and bacterial
occasions [44]. For example, the protozoan parasite Giardia intracytoplasmic membranes
lamblia lacks a morphologically discernible Golgi, and secretory Functional and/or morphological similarity is most readily
functions are performed at specific ER sites [46]. explained by homology, i.e. common ancestry. Thus the common
interpretation of similarities observed among organelles is that of
a single evolutionary origin. However, convergent evolution also
plays a role in subcellular evolution, giving rise to analogous
One organelle, many functions: lysosomes
organelles defying this interpretation. Below, we discuss two
Lysosomes are the primary catabolic site of the animal cell [47] examples: DCGs (dense-core granules), which probably arose
that receive and degrade macromolecules from multiple cellular multiple times in eukaryotes, and the relationship between the
pathways (secretory, endocytic, autophagic and phagocytic) IMSs of Plantomycetes and those of eukaryotes.
[48] in their characteristic acidic lumen. The maintenance of DCGs are specialized secretory vesicles with a characteristic
lysosomal function depends on constant influx of hydrolases and condensed protein core involved in regulated secretion [58,59].
Schwarz, R., Kaplan, A., Ohad, I. and Reich, Z. (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO J. 26, 1467–1473, c 2007. 5, Thylakoids
and carboxysomes in a dividing cell. Scale bars: left, 200 nm; right, 50 nm. From Kerfeld, C.A., Sawaya, M.R., Tanaka, S., Nguyen, C.V., Phillips, M., Beeby, M. and Yeates, T.O. (2005) Protein
structures forming the shell of primitive bacterial organelles. Science 309, 936–938. Reprinted with permission from AAAS. 6, Chlorosomes in a cell with a central inclusion. Taken from Springer,
Photosynthesis Research , 86, 2005, 145–154, The ultrastructure of Chlorobium tepidum chlorosomes revealed by electron microscopy, by Hohmann-Marriott, M.F., Blankenship, R.E. and Roberson,
R.W., Figure 1B, c 2005 Springer, with kind permission from Springer Science and Business Media. 7, A Gammaproteobacterial endosymbiont (γ -prot.) living in a Betaproteobacterial host, itself an
endosymbiont of the mealy bug. b, bacteria; hc, host cell cytoplasm; im, inner membrane; om, outer membrane; ss, symbiotic sphere (white arrows indicate the three membranes of the sphere). Scale
bar, 0.0706 μm. Reprinted by permission from Macmillan Publishers Ltd: Nature , von Dohlen, C.D., Kohler, S., Alsop, S.T. and McManus, W.R. (2001) Mealybug β-proteobacterial endosymbionts
contain γ -proteobacterial symbionts. Nature 412, 433–436, c 2001. 8, Intravacuolar Betaproteobacterial endosymbiont (β-prot.) living in a Gammaproteobacterium. IVS, intravacuolar structures.
Reprinted with permission from Larkin, J.M. and Henk, M.C. (1996) Filamentous sulfide-oxidizing bacteria at hydrocarbon seeps of the Gulf of Mexico, Microscopy Research and Technique , 33, 23–31.
c 1996 Wiley-Liss, Inc. 9, BMC, originally called an enterosome (arrowhead) [77]. From Applied and Environmental Microbiology , 2001, 67, 5351–5361, 10.1128/AEM.67.12.5351.5361.2001.
Reproduced with permission from American Society for Microbiology. 10, Chromatophores (photosynthetic membranes). B, poly-β-hydroxybutyrate granules; C, ribosome-containing cytoplasm;
CM, cytoplasmic membrane; N, nucleoplasm with DNA threads; P, polyphosphate granule; Th, thylakoid; ZW, cell wall. The arrow shows the site of cytoplasmic membrane invagination. Taken
from Springer, Archiv für Mikrobiologie , 59, 1967, 385, Thylakoidmorphogenese bei Rhodopseudomonas palustris , Tauschel, H.D. and Draws, G., with kind permission from Springer Science and
Business Media. 11, Bacterial acidocalcisomes. The arrow indicates a vacuole, containing an electrondense material in the periphery. Scale bar, 0.1 μm. Reproduced from Seufferheld, M., Vieira,
M.C., Ruiz, F.A., Rodrigues, C.O., Moreno, S.N. and Docampo, R. (2003) Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J. Biol. Chem. 278, 29971–29978.
c 2003 The American Society for Biochemistry and Molecular Biology. 12, Magnetosomes with empty membranous vesicles (MV). Scale bar, 250 nm. From the Journal of Bacteriology , 1988, 170,
834–841, reproduced with permission from American Society for Microbiology. 13, Internal membranes forming a compartment claimed to resemble the eukaryotic nucleus. ICM, intracytoplasmic
membrane; N, nucleoid; NE, nuclear envelope; P, paryphoplasm. Republished with permission of Annual Reviews, Inc., from Intracellular compartmentation in plantomycetes, by Fuerst, J.A.,
Annual Reviews in Microbiology 59, 299–328, 2005; permission conveyed through Copyright Clearance Center, Inc.

