Download Membrane Remodeling and Organization: Elements Common to

Critical Review
Membrane Remodeling and Organization:
Elements Common to Prokaryotes and
Eukaryotes
Luz A. Vega-Cabrera
pez
Liliana Pardo-Lo
noma de Me
xico,
Instituto de Biotecnologıa, Universidad Nacional Auto
xico
Apdo. Postal 510-3, Cuernavaca, Morelos, Me
Abstract
Membrane remodeling processes in eukaryotes, such as those
involved in endocytosis and intracellular trafficking, are mediated by a large number of structural, accessory and regulatory
proteins. These processes occur in all cell types, enabling the
exchange of signals and/or nutrients with the external medium
and with neighboring cells; likewise, they are required for the
intracellular trafficking of various cargo molecules between
organelles, as well as the recycling of these structures. Recent
studies have demonstrated that some elements of the molecular machinery involved in regulating and mediating endocytosis in eukaryotic cells are also present in some bacteria, where
they participate in processes such as cell division, sporulation
and signal transduction. However, the mechanism whereby
this prokaryotic machinery carries out such functions has
barely begun to be elucidated. This review summarizes recent
information about the cytoskeletal and membrane-organizing
proteins for which bacterial homologs have been identified; given their known functions, they may be considered to be part of
an ancestral membrane organization system that first emerged
in prokaryotes and which further evolved into the more complex
C 2017 IUBMB Life,
regulatory networks operating in eukaryotes. V
69(2):55–62, 2017
Keywords: Bacillus subtilis; membrane elements; cytoskeleton; actin;
tubulin; flotillin; dynamin; arrestin
Introduction
For decades, the main characteristic used to distinguish prokaryotic from eukaryotic cells has been the presence of
membrane-bounded organelles in the later, including an endomembrane system that enables the exchange and traffic of
substrates among these structures. The eukaryotic endomembrane system is a dynamic network of membranes, whose evolutionary origin can be traced to the eubacteria ancestral
group (1). These organisms lack a cell wall, and their cell
membranes are composed of lipid esters; these lipids are
C 2017 International Union of Biochemistry and Molecular Biology
V
Volume 69, Number 2, February 2017, Pages 55–62
pez, Instituto de Biotecnologıa,
*Address correspondence to: Liliana Pardo-Lo
noma de Me
xico, Apdo. Postal 510-3, Cuernavaca,
Universidad Nacional Auto
xico. Tel: 152-777-3291-624. Fax: 152-777-3291-624.
Morelos 62250, Me
E-mail: [email protected]
Received 14 November 2016; Accepted 15 December 2016
DOI 10.1002/iub.1604
Published online 23 January 2017 in Wiley Online Library
(wileyonlinelibrary.com)
IUBMB Life
capable of bearing a load of folding and invaginations, which
are believed to have gradually specialized, eventually giving
rise to the organelles now recognized in eukaryotes (2).
De Duve and Wattiaux (1966) have proposed that the evolutionary force behind the emergence and permanence of this
endomembrane system was the energetic and metabolic
advantage offered by the intracellular digestion of substrates.
Having this tool, heterotrophic organisms do not have to
restrict their residence to sites of high nutrient availability.
Another advantage of this system is the elimination of toxic
agents that cells can perform when they internalize bacteria
and other cargoes, and degrade them in specialized organelles, such as lysosomes (3).
With the advent of this new system, all the intracellular
architecture was modified. Cytoskeletal proteins—such as
actin, tubulin and clathrin—were originally thought to have
emerged in events subsequent to the prokaryote–eukaryote
evolutionary separation. Recently, however, protein homologs
of various eukaryotic cytoskeletal elements have been found in
prokaryotes; these homologs have been associated to bacterial
processes related to membrane remodeling and cytoskeleton
organization (4,5). De Duve (3) has proposed that this finding
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could be indicative of these elements having emerged at par
with the acquisition of the internal system of membranes,
enabling the mobility of the elements that shape the network
as well as their proper functionality. Additionally, it could be
considered as an indicator of the evolutionary conservation of
proteins involved in the organization of the plasma membrane
and of its dynamics during processes such as cell division;
these transcendental functions require a complex regulation
that up until recently was thought to be absent in ancestral
organisms.
