[show abstract][hide abstract] ABSTRACT: The Neoproterozoic (1000-542 million years ago, Mya) was characterized by profound global environmental and evolutionary changes, not least of which included a major rise in atmospheric oxygen concentrations [1, 2], extreme climatic fluctuations and global-scale glaciation , and the emergence of metazoan life in the oceans [4, 5]. We present here phylogenomic (135 proteins and two ribosomal RNAs, SSU and LSU) and relaxed molecular clock (SSU, LSU, and rpoC1) analyses that identify this interval as a key transition in the marine nitrogen cycle. Specifically, we identify the Cryogenian (850-635 Mya) as heralding the first appearance of both marine planktonic unicellular nitrogen-fixing cyanobacteria and non-nitrogen-fixing picocyanobacteria (Synechococcus and Prochlorococcus ). Our findings are consistent with the existence of open-ocean environmental conditions earlier in the Proterozoic adverse to nitrogen-fixers and their evolution-specifically, insufficient availability of molybdenum and vanadium, elements essential to the production of high-yielding nitrogenases. As these elements became more abundant during the Cryogenian [7, 8], both nitrogen-fixing cyanobacteria and planktonic picocyanobacteria diversified. The subsequent emergence of a strong biological pump in the ocean implied by our evolutionary reconstruction may help in explaining increased oxygenation of the Earth's surface at this time, as well as tendency for glaciation.
Current biology: CB 02/2014; · 10.99 Impact Factor
[show abstract][hide abstract] ABSTRACT: Photosynthetic life requires sufficient photosynthetically active radiation
(PAR) to metabolise. On Earth, plant behaviour, physiology and metabolism are
sculpted around the night-day cycle by an endogenous biological circadian
The evolution of life was influenced by the Earth-Sun orbital dynamic, which
generates the photo-environment incident on the planetary surface. In this work
the unusual photo-environment of an Earth-like planet (ELP) in 3:2 spin orbit
resonance is explored. Photo-environments on the ELP are longitudinally
differentiated, in addition to differentiations relating to latitude and depth
(for aquatic organisms) which are familiar on Earth. The light environment on
such a planet could be compatible with Earth's photosynthetic life although the
threat of atmospheric freeze-out and prolonged periods of darkness would
present significant challenges. We emphasise the relationship between the
evolution of life on a planetary body with its orbital dynamics.
[show abstract][hide abstract] ABSTRACT: The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic – combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies.
[show abstract][hide abstract] ABSTRACT: A matrix of photobioreactors integrated with metabolic sensors was used to examine the combined impact of light and temperature variations on the growth and physiology of the biofuel candidate microalgal species Nannochloropsis oculata. The experiments were performed with algal cultures maintained at a constant 20°C versus a 15°C to 25°C diel temperature cycle, where light intensity also followed a diel cycle with a maximum irradiance of 1920 µmol photons m(-2) s(-1). No differences in algal growth (Chlorophyll a) were found between the two environmental regimes; however, the metabolic processes responded differently throughout the day to the change in environmental conditions. The variable temperature treatment resulted in greater damage to photosystem II due to the combined effect of strong light and high temperature. Cellular functions responded differently to conditions before midday as opposed to the afternoon, leading to strong hysteresis in dissolved oxygen concentration, quantum yield of photosystem II and net photosynthesis. Overnight metabolism performed differently, probably as a result of the temperature impact on respiration. Our photobioreactor matrix has produced novel insights into the physiological response of Nannochloropsis oculata to simulated environmental conditions. This information can be used to predict the effectiveness of deploying Nannochloropsis oculata in similar field conditions for commercial biofuel production.
