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FEATURE ARTICLE
Membrane-Bound Compartments in Bacteria
Membrane-bound structures within gram-negative photosynthetic and
magnetotactic bacteria help overturn an old dogma about prokaryotes
Milton Saier
Once thought to be mere bags of enzymes, bacterial cells are remarkably more complex. Like eukaryotes, for example, bacteria are compartmentalized. Traditionally, living organisms were
divided into prokaryotes and eukaryotes, and the
members of the two groups were thought to differ
in very basic respects. Thus, eukaryotes were classifıed as having complex cell structures, including
cytoskeletons and intracellular membranebounded organelles, whereas prokaryotes were
believed to lack them.
Textbooks and current research sources still
cite this distinction. For example, the 2009 textbook Functional Anatomy of Prokaryotic and Eukaryotic Cells by Gerard J. Tortora, Berdell R.
Funke, and Christine L. Case states: “Prokaryotes
lack membrane-enclosed organelles, specialized
structures that carry on various activities.” Under
the heading “Prokaryote” in Wikipedia, a free
Web-based encyclopedia, the following statement appears: “The prokaryotes are a group of
organisms whose cells lack a cell nucleus (karyon) or any other membrane-bounded organelles.”
However, membrane-bounded organelles and
proteinaceous microcompartments are the subjects of two written symposia from 2013 that were
published in the Journal of Molecular Microbiol-
SUMMARY
➤ Bacteria, once thought to lack cellular compartments, contain both membrane-bounded organelles and protein-bound microcompartments.
➤ Bacterial organelles include mesosomes, calcisomes, chromatophores, and
magnetosomes, all of which probably arise by invagination of the plasma
membrane.
➤ Some bacteria, including members of the Planctomycetes, have nuclear
envelopes and specialized organelles for producing energy.
➤ Understanding the biogenesis of prokaryotic microcompartments is likely
to reveal common features and shed light on the origins of more complex
eukaryotic structures.
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Microbe—Volume 9, Number 9, 2014
ogy and Biotechnology. These two compendia
of articles by experts reveal that earlier generalizations about bacteria, indicating that they
lack subcellular compartments, are blatantly in
error.
Intracellular Membranes of Bacteria
Bacteria have intracellular and extracellular vesicular structures with well-characterized functions. The bacterial workhorse Escherichia coli
can produce extensive intracellular membranes
(ICMs), particularly when integral membrane
proteins are being produced in large quantities
(Fig. 1).
For the bacteria, these membranes serve important needs under normal physiological conditions. However, biologists fınd these membranes
useful for producing large quantities of native
membrane proteins—for example, when conducting X-ray crystallographic studies on those
proteins. Similarly when recombinant DNA
technologies are used to induce bacteria to overproduce proteins, the engineered cells tend to
form inclusion bodies, consisting primarily of
denatured or partially denatured protein in the
cell cytoplasm. Meanwhile, however, integral
membrane proteins overproduced in the ICM
usually are kept intact in their native, properly
folded states.
Some membrane proteins appear in various
forms within the cell cytoplasm. These include
cytoplasmic micelles and intracellular membrane
vesicles in addition to ICMs. Mesosomes, which
play roles in extracellular digestion, are found in
both gram-positive and gram-negative bacteria,
although they have been characterized most extensively in the former.
Mesosomes appear to arise when the plasma
membrane invaginates. Moreover, chromatophorous ICMs of photosynthetic bacteria and
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FEATURE ARTICLE
FIGURE 1
Electron micrographs of thin sections of Escherichia coli cells overproducing the b-subunit of the F-type ATPase. (A)
3 hours after initiation of overproduction at 37°. (B) 3 hours after initiation of overproduction at 25°. Reproduced
from I. Arechaga et al., 2013 (Figure 1C) with permission.
magnetosomes of magnetotactic bacteria are also
believed to have their origins in plasma membrane sites of invagination. It may be that all
bacterial ICMs have related modes of biogenesis,
but it is too early to make such a sweeping generalization with confıdence.
Chromatophores in Photosynthetic Bacteria
Photosynthetic bacteria possess intracellular pigmented membrane structures (Fig. 2) that catalyze light-driven reactions, including photophosphorylation and proton motive force (PMF)-driven
ATP synthesis. This intracellular photosynthetic
apparatus, quantitatively different in lipid and
protein composition from the cytoplasmic membranes of these organisms, assumes various morphological types, some continuous with and others discontinuous with the plasma membranes,
depending on the organism. The biogenesis of
these photosynthetic membranes is an exciting
area of research with the potential of revealing
novel mechanisms of membrane differentiation.
These membranous structures contain the light
harvesting complexes as well as the bacteriochlorophyll-containing reaction centers where light
energy begins to be converted into a PMF.
