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Diatom cell division in an environmental context
Chris Bowler1, Alessandra De Martino2,5 and Angela Falciatore3,4
Studies of cell division in organisms derived from secondary
endosymbiosis such as diatoms have revealed that the
mechanisms are far from those found in more conventional
model eukaryotes. An atypical acentriolar microtubleorganizing centre, centripetal cytokinesis combined with
centrifugal cell wall neosynthesis, and the role of sex in relation
to cell size restoration make diatoms an exciting system to reinvestigate the evolution, differentiation and regulation of cell
division. Such studies are further justified considering the
ecological relevance of these microalgae in contemporary
oceans and the need to understand the mechanisms
controlling their growth and distribution in an environmental
context. Recent work derived from genome-wide analyses on
representative model diatoms reveals that the cell cycle is finely
tuned to inputs derived from both endogenous and
environmental signals.
Addresses
1
Environmental and Evolutionary Genomics Section, Institut de Biologie
de l’Ecole Normale Supérieure, Centre National de la Recherche
Scientifique UMR8197 INSERM U1024, F-75005 Paris, France
2
Algenics, Pole Bio ouest, F-44800 St Herblain, France
3
Laboratoire de Génomique des Microorganismes, Université Pierre et
Marie Curie, Centre National de la Recherche Scientifique FRE3214,
F-75006 Paris, France
4
Laboratory of Ecology and Evolution of Plankton, Stazione Zoologica
Anton Dohrn, Villa Comunale, I-80121 Naples, Italy
5
Algenics S.A.S. Pole Bio Ouest, rue du moulin de la rousselière, 44800
Saint Herblain, France.
Corresponding author: Bowler, Chris ([email protected])
Current Opinion in Plant Biology 2010, 13:623–630
This review comes from a themed issue on
Cell biology
Edited by Christian Luschnig and Claire Grierson
Available online 20th October 2010
1369-5266/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2010.09.014
Introduction
Our understanding of the mechanisms regulating cell
division in eukaryotes has progressed enormously in
recent decades, thanks largely to highly focused studies
in powerful model systems such as yeast, mammalian
cells, and Arabidopsis. Notwithstanding, diatoms were
one of the most advanced models of cell division in the
late 19th century, as witnessed by the remarkable works
of Robert Lauterborn. Although extended up to more
recent times by the likes of Hans Cande and Jeremy
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Pickett-Heaps (for an in-depth review see [1]), the
subject has never attained mainstream status. Furthermore, many of the studies were performed before whole
genome sequences and tools for genetic manipulation
became available for diatoms.
Our view of cell division in eukaryotes has thus become
somewhat distorted because the organisms most intensively studied represent only two subgroups within the
extensive eukaryotic crown groups [2]. It is therefore
unclear how universal the described mechanisms of cell
division will be throughout other eukaryotic groups.
Diatoms, for example, are part of the stramenopile group
that assembles brown algae with other chromist algae and
oomycetes. They are believed to be derived from serial
secondary endosymbiotic events occurring at least 700
million years ago that brought together three partners; a
red alga, a green alga, and a eukaryotic heterotroph [3].
Additionally, their genomes testify to the pervasive acquisition of bacterial genes over evolutionarily significant
time scales by horizontal gene transfer [4]. It is therefore
highly likely that they have evolved unorthodox mechanisms to control their proliferation.
The most characteristic feature of diatoms is their cell
wall or exoskeleton (known as frustule), built of amorphous silica, and typically displaying astounding speciesspecific nanometre-scale complexity [5]. The frustule is
composed of two valves with the smaller fitting into the
larger like the base and lid of a Petri dish (Figure 1).
During mitosis new valves are synthesized inside the
existing valves, which results in one of the two daughter
cells decreasing in size. Once the cells have reached a
critical size threshold they typically then require a round
of sexual activity in order to return to their maximal size
([6] and Figure 1). Furthermore, the silicified cell wall is
constructed intracellularly within a specialized vesicle
known as the Silica Deposition Vesicle (SDV) that
extends over one half of a dividing cell before being
extruded out of the cell in one of the most remarkable
examples of exocytosis known [7].
