An ecological and evolutionary context for integrated nitrogen
metabolism and related signaling pathways in marine diatoms
Andrew E Allen1,2, Assaf Vardi2 and Chris Bowler2,3
Whole-genome sequence analysis has revealed that diatoms
contain genes and pathways that are novel in photosynthetic
eukaryotes. More generally, the unique evolutionary footprint of
the chromalveolates, which includes a genome fusion between
a heterotrophic protist and a red alga in addition to a major
prokaryotic influence, has fostered their inheritance of a unique
complement of metabolic capabilities. Many aspects of
nitrogen metabolism and cell signaling appear to be linked in
diatoms. This new perspective provides a basis for
understanding the ecological dominance of diatoms in
contemporary oceans.
Addresses
1
Princeton University, Department of Geosciences, Guyot Hall,
Princeton, New Jersey 08540, USA
2
Laboratory of Diatom Signaling and Morphogenesis, CNRS FRE 2910
Ecole, Normale Supérieure, 46 rue d’Ulm, 75230 Paris, Cedex 05,
France
3
Cell Signalling Laboratory, Stazione Zoologica, Villa Comunale, Naples,
Italy
Corresponding author: Bowler, Chris ([email protected])
Current Opinion in Plant Biology 2006, 9:264–273
This review comes from a themed issue on
Physiology and metabolism
Edited by Eran Pichersky and Krishna Niyogi
1369-5266/$ – see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.03.013
Introduction
The oceans cover 70% of the Earth’s surface, contain an
extraordinary diversity of microbial life, and constitute the
largest ecosystem on our planet. Diatoms are one of the
most prominent phytoplankton groups and are of crucial
importance in marine systems from an ecological and
biogeochemical point of view. The ability of diatoms to
thrive in upwelling-induced, periodically nutrient-rich
conditions makes them the basis for the world’s shortest
and most energy-efficient food webs. Some of the world’s
largest fisheries are driven and maintained primarily by
diatom-based new production (i.e. CO2 fixation that is
fueled by upwelled NO3 ). Diatom photosynthesis is estimated to account for between 25% and 40% of the 45–50
billion tons of organic carbon fixed annually in the sea [1].
Diatoms range across three orders of magnitude in size
and are found in all marine and fresh-water open water
Current Opinion in Plant Biology 2006, 9:264–273
masses; they also exist as benthic forms and constitute a
large portion of the algae that are associated with polar sea
ice. Despite the extraordinary ecological flexibility and
dominance of diatoms, and their enormous importance in
the biogeochemical cycling of carbon (C), nitrogen (N),
phosphorus (P), silica (Si), iron (Fe), and other trace metals,
very little is known about the molecular underpinnings of
their success. Emerging techniques for diatom biology that
emphasize the functional characterization of genes and
proteins offer exciting new approaches for discovering
unique adaptations among eukaryotic photosynthetic
organisms to specific nutrient limitation in aquatic environments [2,3]. Such techniques are predicated on wellannotated molecular sequence databases. The molecular
era of diatom biology began in earnest with the analysis of
1000 expressed sequence tags (ESTs) from the pennate
diatom Phaeodactylum tricornutum [4]. Subsequently, molecular databases for marine diatoms have continued to
expand [5]. Most notably, the analysis and publication
of the complete genome sequence of the plastid, mitochondrial, and nuclear genomes of the centric marine
diatom Thalassiosira pseudonana has dramatically altered
the landscape of diatom biology research by providing
novel insights into the ecology, evolution, and behavior
of diatoms, as well as a genomics and molecular framework
for basic investigations [6]. This review emphasizes
important recent research on diatom molecular biology
and evolution, physiology, metabolism, and biogeochemistry. It attempts to integrate these findings conceptually
within the context of genes and pathways, discovered
through EST and genome-sequencing efforts, that are
novel for photosynthetic eukaryotic organisms.
Evolutionary, ecological, and biogeochemical
considerations
Approximately one-third of all marine phytoplankton
species belong to the phylum Bacillariophyta [7], which
consists exclusively of diatoms. Diatoms comprise three
of the 17 currently recognized classes of a group of
chlorophyll c-containing algae known as heterokonts
[8]. The chlorophyll c-containing algae are included in
four major lineages: heterokonts, dinoflagellates, haptophytes, and cryptophytes. All of these lineages acquired
their plastid through a secondary endosymbiotic event,
whereby a free-living eukaryotic heterotrophic protist
engulfed an existing eukaryotic alga and reduced it into
what is known as a secondary plastid. Molecular phylogenetic data support the idea of a single ancient secondary
endosymbiosis, and consequently, of a monophyletic
association among extant secondary plastid and chlorophyll c-containing algae. These data indicate that the
www.sciencedirect.com
Integrated nitrogen metabolism and related signaling pathways in marine diatoms Allen, Vardi and Bowler 265
origin of these plastids is an ancient red alga [9,10].
Collectively, all of the descendents of the red algal
secondary endosymbiosis, including some heterotrophic
organisms (e.g. heterotrophic and ciliates and oomycetes)
that have lost their plastid, are known as chromalveolates.
Plastids that have been acquired by secondary endosymbiosis are surrounded by four, and in some cases three,
membranes [11]. As a result, a unique evolutionary feature of secondary endosymbiotic algae is the utilization of
signal sequences and protein import machinery that are
capable of targeting and transporting proteins into secondary plastids. Recent studies have identified critical
targeting sequences and proteins that are involved in
trafficking and transporting proteins into complex secondary plastids [11,12].
Nitrogen and iron biogeochemistry, physiology, and
ecology
Collectively, chlorophyll c-containing secondary endosymbiotic organisms are known as chromist algae, and
taken together, they comprise around 50% of the total
number of marine phytoplankton species [7]. Nearly all
of the major bloom-forming organisms in marine waters
are chromist algae. Within marine phytoplankton, diatoms are among the best competitors for high levels of
NO3 [13]. On an evolutionary time-scale, changes in
nutrient availability that result from changes in oceanmixing regimes are thought to drive macroevolutionary
modifications in the size of marine pelagic diatoms [14].
In regions where high rates of nutrient supply are sustained, such as upwelling environments and continental
margins, diatoms often constitute a large fraction of the
photosynthetic biomass [13]. In the past decade, it has
become increasingly clear that Fe availability plays a
major role in determining the size structure and community composition of the plankton community in open
ocean and coastal upwelling regions. Diatoms, in particular, are sensitive to Fe limitation and appear to be
impaired in their ability to effectively assimilate NO3
when bioavailable Fe is scarce [15]. A synthesis of all of
the data collected from nine large-scale oceanographic
Fe-enrichment experiments conducted during the past
decade in Fe-limited waters indicates that diatoms, relative to other phytoplankton taxa, are highly responsive to
Fe availability and that Fe nutrition is crucial to the
impact of diatoms on the biogeochemistry of macronutrients such as C, N, P, and Si [16].