Temporal and spatial proteomic approaches
helped researchers to identify four pigmented
fractions, the reaction center-light harvesting 1
(RC-LH1) core complex, the LH2 peripheral an-
tenna, and two fractions with distinct associations of LH2 with core complexes. The ratios of
these different constituent complexes change as
the ICM develops. Changes followed under different growth conditions reveal, for example, that
oxic conditions quickly stop plasma membrane
growth sites from forming vesicular ICMs. The
mechanisms of vesiculation and its regulation are
under intensive investigation.
FIGURE 2
Transmission electron micrograph (TEM) of the ICM
in negatively stained thin sections of a fresh Rhodobacter sphaeroides cell. The asterisk indicates a
storage granule. Reproduced with permission from
P.G. Adams et al., 2011 (Figure 3A, top).
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Microbe—Volume 9, Number 9, 2014
• 369
FEATURE ARTICLE
Magnetosomes in Magnetotactic Bacteria
Magnetotactic bacteria and the chains of magnetosomes that allow these organisms to align in the
Earth’s magnetic fıeld are another hot topic of
study. Magnetosomes contain Fe3O4 (magnetite)
or, in anaerobic bacteria, Fe3S4 (greigite), often as
small cubo-octahedral crystals. Chains of these
magnetic materials grow by deposition of new
membrane-enclosed magnets at the ends of the
chains. The mechanisms of biogenesis and magnetic fıeld detection are beginning to be understood.
Magnetotaxis is well documented for animals
that use the Earth’s magnetic fıeld for navigation
purposes. These animals use magnets linked to
nerves. Examples include birds such as homing
pigeons, bees that depend on magnets to fınd
their way back to the hive after foraging, fısh
during lengthy migrations, and sea turtles, some
of which circle the globe within their lifetimes.
Some humans have an immutable sense of direction, and imposition of strong magnetic fıelds to
the brains of epileptic patients causes large increases in the frequency of seizures. Crystals of
magnetite have been identifıed in the brains of
humans and many animals using magnetic resonance imaging.
Meanwhile, each crystal within bacterial magnetosomes is surrounded by a membrane of lipids similar to those of the plasma membrane but
containing unique proteins. The magnetic crystals align in chains yielding large magnetic moments. Each chain has up to 100 magnetosomes
per bacterium (Fig. 3), and they orient in the
Earth’s magnetic fıeld, allowing the bacteria to
move sideways up and down in the water column
in response to geomagnetism. Magnetotactic
bacteria come from several diverse bacterial
groups, and magnetofossils have been characterized, suggesting that these organelles are of ancient origin.
Nuclear Envelopes and Anammoxosomes
in Planctomycetes
The Planctomycetes represent an unusual and relatively recently discovered group of organellecontaining bacteria. They have complex internal
cell structures that are just now becoming appreciated and understood. Their outermost membrane is considered to be the cytoplasmic membrane, and they have a membrane-bounded
370 •
Microbe—Volume 9, Number 9, 2014
FIGURE 3
Low-resolution magnetosome chains (left) and
high-resolution view of membrane-bounded magnetite crystals (right) in Magnetospirillum gryphiswaldense as revealed by transmission electron
microscopy. Reproduced from D.A. Bazylinki and D.
Schuler (2009) Microbe 4 124 –130 with permission.
nucleoid, analogous in some respects to the nuclei of eukaryotic cells.
Some planctomycetes also have energy-producing, mitochondrion-like organelles referred
to as anammoxosomes (anaerobic ammonium
oxidation organelles) with unusually rigid lipids
called “ladderanes” because of their inflexible ladder-like structures. These lipids probably contribute to energy conservation by creating a
membrane that is good at retaining protons, allowing anammoxosomes to generate a PMF
across their membranes via a quinone-dependent
process. The PMF thus generated can then be
used to make ATP. Since anammoxosomes are
separate membrane-enclosed compartments
with unique lipid and protein compositions, they
qualify as genuine intracellular organelles.
Acidocalcisomes and the Origins of
Intracellular Compartmentalization
Acidocalcisomes are calcium/polyphosphaterich acidic, membrane-enclosed organelles that
are found in organisms belonging to all three
domains of life (Fig. 4). Their membranes may
contain a variety of transport systems, including
aquaporins, ion-pumping ATPases, cation exchangers, and proton-pumping pyrophosphatases.
The functions of acidocalcisomes include stor-
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FEATURE ARTICLE
FIGURE 4
An acidocalcisome in an intact cell of Agrobacterium
tumefaciens. Reproduced with permission from Docampo and Moreno, 2011.
age of cations and polyphosphates, osmo-, pHand Ca2⫹-homeostasis, and energy metabolism.
They superfıcially resemble eukaryotic lysosomes
in their acidic properties and contents. They undoubtedly arose in prokaryotes and were transmitted vertically to their eukaryotic progeny.