Studies of the molecular components controlling diatom
cell division have now been boosted by the availability of
two complete genome sequences from the major diatom
groups; centrics (represented by Thalassiosira pseudonana)
and pennates (represented by Phaeodactylum tricornutum)
[4,8]. Tools for gene manipulation have also been developed, most notably for P. tricornutum, and include
methods for protein overexpression, fluorescent protein
fusions, and gene knockdown [9,10]. In addition to understanding the novel aspects of cell division, these
Current Opinion in Plant Biology 2010, 13:623–630
624 Cell biology
Figure 1
Overview of the diatom cell cycle. Diatoms divide principally asexually, through mitosis (a–g). The process includes several unique features [1], as
highlighted in the figure. Diatom cells are confined within a rigid glass house consisting of two silicified valves organized with the smaller fitting into the
larger like the base (hypovalve (hyp)) and the lid (epivalve (ep)) of a Petri dish. The neosynthesis of one valve is always the smaller one (hyp) which
results in one of the two daughter cells decreasing in size (g–a). Once a critical size is reached, the sexual cycle is induced to restore the maximal cell
size (h). Chloroplast segregation (b) precedes karyokinesis (e) and cytokinesis (f). One chloroplast segregates in two, positioned on each side of the
future plane of division. Mitosis is open, with partial nuclear envelope breakdown (NEBD), and involves a unique MTOC (Microtubule Organizing
Centre) consisting of the Microtubule Centre (MC) in interphase cells and the Polar Complex (PC) in pre-mitotic and mitotic cells (a, c, d, f, g). At
cytokinesis, cells divide into two by centripetal invagination of the plasma membrane, which also involves the MC (f). A new hypovalve is generated by
the polarized formation of a Silica Deposition Vesicle (SDV) (f) which extends centrifugally before being exocytosed. Analyses performed on a few
species have indicated the presence of two checkpoints, in G1 and G2, dependent on light and nutrient availability. Progression through G2 appears to
require silicate for those species requiring it. The electron micrographs represent transverse sections of P. tricornurtum cells at different stages of cell
division. (a) Interphase cell with one nucleus (n), one chloroplast (ch) with one pyrenoid (py), mitochondria (m), epivalve (ep), and hypovalve (hyp); (b)
cell with two daughter chloroplasts; (e) cells after karyokinesis; (g) daughter cells. Fluorescent images represent confocal images of P. tricornutum cells
in interphase (a), with divided chloroplasts (b), and with two nuclei (e). Red: chlorophyll autofluorescence; green: nuclei with histone H4-GFP
fluorescence. Scale bars are 1 mm in electron micrographs and 2 mm in the fluorescent images.
resources can also be used to investigate the environmental constraints on cell division. This is all the more
important considering current interest in culturing diatoms for biofuel production [11], as well as the ecological
and biogeochemical importance of diatoms as buffers of
climate change [12]. Although data are only fragmentary, current information suggests they are responsible for
around 40% of net primary productivity in the ocean [13],
Current Opinion in Plant Biology 2010, 13:623–630
and in addition they are major contributors to the biological carbon pump, through which carbon is exported to
the ocean interior [14,15]. Here we summarize our
current knowledge of the novel aspects of diatom cell
division and highlight several promising fields of study
that could lead to major insights into understanding their
extraordinary success in highly variable environments.
Because of size constraints the principle focus of this
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Cell division in diatoms Bowler, De Martino and Falciatore 625
review is on vegetative cell division and we are unable to
cover diatom sexual cycles in any great detail. Interested
readers are therefore encouraged to read other recent
reviews that cover this subject [6,16].
[21] but there is growing evidence for the existence of
additional finely tuned internal timing mechanisms controlling their life cycles as well. Below we provide a brief
overview of the principal abiotic and biotic factors that have
been linked to cell cycle control.
Update on cell division in diatoms
The elegant studies of Lauterborn, Cande, PickettHeaps and others have revealed several unconventional
aspects that define diatom cell division (reviewed in [1]
and summarized in Figure 1). For example, the diatom
microtubule organizing centre (MTOC) is composed of
two distinct structures, the microtubule centre (MC) and
the polar complex (PC) that initiate mitosis outside the
nucleus. Following partial nuclear envelope breakdown
(NEBD), the chromosomes organize in a ring around the
mitotic spindle and do not appear to be attached via
conventional kinetochores. Plant cells, by contrast, do
not possess an MTOC and mitosis is fully open. Furthermore, in diatoms cytokinesis involves a cleavage furrow
that develops centripetally, as in animal cells, and
centrifugal cell wall neosynthesis, as in plant cells. Manual annotation of the two genome sequences has revealed
some of the putative components mediating cell division
[1], but experimental work is required to investigate the
diatom-specific aspects of the process. To date, three
approaches have been particularly rewarding: quantitative PCR (qPCR) and cDNA-AFLP to examine gene
expression in synchronized cells [17,18], and timelapse imaging of fluorescently labelled cellular structures
during cell division [1].