In this review, we summarize information about plasma
membrane organization systems and the cytoskeleton, whose
bacterial counterparts have been described and associated to
processes of membrane remodeling, such as cell division and
sporulation. The existence of such functional associations
prompt us to suggest that these fundamental processes might
represent an ancestral system that initially appeared in prokaryotes and was maintained in eukaryotes, where it has
evolved into a complex intracellular network for the transport
of nutrients and waste materials.
PVC Superphylum: A Special Case of
Shared Characteristics
When the division of the three domains of life arose it was
established that two kinds of cells conformed them; prokaryotic cells integrating the Bacteria and Archaea domains and
eukaryotic cells representing the domain Eukarya. The differences that were determined as distinctive of these two cells
were the existence in the later of a nucleus surrounded by an
envelope that separates the genetic material from the rest of
the cell and an endomembranous system, composed of organelles with specialized functions and an internal membrane network that connects these organelles and allowed traffic of substrates from and towards the plasma membrane. This
distinction was first challenged with the discovery of a prokaryote phylum that shared some of these eukaryotic distinctive features, the Planctomycetes (6). To date, the particular
characteristics of Planctomycetes have been demonstrated to
exist in other bacterial phyla (7), allowing the emergence of
the PVC (from Planctomycetes, Verrucomicrobiae and Chlamydiae) superphylum, that includes the Planctomycetes, Verrucomicrobiae, Chlamydiae, Poribacteria, Lentisphaerae and
the OP3 candidate phyla (8).
These organisms share a set of special features that differentiate them from the whole set of known bacteria and make
them more similar to archaea or eukaryotes (reviewed in
(8,9)): its internal membrane is invaginated, conforming the
intracytoplasmic membrane (ICM) that separates the cell in
different compartments, the paryphoplasm and the riboplasm,
which contains the ribosomes and nucleoid. Members of the
genus Gemmata sp. have nuclear organization and condensation similar to histones (10). Referent to the membrane organization, they are the only bacteria that contain homologs of
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membrane coat proteins (11) and structures that could be catalogued as specialized organelles, as is the case of the ammonium metabolism organelle, anammoxosome (12). The lipids
present in their membranes are typical of eukaryotes and they
can synthesize sterols (13), important regulators of membrane
fluidity that can be involved in the ICM invaginations (8). The
PVC members divide by budding independent of FtsZ, an
important cell division protein among bacteria, and its cell
wall lack peptidoglycan; instead it is composed mainly of proteins (14). However, FtsZ homologs, tubulin homologs or both,
can be found in their genomes (15). Finally, members of the
genus Gemmata sp. are able to internalize totally folded proteins in an energy-dependent and receptor-mediated process
(16), similar to endocytosis, previously thought to be specific of
eukaryotic cells.
The discovery of the PVC superphylum has open a controversial discussion about the cell complexity emergence, and
even has allowed the occurrence of a new proposal, the cauldron hypothesis, which suggest continuity between the three
domains of life (9). However, PVC features are singular; they
are not distributed among all bacteria. Instead, most bacterial
membranes contain only some homolog elements that are
shared with eukaryotes and give them common organizational
and functional similarities.
Organization of the Plasma Membrane
Biological membranes are composed of lipids and proteins
organized into microdomains —structures that generate a heterogeneous distribution of these components-, which is essential for their functionality. In the case of eukaryotic membranes, specialized proteins may be arranged into structures
called membrane rafts or lipid rafts, which are enriched in
special lipids, such as cholesterol, and are important for the
functionality of several cellular processes (reviewed in ref. 17).
The organization of these lipid rafts has been considered to be
a distinctive element in the evolution of cellular complexity,
and as such, an exclusively eukaryotic element. However,
functional membrane microdomains (FMMs) have been recently discovered in bacteria, along with bacterial lipid rafts where
specific proteins are arranged, such as those involved in signal
transduction and secretory processes (18). The presence of
these structures in bacteria points to the existence of complex
prokaryotic membrane organization systems.
While eukaryotic lipid rafts are characterized by the presence of cholesterol and sphingolipids (17), the formation of
these structures in bacteria depends on the aggregation of
poly-isoprenoid lipids with a structure similar to that of cholesterol and whose presence is related to membrane fluidity (19)
(further information is reviewed in refs. 18,20). In addition,
bacterial membranes contain noncyclic poly-isoprenoid lipids,
such as carotenoids, which regulate membrane rigidity (21)
and are important constituents of FMMs (22).