Membranous compartments resembling mammalian DCG are shown in Figure 2: 4 and 5 show thylakoids, 3 and 6 show
found in diverse eukaryotic lineages where they serve a wide range chlorosomes, and 10 shows chromatophores). They form a
of functions, e.g. the trichocysts in Paramecium tetraurelia, which proper compartment with characteristic lipid composition [71,72]
function in predator defence, or encystation secretory vesicles harbouring the photosynthetic systems in Cyanobacteria and
in G. lamblia, which provide protection from the environment chloroplasts. In Cyanobacteria, they mainly consist of long
[60]. They share important hallmarks with mammalian granules: lamellae appearing as several flattened and stacked layers.
biosynthesis from the TGN, subsequent maturation and regulated Unlike bacteria performing anoxygenic photosynthesis, thylakoid
secretion upon specific stimuli [60]. The comparison of the membranes are not connected to the plasma membrane [72].
molecules essential for the structural scaffold of DCG in ciliates The discontinuity with the plasma membrane raises an
and mammals showed that the genes in ciliates are lineage-specific important question: the precursors of the photosystems are pre-
innovations. Moreover, key proteins important for maturation, assembled in the plasma membrane, but how are those proteins
e.g. endoproteases, and organellar identity, e.g. SNAREs (soluble and lipids transferred to the thylakoids? The obvious possibilities
N-ethylmaleimide-sensitive fusion protein-attachment protein are via transient membrane connections or by vesicle transport
receptors) and Rabs, are not orthologous. Hence, comparative [71,73], but the definitive mechanism has not yet been determined.
genomics hints at an independent origin of DCG at least in Interestingly, cytoplasmic vesicles have been reported in fixed
ciliates and mammals, implying that an entire organelle can arise samples of some cyanobacterial species, where they were found
repeatedly by convergent evolution. to be located near and partially fused to thylakoids [74]. This
Another important debate regarding homology versus analogy means that bacteria with thylakoids may be capable of long-
is the relationship between the intracytoplasmic membranes range vesicular trafficking, but independent confirmation is still
of Planctomyetes (see, for example, 13 in Figure 2) and the lacking. In support of this hypothesis, thylakoid membranes
eukaryotic ES, in particular the nucleus. Planctomycetes are showed numerous perforations through which substantial flow of
a major bacterial phylum that compartmentalize cytoplasmic cellular material such as ribosomes and storage granules could be
space by internal membranes [61]. In its simplest form, e.g. observed. These features could be adaptations to allow for efficient
in the genus Pirellula, a lipid bilayer sequesters chromosomes intracellular transport, possibly also of membrane-bound vesicles
and ribosomes from other cellular components and forms an [74]. Hence this could mean that when confronted with the
organelle coined the pirellulosome [62]. In some Planktomycetes, corresponding cell-biological challenge, prokaryotes may have
the pirellulosome is itself compartmentalized and contains a the potential to evolve an ES organized according to the same
double-bilayer membrane fenestrated by small pore-like openings principles as eukaryotes.
surrounding the compacted chromosome [63]. These membranes
hence form a structure with obvious morphological parallels to the
Lateral organelle transfer: bacterial magnetosomes
eukaryotic nucleus, although the functional implications of those