Following the availability of whole genome sequences,
one of the most remarkable gene family expansions in
both diatoms was found to concern cyclins, key regulators
of eukaryotic cell division [17]. In addition to the usual
complement of conserved cyclins, each diatom contains
tens of additional copies of diatom-specific cyclins. While
functions are not yet known, their expression during the
cell cycle has been examined by qPCR in synchronized P.
tricornutum cells, and several are indeed expressed at
defined times, providing a valuable basis upon which
to build knowledge of the underlying mechanisms regulating different stages of the diatom life cycle. In our
opinion, myosins represent another cellular component
worthy of investigation because diatoms again contain an
unusual gene family encoding these molecular motors
that regulate vesicle transport along the actin microfilaments [4].
Environmental constraints on cell division and
their ecological implications
Although diatoms are ubiquitous throughout contemporary oceans [19] they tend to dominate during blooms in
well-mixed coastal and upwelling regions [13] and at higher
latitudes ([20] and references therein) (Figure 2). Their
pronounced temporal patterns in occurrence is generally
attributed to proximal factors such as nutrients and light
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Since the last major radiation of diatoms (around 30
million years ago, according to available evidence
(reviewed in [12])), they have diversified into tens of
thousands of species with different shapes and sizes.
Actual genetic diversity is likely to be at least one order
of magnitude higher, if cryptic diversity is taken into
account [22]. Additional phenotypic plasticity in some
species can be provided by the ability to form chains or
colonies (Figure 3). Multiple hypotheses have been proposed to explain such behaviour, for example, defence
against grazing [23], improved nutrient uptake because of
higher diffusion rates of solutes towards the cells [21,24],
decreased sinking rates [21], or perhaps increased
encounter rates of gametes for sexual reproduction. Notwithstanding, the stimuli for inducing a colonial lifestyle
are unknown. Some diatoms aggregate at bloom termination [25], so their increased sinking rates contribute to
the transport of nutrients from the euphotic zone to the
ocean interior [14]. Aggregates have also been observed in
response to stress [26,27] (Figure 3), reinforcing the idea
that these populations of unicellular organisms can
behave collectively. Cell–cell communication, perhaps
mediated by quorum sensing-like mechanisms, has been
only poorly investigated in diatom populations, but may
be an exciting avenue for understanding synchronization
events in diatom populations (see later).
As photosynthetic organisms, the growth and distribution
of diatoms are strongly dependent on ambient light
conditions. Their ability to grow and photosynthesize
over a wide range of light wavelengths and intensities
[28] is likely due to the presence of specific light sensing
and acclimation mechanisms that are now beginning to be
deciphered at the molecular level [4,29,30]. As is typical
in marine algae, cell cycle progression requires a lightdark periodicity, with cell division occurring more frequently during the night [31], and exhibiting typically
two restriction points (in G1 and G2) requiring both
nutrients and light (Figure 1). Light has also been shown
to be a key factor triggering sexual reproduction in the
pennate diatom Haslea ostrearia [32]. Because blue-green
wavelengths (450–550 nm) are prevalent beyond the
upper few metres of the water column, blue light sensing
mechanisms are expected to play an important role in
controlling diatom growth. Consistent with this, a novel
member of the cryptochrome/photolyase family (CPF1)
showing DNA repair and blue-light dependent transcription regulatory activity has been characterized recently in
P. tricornutum [33]. Furthermore, the protein has been
found to modulate the expression of a diatom-specific
cyclin [33], suggesting a precise role during cell division,
Current Opinion in Plant Biology 2010, 13:623–630
626 Cell biology
Figure 2
A phytoplankton bloom viewed by satellite. The image shows spring blooms in the Malvinas Current area off the coast of Argentina in the South Atlantic
Ocean, based on data from the Sea-viewing Wide Field-of-view Sensor (SeaWiFS). The green-coloured blooms most likely contain diatoms, whereas
the blue-coloured blooms are probably coccolithophores. The Malvinas Current is a jet of cold water branching off the Antarctic Circumpolar Current,
which flows northward along the coast of South America until it meets the warm, south-flowing Brazil current. The convergence of the Malvinas and
Brazil currents causes temperature and salt concentrations to vary within a relatively small area, and upwellings draw nutrient-rich water from lower
layers to the surface that feeds the phytoplankton blooms. Image reproduced with kind permission from Earth Observatory, NASA.
perhaps in DNA damage checkpoint control before mitosis or in the maintenance of timing of cell division at
night. An additional class of stramenopile-specific blue
light photoreceptors, denoted aureochromes [34], has also
been found to be expanded in diatoms [35].
In addition to light, diatom life histories are also constrained by the availability of nutrients. Several in situ
enrichment experiments have shown that diatoms form
large blooms upon the relief of iron limitation [36].