Details concerning the mechanism and kinetics of Fe
reduction in marine diatoms and the possible involvement of superoxide anions in such a mechanism are
becoming clear [17]. Evidence from experiments utilizing
transgenic diatoms that express the calcium-sensitive
photoprotein aequorin indicates that responses to Fe
availability, depending on the degree of Fe starvation,
are mediated by calcium-dependent processes [18]. The
importance of the trace metals manganese (Mn) and
www.sciencedirect.com
especially copper (Cu) for the nutrition of Fe-deficient
diatoms has been documented recently [19,20,21]. Interestingly, relative to green algae, chromist algae have low
cellular quotas for Fe and Mn, and this is thought to
reflect an adaptation of the photosynthetic apparatus to
the scarcity of such metals, which is due to the strong
oxidizing conditions that have persisted in ocean surface
waters for the past 250 million years [22].
Nitrogen utilization, physiology, and ecology
NO3 uptake in marine ecosystems is of particular importance in oceanography and biogeochemistry because it
sets an upper limit to biomass yield at higher trophic
levels [1]. Furthermore, it supports new production that,
over large geographic and temporal scales, must equal
export from the system, ignoring N2 fixation and other N
inputs [1]. As a result, an important research focus is the
physiological and molecular basis for N sensing, N status,
and N metabolism in marine diatoms. In marine systems,
phytoplankton that dwell at deeper depths, characterized
by low light availability and excess nutrients, are often
mixed into highly illuminated, relatively nutrient-poor,
surface waters. Such physically forced mixing events
often trigger tremendous increases in phytoplankton biomass. The physiological acclimation associated with this
rapid change in ecological conditions and ensuing productivity has been termed a ‘shift-up’ in phytoplankton
metabolism [23]. Competition among phytoplankton for
resources deriving from fluctuations in nutrient stoichiometry and light-level has a major impact on community
species composition and ecological succession
[24,25,26]. Experiments in which the nutrient status
of phytoplankton communities is manipulated in situ or
in pure cultures of marine diatoms have indicated that
nitrate reductase (NR) and urease (UA) activity are often
reliable physiological markers characterizing a shift-up
response to specific N substrates [23,27].
Nitrogen-responsive molecular markers
A variety of recent studies have focused on the development of molecular tools to characterize functionally and to
assay the diversity and expression of genes that are
putatively of central importance to inorganic N transport
and assimilation. Diatom-specific motifs have been identified and used to detect and examine the diversity of
assimilatory NR genes in natural assemblages of phytoplankton [28]. Conversely, glutamine synthetase II
(glnII) in the centric diatom Skeletonema costatum has been
shown to be a reliable genetic marker for NH4+ assimilation that occurs as a specific result of assimilatory NO3
[29]. In another study utilizing the pennate diatom Cylindrotheca fusiformis, a construct consisting of the NR promoter fused to green fluorescent protein (GFP) was
employed to evaluate NR transcriptional activation in
response to different N sources and levels. Interestingly,
NR is strongly transcribed in the absence of fixed N but
the NR mRNA is not translated into protein; the
Current Opinion in Plant Biology 2006, 9:264–273
266 Physiology and metabolism
inhibition of translation is released by the addition of
NO3 [30]. Several C. fusiformis NH4+ transporters have
been cloned and functionally characterized through complementation of a Saccharomyces cerevisiae strain that lacks
all three native yeast ammonium transporters. Surprisingly, diatom NH4+ transporters (AMT) that are nearly
identical at the DNA-sequence level are not functionally
equivalent. The data suggest that although the primary
role of particular AMT genes is certainly NH4+ transport,
the principal function of other AMT gene products could
be related to NH4+ sensing and signaling through protein–protein interactions [31,32].
Evolutionary ecology of N metabolism
The full complement of genes found within the diatom
lineage that are relevant for primary N metabolism has
not been clarified. It has been noted that the diatom
genomes are highly chimeric and contain major infusions
from multiple lineages [6,33]. Like all photosynthetic
eukaryotes, diatoms contain typical plant-like copies of an
NAD(P)H NR [28] and a plastid-targeted ferredoxinNR. The T. pseudonana and P. tricornutum genomes also
contain a variety of well-conserved genes that are apparently of bacterial origin (e.g. prismane and carbamate
kinase) (Table 1, Figure 1). These genes have wellcharacterized homologs in bacteria and some other protists but have not previously been detected in photosynthetic eukaryotes of any kind. There are several fairly
recent well-documented reports of intracellular symbiotic
cyanobacteria and bacteria living intracellularly within
several species of diatoms [34]. Evidence for lateral gene
transfer (LGT) between prokaryotes and unicellular
eukaryotes has been documented [35], and considering
the close ecological and symbiotic associations between
diatoms and bacteria in aquatic environments, it is not
surprising to find evidence for such LGT events between
prokaryotic organisms and diatoms. In terms of N metabolism, it is interesting to consider pathways that are
present in diatoms and other lineages that are composed
almost exclusively of heterotrophic organisms and do not
include photosynthetic eukaryotes. Another example of a
gene that is involved in such a pathway is agmatinase,
which catalyzes the conversion of agmatine to putrescine
or carbamoyl putrescine and is involved in polyamine
synthesis and secondary metabolite production [36]. In a
recent comparative genomics study, agmatinase was
shown to be present in P. tricornutum but absent from
T. pseudonana and representative green and red algal
genomes [37]. Polyamine synthesis and metabolism
[38] are of particular importance in diatoms because
polyamines represent the primary organic constituent
of diatom biosilica and silaffins, which are the diatom
peptides responsible for silica-precipitation. These peptides have highly specific and synergistic interactions with
polyamine chains [39,40,41].
Alternative electron cycling, energy balance,
and stress management
Non-photochemical quenching and NO3S reduction
Shifts in light intensity and quality, temperature, and
nutrient availability are extremely common in marine
waters and frequently provoke imbalances between light
assimilation and growth. Rapid fluctuations in environmental conditions promote the demand among phytoplankton for effective alternative electron-cycling
pathways [42]. Defining these pathways in diatoms is
an important research challenge. Recently, it was
reported that, compared to the green alga Chlorella vulgaris, the diatom P. tricornutum is capable of a much higher
conversion efficiency of photosynthetic energy to biomass
in a fluctuating light regime [43]. It is well known that
diatoms employ a variety of strategies for excess energy
dissipation, primarily in response to light stress, including
non-photochemical quenching (NPQ) mechanisms,
which operate via the xanthophyll cycle and cyclic electron flow around photosystem II [44,45]. In high-light
cool-water environments, where carbon uptake and metabolism are limited by temperature, phytoplankton are likely
to resort to alternative electron-cycling strategies to
buffer electrons derived from the light reactions that
are in excess of what are required for balanced growth
and metabolism. There is a compelling case for the idea
that NO3 can serve as a terminal electron sink, via NR,
to preserve overall cellular energy balance [46].