IMSs are currently unclear. For example, a clear separation of Magnetosomes are membranous compartments of a diverse
transcription and translation cannot be observed, as ribosomes paraphyletic group of MB (magnetotactic bacteria) (see, for
are present both inside and outside the nuclear body [64]. example, 12 in Figure 2). They are usually organized in one
The discovery of membrane coat-like proteins in these bacteria or more chains of 15–20 organelles. They allow the sensing of
[65], the description of endocytosis-like processes [66] and geomagnetic field lines, which bacteria use to find preferred redox
several other similarities to eukaryotes have fuelled speculations conditions [64]. Magnetosomes are formed by invaginations of the
that Plantomycetes may represent a frozen intermediate stage plasma membrane [75] which house a ∼50 nm magnetic crystal.
between prokaryotes and eukaryotes [67]. This interpretation They contain a characteristic set of proteins in various quantities,
has, however, been strongly opposed [68]. This is a situation which suggests the existence of a dedicated sorting pathway [76].
that exemplifies well the limitations of comparative genomics: The arrangement in chains is achieved by filaments formed by
the claims of homology of some components rely on very homologues of eukaryotic actin. Hence magnetotactic bacteria
sensitive methods to identify distant relationships, necessarily provide an example for prokaryotes, which, like eukaryotes, use
susceptible to false positive errors. Carl Sagan popularized the the cytoskeleton to position their organelles within the cell and
idea that “extraordinary claims require extraordinary evidence”, actively shape and maintain their intracellular organization [64].
considering the time that separates us from these events, any Sequencing of several MB revealed that most of the genes
claim of homology based on remote similarities is to be treated believed to be involved in biogenesis and functioning of
with caution. magnetosomes are comprised within a large genomic island [76a],
which may be sufficient to form a magnetosome [64]. It could be
shown by comparative genomics that the island has been laterally
Thylakoids, bacterial intracellular trafficking? transferred between diverse bacterial species [76b] accounting for
Planctomycetes provide a good illustration of the fact that the patchy phylogenetic distribution of MB.
bacteria are able to evolve IMSs fully detached from the plasma Thus magnetosomes are an example for the lateral transfer of
membrane. Yet, a major difference from the eukaryotic ES is an entire compartment. This process is unique to the prokaryotic
the lack of obvious vesicular trafficking, conceptually separating domain, where it may be rather common: comparative genomics
the endomembranes observed across the two domains of life. suggests that, for example, the proteinaceous compartments
Bacteria do not share the same need for active trafficking as discussed below have been laterally transferred among as much
eukaryotes, as they are in general small enough to rely on diffusion as one-fifth of sequenced bacterial species [77].
[69]. However, some use motor-driven intracellular transport
for cellular movement [70] and indications exist that some
cyanobacteria may have evolved dynamic vesicular trafficking ORGANELLES OF ENDOSYMBIOTIC ORIGIN
pathways in the context of thylakoid membranes.
The universal mitochondria
The thylakoids are one of at least three major types of
photosynthetic membranes [64] (examples of thylakoids and One of the most distinctive features of eukaryotic cells, and
the other two types, chlorosomes and chromatophores, are potentially the critical step in the establishment of the eukaryotic

