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Feature

The mysteries of the diatoms

Understanding the physiology of these unique and spectacularly successful The first two genome sequences
algal species could lead to substantial benefits in a wide range of areas from showed that, in their relatively short
nanotechnology to climate change. Michael Gross reports. evolutionary history, diatom species
have grown apart much more than
Diatoms — single-celled algae Genomes growing apart comparable groups. T. pseudonana
typically enshrined in a cell wall made In recent years, complete genome and P. tricornutum, for instance, only
of intricately laced silica — have sequences of four diatom species parted company around 90 million
fascinated researchers with a whole have become available. In 2004, the years ago, but their genomes are as
range of mysteries, from their group of Virginia Armbrust at the different as human and fish, which
evolutionary origins through to their University of Washington in Seattle evolved separately for 550
morphogenesis and reproduction. reported the genome of the diatom million years.
They entered the plant kingdom Thalassiosira pseudonana, which The genomes also shed light
rather late in evolution, and through was followed by Phaeodactylum on the unusual endosymbiotic
an unusual entry. Researchers believe tricornutum, Fragilariopsis cylindrus origin and gene mixing of diatoms.
they are secondary endosymbionts, and Pseudo-nitzschia multiseries Primary endosymbiosis, the
meaning that their precursor was (Nature (2009) 459, 185–192). Of process that gave us green algae
a eukaryote that engulfed another these, Thalassiosira belongs to the and higher plants, happened
eukaryote, resulting in a quadruple group of centric (radially symmetric) around 1.5 billion years ago
membrane around the chloroplasts diatoms, while the other three are when an ancestral eukaryote
the diatom gained from this act of raphid pennates, where the defining acquired a cyanobacterium, which
piracy. ‘raphe’ is a slit along the bottom that became the ancestor of today’s
The evolutionary success story enables motility on surfaces. chloroplasts.
of diatoms only begins some
200 million years ago, but they
have spread around the globe and
diversified into hundreds of genera
and around 100,000 species in this
short fraction of the geological
timescale. Today, they are present
wherever there is liquid water, in
the oceans, in freshwater, and even
in soil. They have already played a
significant role in the global cycles
of carbon and nitrogen, and are
responsible for large sediments
of silica including diatomaceous
earth.
Why have diatoms been so
successful? Is it to do with their
silica wall, as research from Paul
Falkowski at Rutgers University
has suggested? Silica cell walls are
energy efficient to produce and unlike
the carbonate biominerals of other
species are not sensitive to ocean
pH. Fossil traces of diatoms’ silica
shells (frustules) can be dated back
to 185 million years ago, and their
rise seems to have been unstoppable
since then.
Alternatively, results from Christian
Wilhelm at Leipzig show that they
have a very efficient way to dissipate
excess solar energy, known as non-
photochemical quenching. Some
experts believe that may be a Diatom diversity: In a time span of less than 200 million years, diatoms have branched out
crucial factor explaining their into a multitude of species, which can be as genetically different as humans and fish. (Photo:
success. Wikimedia Commons.)
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on geochemical cycles and our

climate.

Riding the global cycles

Diatoms fix as much carbon dioxide
as all the rainforests of the world
combined, and they may very well
have been the main architects of
our current, moderately cool climate
situation. The rise of the diatoms
began in a much warmer climate than
ours, with no ice caps on the poles.
The atmospheric carbon dioxide
Morphogenesis molecules: Transformant strains of Thalassiosira pseudonana expressing concentration was much higher than
fluorescently labelled cingulins and silaffins. (Photo: Nils Kröger.) today. In the Cretaceous, around
100 million years ago, when diatoms
began to become widespread and
In secondary endosymbiosis, as soon as a nutrient limitation is developed great diversity, the carbon
by contrast, a eukaryote engulfed removed. The study also shows an dioxide level was fivefold higher
another eukaryote, namely intriguing interaction of the ‘animal- than today, and oxygen was lower.