NAD(P)H NR and prismane (Table 1, Figure 1) occur
on the same operon in bacteria. In bacteria, prismane
functions as a hydroxylamine reductase protein [47].
Together, these bacterial-like copies of nitrite and
Table 1
Well-conserved diatom genes involved in nitrogen metabolism that are of probable bacterial origin and are missing in photosynthetic
eukaryotes.
Name
Function
EC
Predicted targeting
Tp
Pt
Prismane
NAD(P)H nitrite reductase
Carbamate kinase
Glutamine synthetase III
Agmatinase
Hydroxylamine or NO reduction
NO2 reduction
Carbamoyl phosphate synthesis
Ammonium assimilation
Polyamine synthesis and secondary metabolites
1.7.99.1
1.7.1.4
2.7.2.2
6.3.1.2
3.5.3.11
Mitochondria
Unknown
Mitochondria
Mitochondria
Mitochondria
Y
Y
Y
Y
N
Y
Y
Y
Y
Y
Y (Yes, present), N (No, not present) in T. pseudonana (Tp) or P. tricornutum (Pt).
Current Opinion in Plant Biology 2006, 9:264–273
www.sciencedirect.com
Integrated nitrogen metabolism and related signaling pathways in marine diatoms Allen, Vardi and Bowler 267
Figure 1
Inferred phylogenetic relationships of (a) prismane, also known as the hybrid-cluster protein (HCP), which is involved in the reduction of hydroxylamine
and NO, and (b) carbamate kinase (CK), which catalyzes the formation of carbamoyl phosphate by ATP-phosphorylation of carbamate. Bootstrap
values greater than 65 (out of 100) are shown at the nodes. Neighbor-joining trees, rooted at the internode, were computed with the TREECON
software package. Alignments consisting of 510 and 320 amino acids for HCP and CK were used as input files for tree construction.
hydroxylamine reductase could serve as additional electron sinks for redox balancing. They could also aid in the
downstream metabolism of any NO2 that results from
alternative electron-cycling nitrate reduction, including
the possible conversion of NO2 to nitric oxide (NO)
and its subsequent reduction.
phytoplankton growth efficiency and pelagic C and N
biogeochemistry. In vascular plants, photorespiratory
CO2 release is estimated to account for approximately
25% of the net CO2 assimilation and NH3 loss (in the
absence of recycling mechanisms), and far exceeds primary NH3 assimilation from NO3 reduction [49].
Operationally, this form of NO3 reduction is very similar
to photorespiration in that it facilitates a type of alternative electron cycling. Photorespiration is the lightdependent release of CO2 that results from glycolate
metabolism following the oxygenase reaction of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco).
Photorespiration, which in C3 vascular plants is known
to be a necessary pathway for the dissipation of excess
photochemical energy, functions as an important protective mechanism against photooxidative stress [48]. It is a
key physiological pathway with major implications for
Photorespiration and resulting C and N fluxes
www.sciencedirect.com
The first molecular investigations of the photorespiratory
pathway in diatoms was recently documented in a series
of experiments in which the expression of a variety of
genes that are central to C and N metabolism and photorespiration were examined. These studies attempted to
infer the relative importance of alternative electron
cycling and metabolic pathways in response to differences
in light level, temperature, and inorganic N source (NH4+
compared to NO3 ) [50,51]. Numerous novel relationships and themes related to the effect of light level,
Current Opinion in Plant Biology 2006, 9:264–273
268 Physiology and metabolism
temperature, and N source on cellular energy management
and on C and N metabolism were revealed by this work
[42]. For example, T. pseudonana cells cultured on NO3
under high-light, cold-temperature conditions appear to
utilize nitrate reduction as a means of diverting excess
electrons from CO2 fixation. However, when NO3 is not
available, photorespiratory metabolism is enhanced significantly. Growth on NH4+ under a high-light and coldtemperature regime is proposed to induce the strongest
flux of metabolites and energy through photorespiration.
These data suggest that, as expected, photorespiratory
activity is greater in high light than in low light but that
temperature and N source are also important variables
[51].
Recent evidence from the centric diatom Thalassiosira
weissflogii supports the idea that a significant fraction of
the CO2 flux through Rubisco is derived from C4 organic
acids [52,53]. The existence of such a CO2-concentrating mechanism (CCM), and of a variety of other
mechanisms involving different types of carbonic anhydrases [54,55], would probably diminish the flux of C
and N through photorespiratory pathways in diatoms. A
major research challenge is to conceptually integrate
photorespiratory metabolism in diatoms into the framework of overall cellular energy balance, stress management, and C and N status and turnover. The dynamics of
glycolate metabolism in diatoms remains an important
research topic. We do not yet know whether or not
glycolate is converted completely to NH3 and CO2,
partially metabolized and converted to the important
antioxidant glutathione [56], or released from the cell.
Also, the interaction between the fate of C and N that is
cycled through photochemically based alternative electron pathways, such as nitrate reduction and photorespiration, is not clear and is of great importance to our
understanding of diatom biology.
The urea cycle, NO, and GABA
The detection of the components for a complete urea
cycle, previously thought to be an exclusively metazoan
feature, was one of the major surprises of the recent T.
pseudonana genome analysis [6]. C and N fluxes through
diatom urea are presumably driven and regulated by the
mitochondrial protein carbamoyl phosphate synthetase
III (CPS III) [57]. CPS III is responsible for incorporating
NH4+ or glutamine and CO2 into carbamoyl phosphate,
which is then available for conversion into arginine, the
signaling molecule NO, the polyamine and proline precursor ornithine, or the high-energy molecule creatine
phosphate (Figure 2). It is tempting to speculate that the
mitochondrial photorespiratory derivatives NH3 and CO2
can be recovered through the activity of CPS III and the
urea cycle. Diatoms also appear to contain a bacterial-type
Figure 2
The urea cycle and associated pathways that are important to diatom nitrogen metabolism, turn-over, and signaling. Carbamoyl phosphate that is
synthesized in the mitochondria condenses with ornithine to produce citrulline. Once in the cytosol, the citrulline reacts with aspartate to continue
the urea cycle. Arginine can be converted to ornithine and urea by arginase or oxidized to citrulline and NO by NOS. The latter reaction forms
the basis of a citrulline–NO cycle, which can bypass the urea cycle. The specific enzymes indicated are the following: (1) carbamoyl phosphate
synthetase, (2) carbamate kinase, (3) ornithine transcarbamoylase, (4) argininosuccinate synthetase, (5) argininosuccinase, (6) arginase and (7)
NO synthase.