cell plan [78], is the presence of mitochondria. They are the Parasites versus endosymbionts
result of an ancient endosymbiosis predating the radiation of Mitochondria and chloroplasts represent one extreme of full
eukaryotes, as all eukaryotic cells have mitochondria or MROs integration between endosymbiotic organelle and host. At the
(mitochondria-related organelles) such as hydrogenosomes or opposite end of the spectrum are compartments formed by
mitosomes [79–81]. This second group is sometimes genome- intracellular parasites that invade and parasitize eukaryotic cells
less, but biochemical similarity and molecular composition have for several resources, occupying different intracellular niches
established them as derived mitochondria ([82], and reviewed (phagosomes, lysosomes, cytosol, etc.) and having a deleterious
in [80,81]). In most cases, mitochondria and MRO seem to effect on the host [94–96]. Examples are the agents of Lyme
be involved in the generation of ATP, either by aerobic or disease, typhus or leprosy. In between these two extremes, we
anaerobic respiration [79]. Sometimes, this function may be find multiple independent cases of endosymbiosis of bacteria from
shared with other prokaryote-derived organelles, such as in ciliates diverse taxonomic groups with various degrees of integration with
living under anaerobic conditions, which have acquired multiple organisms from the majority of eukaryotic taxa.
archaeal endosymbionts that consume produced hydrogen and use It is unclear where to draw the line between parasite
it to reduce carbon dioxide [83]. These observations have fuelled and endosymbiont. In the case of the associations of
the hypothesis that mitochondria provided the energy necessary Buchnera sp. with several insects, the endosymbiont supplies the
for the establishment of the complex eukaryotic cell plan [78]. host cell with essential amino acids that it cannot synthesize or
However, the only mitochondrial function that is never lost, even obtain from the environment, and its presence has no obvious
in very derived MRO, is the synthesis of iron–sulfur clusters fitness cost, suggesting (endo)symbiosis [97]. On the other hand,
[80,84]. This suggests that the dependence of the cell on the the association of Wolbachia with several insects is less clear:
energy produced by mitochondria may be reduced, for example it provides protection against viral and bacterial infections,
in the context of parasitic relationships. while inducing a series of reproductive alterations on the host
organisms via feminization, male-killing, parthenogenesis and/or
cytoplasmic incompatibility [98]. Hence fitness trade-offs exist
and the distinction between parasite and symbiont is less obvious.
However, unlike Buchnera, Wolbachia is not essential, suggesting
Same organelle, repeatedly: plastids that the parasite has not fully integrated with the host. It is
tempting to speculate that endosymbiotic compartments may start
Plastids are found in a variety of phylogenetic lineages. However, off as a parasitic relationship that evolved to mutual benefit, to the
their evolutionary relationships are not straightforward, as point where the endosymbiont becomes an essential compartment
successive endosymbiotic events resulted in cells consisting of of the host cell. Endosymbiotic associations have been reviewed
several nested organisms. extensively elsewhere [99–104].
A single ancient endosymbiosis gave rise to the chloroplasts
found in the Plantae supergroup (Glaucophyte, and red and
green algae) (reviewed in [85–87]). This stable relationship
was established between a putative phagotropic mitochondria- Moving genes and proteins around: EGT (endosymbiotic
containing host cell and a cyanobacterium. Subsequent gene transfer)
independent symbiotic events of chloroplast-containing algae Endosymbiotic and obligate endoparasitic relationships are
with several protozoa gave rise to the plastids found in accompanied by extensive gene loss, as these bacteria ‘outsource’
Chromalveolata, Rhizaria and Excavata (see [85–88] for reviews). many of their normal metabolic requirements to the host [100].
These secondary endosymbioses are well illustrated by the Endosymbionts such as Carsonella rudii exemplify how far this
existence of typically four plastid membranes, as opposed genome miniaturization can go, retaining only 182 open reading
to the two membranes observed in organelles derived from frames and a 160 kb genome [105]. Genes from the bacterial
a primary endosymbiosis (mitochondria and chloroplasts). endosymbiont are frequently transferred to the nucleus, and
Furthermore, in Dinoflagellates, even tertiary endosymbiotic infrequently retained. For example, Wolbachia-derived transfers
events have occurred, leading to organisms with an intriguingly of various sizes have been detected in a large range insects and
complex compartmentalized cell plan [86]. Interestingly, the nematodes, ranging from individual genes to almost complete
amoeba Paulinella chromatophora acquired a cyanobacterial genomes [106].
endosymbiont which has been argued to represent a second In the case of the mitochondria and chloroplasts, this genome
independent origin of a primary plastid. It is, however, still a reduction has been even more extreme and was accompanied by a
matter of debate whether the level of genetic integration [89] and substantial transfer of the organelle’s genes to the nuclear genome
the protein-targeting system [90] qualify the endosymbiont as a and by the loss of the corresponding genes from the organelle
bona fide organelle [91]. genome. This led to a reliance on the host to synthesize the gene
Primary plastids (chloroplasts) are photosynthetic organelles products and target them to the symbiont, requiring the evolution
that can differentiate in a reversible manner into storage functions. of targeting and transport systems. This process is termed EGT
Some secondary plastids retained their photosynthetic function, (reviewed in [107]), and was argued to represent the defining step
as, for example, is the case for members of the genus Euglena, in the transition from an endosymbiont to an organelle (for a
while others lost it (see [88] for a review). The function of discussion, see [108]).
these latter plastids is unclear, even though their existence in Mitochondrial proteins are synthesized in the cytosol and
human pathogens as, for example, the causative agents of malaria, maintained in an unfolded translocation-ready conformation by
toxoplasmosis and cryptosporidiosis has made them subject of the action of chaperones. Their import into mitochondria is
intense interest (see [92,93] for reviews). Thus plastids represent mediated by the TIM (transporter of the inner mitochondrial mem-
yet another example of one organelle with multiple taxon-specific, brane)–TOM (transporter of the outer mitochondrial membrane)
cell-type-specific and condition-specific functions, illustrating complexes via sophisticated pathways (reviewed extensively in
how the principle discussed for lysosomes applies also to [109]). Proteins destined to the plastid are mostly synthesized
organelles of endosymbiotic origin. in the cytosol and targeted to the TIC (transporter of the inner