a red alga, complete with its like’ urea cycle with other metabolic Remarkably, diatoms managed to
chloroplasts, mitochondria, and reactions enabled by the products thrive and expand during a period
its nuclear genome. The alga in of genes acquired by horizontal of extreme climate change, and they
question may also have been gene transfer from bacteria, e.g., also seem to have come through
infected by intracellular bacteria. for the biosynthesis of polyamines. the mass extinction that saw off
The descendants of this more Allen’s group also conducted the the dinosaurs without too many
complicated merger, which happened first comprehensive analysis of small problems. The opening of the Drake
only around one billion years ago, RNAs in a diatom, Thalassiosira Passage around 40 million years
include diatoms, brown macroalgae, pseudonana (PLoS ONE 6, e22870). ago, which created the continent of
and oomycetes, important plant The researchers found that the RNAi Antarctica, was particularly beneficial
pathogens. machinery of diatoms most closely for the diatoms because they began
In the diatom genomes, researchers resembles that of plants. to proliferate dramatically in the cold
found a very eclectic mixture of Diatoms, suggests Chris Bowler, turbulent waters of the Southern
genes, some resembling plants, seem to have mastered the art of Ocean.
others animals or bacteria. “One combining physiological reactions As diatoms evolved thicker and
might say diatoms are animals with from different sources to create denser cell walls and spread across
chloroplasts,” says Nicole Poulsen something new, such as the the oceans, it became more likely
from the B CUBE Centre at the polyamines generated from the urea that dead diatoms might sink to the
Technical University Dresden. Chris cycle, which enable them to build ocean floor and thus sequester their
Bowler from the Ecole Normale their silica shells, as discussed below. carbon. This became a significant
Supérieure at Paris thinks this clash Another example is the complex cause of carbon dioxide reduction at
of concepts just represents our interaction between their chloroplasts the planetary level in the next tens of
anthropocentric and simplistic world and mitochondria, both likely millions of years, until carbon dioxide
view. “While we might want to call derived from different sources during approached the level that we used to
diatoms ‘plantimals,’ these things are diatom evolution, which Bowler and have before the Industrial Revolution.
much more complex than we think,” colleagues have analysed in a recent Currently, by burning fossil fuels such
he says. review article (Journal of Experimental as petroleum that were generated
Like animals, for instance, diatoms Botany (2012) doi:10.1093/jxb/err441). in the past by diatoms and other
possess a complete urea cycle, This ability to create a mix-and-match plankton, we are undoing much of the
inherited from the heterotrophic host physiology may also be part of the carbon sequestration work that these
of the secondary endosymbiosis. explanation for their spectacular diatoms did.
The group of Chris Bowler together success. Recognition of the importance of
with Andrew Allen at the J. Craig These complexities show, says diatoms for the Earth’s carbon cycle
Venter Institute in San Diego, Bowler, “that model organisms give has led to the idea of encouraging
California, has recently used us only a very biased view of how life them to step up their current
knockdown studies of urea cycle works.” Escherichia coli, Drosophila, sequestration activities in the oceans.
enzymes to show that the cycle Arabidopsis and yeast have provided Iron is a limiting nutrient in large parts
enables diatoms to recover quickly us with deep insights into how of the oceans, so fertilisation with
after prolonged periods of nitrogen biology works in these particular iron could lead to diatom blooms
limitation (Nature (2011) 473, systems, but they don’t help us much (Curr. Biol. (2009) 19, R143–R144).
203–207). This fits in with numerous to understand the physiology of Large-scale experiments designed
observations of the diatoms’ ‘bloom diatoms. And understanding this is to test the idea indicated that the
and bust’ response, i.e. their ability becoming more and more important, expected diatom bloom duly arrived,
to outcompete all other species as diatoms have a huge influence but that only negligible parts of the
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carbon dioxide used by the diatoms

were sequestered to the sea floor.
Instead, initial studies showed most
of the carbon just entered the food
chain and was recycled back into the
atmosphere. By contrast, a new study
published in July 2012 suggests that
at least half the bloom biomass sinks
below a depth of 1,000 metres, from
which the authors conclude that a
substantial portion is likely to reach
the ocean floor (Nature (2012) 487,
313–319).