Current Opinion in Plant Biology 2006, 9:264–273
www.sciencedirect.com
Integrated nitrogen metabolism and related signaling pathways in marine diatoms Allen, Vardi and Bowler 269
carbamate kinase (CK) gene (Figure 1). CK also catalyzes
the formation of carbamoyl phosphate [58].
NO production
The possibility of the involvement of a CPS III-driven
urea cycle in NO production is especially intriguing and
represents a potentially novel source of NO for photosynthetic eukaryotes. In plants, NO regulates diverse
physiological, pathological, and developmental responses
[59]. NO, in the form of iron-nitrosyl complexes, has
also recently emerged as a major new player in plant Fe
metabolism and homeostasis [60]. In plants and green
algae, a role for NR and nitrite reductase (NiR) in the
generation of NO has been documented. Nitrite can be a
source or a substrate for NO generation in various pathways. In plants, NO is known to be produced enzymatically
by an NAD(P)H-dependent NR, by non-enzymatic reduction of apoplastic nitrite, by a membrane-bound enzyme,
and in the mitochondria [61–63]. High NO emission rates
correlate with high nitrite levels and NR activation during
anoxia and darkness. In animals, NO is produced by the
conversion of L-arginine to citrulline, principally by a
family of enzymes termed NO synthases (NOS). Recent
reports have highlighted a new type of NOS in plants that is
distinct from the animal NOS and shares similarity with a
mollusk gene that co-purifies with NOS activity
[59,64,65]. Analysis of the whole-genome sequence of
the diatom T. pseudonana, and of the draft genome
sequence of P. tricornutum, revealed a diatom ortholog of
the plant NOS.
NO signaling
Our recent work indicates a central function for NO and
intracellular calcium transients as second messengers that
are involved in stress perception and response in diatoms
[66]. We found that diatoms might use a sophisticated
stress surveillance system that is based on diatom-derived
unsaturated aldehydes that are produced only by
wounded cells [67,68]. Such aldehydes trigger intracellular calcium transients and the generation of NO by a
calcium-dependent NO-synthase-like activity.
Furthermore, the T. pseudonana and P. tricornutum genomes each appear to contain an alternative oxidase (AOX)
gene. AOX catalyzes the transfer of electrons from ubiquinol to oxygen, and is known to be regulated by environmental stresses and to have a role in preventing damage
associated with the formation of reactive oxygen species
(ROS). In P. tricornutum, AOX is upregulated in response to
NO3 depletion (AE Allen, A Vardi, C Bowler, unpublished). Prismane and AOX are both known to have a role in
NO scavenging [69,70]. In diatoms, both the prismane and
the AOX gene contain a putative mitochondria-targeting
sequence, and it seems likely that they could be involved in
mitochondrial NO metabolism. Stress-responsive utilization of ROS and NO by phytoplankton has been shown to
regulate cell fate (e.g. cell death) and is proposed to
www.sciencedirect.com
mediate cell–cell communication [71,72]. Such observations provide a novel context for understanding algal bloom
dynamics and the resulting biogeochemical fluxes. Various
forms of regulated programmed cell death (PCD) have
recently been described in a wide range of unicellular
eukaryotes and prokaryotes [73]. Such cell-death mechanisms have also recently been reported in several phytoplankton species, particularly in response to nutrient stress
[71,74,75,76,77,78].
Signals derived from organic N substrates
Although most phytoplankton are capable of utilizing
organic N as a sole N source [79], specific N metabolites
can also act as stress signals and inducers. For example, gaminobutyric acid (GABA), a well-known neurotransmitter [80], is known to have a signaling and defense role in
plants [81] and to act as a chemical cue that is produced
by various algae to induce the recruitment of planktonic
larvae [82]. We have recently detected GABA in P.
tricornutum cultures exposed to the NO donor sodium
nitroprusside (SNP) (AR Fernie, N Schauer, pers.
comm.). The draft sequence of the P. tricornutum genome
contains a predicted GABA transporter that contains 13
transmembrane domains and a putative extracellular leucine-rich repeat (LRR) domain. Such a protein can easily
be imagined to function as a GABA receptor that is
involved in stress perception and the transduction of
intercellular communication signals.
In the cyanobacterium Synechococcus PCC 7002, urea is
known to function as a stress signal that is capable of
initiating signal transduction events that can trigger membrane peroxidation followed by pigment bleaching and
rapid cell death [83]. The release of the amino acid
asparagine by endophytic green algae has been reported
to elicit a rapid defense reaction in host red algae [84]. The
existence of a urea cycle in diatoms, which is apparently
absent from the plant kingdom, adds another level of
complexity to arginine metabolism. Citrulline, a product
of arginine oxidation in the NOS reaction, can be recycled
via the urea cycle by argininosuccinate synthetase and
argininosuccinase (Figure 2). Argininosuccinase condenses
citrulline and aspartate to form a molecule of argininosuccinate, the immediate precursor of arginine [85]. Thus, the
urea cycle in mammals can be bypassed by the NOS
reaction, creating a new cycle called the citrulline–NO
cycle. Overexpression of argininosuccinase leads to an
enhanced capacity for NO production in vascular smooth
muscle cells and co-induction of argininosuccinate synthetase and endothelial nitric oxide synthase (eNOS) and
inducible nitric oxide synthase (iNOS) have been shown
in various cell types [86]. It is probable that arginase, as the
final step of the urea cycle, competes with NOS for the
substrate arginine. Further understanding of the origin of
NO in diatoms and of the cross-talk between nitrite- and
arginine-dependent pathways [59] will shed light on the
role of NO in phytoplankton, and on the way in which it is
Current Opinion in Plant Biology 2006, 9:264–273
270 Physiology and metabolism
involved in the death or defense signaling cascade in
response to environmental cues.
The analysis of the complete 34-Mb genome sequence of T. pseudonana
revealed many novel features related to silica, fatty-acid, nitrogen, and
metal metabolism. The diatom genome sequence supports the red algal
origin of chromoalveolate secondary plastids.
Conclusions
7.
Considering the tremendous importance of diatoms to
marine biogeochemistry and ecology in terms of biomass
production and species diversity, they are excellent
model organisms for many important research topics.
Diatom biology is now entering the post-genomics era.