chloroplast membrane)–TOC (transporter of the outer chloroplast origins of some or even most of the prokaryotic endosymbionts
membrane) complexes. These complexes are molecularly of bacteria.
unrelated to each other, suggesting independent evolutionary
origins. Bacteria contain many proteins with similarity to the
mitochondrial translocation and targeting machineries, suggesting PROTEIN-BASED ORGANELLES
that the latter were assembled from the former [110,111].
Similarly, the TIM–TOM system appears to have evolved from Although the creation of physical separation between two
pre-existing prokaryotic and eukaryotic components [112]. environments has been most visibly achieved by lipid membranes,
Interestingly, a subset of proteins that are destined to the both prokaryotes and eukaryotes have also used proteins for the
chloroplast are also trafficked through the ES, by an as yet same purpose.
unknown mechanism [113–115]. This has been hypothesized to
represent an ancient transport pathway, which appeared before
the establishment of the TIC–TOC pathway [87]. Supporting this Protein shells everywhere
argument is a recent endosymbiosis of a Cyanobacteria by the Prokaryotes possess a variety of protein-bound organelles. These
amoeba P. chromatophora [116] (reviewed in [86–88]), where compartments present a relatively recent paradigm of prokaryotic
several genes suffered EGT [89], and some have been shown organization, and few of these organelles have been studied
to be translated in the amoeba’s cytosol and then transported to thoroughly. Better known are for example gas vesicles found in
the endosymbiont in a Golgi-mediated pathway [90]. There is archaea (see, for example, 1 in Figure 2) and bacteria [127], and a
growing evidence that mitochondria can sort material into and certain class of BMCs (bacterial microcompartments) defined by
from vesicles that are then transported to peroxisomes (reviewed homologous shell protein families which we discuss below.
in [117]). Recent work revealed further that oxidized proteins can BMCs are a widely distributed functionally diverse organelle
be trafficked from mitochondria to the lysosome via vesicular family which is defined by its characteristic proteinaceous shell
intermediates [118]. Thus, although bona fide organelles have [77]. The shell is assembled from a few thousand members
evolved specific targeting and transport systems, these coexist of the conserved BMC family of shell proteins, giving rise
with vesicle-mediated transport. It is interesting to note that the to organelles up to ∼150 nm in size. Some BMCs store
ES is frequently subverted by intracellular pathogens [119,120], special compounds [128], whereas others create an internal
supporting the notion that endosymbiosis may, in some cases, microenvironment in which metabolic enzymes and auxiliary
derive from a parasitic association. proteins are concentrated. This enhances the catalytic efficiency
by enabling substrate channelling and due to increased local
metabolite concentrations which help to overcome poor enzyme
affinities for their substrate, or serves to spatially confine toxic
Prokaryotes inside prokaryotes
or volatile intermediates [77]. First described in 1956 [128a],
Less appreciated than endosymbiosis between pro- and eu- BMCs have long been studied mostly by electron microscopy,
karyotes is the fact that bacteria have also found replication niches which makes it difficult to estimate their abundance and diversity
inside other prokaryotes, which lends support to the idea that throughout bacteria. Examples of BMCs include carboxysomes
the endosymbiotic event that resulted in mitochondria did not (see, for example, 4 and 5 in Figure 2), which can be
necessarily require a pre-existing ES. One type of bacteria that found in all Cyanobacteria and concentrate Rubisco (ribulose-
contain prokaryotic endosymbionts are Gammaproteobacterial 1,5-bisphosphate carboxylase/oxygenase), the Pdu compartment
Beggiatoa spp. (8 in Figure 2), sulfide-oxidizing organisms, found in Salmonella enterica (see, for example, 9 in Figure 2)
found in freshwater and marine habitats. They harbour a variety or the Eut microcompartment also found in Escherichia coli.
of prokaryotic endosymbionts, but the metabolic nature of Relatively little is known about the cell biology of this special
the relationship is still elusive [121]. A better studied case class of organelles. A basic challenge is the sorting of enzymes to
is a secondary endosymbiosis in the endosymbiont of the the interior of the protein shell. Most interestingly, in Salmonella,
mealy bug (7 in Figure 2). This nested constellation consists short N-terminal targeting signals have been described that are
of a Gammaproteobacteria living as an endosymbiont of a sufficient to direct proteins to the lumen of these organelles [129].
Betaproteobacteria, which in turn is an endosymbiont of an Thus proteinaceous organelles can employ a system analogous to
insect, the mealybug [122]. Genomic analysis revealed extreme the targeting system known from secretion in bacteria and the two
metabolic integration between the two endosymbionts, with major types of lipid-bound organelles in eukaryotes.
the Gammaproteobacteria complementing several amino acid Recent molecular characterization of the shell proteins allowed
biosynthetic pathways of the Betaproteobacteria [100]. Even the computational screening of bacterial genomes, which revealed
mitochondria have been targeted by other prokaryotes, such homologous domains in more than 400 or one-fifth of the
as ‘Candidatus Midichloria mitochondrii’, an endosymbiont of sequenced bacteria analysed [77]. The phylogenetic distribution
the tick Ixodes ricinus. Although it resides in the cytosol, suggests frequent horizontal gene transfer of BMC shell genes,
it can invade and replicate inside mitochondria and consume which are organized in gene clusters facilitating their modular
them [123,124]. transfer. It could be shown by the artificial expression of an
Our understanding of the associations between prokaryotes empty microcompartment in E. coli that the genetic information
is still in its infancy. We do not know how frequent they in such a cluster is indeed sufficient for the formation of BMCs
are, the type of metabolic trade-offs they may involve or [130].
how inheritance of the endosymbiont is achieved after division Although less known, eukaryotes also have protein
of the host cell. Furthermore, the entry mechanisms involved shells forming small organelles, termed ‘vaults’. Vaults are
in these associations remain to be determined. They may be ribonucleoprotein particles consisting of two identical cups, each
similar to those used by the Deltaproteobacteria endoparasite with a characteristic eight-fold symmetrical shell structure. They
Bdellovibrio bacteriovorus that invades and replicates inside other sequester an interior volume large enough to capture hundreds of
bacteria [125]. Bacterial predators are, in fact, quite frequent proteins and multiple copies of small RNAs [131], and are found
and phylogenetically widespread [126], and could represent the mostly in the cytoplasm, although some localize to the nucleus