Cardiolipin is a diphosphatidylglycerol-like lipid found in
the internal membrane of mitochondria. In bacteria,
Conserved Elements in Membrane Organization
cardiolipin is necessary for the control of membrane fluidity
under stress conditions, and it is found in membrane domains,
mainly in the cell poles and the septum region, both in Escherichia coli and Bacillus subtilis (23,24). It has been proposed
that cardiolipin is a constituent element of FMMs, and that it
partakes in the recruitment of proteins that require to be
localized in these structures for their proper functionality
(18,22,24). The localization pattern of this lipid was found to
be related to cell division and differentiation processes (24).
In addition to their differential lipid composition, membrane rafts are enriched with specific proteins, such as flotillins, whose role is to recruit additional proteins to the rafts to
facilitate their interactions and oligomerization (25,26). In
eukaryotes, flotillins are involved in plasma membrane organization, cytoskeletal rearrangements, signal transduction, endocytosis and chromosome segregation during mitosis (information reviewed in refs. 27,28).
Flotillins are elements conserved among vertebrates and
invertebrates, and they are ubiquitous. They belong to a family
of proteins that contain a conserved SPFH (Stomatin, Prohibitin, Flotillin, HlfK/C) N-terminal domain and a C-terminal
domain required for their oligomerization (29). Flotillin homologs have been identified in B. subtilis (Fig. 1A), namely FloA
and FloT; they are localized in FMMs (30) and have been related to the recruitment of integral membrane proteins (31), the
localization and functionality of certain transport proteins
(31,32) and the formation of structures that promote membrane fusion and invagination during cell division and sporulation (30,33). It has been demonstrated that B. subtilis flotillins
can be clustered into domains in eukaryotic cells, even in the
absence of any other bacterial elements (32), suggesting their
function is evolutionarily conserved. Similarities and special
characteristic of eukaryotic and prokaryotic flotillins are summarized in Table 1.
The absence of flotillins in B. subtilis leads to alterations
of diverse processes; for example, it causes decreased sporulation and genetic competence, it alters membrane integrity and
cell motility (32), and septum formation does not occur in an
efficient fashion (30). In general, the involvement of flotillins in
all these cellular processes is related to their ability to organize the plasma membrane and to recruit the specific proteins
involved in these processes into membrane domains. It is conceivable that all bacteria might contain FMMs, since at least
one copy of a flotillin gene has been identified in all fully
sequenced bacterial genomes. While the mechanism of action
of bacterial flotillins has been characterized in Gram-positive
bacteria, it remains to be fully elucidated in Gram-negative
bacteria (48). The presence of FMMs in bacteria, along with
their specific lipid and protein composition, indicate their evolutionary conservation, presumably due to the functional
importance that their existence implies.
Additional to flotillins, small GTPases constitute essential
signaling membrane elements that are conserved between
eukaryotes and prokaryotes. Similarities and particular characteristics are mentioned in Table 1. In eukaryotic cells, Ras
Vega-Cabrera and Pardo-Lopez
superfamily of small GTPases are ubiquitous proteins, divided
in five families according to their sequences and functionality:
Ras, Rab, Rho, Arf and Ran, that regulate vesicular transport,
signaling, nucleocytoplasmic transport, actin dynamics, cell
motility and polarity (34). In prokaryotes the MglA and Rup
families of small GTPases have been identified through a phylogenomic analysis (35); they are involved in development (49),
antibiotic resistance (50) and regulation of cell polarity (51);
however, the majority of the members of these families have
not been experimentally characterized. Both, eukaryotic and
prokaryotic small GTPases act as molecular switches that contain a single G domain that cycles between the GDP-bound, or
inactive form and the GTP-bound, or active form. They share
structural common motifs and its active form interacts with
downstream effectors to trigger the specific cell responses
(34,35).
Previously, the existence of small GTPases was considered
to be exclusive to eukaryotes, nevertheless, the discovery of
homologs in prokaryotes suggests that they might have an evolutionary origin, reflected in the conserved structure and functionality, and an ancestry relationship has been suggested
(52). This would have important evolutionary implications,
since these proteins are involved in the eukaryotic compartmentalization and transport, then their emergence would be
related to the arose of these eukaryotic features (52).
Cytoskeleton Elements
Cytoskeleton elements in eukaryotic cells are essential for the
regulation of cell shape, motility, cell division, intracellular
trafficking and phagocytosis, among other cellular processes.