To better understand the role of
diatoms in our climate, and to find Light work: Extraordinary optical transmission through a gold C. asteromphalus diatom frus-
out whether they can help us to tule replica (Photo: Ken Sandhage).
avert climate change, says Chris
Bowler, we need to find out a lot
more about them. “We need a better the worst case scenario they could such as peptide sequencing. This
understanding of their physiology produce a positive feedback effect. problem could eventually be pinned
at the molecular level in order to For instance, says Bowler, if bigger down to the presence of a large
understand how they affect planetary diatoms go extinct and are replaced number of side-chain modifications,
level processes,” Bowler says. “For by smaller phytoplankton species, mainly consisting of phosphate
example, we need to understand these will be less efficient at carbon residues and unusual polyamines.
how they take up nutrients, and their sequestration via the biological Further research showed that the
capacity to store and metabolise iron, carbon pump, so the net effect will sequence of the silaffins as such
nitrogen, silicon and carbon, and be a further increase in atmospheric is less important for their function
we need to learn much more about carbon dioxide concentrations. than the presence and the nature of
their biogeography and the factors these polyamines, and that, under
that govern their sudden proliferation Mysteries of morphogenesis certain conditions, suitably structured
in response to episodic nutrient One of the most intriguing mysteries polyamines without any protein
upwellings, and their subsequent of the diatoms is the morphogenesis component can take over silaffin-style
demise following bloom events.” of their most conspicuous feature, the functions.
For instance, the iron storage silica cell wall. Shapes and sizes of While the silaffins and polyamines
protein ferritin is present only in a these microscopically small frustules are able to generate nanoscopic
small group of pennate diatoms vary widely. In centric diatoms they particles of silica from silicic acid
(Nature (2009) 457, 467–470), and it are radially symmetrical, while in solutions, they still don’t explain
is less obvious how other species pennate diatoms they have bilateral the genetically inherited patterns in
cope with variable concentrations of symmetry. In all cases, however, the silica shells. Only in February 2011
the metal. In a recent study, Adrian frustule consists of two halves (theca), could Kröger report the discovery
Marchetti, Virginia Armbrust and which fit together like a Petri dish and of a new class of proteins that
colleagues have investigated the its lid (hypo- and epitheca), and they appear to be crucial cornerstones
transcriptional response to increased have lace-like patterns of nanometre- in the molecular puzzle of silica
iron availability in an environmental scaled pores which are species- morphogenesis.
sample containing diatoms. They specific and thus presumably genetic. “We thought about how we could
found that hundreds of diatom genes The search for the biomolecules that search for silaffin-like proteins in the
responded quickly to the change in determine these patterns turned out genome of Thalassiosira, given that
nutrient availability, linking iron uptake to be extremely challenging. silaffin sequences are highly variable
to many other metabolic reactions In 1990, Nils Kröger started the and apparently not very important for
including photosynthesis, nitrate search for morphogenesis proteins their function,” says Kröger, who has
assimilation, the urea cycle, and in his undergraduate work with just relocated his lab from the Georgia
carbohydrate synthesis (Proc. Natl. Manfred Sumper at the University Institute of Technology in Atlanta to
Acad. Sci. USA (2012) 109, E317– of Regensburg, and found nothing. the newly set-up B CUBE Centre at
E325). This massive transcriptional He persisted in his PhD and the Technical University of Dresden.
response also helps to explain the postdoctoral work with rather more “We decided to look for silaffin-like
very rapid blooming of diatoms drastic methods, such as dissolving amino acid composition instead,
after large-scale iron fertilisation the frustules in anhydrous hydrogen in combination with relevant signal
experiments. fluoride, and eventually discovered sequences. We identified 86 silaffin-
As researchers are only beginning a group of proteins now called the like proteins and concentrated on six
to understand the complex physiology silaffins, as they have a marked affinity of these. Hybridising them with GFP
of diatoms and its interaction with to silica and promote its precipitation we could show that they are located
global geochemical cycles, it is not from solutions of silicic acid. in the girdle band, or cingulum, of
yet possible to predict how climate Initially, the silaffins resisted Thalassiosira, so we called them
change will affect diatoms — in characterisation by routine methods cingulins.”
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silver, gold, nickel) onto diatom

frustules. Selective dissolution of
the underlying silica then yielded
3D metallic replicas of the starting
frustules (Adv. Funct. Mater. (2012)
22, 2550–2559). “As one example,
we converted the frustule of the
Coscinodiscus asteromphalus diatom
into a nanocrystalline gold replica
that retained the quasi-periodic pore
structure of the frustule,” Sandhage
explains. “These gold replicas were
found to exhibit a phenomenon called
‘extraordinary optical transmission’.