Figure 3 Evolutionary processes shaping the genetic basis of an organelle, illustrated using the nucleus as an example
Evolutionary processes which have the potential to alter the set of genes underlying an organelle. In a given structure, these processes do not exclude each other. Examples of nuclear genes which
probably evolved following the corresponding process, taken from [153], are given. FG repeat, phenylalanine–glycine repeat; GP210, glycoprotein 210; HGT, horizontal gene transfer; NTF2, nuclear
transport factor 2.
[132]. Homologues of the highly conserved vault constituents not form cilia [146]. The integration of cilia with other transport
can be found in diverse eukaryotes [133], and occur in numbers systems has become even more apparent with the discovery that
potentially as high as 104 –107 per cell [134]. Since their discovery ciliary entry of KIF17 (kinesin family member 17), an IFT motor,
in 1986 [134a], several putative functions have been put forth, e.g. is regulated by importin-β2 and RanGTP [147], key regulators of
roles in multidrug resistance, signalling and innate immunity, but nucleocytoplasmic transport.
their exact function remains elusive. The vault shell has been Thus the cilium represents an alternative way to create a
shown to be dynamic, opening the possibility that the vault’s distinct compartment within the ES. Although its biogenesis
interior may be able to interact functionally with the rest of and maintenance, like that of all other organelles within the ES,
cell [135]. requires the sorting and targeting of components using vesicular
intermediates, the physical separation of the space is not achieved
by enclosing it in a membrane, but rather by different protein-
Protein-based compartments in the ES: eukaryotic cilium based macromolecular machinery.
Above, we discussed the integration between the endosymbiotic
organelles and the ES. Now, we turn to the cilium in order
THE MOLECULAR BASIS OF ORGANELLAR EVOLUTION
to illustrate the integration of different types of organelles,
proteinaceous and membranous. We refer the reader to several The ability to sustain a compartmentalized cell plan in general, and
reviews on the functions and structure of the cilium and its any one organelle in particular, requires molecular machinery for
connection to the centrosome [136–138]. its assembly, maintenance, inheritance and for diverse trafficking
The eukaryotic cilium or flagellum (we use these terms routes. We discuss commonalities and major differences of how
interchangeably) is a microtubule-based protrusion from the these pathways evolved at the molecular level, both between
plasma membrane that is templated by a mostly invariant nine-fold eukaryotes and prokaryotes, as well as between the different
symmetrical microtubule-based cylinder termed the basal body, types of organelles.
from which the axoneme protrudes. Active-transport mechanisms In eukaryotes, organelles of the ES usually share a conserved
involving molecular motors move microtubule subunits and core of genes throughout all lineages which is complemented by
membrane receptors within, into and out of the cilium in a highly lineage-specific genes. This pattern arises from the interplay of
dynamic process. At the base of the cilium are protein-based two opposing evolutionary forces: lineage-specific gene losses
physical barriers that separate an internal and external space, as and gains. Genes gained in specific lineages mostly derive
well as protein-based physical barriers preventing lateral diffusion from two processes: co-option of previously unrelated genes
of proteins in the plasma membrane [136,139–141]. Cilia are and paralogous expansion of protein families already involved
found in all eukaryotic groups, and are thus believed to pre-date with the organelle (see, for example, [148,149]). Co-opted genes
the radiation of eukaryotes (reviewed in [141]). themselves can originate from different sources: they can be
The cilium appears to be a unique organelle in having internal endosymbiotic, horizontally transferred or the result of gene
microtubules. However, it has many connections to the ES. duplication. The second process contributing lineage-specific
The set of molecular motors which regulate the process of genes is paralogous expansion, which happens frequently and
IFT (intraflagellar transport) [142,143] within the cilium are is the result of gene duplications followed by preservation of
homologous with those functioning in endomembrane trafficking. both duplicates mostly due to sub- or neo-functionalization [150].
The assembly of axonemes and delivery of receptors to the ciliary Co-option and duplication are not the only possibilities for the
membrane depends on polarized trafficking. Cargo destined emergence of lineage-specific genes. Other possibilities are the
for the cilium is assembled and sorted at the Golgi and delivered at de novo origin of genes and domain shuffling, i.e. the evolution
the flagellar base, in a process dependent on canonical regulators of new genes by combining pre-existing protein domains in new
of trafficking in the ES (reviewed in [139,144]). This has led to ways [151,152]. All of these possibilities have been shown to
the proposal that cilia represent an elaboration of a pre-existing have contributed genes forming the NE and the NPC [153]
polarized trafficking from the Golgi to the plasma membrane (Figure 3). Gene duplications may be particularly important for
[145]. This hypothesis is supported by the discovery that IFT the functional diversification and evolution of new organelles
components are required for polarized secretion in cells that do in eukaryotes. For example, the organellar paralogy model