Many poorly understood aspects of diatom evolution and
behavior are becoming clear and new research horizons
are emerging. Because of the unique multi-lineage content and chimeric nature of the diatom genome, many
novel metabolic networks and pathways probably await
discovery in these organisms. One major challenge is to
understand the adaptation and role of typically animal or
bacterial-like properties and metabolism in the context of
the photosynthetic lifestyle and life-history strategy of
diatoms.
Acknowledgements
The authors would like to thank Bess Ward and Aaron Kaplan for critical
reading of the manuscript. We also thank Alisdair Fernie and Nic Schauer of
the Max Planck Institute of Plant Molecular Physiology in Golm, Germany
for the use of gas chromatography-mass spectrometry techniques to detect
GABA in diatom cultures. Work in our laboratory is funded by the European
Union Margenes, Diatomics and Marine Genomics Europe projects and by
the Centre National de la Recherche Scientifique (CNRS). AA was
supported by a US National Science Foundation (NSF) post-doctoral
fellowship in microbial biology and AV is supported by a Marie Curie IntraEuropean Fellowship.
References and recommended reading
Papers of particular interest, published within the annual period of
review, have been highlighted as:
of special interest
of outstanding interest
1.
Falkowski PG, Raven JA: Aquatic photosynthesis. Malden, MA:
Blackwell Sciences; 1997.
2.
Walker TL, Collet C, Purton S: Algal transgenics in the genomic
era. J Phycol 2005, 41:1077-1093.
3.
Raven JA, Andrews M, Quigg A: The evolution of oligotrophy:
implications for the breeding of crop plants for low input
agricultural systems. Ann Appl Biol 2005, 146:261-280.
This interesting review discusses the role that nutrient resource limitation
has had on the evolution of photosynthetic organisms. Special consideration is given to particular elemental and biochemical restrictions and to
molecular and physiological mechanisms that are likely adaptations to life
in oligotrophic environments. Oligotrophic conditions that constrain
photosynthesis in the ocean are discussed.
4.
Scala S, Carels N, Falciatore A, Chiusano ML, Bowler C: Genome
properties of the diatom Phaeodactylum tricornutum.
Plant Physiol 2002, 129:993-1002.
5.
Maheswari U, Montsant A, Goll J, Krishnasamy S, Rajyashri KR,
Patell VM, Bowler C: The diatom EST database. Nucleic Acids
Res 2005, 33:D344-D347.
This paper describes the construction and features of a diatom EST
database. The EST sequences are organized into a non-redundant set for
P. tricornutum and T. pseudonana and can be searched according to
Pfam domains, clusters of orthologous groups (COG), and gene ontologies (GO).
6.
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D,
Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M et al.:
The genome of the diatom Thalassiosira pseudonana:
ecology, evolution, and metabolism. Science 2004, 306:79-86.
Current Opinion in Plant Biology 2006, 9:264–273
Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O,
Taylor FJR: The evolution of modern eukaryotic phytoplankton.
Science 2004, 305:354-360.
Synopsis of biogeochemical and geological aspects of the rise of redlineage phytoplankton (chromoalveolates) and of the evolution of dinoflagellates, coccolithophores, and diatoms.
8.
Andersen RA: Biology and systematics of heterokont and
haptophyte algae. Am J Bot 2004, 91:1508-1522.
9.
Bachvaroff TR, Puerta MVS, Delwiche CF: Chlorophyll
c-containing plastid relationships based on analyses of a
multigene data set with all four chromalveolate lineages.
Mol Biol Evol 2005, 22:1772-1782.
A phylogenetic analysis of ten plastid genes for each of the four major
chromalveolate lineages is presented. This study represents the first
organellar genome-scale analysis to include both haptophytes and dinoflagellates. Overall, molecular phylogenetics supports the idea of a single
origin of chlorophyll c-containing plastids from red algae. The authors
emphasize, however, that the data do not preclude the possibility of serial
transfer of chlorophyll c-containing plastids to various hosts.
10. Yoon HS, Hackett YD, Ciniglia C, Pinto G, Bhattacharya D: A
molecular timeline for the origin of photosynthetic eukaryotes.
Mol Biol Evol 2004, 21:809-818.
A multi-gene dataset and reliable fossil constraints are used to calculate a
time-line for major splits and endosymbiotic events that govern the algal
tree of life and that facilitated the spread photosynthesis across different
lineages.
11. Chaal BK, Green BR: Protein import pathways in ‘complex’
chloroplasts derived from secondary endosymbiosis involving
a red algal ancestor. Plant Mol Biol 2005, 57:333-342.
12. Kilian O, Kroth PG: Identification and characterization of a new
conserved motif within the presequence of proteins targeted
into complex diatom plastids. Plant J 2005, 41:175-183.
Through the manipulation and fusion to GFP of diatom plastid presequence motifs, the authors discover a single conserved phenylalanine
that is essential for protein transport into diatom plastids.
13. Sarthou G, Timmermans KR, Blain S, Treguer P: Growth
physiology and fate of diatoms in the ocean: a review.
J Sea Res 2005, 53:25-42.
14. Finkel ZV, Katz ME, Wright JD, Schofield OME, Falkowski PG:
Climatically driven macroevolutionary patterns in the size of
marine diatoms over the cenozoic. Proc Natl Acad Sci USA
2005, 102:8927-8932.
A database of the size of diatom silica frustules over the Cenozoic is
constructed and analyzed. The largest changes in the mean size of the
diatom frustule are inferred to correspond with Miocene and Eocene
changes in the intensity of oceanic temperature gradients, as estimated
from the temperature difference between surface and deep waters. The
authors conclude that during periods of intense thermal stratification,
such as in the Neogene, the average size of individual cells within the
diatom community decreased as a result of reduced nutrient supply.
15. Price NM: The elemental stoichiometry and composition of an
iron-limited diatom. Limnol Oceanogr 2005, 50:1159-1171.
The centric diatom Thalassiosira weissflogii was cultured over a range of
Fe-limiting conditions with nitrate or ammonium as the N source. N:P and
C:P ratios were found to decline significantly as a function of Fe limitation.
The elemental stoichiometry and uptake rate ratios for Fe-limited and
nutrient replete cells were measured and are discussed.
16. de Baar HJW, Boyd PW, Coale KH, Landry MR, Tsuda A, Assmy P,
Bakker DCE, Bozec Y, Barber RT, Brzezinski MA et al.:
Synthesis of iron fertilization experiments: from the iron age in
the age of enlightenment. J Geophys Res - Oceans 2005,
110:C09S1610.1029/2004JC002601.