That is, infrared light of a particular
wavelength could pass through
these gold replicas, even though the
wavelength of the IR light was larger
than the diameter of the pores in
the replicas. Such metallic diatom
frustule replicas could be used for
optical filtration and, when properly
Messy business: Biofouling on the hulls (and even propellers) of ships is a major economic functionalized, for the detection of
problem. (Photo: Gail Ashton, Smithsonian Environmental Research Center.)
various analytes in fluids.”
In a similar approach, the group
By contrast, the earlier silaffins are at Regensburg, and chitin, which they of Eike Brunner at Dresden has
located in the top and bottom parts suspect to play a structural role in coated diatom frustules with noble
of the frustule. In earlier preparations diatom frustules. Although the chitin metals (silver, gold, platinum) and
of silaffins, the cingulum had been left does not seem to influence silica with cadmium telluride nanoparticles.
aside as an insoluble residue. Now the deposition directly, it may act as a The researchers foresee applications
GFP-fluorescence showed that the scaffold that enables the appropriate in surface-enhanced Raman
molecules of interest were precisely in display of chitin-binding proteins or spectroscopy (SERS), scanning
this residue. Attempts to solubilise the protein complexes that carry silica- electron microscopy and catalysis
cingulins by dissolving the silica (with forming domains (ChemBioChem (Chem. Asian J. (2012), 7, 85–90).
ammonium fluoride) and digesting the (2011) 12, 1362–1366). Another aspect of diatom biology
chitin that is also part of the matrix of interest for possible applications is
revealed microscale rings that closely Applications the glue that raphid pennates, such
resemble the morphology of the girdle The silica frustules with their intricate as Amphora coffeaeformis, secrete
band where they are found (Proc. Natl. nanoscale patterns can make any through their raphe while they glide
Acad. Sci. USA (2011) 108, 3175– nanotechnologist jealous. Nature across a surface. Nicole Poulsen at
3180). Intriguingly, the protein matrix can produce such structures at Dresden is currently spending much
of the girdle band survives these ambient temperature and under of her time scraping diatom glue off
harsh procedures intact. Specifically, benign conditions, an achievement surfaces, to get sufficient material for
the rings show dark, parallel stripes that our technology cannot match proper molecular analyses. “It took
which occasionally fuse or branch yet. However, while they are waiting a long year, just to get a method to
out, a pattern that is reflected in the for the ‘recipe’ to emerge from obtain pure material,” Poulsen says,
anatomy of the girdle band in the live the fundamental research into but now she’s getting results, so
cell wall. morphogenesis, nanotechnologists watch this space.
Thus, cingulins are the first can use the natural structure as a Diatom adhesives are of interest for
biomolecules from diatoms that template, either to coat it with other two opposite reasons — some may
offer not only the catalytic activity to substances, or to replace the silica want to mimic bioadhesives like these
precipitate silica, but also the scaffold with other materials. to produce better glues that work
to arrange it in the desired form. The The group of Ken Sandhage at the under difficult conditions, for instance
researchers have also discovered Georgia Institute of Technology has under water. Others want to stop
analogous compounds in several developed methods for the reactive diatoms from sticking to things under
other diatom species and hypothesise conversion of an existing structure to water, such as ships. The problem is,
that they are generally involved in the a new chemical identity, producing Poulsen explains, that the glue left
morphogenesis of the girdle band. frustule replicas made of materials behind by a moving diatom, together
Kröger’s new colleagues at such as titanium dioxide, magnesium with other microorganisms (e.g.
Dresden, Eike Brunner and Karl- oxide, silicon, or carbon. bacteria), primes the surface, allowing
Heinz van Pée, are also studying Recently, the group developed a for the attachment of other organisms,
further structural biomolecules from wet chemical process for applying and thus leads to the formation
diatoms, including the silacidins thin, shape-hugging layers of various of a biofilm and ultimately to the
originally discovered in Sumper’s lab nanocrystalline metals (e.g. copper, attachment of larger macroorganisms
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(e.g. seaweeds, barnacles). This

coating adds significantly to the drag Q&A
of large ships and thus increases
fuel consumption. The only chemical
solution known to prevent this from Edvard and
happening is tributyl tin, which
was banned in the late 1980s on
May-Britt Moser
environmental grounds.