proposes that duplication/divergence of the key gene families of trafficking exists. Endosymbiosis is apparently the exception
an organelle could give rise to new organelles, free to diverge and rather than the rule in prokaryotes, whereas endosymbionts
acquire new functions analogous to the process at the gene level are ubiquitous in eukaryotes which all have at least one,
[154]. the mitochondrion or MROs. Furthermore, prokaryotes tend
In endosymbiotic organelles of eukaryotes, the driving force to have one type of compartment and not the coexistence
seems to be genome reduction by extensive gene loss [100,155]. of multiple organelles that characterizes eukaryotes. Thus,
One extreme case is observed in human mitochondria, which although the presence of intracellular compartments no longer
have only 13 protein-coding genes. Although only one genome distinguishes prokaryotes from eukaryotes, the complexity of
of a prokaryotic endosymbiont of prokaryotes has been well the compartmentalized cell plan is still substantially higher in
characterized, it suggests that genome reduction is also observed eukaryotes.
[100]. Inheritance of mitochondria involved the co-option of the Under this scenario, the debate on the origins of eukaryotes
machinery that insures segregation of the ES to the daughter needs to be formulated differently: what is the reason for the divide
cells after division [156]. More recent endosymbionts may have in complexity between the eukaryotic and prokaryotic cell plan?
also followed the same route, as exemplified by Wolbachia’s It has been proposed that energy limitations in prokaryotes may
segregation to the centrosome during cell division and its constrain their genome size and therefore preclude the evolution
microtubule-based inheritance [157]. of a more complex compartmentalized cell [78]. Under this
The molecular machineries underlying prokaryotic membrane- scenario, the acquisition of mitochondria was thus the key step
based organelles as well as protein-based compartments are still en route to the more complex eukaryotic cell plan. This suggests
poorly understood. However, in addition to the mechanisms an intrinsic limit to the complexity of extant compartmentalized
described for eukaryotes, a different process is important: prokaryotes. Yet, notably this lack of complexity has not limited
horizontal transfer of entire genomic islands containing the the success of prokaryotes, which are clearly the dominant
genes necessary to form a compartment. This appears to be lifeform on our planet. In contrast, eukaryotes appear to be
a frequent event both for membranous organelles, such as ‘condemned’ to a compartmentalized cell plan, which may at
magnetosomes, and proteinaceous organelles such as BMCs, best be slightly simplified with the loss of a small number of
which are the most widely distributed form of compartment in organelles.
prokaryotes. A question closely linked to the above considerations is
how easy it is to evolve a compartment, and if the potential
differs between the domains of life. In eukaryotes, endosymbiotic
events appear to be more frequent than in prokaryotes. However,
CONCLUSIONS
reaching the high degree of integration, as, for example, achieved
The origin of eukaryotes has been identified as one of the by mitochondria and plastids, appears uncommon even in
major transitions in evolution [158]. Whereas this is frequently eukaryotes. The emergence of an ES is a rare event, having
equated with the evolution of compartmentalization, the only happened once. It then served as a template to many
present review hopefully contributes to raise awareness that lineage-specific organelles. This suggests that it may be simpler
compartmentalization exists in all domains of life. and sufficient to build new organelles by variations of the
The prokaryotic cell plan is emerging as increasingly more existing system. This is strongly supported by the examples of
complex than previously thought. It is currently unclear analogous organelles within the ES [60], suggesting that evolving
how widespread compartmentalization is in prokaryotes, and a compartment in response to similar challenges is possible. In
how much more diversity will emerge from broader sampling contrast, different IMSs exist in multiple independent prokaryotic
of the prokaryotic world. In particular, the extent of lineages, suggesting that these rudimentary forms are somehow
compartmentalization of archaea is still largely unknown, as simpler to establish. We must then reach the conclusion that
most studies have focused on bacteria (Figure 2). Especially, compartmentalization evolved independently more frequently in
the discovery of archaeal compartments may have profound prokaryotes than in eukaryotes. Furthermore, in prokaryotes, the
implications for our understanding of cellular evolution, as genetic clustering of some of the systems into genomic islands
exemplified by recent claims that acidocalcisomes could be and the ease of lateral transfer result in frequent transfer of
present in all domains of life and may thus date back as far whole organelles between species. It is interesting to note that
as to the last universal common ancestor [159]. However, these overexpression of a foreign gene in E. coli has been observed to
are currently speculations and other interpretations for example be enough to induce the formation of massive intracellular vesicles
of eukaryotic acidocalcisomes as LROs exist [160]. [162]. Yet, as argued in [17], it remains unclear how functionless
In both prokaryotes and eukaryotes, compartments come in lipid vesicles could be co-opted to form compartments without
different flavours: they are bound either by membranes or by being purged by purifying selection.
proteins, and can be of autogenous origin or derived from an At the molecular level, an issue that has attracted much attention
endosymbiotic event. Examples for each of these classes exist in is the evolutionary relationship between genes underlying the
both domains of life (Figure 1). Yet, there are clear differences different types of compartments, particularly those seemingly
between the compartments in prokaryotes and eukaryotes. present in both prokaryotes and eukaryotes. Yet, most prokaryotic
Eukaryotes are derived from a highly compartmentalized cell, compartments have little functional and molecular data associated
frequently termed the LECA (last eukaryotic common ancestor), to them. Thus we expect that exciting findings will arise
which already possessed an elaborate ES [161]. All eukaryotes from sequencing of more genomes of compartmentalized
have more or less retained this complex compartmentalized prokaryotes, and from the cell-biological dissection of prokaryotic
cell plan. In contrast, prokaryotic membrane organelles are compartments, potentially settling some of the debates on
phylogenetically scattered and apparently evolved independently, homology. Without a better understanding of prokaryotic
although potential exceptions such as acidocalcisomes exist. Also, compartments, i.e. their diversity and molecular basis, little
they have not generally reached the same level independence progress is likely to be made in elucidating the most fascinating
from the plasma membrane compared with their eukaryotic problems of compartmentalization, complexity and ultimately the
counterparts as no definitive evidence for prokaryotic vesicular origin of eukaryotes themselves.