This exhaustive analysis compares and summarizes eight large-scale
iron-enrichment experiments. Large diatoms apparently always benefit
more than smaller diatoms from Fe addition and Pseudo-nitzschia spp.
are consistently the most responsive of the smaller diatoms.
17. Kustka AB, Shaked Y, Milligan AJ, King DW, Morel FMM:
Extracellular production of superoxide by marine diatoms:
contrasting effects on iron redox chemistry and bioavailability.
Limnol Oceanogr 2005, 50:1172-1180.
www.sciencedirect.com
Integrated nitrogen metabolism and related signaling pathways in marine diatoms Allen, Vardi and Bowler 271
18. Falciatore A, d’Alcala MR, Croot P, Bowler C: Perception of
environmental signals by a marine diatom. Science 2000,
288:2363-2366.
19. Peers G, Price NM: A role for manganese in superoxide
dismutases and growth of iron-deficient diatoms.
Limnol Oceanogr 2004, 49:1774-1783.
34. Schmid AMM: Endobacteria in the diatom Pinnularia
(Bacillariophyceae). I. ‘Scattered ct-nucleoids’ explained:
DAPI–DNA complexes stem from exoplastidial bacteria boring
into the chloroplasts. J Phycol 2003, 39:122-138.
35. Andersson JO: Lateral gene transfer in eukaryotes.
Cell Mol Life Sci 2005, 62:1182-1197.
20. Peers G, Quesnel SA, Price NM: Copper requirements for
iron acquisition and growth of coastal and oceanic diatoms.
Limnol Oceanogr 2005, 50:1149-1158.
36. Sekowska A, Danchin A, Risler JL: Phylogeny of related
functions: the case of polyamine biosynthetic enzymes.
Microbiol 2000, 146:1815-1828.
21. Wells ML, Trick CG, Cochlan WP, Hughes MP, Trainer VL: Domoic
acid: the synergy of iron, copper, and the toxicity of diatoms.
Limnol Oceanogr 2005, 50:1908-1917.
This interesting study suggests that Pseudo-nitzschia spp., a diatom that
produces the neurotoxin domoic acid, has the ability to utilize iron that is
strongly complexed by organic ligands. Apparently, domoic acid and
copper are functional components of this unusual high-affinity iron
acquisition system.
37. Montsant A, Jabbari K, Maheswari U, Bowler C: Comparative
genomics of the pennate diatom Phaeodactylum tricornutum.
Plant Physiol 2005, 137:500-513.
This comparative genomics study is the first large-scale comparison of
diatoms and red and green algae. Several intriguing differences, related
to carbon and nitrogen metabolism, between diatoms and other algae
and between pennate and centric diatoms are revealed.
22. Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y, Ho TY, Reinfelder JR,
Schofield O, Morel FMM, Falkowski PG: The evolutionary
inheritance of elemental stoichiometry in marine
phytoplankton. Nature 2003, 425:291-294.
23. Berges JA, Gibson CE, Stewart BM: Physiological responses of
phytoplankton communities in the Irish Sea to simulated
upwelling. Hydrobiologia 2004, 517:121-132.
24. Klausmeier CA, Litchman E, Daufresne T, Levin SA: Optimal
nitrogen-to-phosphorus stoichiometry of phytoplankton.
Nature 2004, 429:171-174.
The authors use a stoichiometrically based model of phytoplankton
physiology to evaluate competitive trade-offs in P-limited and N-limited
environments. The model predicts that N:P ratios will vary from 8.2 to 45
depending on the ecological conditions.
25. Klausmeier CA, Litchman E, Levin SA: Phytoplankton growth
and stoichiometry under multiple nutrient limitation.
Limnol Oceanogr 2004, 49:1463-1470.
26. Floder S, Burns CW: The influence of fluctuating light on
diversity and species number of nutrient-limited
phytoplankton. J Phycol 2005, 41:950-956.
27. Lomas MW: Nitrate reductase and urease enzyme activity in
the marine diatom Thalassiosira weissflogii
(Bacillariophyceae): interactions among nitrogen substrates.
Mar Biol 2004, 144:37-44.
28. Allen AE, Ward BB, Song BK: Characterization of diatom
(Bacillariophyceae) nitrate reductase genes and their detection
in marine phytoplankton communities. J Phycol 2005, 41:95-104.
This study provides sequence information for a variety of diatom NR gene
fragments. It also identifies a PCR primer set that is capable of detecting
and assaying the diversity and expression of diatom NR genes in situ in
marine phytoplankton assemblages.
29. Takabayashi M, Wilkerson FP, Robertson D: Response of
glutamine synthetase gene transcription and enzyme activity
to external nitrogen sources in the diatom Skeletonema
costatum (Bacillariophyceae). J Phycol 2005, 41:84-94.
30. Poulsen N, Kroger N: A new molecular tool for transgenic
diatoms — control of mRNA and protein biosynthesis by an
inducible promoter-terminator cassette. FEBS J 2005,
272:3413-3423.
This important study evaluates the transcriptional response of NRs in the
pennate diatom Cylindrotheca fusiformis by using transgenic diatoms
containing the NR promoter fused to GFP. Nitrate reductase mRNA levels
are highly sensitive to overall N availability but the mature NR protein is
not processed and folded properly unless NO3 is available.
31. Hildebrand M: Cloning and functional characterization of
ammonium transporters from the marine diatom
Cylindrotheca fusiformis (Bacillariophyceae). J Phycol 2005,
41:105-113.
38. Sumper M, Brunner E, Lehmann G: Biomineralization in diatoms:
characterization of novel polyamines associated with silica.
FEBS Lett 2005, 579:3765-3769.
39. Lopez PJ, Descles J, Allen AE, Bowler C: Prospects in diatom
research. Curr Opin Biotechnol 2005, 16:180-186.
40. Poulsen N, Kroger N: Silica morphogenesis by alternative
processing of silaffins in the diatom Thalassiosira
pseudonana. J Biol Chem 2004, 279:42993-42999.
The five major silaffins from the diatom Thalassiosira psuedonana, which
are unusual phosphoproteins that are involved in biosilica formation, are
isolated, functionally analyzed, and structurally characterized. Silaffins
from T. pseudonana and another diatom Cylindrotheca fusiformis are not
homologous but are similar in terms of amino acid composition and posttranslational modifications. The authors identify higher molecular mass
isoforms of particular silaffins that result from alternative processing steps
that are necessary for the formation of porous silica in vitro.
41. Kroger N, Lorenz S, Brunner E, Sumper M: Self-assembly of
highly phosphorylated silaffins and their function in biosilica
morphogenesis. Science 2002, 298:584-586.
42. Allen AE: Defining the molecular basis for energy balance in
marine diatoms under fluctuating environmental conditions.