Special Delivery: Outer Membrane
Vesicle Trafficking in Prokaryotes
Gram-negative bacteria bleb off outer membrane
vesicles (OMVs), releasing them into the external
medium. These OMVs are used for several purposes, including (1) delivery of toxins to eukaryotic cells, (2) protein and DNA transfer between
bacterial cells, (3) traffıcking of cell-cell signals,
(4) delivery of proteases and antibiotics, and (5)
removal of harmful, incorrectly folded periplasmic proteins. Some of these roles appear to be
generalized among gram-negative bacteria, while
others are restricted to specifıc bacterial species.
Many bacteria use extracellular signals to
communicate and coordinate social activities, a
process referred to as quorum sensing. Some
quorum signal molecules are hydrophobic and
not soluble in water. The opportunistic human
pathogen Pseudomonas aeruginosa packages the
signaling molecule 2-heptyl-3-hydroxy-4-quinolone (Pseudomonas quinolone signal, or PQS)
into membrane vesicles that disseminate this
molecule within a population. Removal of these
vesicles from the bacterial population halts cellcell communication and inhibits PQS-controlled
group behavior. Thus, prokaryotes possess signal
traffıcking systems with features common to
those used by higher organisms.
The extracellular matrix helps defıne the ar-
chitecture and infrastructure of bacterial biofılms
and also contributes to their resilient nature.
OMVs are a common particulate feature of the
matrix of a biofılm. The ubiquity of OMVs was
supported by observations of biofılms from natural environments outside the laboratory that established OMVs as common biofılm matrix constituents.
OMVs released by pathogenic bacteria can
transmit virulence factors to host cells. They also
provide a mechanism for removing denatured
proteins from the periplasm. The multifaceted
functions of these structures allow us to suggest
that many more functions will be discovered.
Concluding Remarks
Although once thought to lack organelles, the
near ubiquity of intracellular and extracellular
membrane-bounded and proteinaceous structures that compartmentalize prokaryotic cells is
now established. Recent research with E. coli and
other bacteria suggests that intracellular membranes (ICMs) occur among a large range of bacteria that had previously been thought to lack
such structures. Similarly, recognition that outer
membrane vesicles (OMVs) in gram-negative
bacteria serve a plethora of functions provides
novel impetus to study these structures in much
greater detail.
The recent suggestion that ICMs in E. coli,
photosynthetic bacteria, and magnetotactic bacteria may all derive from the plasma membrane
by invagination leads to the exciting possibility
that chromatophore and magnetosome biogenesis share mechanistic features with ICM formation in E. coli. This unifying consideration leads
to the proposal that studies in the prokaryotic
workhorse, E. coli, may prove to be applicable to
organellar phenomena in other prokaryotes as
well as eukaryotes.
Milton Saier is Professor of Molecular Biology at the University of
California in San Diego, La Jolla.
Suggested Reading
A comprehensive written symposium on “Prokaryotic
Membrane-bound Organelles” appeared in the Journal of Molecular Microbiology and Biotechnology,
volume 23, issues 1–2, 2013, and a second volume,
published later in 2013, focused on “Bacterial Microcompartments and Protein Machines” (J. Mol. Microbiol. 23, issues 4 –5, 2013. The articles included in
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Microbe—Volume 9, Number 9, 2014
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FEATURE ARTICLE
these volumes provide detailed information about the
multitude of organelles and microcompartments of
bacteria.
Arechaga, I. 2013. Membrane invaginations in bacteria
and mitochondria: common features and evolutionary scenarios. J. Mol. Microbiol. Biotechnol. 23:
13–23.
Fuerst, J. A., and E. Sagulenko. 2011. Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nature Rev. Microbiol.
9:403– 413.
Hsin, J., D. E. Chandler, J. Gumbart, C. B. Harrison, M.
Sener, J. Strumpfer, and K. Schulten. 2010. Self-assembly of photosynthetic membranes. Chemphyschem. 11:1154 –1159.
Lefèvre, C. T. and D. A. Bazylinski. 2013. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol. Mol. Biol. Rev. 77:497–526.
Tortora, G J., B. R. Funke, and C. L. Case. 2009. Microbiology: an introduction (10th edition). Benjamin
Cummings, San Francisco, Calif.
van Teeseling, M. C., S. Neumann, and L. van Niftrik.
2013. The anammoxosome organelle is crucial for the
energy metabolism of anaerobic ammonium oxidizing bacteria. J. Mol. Microbiol. Biotechnol. 23:104 –
117.
Schertzer, J. W., and M. Whiteley. 2013. Bacterial outer
membrane vesicles in traffıcking, communication and
the host-pathogen interaction. J. Mol. Microbiol. Biotechnol. 23:118 –130.
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