Jim Callow at the University of Interviewed by Nancy Bazilchuk
Birmingham is among the very small and Hege J. Tunstad
number of people investigating this
phenomenon and looking for new Edvard and May-Britt Moser are
solutions. “Our main test species is the founding directors of the
the green macroalga (seaweed) Ulva Norwegian University of Science
but we also use the unicellular diatom and Technology’s (NTNU) Centre
Navicula specifically because diatoms for the Biology of Memory and
show opposite adhesion preferences,” the Kavli Institute for Systems
Callow explains. “Ulva tends to adhere Neuroscience (KI/CBM). They grew
most strongly to hydrophilic coatings up on two small but adjacent islands
while diatoms such as Navicula off the west coast of Norway. They
adhere most strongly to hydrophobic first met in high school, but didn’t
coatings, especially those that are really get to know each other until
silicone-based. The frontiers of this their paths crossed as students at
subject lie in the development of the the University of Oslo. They found
Photo credit: Ned Alley.
next generation of marine antifouling/ out that they had similar interests
fouling-release coatings based on and decided to go into psychology
amphiphilic surface-active block together, graduating with degrees Both are members of the
copolymers coatings that are able to in Psychology from the University of Norwegian Academy of Science
resist both types of algae.” Oslo in 1990. At the same time, they and Letters and have been elected
A final application of diatoms brings found out they had an interest in to the European Molecular Biology
us back to climate change — some each other as well. Organization (EMBO). They have
species of diatoms are investigated The pair obtained their PhDs also been recognized with a wealth
with the aim of developing them for in Neurophysiology from the of scientific and research prizes
the industrial production of biofuels. University of Oslo in 1995, under over the years, including the 2011
This sounds surprising, as their most the supervision of Per Andersen. Louis-Jeantet Prize for Medicine and
conspicuous attribute is their silica They have also worked periodically the 2011 Anders Jahre’s Award for
shell, which doesn’t help with the with Richard Morris at the Centre Medical Research.
biofuel production and would have to for Neuroscience, University of
be recycled. Edinburgh from 1992–1996, and What turned you on to biology in
However, as Kröger explains, some with John O’Keefe at the University the first place?
species can survive without silicon. College of London in 1996. Both Edvard: For my part it was quite
Phaeodactylum tricornutum, for were appointed associate professors random because I was interested
instance, can switch between three at NTNU in 1996, and full professors in lots of things. I wanted to
different morphotypes in response in 1998 (E.M.) and 2000 (M.B.M.). start with nuclear physics, and
to specific environmental conditions, Their work at NTNU has focused I was interested in geology, and
and only one of the forms needs on how spatial location and spatial evolution. It was actually quite
silicon (Protist (2011) 162, 462–481). memory are computed in the brain. random. I began in chemistry,
“The idea is that if we remove Their most famous achievement to inorganic chemistry, and I thought
certain nutrients like nitrogen or date is probably the discovery in that was boring, so then I turned
silicon from the medium, the diatoms 2005 of entorhinal grid cells, which to psychology. And met May-Britt.
accumulate lipids. The challenge is points to the entorhinal cortex as We soon found out that the few
to find conditions where they do that a hub for the brain network that pages in our textbooks that were
and still grow to good yields,” Kröger enables us to find our way. In about neuroscience were the most
explains. Here, as in the geochemical conjunction with researchers at the interesting. And then we turned
role of diatoms discussed above, KI/CBM, they have also shown how to the brain. This was in the early
progress is limited by the incomplete a variety of functional cell types in 1980s.
understanding of the molecular the entorhinal microcircuit contribute
physiology of diatoms. More research to representation of self-location, What was it like to make
into these intriguing organisms is how the outputs of the circuit are the transition from studying
definitely needed. used by memory networks in the traditional psychology to studying
hippocampus, and how episodic neuroscience, as you have done?
Michael Gross is a science writer based at memories are separated from each May-Britt: There was no transition.
Oxford. He can be contacted via his web other in the early stages of the When we decided to start in
page at www.michaelgross.co.uk hippocampal memory storage. psychology, both of us had this