J Phycol 2005, 6:1073-1076.
43. Wagner H, Jakob T, Wilhelm C: Balancing the energy flow from
captured light to biomass under fluctuating light conditions.
New Phytol 2005, 169:95-108.
The photosynthetic efficiency of biomass production was quantified for
the diatom Phaeodactylum tricornutum and the green alga Chlorella
vulgaris by estimating carbon accumulation into new biomass as a
function of absorbed quanta. Under non-fluctuating light conditions,
the photosynthetic efficiency of biomass production was found to be
identical for both algae. Under a fluctuating light regime, however, a much
higher conversion efficiency of photosynthetic energy into biomass was
observed in the diatom compared to the green alga.
44. Lavaud J, van Gorkom HJ, Etienne AL: Photosystem II electron
transfer cycle and chlororespiration in planktonic diatoms.
Photosynth Res 2002, 74:51-59.
45. Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P,
Etienne AL: The super-excess energy dissipation in diatom
algae: comparative analysis with higher plants. Photosynth Res
2004, 82:165-175.
The results of this study suggest that P. tricornutum possesses more than
five times the capacity to dissipate excess energy of vascular plants. The
authors conclude that the capacity for non-photochemical chlorophyll
fluorescence quenching (NPQ) is higher in diatoms than in vascular
plants.
46. Lomas MW, Gilbert PM: Temperature regulation of nitrate
uptake: a novel hypothesis about nitrate uptake and reduction
in cool-water diatoms. Limnol Oceanogr 1999, 44:556-572.
32. Allen AE: Beyond sequence homology: redundant ammonium
transporters in a marine diatom are not functionally
equivalent. J Phycol 2005, 41:4-6.
47. Cabello P, Pino C, Olmo-Mira MF, Castillo F, Roldan MD,
Moreno-Vivian C: Hydroxylamine assimilation by Rhodobacter
capsulatus E1F1 – requirement of the hcp gene (hybrid cluster
protein) located in the nitrate assimilation nas gene region for
hydroxylamine reduction. J Biol Chem 2004, 279:45485-45494.
33. Obornik M, Green BR: Mosaic origin of the heme biosynthesis
pathway in photosynthetic eukaryotes. Mol Biol Evol 2005,
22:2343-2353.
48. Wingler A, Lea PJ, Quick WP, Leegood RC: Photorespiration:
metabolic pathways and their role in stress protection.
Philos Trans R Soc Lond B Biol Sci 2000, 355:1517-1529.
www.sciencedirect.com
Current Opinion in Plant Biology 2006, 9:264–273
272 Physiology and metabolism
49. Keys AJ, Bird IF, Cornelius MJ, Lea PJ, Wallsgrove RM, Miflin BJ:
Photorespiratory nitrogen cycle. Nature 1978, 275:741-743.
50. Parker MS, Armbrust EV, Piovia-Scott J, Keil RG: Induction
of photorespiration by light in the centric diatom Thalassiosira
weissflogii (Bacillariophyceae): molecular characterization
and physiological consequences. J Phycol 2004, 40:557-567.
Gene expression levels of the T protein of glycine decarboxylase (GDCT)
were monitored concomitantly with glycolate release in cells that were
pre-acclimated to 15 and 400 mmol photons m 2 s 1 before being placed
in the dark for 24-h and subsequently transferred to high light (400 mmol
photons m 2 s 1). A three-fold increase in GDCT transcript abundance as
well as significant glycolate release was observed in treatments that
received the most extreme shift in light intensity. The authors conclude
that high-light conditions provoke an induction of photorespiration in
marine diatoms, and that whether or not photorespiratory glycolate is
metabolized intracellularly or released from the cell depends largely on
the extent of physiological acclimation to high-light conditions.
51. Parker MS, Armbrust EV: Synergistic effects of light,
temperature, and nitrogen source on transcription of genes
for carbon and nitrogen metabolism in the centric diatom
Thalassiosira pseudonana (Bacillariophyceae). J Phycol 2005,
41:1142-1153.
This molecular investigation of photorespiration and carbon and nitrogen
metabolic pathways reveals several metabolic trade-offs that occur as a
result of N source, temperature, and light availability. The photorespiratory pathway is upregulated under conditions of high light, cold temperatures, and growth on NH4+ as the sole N substrate.
52. Reinfelder JR, Milligan AJ, Morel FMM: The role of the C-4
pathway in carbon accumulation and fixation in a marine
diatom. Plant Physiol 2004, 135:2106-2111.
53. Granum E, Raven JA, Leegood RC: How do marine diatoms fix
10 billion tonnes of inorganic carbon per year? Can J Bot 2005,
83:898-908.
54. Lane TW, Morel FMM: Regulation of carbonic anhydrase
expression by zinc, cobalt, and carbon dioxide in the
marine diatom Thalassiosira weissflogii. Plant Physiol 2000,
123:345-352.
55. Tanaka Y, Nakatsuma D, Harada H, Ishida M, Matsuda Y:
Localization of soluble beta-carbonic anhydrase in the marine
diatom Phaeodactylum tricornutum. Sorting to the
chloroplast and cluster formation on the girdle lamellae.
Plant Physiol 2005, 138:207-217.
56. Tang D, Shafer MM, Karner DA, Armstrong DE: Response of
nonprotein thiols to copper stress and extracellular release of
glutathione in the diatom Thalassiosira weissflogii.
Limnol Oceanogr 2005, 50:516-525.
57. Holden HM, Thoden JB, Raushel FM: Carbamoyl phosphate
synthetase: an amazing biochemical odyssey from substrate
to product. Cell Mol Life Sci 1999, 56:507-522.
58. Marina A, Alzari PM, Bravo J, Uriarte M, Barcelona B, Fita I,
Rubio V: Carbamate kinase: new structural machinery for
making carbamoyl phosphate, the common precursor of
pyrimidines and arginine. Protein Sci 1999, 8:934-940.
59. Crawford NM, Guo FQ: New insights into nitric oxide
metabolism and regulatory functions. Trends Plant Sci 2005,
10:195-200.
This review deciphers various sources of NO production in plants (comparing NO2 - and arginine-dependent NO production) and highlights
implications that are associated with the recent discovery of a novel
plant NOS.
60. Graziano M, Lamattina L: Nitric oxide and iron in plants:
an emerging and converging story. Trends Plant Sci 2005,
10:4-8.
This comprehensive review highlights an important emerging theme in
cellular Fe homeostasis. The formation of nitric oxide and iron–nitrosyl
complexes are important players in the dynamic network that governs
cellular Fe status.