Diatoms are able to sense iron bioavailability [37] and
specific retrenchment responses have been identified that
allow them to survive in iron limiting conditions. Transcriptomic and metabolomic approaches have shown that
Current Opinion in Plant Biology 2010, 13:623–630
P. tricornutum modulates its metabolism by downregulating processes that require iron [38], and a subset of
pennate diatoms also contain ferritin, an iron storage
molecule [39]. Nitrogen, together with iron, is generally
considered to be another major limiting factor of primary
production in the oceans [40]. Recently, qPCR analysis of
cyclin genes during the cell cycle in different nutrient
starvation-repletion experiments has highlighted the
importance of nitrate and phosphate as cell cycle ratelimiting nutrients in P. tricornutum [17].
Biological traits controlled by genetic diversity in individual species or ecotypes have long been credited with
generating the seasonal cycles of phytoplankton blooms
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Cell division in diatoms Bowler, De Martino and Falciatore 627
Figure 3
Morphotype transformation in P. tricornutum and how it can be leveraged to explore the influence of environmental signals on diatom life histories. P.
tricornutum has only a facultative requirement for silicon and is known to be pleiomorphic with three main morphotypes (triradiate, fusiform and
oval). A fourth morphotype, denoted ‘round’ has also been described [26]. Fusiform and triradiate cells do not have silicified cell walls, and consist of
a central body (CB) prolonged by two or three arms containing vacuoles (V). By contrast, oval cell walls can be silicified and cells are reduced to only
a central body. These four morphotypes also display different physiological properties [26,27], and depending on culture conditions the
morphotypes can inter-convert. Oval and round cells are known to increase in abundance on solid media and in stressful conditions whereas
fusiform and triradiate cells are most abundant in nutrient-replete liquid media [27]. Triradiate, fusiform and oval morphotypes are able to make
chains, whereas oval and round cells make aggregates. The round cells can also adhere on surfaces and form biofilms. Images captured by DIC light
microscopy or scanning electron microscopy. Fluorescent images are from cells overexpressing a cytosol-localized GFP fusion (red: chlorophyll
autofluorescence; green: cytosolic GFP).
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Current Opinion in Plant Biology 2010, 13:623–630
628 Cell biology
[41]. One of the most intriguing questions for marine
microbial ecologists is which factors and regulatory
mechanisms control these periodic proliferation and
termination events. Seasonal variables in light quality
and quantity, nutrient availability, mixing of different
water masses, pathogens and grazers have all been
invoked (reviewed in [12]), and in addition several
studies have revealed the role of allelopathic signals in
population control. As a case in point, toxigenic effects of
diatom-derived oxylipins have been documented on
grazers, phytoplankton and other microbes [42]. Some
of these molecules are also toxic to the diatoms themselves and can trigger programmed cell death [43].
Recent studies have shown that P. tricornutum can accurately sense a potent oxylipin, decadienal, and highlight
the existence of a stress surveillance system based on
calcium and nitric oxide that can induce immunity or
death, depending on the concentration of decadienal the
cells are exposed to. Such observations have led to novel
hypotheses about the cellular mechanisms responsible
for acclimation versus death during phytoplankton
bloom successions [44].
dissecting diatom cell division. An additional intriguing
feature of P. tricornutum is that the species is pleiomorphic, existing in three interconvertible morphotypes
(oval, fusiform and triradiate) that show differential sensitivity to stress ([26] and Figure 3). Furthermore, unlike
other diatoms it has only a facultative requirement for
silicic acid, and the oval form is the only one with a silica
frustule characteristic of diatoms. It can therefore grow in
the absence of silicon, unlike other diatoms whose growth
is completely arrested when this element is limiting.
Although unusual, this characteristic can be exploited
experimentally to understand the specific mechanisms
utilized for silica exoskeleton biosynthesis because they
are likely to be conserved in all diatoms [7]. Furthermore,
because each morphotype can generate chains or aggregates, the species can also be used to study these important phenomena that characterize diatom adaptation in
pelagic and benthic environments (Figure 3). We consider therefore that P. tricornutum can teach us a lot about
several key aspects of diatom life histories, and that
progress can be much more rapid than in other species
because of the tools that are available.
In spite of these recent findings, the role of abiotic and
biotic factors in controlling seasonal blooms remains
controversial. Additionally, the existence of endogenous
signals regulating annual growth patterns have been
hypothesized following analysis of annual patterns of
species abundance at Long Term Ecological Time Series
sites [45] and by evidence for photoperiodic control of
germination and/or growth of diatom resting spores [46].