During several years these elements were believed to have
eukaryotic origins; however, the existence of bacterial protein
complexes that resemble the organization of the eukaryotic
cytoskeleton has been recently demonstrated. The most important examples are MreB, the protein homolog of actin, and
FtsZ, the homolog of tubulin, which are involved in maintenance of cell shape and cell division, respectively. Table 1
resumes similarities and special characteristic of both, eukaryotic and prokaryotic actin and tubulin.
Actin is one of the most abundant proteins in eukaryotic
cells; it consists of globular monomers that assemble into actin
filaments through an ATP-dependent process. The organization of these filaments within the cell is the main determinant
of the cell’s shape. Actin polymerization is a very dynamic process that has been widely studied in eukaryotes (37,53); it is
involved in several cellular functions, including intracellular
trafficking, endocytosis and morphology maintenance. Actin
homologs among eukaryotes share high similarity both in their
structure and in their ability to polymerize into filaments
(4,54). A group of proteins with a relatively low sequence similarity to actin has been described in bacteria; it is called the
MreB protein family, or bacterial actins. These proteins share
conserved amino acid motifs clustered around an ATP binding
site, which is an essential feature in the structure of all actins
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FIG 1
Ribbon structure comparisons of eukaryotic cytoskeleton elements and proteins related to membrane organization with their
prokaryotic homologs. Sequence similarity values between the eukaryotic protein and its prokaryotic counterpart are low; however, their tridimensional structure is very similar and it is related to an evolutionarily conserved function. (A): SPFH domain of
the flotillin family of proteins (PDB number D1WINA). For the FloT protein, we obtained a threading model using the Phyre2
commercial software (47). (B): Monomeric actin (PDB numbers 2HF3 and 1JCF). (C) a-b tubulin (PDB numbers 1JFF and 1FSZ).
(D): Dynamin (PDB numbers 3W6N and C2J69D). (E): N domain of the arrestin family of proteins (PDB numbers 4GEJ and
5CL2).
(4,54,55). Bacterial actins also contain additional domains
according to their unique specialized functions (56); for example, the Hsp70 chaperone contains a peptide-binding pocket
required for it to proofread the structure of proteins (56). FtsA
is another member of this family; its structure is more similar
to that of eukaryotic actin and it has additional domains that
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allow it to bind to the cell membrane (57), to interact with
FtsZ (58) and to participate in cell division (36). Finally, this
protein family also includes two cell shape determinants,
namely MreB and Mbl (55).
MreB and Mbl are the bacterial proteins that exhibit the
highest degree of similarity with eukaryotic actin, both
Conserved Elements in Membrane Organization
TABLE 1
Similarities and special characteristic of the eukaryotic and prokaryotic membrane organization homologs
Protein or
protein family
Similarities
Eukaryotic special
characteristics
Prokaryotic special
characteristics
Flotillin
Conformation of lipid rafts
allowing functional membrane
domain organization and signaling; SPFH domain (22,31)
Involvement in endocytosis and
vesicle sorting and trafficking;
participation in signal transduction pathways through
receptor tyrosine kinases (27)
Participation in sporulationrelated processes, biofilm formation, competence and cell
division (30,32)
Small GTPases
Contain a single G domain,
capacity to bind GDP/GTP to
activate signal transduction
pathways; GTP hydrolysis;
participation in the regulation of cell polarity (34,35)
Participation in nucleocytoplasmic transport and vesicle
transport; members of the
eukaryotic Ras superfamily
are post-translationally modified by lipids, to allow membrane binding (34)
Involvement in antibiotic resistance, participation in signal
transduction in two component systems (35)
Actin/MreB
Capacity to polymerize and act
as cell shape determinants;
interaction with cell membrane and other cytoskeleton elements; ATP binding
(36)
Polar organization of the actin
filaments, which allows spatial organization of the cell;
association with motor proteins; participation in cytokinesis, phagocytosis and motility
(37)
Bacterial actins contain additional domains that specify
their functions, such as chaperones or cell division elements; association with PBPs
to direct cell shape determination and elongation (38–40)
Tubulin/FtsZ
Involved in cell division; capacity to polymerize; interaction
with other cell division and
cytoskeleton proteins; GTPase
activity (36)
Association with motor proteins; conformation of the
mitotic spindle during chromosome segregation; conformation of flagella and
cilia; positioning of the cellular organelles (41)
Conformation of the Z ring during cell division and sporulation; recruitment of other
elements of the divisome;
association with PBPs to
define cellular location of the
cell wall (39,40)
Dynamin/DynA
GTPase activity; capacity to
oligomerize; participation in
membrane fusion and membrane remodeling processes
(42,43)
Helicase activity during scission
of membranes in endocytosis; participation in cytokinesis and organelles division
(42)
Capacity to fuse membranes in
vitro in a process independent
of GTP, dependent of Mg12
(43); it is located to the division
site and it has been related to
cell division possibly through
interaction with flotillins (33)
Arrestin/Spo0M
Tertiary structure conservation
of the N domain, involved in
receptor specificity (44,45)
Ability to interact with a wide
variety of receptors and act as
molecular adaptors in signaling; presence of a C domain
that allows oligomerization
and endocytosis-related proteins interaction (44)
Regulation of sporulation (45);
C terminal domain of Spo0M
has structural homology
with a human proteasome
inhibitor protein, the functional implication of this
finding is unknown (46)
structurally and functionally (59) (Fig. 1B), and just as their
eukaryotic homolog, they are involved in cell shape maintenance (55,60). B. subtilis mreB null mutants are not viable,
while an inducible mreB null mutant exhibits diminished
growth rate, an altered morphology (cells have a rounded
shape), and is susceptible to lysis (55). Mbl is not essential for
B. subtilis; mbl null mutants exhibit cell shape defects, for
Vega-Cabrera and Pardo-Lopez
example, bacilli are bent at irregular angles, are wider than
the wild type and have membrane protuberances (60).