ACKNOWLEDGEMENTS 32 Lynch, M. (2007) The Origins of Genome Architecture, Sinauer, Sunderland, MA

33 Hettema, E. H. and Motley, A. M. (2009) How peroxisomes multiply. J. Cell Sci. 122,
J.B.P.-L. thanks Damien Devos and Bill Martin for helpful discussions. We also thank José 2331–2336
Feijó, Patrı́cia Brito, Artemy Kolchinsky and members of the Computational Genomics 34 Schluter, A., Fourcade, S., Ripp, R., Mandel, J. L., Poch, O. and Pujol, A. (2006) The
Laboratory for a critical reading of the paper. evolutionary origin of peroxisomes: an ER–peroxisome connection. Mol. Biol. Evol. 23,
838–845
35 Gabaldon, T. (2010) Peroxisome diversity and evolution. Philos. Trans. R. Soc. London
FUNDING Ser. B 365, 765–773
36 Gabaldon, T., Snel, B., van Zimmeren, F., Hemrika, W., Tabak, H. and Huynen, M. A.
Y.D. is funded by a Fundação para a Ciência e Technologia (FCT) fellowship [grant number
SFRH/BD/33860/2009]. (2006) Origin and evolution of the peroxisomal proteome. Biol. Direct 1, 8
37 Hoepfner, D., Schildknegt, D., Braakman, I., Philippsen, P. and Tabak, H. F. (2005)
Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122, 85–95
38 Martin, W. (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes.
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Received 12 June 2012/10 September 2012; accepted 17 September 2012

Published on the Internet 14 December 2012, doi:10.1042/BJ20120957


Evolution of Intracellular Compartmentalization

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Biochem. J. (2013) 449, 319–331 (Printed in Great Britain) doi:10.

Not surprisingly, comparative genomics has its own limitations.

The autogenous versus exogenous debate: peroxisomes

Figure 2 Ultrastructure of selected prokaryotic compartments

ACKNOWLEDGEMENTS 32 Lynch, M. (2007) The Origins of Genome Architecture, Sinauer, Sunderland, MA

Received 12 June 2012/10 September 2012; accepted 17 September 2012

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