These data support the involvement of an internal clock
that synchronizes bloom events, somewhat analogous to
the regulation in terrestrial plants of vernalisation in
overwintering species and flowering in photoperiod-sensitive species (reviewed in [12]). Additional evidence
for a strong endogenous rhythm in diatoms derives from a
recent analysis of sexual reproduction in Pseudonitzschia
multistriata in the Gulf of Naples, which has been shown
to occur with a biennial frequency [47]. Taken together
the data indicate that these populations are tuned to their
environment and that their life cycle and growth is not
merely the response to short-term variability of proximate
factors, but to internal sensing of cell size. Considering
the ecological and biogeochemical relevance of diatom
bloom events, we need to improve our understanding of
such processes. This will require the use of integrative
approaches incorporating modern oceanography and
genomics, as well as novel genetic and epigenetic
analyses on selected model species and subsequently
on phytoplankton populations in situ [12].
In spite of the power of T. pseudonana and P. tricornutum as
experimental organisms, neither of them displays size
reduction, and sex has never been observed. An alternative model that does display these features and which is
amenable to experimental manipulation (albeit not yet
genetic transformation) is Seminavis robusta [16]. Elegant
studies of synchronized cultures of S. robusta using
cDNA-AFLP have revealed genes induced at precise
stages during its life cycle and have defined a set of genes
putatively involved in sexual reproduction [18]. The
availability of a genome sequence and protocols for
genetic transformation would further reinforce the value
of this species to study these novel aspects of diatom life
cycles.
Advantages and limitations of current models
Without doubt, the availability of complete genome
sequences from T. pseudonana and P. tricornutum, together
with tools for genetic manipulation developed for both
organisms, make them powerful experimental systems for
Current Opinion in Plant Biology 2010, 13:623–630
Conclusions
Comparative and functional genomic analyses have provided the first molecular information about diatom cell
division mechanisms, and their regulation in response to
environmental conditions. Furthermore, some diatomspecific molecular markers of the cell cycle have been
pinpointed and studied in situ [48]. Our extensive knowledge of the cell cycle in other organisms, together with
the elegant studies of diatom biology in the last century,
therefore provides an excellent foundation for deepening
our knowledge of diatom life histories in the post-genomics era.
Notwithstanding, significant work remains to be done to
understand the roles of the 5000 plus diatom genes that
cannot be assigned functions in comparison to genes
found in better characterized experimental organisms.
The remarkable morphological and functional diversity
of diatoms also indicates that a handful of experimentally
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Cell division in diatoms Bowler, De Martino and Falciatore 629
tractable diatom species will be insufficient to dissect the
reasons underlying their ecological success.
8.
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D,
Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M et al.: The
genome of the diatom Thalassiosira pseudonana: ecology,
evolution, and metabolism. Science 2004, 306:79-86.
In our opinion, an improved understanding will also require
the incorporation of approaches to follow diatom proliferation events in natural environments, for example, using
metatranscriptomics to explore gene expression patterns
alongside studies of genetic and epigenetic diversity,
combined with methods adapted from modern cell biology
to follow cell signalling events by microscopy and flow
cytometry. To potentiate such studies, fluorescent dyes
have been described recently to label the SDV and silicified exoskeleton [49]. When combined with an in-depth
analysis of contextual physico-chemical parameters in
different environments, such approaches could lead to
the identification of candidate regulatory genes and processes that can then be further examined by targeted gene
knockouts in model diatoms. Although considerable technical challenges prohibit such approaches today, the
advent of improved sampling regimes, new sequencing
technologies, and in situ monitoring devices [50] make such
approaches foreseeable in coming years.
9.
Siaut M, Heijde M, Mangogna M, Montsant A, Coesel S, Allen A,
Manfredonia A, Falciatore A, Bowler C: Molecular toolbox for
studying diatom biology in Phaeodactylum tricornutum. Gene
2007, 406:23-35.
Acknowledgements
We would like to thank colleagues at the Stazione Zoologica Anton Dohrn of
Naples and in particular Maurizio Ribera d’Alcalà for critical suggestions,
Diano Sarno (Taxonomy & Identification of Marine Phytoplankton Service)
and Giovanna Benvenuto (Microscopy Service) for providing images of
diatoms isolated from the Bay of Naples. Works in the authors’ laboratories are
supported by the Agence Nationale de Recherche to CB and a Human
Frontiers Science Programme-Career Development Award (0014/2006) and
an ATIP award from the Centre Nationale de la Recherche Scientifique to
AF.
References and recommended reading
Papers of particular interest, published within the period of review,
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of special interest
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