Homologs of MreB and Mbl exist in diverse bacterial and
archaeal genera; however, these proteins are not present in
coccoid bacteria. Apparently, cells acquire a spherical shape
by default, while more complex shape phenotypes require an
MreB-like system to properly organize cell morphology (61).
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It has been suggested that the distinct architecture of
MreB and Mbl filaments is related to their unique functions in
different aspects of cell morphology. On one hand, MreB
appears to control cell width, forming short structures that
localize in the middle of the cell, almost perpendicular to its
longitudinal axis, thus regulating the cell’s diameter. On the
other hand, Mbl maintains orientation and shape in the longitudinal axis of the cell, forming longer structures that extend
from one cell pole to the other (55,60).
Rather than acting as a scaffold, MreB and Mbl probably
work in conjunction with the cell wall synthesis machinery.
The cell wall is a complex bacterial structure that maintains
cell shape and its main constituent is peptidoglycan. Peptidoglycan is a macromolecular complex synthesized by Penicillin
Binding Proteins (PBPs) that function as glycosyl-transferases
and transpeptidases, synthesizing and linking glycan and peptide chains (62). It has been proposed that MreB filaments
direct peptidoglycan synthesis, and that together, these structures regulate cell shape (54,55).
Another function that could be attributed to MreB is the
organization of high-fluidity membrane domains (54) that promote the activity of certain proteins by reducing membrane
viscosity and by stimulating their catalytic activity and/or their
diffusion (54). In eukaryotes, actin participates in the maintenance of lipid rafts (63,64) and by doing so, in the localization
and diffusion of integral membrane proteins (65). It is thus
conceivable that the ability that MreB and actin have to induce
and organize membrane domains could have a common evolutionary origin. Further details on the functional diversity of
bacterial homologs of actin have been reviewed elsewhere
(38,39,61). Thereby, bacterial cells contain structures with at
least one function that is conserved in the eukaryotic actin
cytoskeleton: cell shape maintenance. Jones et al. (2001), have
proposed that the MreB protein family and actin evolved from
a common ancestor that would have emerged before the
eukaryote–prokaryote divergence (55).
Besides actin, another important component of the eukaryotic cytoskeleton consists of microtubules. Microtubules constitute a transporting system formed by motor intracellular proteins that facilitate vesicle trafficking and dynamics in the
eukaryotic endomembrane system. Microtubules are primarily
composed of tubulin. In bacteria, FtsZ is a homolog of tubulin
that participates in the process of cell division, where it is the
main constituent of the Z ring, a structure formed in the future
site of division, and which is constrained to mediate cytokinesis (5). Just as in the case of actin, the degree of sequence
identity between tubulin and FtsZ is not high, but yet they
have a very similar protein structure and they both possess
GTPase activity (Fig. 1C), supporting that these two proteins
have a common ancestor (66).