61. Planchet E, Gupta KJ, Sonoda M, Kaiser WM: Nitric oxide
emission from tobacco leaves and cell suspensions: rate
limiting factors and evidence for the involvement of
mitochondrial electron transport. Plant J 2005, 41:732-743.
62. Bethke PC, Badger MR, Jones RL: Apoplastic synthesis of nitric
oxide by plant tissues. Plant Cell 2004, 16:332-341.
Current Opinion in Plant Biology 2006, 9:264–273
63. Tischner R, Planchet E, Kaiser WM: Mitochondrial electron
transport as a source for nitric oxide in the unicellular green
alga Chlorella sorokiniana. FEBS Lett 2004, 576:151-155.
64. He YK, Tang RH, Hao Y, Stevens RD, Cook CW, Am SM, Jing LF,
Yang ZG, Chen LG, Guo FQ et al.: Nitric oxide represses the
Arabidopsis floral transition. Science 2004, 305:1968-1971.
65. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W,
Hutzler P, Durner J: Innate immunity in Arabidopsis thaliana:
lipopolysaccharides activate nitric oxide synthase (NOS) and
induce defense genes. Proc Natl Acad Sci USA 2004, 101:1581115816.
66. Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A,
Bowler C: A stress surveillance system based on calcium and
nitric oxide in marine diatoms. PLoS Biol 2006, 4:e60.
This study reports, for the first time, on the role of nitric oxide signaling in
phytoplankton populations. Exposure to diatom-derived reactive aldehydes triggers intracellular calcium transients and the generation of NO
by calcium-dependent NO-synthase-like activity, which determines cell
fate (i.e. immune resistance versus cell death).
67. Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G,
Casotti R, Pohnert G, Wichard T, Colucci-D’Amato L et al.:
Aldehyde suppression of copepod recruitment in blooms of a
ubiquitous planktonic diatom. Nature 2004, 429:403-407.
68. Pohnert G: Diatom/copepod interactions in plankton: the
indirect chemical defense of unicellular algae. ChemBioChem
2005, 6:946-959.
69. Filenko NA, Browning DF, Cole JA: Transcriptional regulation
(prismane) protein of a hybrid cluster. Biochem Soc Trans 2005,
33:195-197.
70. Huang X, von Rad U, Durner J: Nitric oxide induces
transcriptional activation of the nitric oxide-tolerant
alternative oxidase in Arabidopsis suspension cells. Planta
2002, 215:914-923.
71. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A,
Levine A: Programmed cell death of the dinoflagellate
Peridinium gatunense is mediated by CO2 limitation and
oxidative stress. Curr Biol 1999, 9:1061-1064.
72. Vardi A, Schatz D, Beeri K, Motro U, Sukenik A, Levine A, Kaplan A:
Dinoflagellate–cyanobacterium communication may
determine the composition of phytoplankton assemblage in a
mesotrophic lake. Curr Biol 2002, 12:1767-1772.
73. Ameisen JC: Looking for death at the core of life in the light of
evolution. Cell Death Differ 2004, 11:4-10.
74. Casotti R, Mazza S, Brunet C, Vantrepotte V, Ianora A, Miralto A:
Growth inhibition and toxicity of the diatom aldehyde 2-trans,
4-trans-decadienal on Thalassiosira weissflogii
(Bacillariophyceae). J Phycol 2005, 41:7-20.
75. Bidle KD, Falkowski PG: Cell death in planktonic,
photosynthetic microorganisms. Nat Rev Microbiol 2004,
2:643-655.
This is an excellent review that summarizes what is known about programmed cell death (PCD) in marine plankton communities.
76. Berges JA, Falkowski PG: Physiological stress and cell death
in marine phytoplankton: induction of proteases in
response to nitrogen or light limitation. Limnol Oceanogr 1998,
43:129-135.
77. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG: The demise
of the marine cyanobacterium, Trichodesmium spp., via an
autocatalyzed cell death pathway. Limnol Oceanogr 2004,
49:997-1005.
78. Chung C-C, Hwang S-PL, Chang J: Co-occurrence of ScDSP
gene expression, cell death, and DNA fragmentation in a
marine diatom, Skeletonema costatum. Appl Environ Microbiol
2005, 71:8744-8751.
Using a cDNA subtraction library from death-stage culture, the authors
identify a novel death-specific gene, ScDSP. It is likely that ScDSP plays a
role in the molecular mechanism of self-destructive autolysis.
79. Berman T, Bronk DA: Dissolved organic nitrogen: a dynamic
participant in aquatic ecosystems. Aquat Microb Ecol 2003,
31:279-305.
www.sciencedirect.com
Integrated nitrogen metabolism and related signaling pathways in marine diatoms Allen, Vardi and Bowler 273
80. Belelli D, Lambert JJ: Neurosteroids: endogenous regulators of
the GABA(A) receptor. Nat Rev Neurosci 2005, 6:565-575.
81. Bouche N, Fromm H: GABA in plants: just a metabolite? Trends
Plant Sci 2004, 9:110-115.
New roles for GABA as a possible signaling molecule have emerged. This
review provides a modern synopsis of the various roles of GABA in plants.
The GABA metabolic pathway also has a role in response to stress and
carbon:nitrogen metabolism. The authors outline the challenges associated with uncoupling the signaling and metabolic roles of GABA.
82. Morse DE, Hooker N, Duncan H, Jensen L: Gamma-aminobutyric
acid, a neurotransmitter, induces planktonic abalone
larvae to settle and begin metamorphosis. Science 1979,
204:407-410.
83. Sakamoto T, Delgaizo VB, Bryant DA: Growth on urea can trigger
death and peroxidation of the Cyanobacterium
www.sciencedirect.com
synechococcus sp. strain PCC 7002. Appl Environ Microbiol
1998, 64:2361-2366.
84. Weinberger F, Pohnert G, Berndt ML, Bouarab K, Kloareg B,
Potin P: Apoplastic oxidation of L-asparagine is involved in the
control of the green algal endophyte Acrochaete operculata
Correa & Nielsen by the red seaweed Chondrus crispus
Stackhouse. J Exp Bot 2005, 56:1317-1326.
85. Husson A, Brasse-Lagnel C, Fairand A, Renouf S, Lavoinne A:
Argininosuccinate synthetase from the urea cycle to the
citrulline–NO cycle. Eur J Biochem 2003, 270:1887-1899.
86. Nussler AK, Billiar TR, Liu ZZ, Morris SM: Coinduction of
nitric-oxide synthase and argininosuccinate synthetase
in a murine macrophage cell-line — implications for
regulation of nitric-oxide production. J Biol Chem 1994,
269:1257-1261.
Current Opinion in Plant Biology 2006, 9:264–273