The process of cell division in bacteria is not simple; it
requires the participation of an entire group of positive and
negative regulators for the assembly of the Z ring. The entire
molecular machinery receives the name of divisome. The positive regulatory elements stabilize the ring in the membrane
60
and avoid its depolymerization, while the negative regulatory
elements impede polymerization for ring formation and destabilize its lateral unions with the membrane. Information about
these regulatory elements of Z ring formation and stabilization
has been reviewed before (67,68). In eukaryotes, the process
of cell division is highly regulated; however, in addition to
tubulin, it requires regulatory elements that do not share
structural nor functional homology with those of bacteria.
Nonetheless, the capacity to polymerize and the GTPase activity of eukaryotic and bacterial tubulin are essential for their
function and are indicative or their evolutionary conservation.
Another bacterial protein that has a homolog in eukaryotic
cells and is found in B. subtilis, is the cell division-related protein, DynA. In eukaryotes, dynamin is a GTPase involved in
endocytosis; in this process, it assembles into a spiral around
the neck of the vesicle being internalized, thus enabling its
separation from the plasma membrane (42). DynA is a bacterial dynamin homolog that shares the GTPase activity and the
capacity to oligomerize (33) (Fig. 1D). Table 1 resumes more
common and specific characteristic of dynamin and DynA. It
has been shown that DynA can mediate membrane fusion in
vitro and that it acts at different stages during cell division
(43). DynA is localized to the septum region and colocalizes
with FtsZ, affecting Z ring formation. A bacterial dynamin and
flotillin double mutant is severely affected in cell shape and
motility, which suggests that these two proteins act together
during cell division events. It has been proposed that DynA
might facilitate membrane invagination during cell division or
couple this process with Z ring formation, while flotillin helps
in the recruitment of proteins necessary for cell division (33).
In eukaryotic cells, several processes of endocytosis require
the joint involvement of flotillin and dynamin, so that the association of these proteins in membrane remodeling processes
could be considered to have a conserved evolutionary origin.
Finally, we would like to mention the arrestin family of
proteins, one more family of eukaryotic proteins for which a
prokaryotic ancestor could be found. Arrestins are ubiquitously distributed proteins that perform a wide range of cellular
activities in eukaryotic organisms, including receptor desensitization, endocytosis, signal transduction, genetic expression
regulation, cellular reorganization, chemotaxis and apoptosis
(69). While members of this family have low sequence identity,
all of them share a highly similar tridimensional structure,
conformed of two domains, namely N and C, which are separated by a polar core that stabilizes the protein in its inactive
form (44). Arrestins interact with their ligand through their N
domain, and they dimerize through their C domain (44). The
arrestin family is divided into two categories: visual arrestins
or a-arrestins and nonvisual arrestins or b-arrestins (70,71).
It was previously believed that arrestins emerged after the
evolutionary divergence of the first eukaryotes; however it has
been reported that Spo0M, a sporulation control protein of B.
subtilis (45), contains structural moieties that resemble those
found in the N domain of eukaryotic visual arrestins (72). In a
recent study, Sonoda et al. (46) reported the crystal structure
Conserved Elements in Membrane Organization
of Spo0M, demonstrating that it is highly similar to the N
domain of known visual arrestins, such as the thioredoxin
interacting protein (TXNIP) or the arrestin domain-containing
protein 3 (ARRDC3) (Fig. 1E and Table 1). Unfortunately, there
is still a lack of experimental evidence to confirm that Spo0M
is a truthful ancestor of arrestin in prokaryotes; a shared origin is suggested by the conserved functionality associated to
the secondary structure of this family of proteins.
Conclusions
Membrane remodeling processes constitute key events in all
cells and require a high degree of spatiotemporal regulation.
Complex regulatory mechanisms for these processes are
observed in eukaryotic cells and, according to current molecular evidence, they do not appear to have arisen after the evolutionary divergence between eukaryotes and bacteria. The existence of bacterial protein homologs that participate in such
regulatory events has been demonstrated, reflecting the presence of complex regulation in bacteria that had previously
been ignored. Emerging technologies used in the analysis of
intracellular structures, such as super resolution microscopy
techniques, which are acquiring higher resolution as time goes
by, will enable a highly detailed analysis of the bacterial cytoskeleton. At the same time, this should help us to identify
additional regulatory elements of membrane dynamics that
are evolutionarily conserved in these two domains of life, erstwhile considered to be rather different.
Acknowledgements
The authors thank Shirley Ainsworth for bibliographical assistance and Ricardo Ciria for computer support. This work was
supported partially by CONACyT 176381 and DGAPA IN
204016. Luz Adriana Vega-Cabrera was supported by a CONACyT and DGAPA scholarship.
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Conserved Elements in Membrane Organization