PLoS ONE 01/2014; 9(1):e86047. · 3.73 Impact Factor
[show abstract][hide abstract] ABSTRACT: Minimum energy (as photon) costs are predicted for core reactions of photosynthesis, for photorespiratory metabolism in algae lacking CO2 concentrating mechanisms (CCMs) and for various types of CCMs; in algae, with CCMs; allowance was made for leakage of CO2 from the internal pool. These predicted values are just compatible with the minimum measured photon costs of photosynthesis in microalgae and macroalgae lacking or expressing CCMs. More energy-expensive photorespiration, for example for organisms using Rubiscos with lower CO2-O2 selectivity coefficients, would be less readily accommodated within the lowest measured photon costs of photosynthesis by algae lacking CCMs. The same applies to the cases of CCMs with higher energy costs of active transport of protons or inorganic carbon species, or greater allowance for significant leakage from the accumulated intracellular pool of CO2. High energetic efficiency can involve a higher concentration of catalyst to achieve a given rate of reaction, adding to the resource costs of growth. There are no obvious mechanistic interpretations of the occurrence of CCMs algae adapted to low light and low temperatures using the rationales adopted for the occurrence of C4 photosynthesis in terrestrial flowering plants. There is an exception for cyanobacteria with low-selectivity Form IA or IB Rubiscos, and those dinoflagellates with low-selectivity Form II Rubiscos, for which very few natural environments have high enough CO2:O2 ratios to allow photosynthesis in the absence of CCMs.
Photosynthesis Research 01/2014; · 3.15 Impact Factor
[show abstract][hide abstract] ABSTRACT: Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes, and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A. thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus (“delayed greening”), with young leaves having very low levels of chlorophyll and Calvin-Benson cycle enzymes. In mature leaves, soluble protein and Calvin-Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A. thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: less P is invested in ribosomes; the rate of growth and, hence, demand for P is low; the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin-Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effectively use.
Plant Cell and Environment 11/2013; · 5.14 Impact Factor
[show abstract][hide abstract] ABSTRACT: The biosignatures of life on Earth do not remain static, but change
considerably over the planet's habitable lifetime. Earth's future biosphere,
much like that of the early Earth, will consist of predominantly unicellular
microorganisms due to the increased hostility of environmental conditions
caused by the Sun as it enters the late stage of its main sequence evolution.
Building on previous work, the productivity of the biosphere is evaluated
during different stages of biosphere decline between 1 Gyr and 2.8 Gyr from
present. A simple atmosphere-biosphere interaction model is used to estimate
the atmospheric biomarker gas abundances at each stage and to assess the
likelihood of remotely detecting the presence of life in low-productivity,
microbial biospheres, putting an upper limit on the lifetime of Earth's
remotely detectable biosignatures. Other potential biosignatures such as leaf
reflectance and cloud cover are discussed.
[show abstract][hide abstract] ABSTRACT: Acclimation to environmental changes involves a modification of the expressed proteome and metabolome. The reproductive advantage associated with the higher fitness that acclimation provides to the new conditions more than compensates for the costs of acclimation. To exploit such an advantage, however, the duration of the perturbation must be sufficiently long relative to the growth rate. Otherwise, a selective pressure may exist in favour of responses that minimize changes in carbon allocation and resource use and do not require reversal of the acclimation after the perturbation ceases (compositional homeostasis). We hypothesize that the choice between acclimation and homeostasis depends on the duration of the perturbation relative to the length of the cell cycle. To test this hypothesis, we cultured the green alga Tetraselmis suecica at two growth rates and subjected the cultures to three environmental perturbations. Carbon allocation was studied with Fourier transform infrared (FTIR) spectroscopy; elemental stoichiometry was investigated by Total Reflection X-Ray Fluorescence (TXRF) spectroscopy. Our data confirmed that growth rate is a crucial factor for C allocation in response to external changes, with a higher degree of compositional homeostasis in cells with lower growth rate.
Plant Cell and Environment 08/2013; · 5.14 Impact Factor
[show abstract][hide abstract] ABSTRACT: Photolithotrophs are divided between those that use water as their electron donor (Cyanobacteria and the photosynthetic eukaryotes) and those that use a different electron donor (the anoxygenic photolithotrophs, all of them Bacteria). Photolithotrophs with the most reduced genomes have more genes than do the corresponding chemoorganotrophs, and the fastest-growing photolithotrophs have significantly lower specific growth rates than the fastest-growing chemoorganotrophs. Slower growth results from diversion of resources into the photosynthetic apparatus, which accounts for about half of the cell protein. There are inherent dangers in (especially oxygenic) photosynthesis, including the formation of reactive oxygen species (ROS) and blue light sensitivity of the water spitting apparatus. The extent to which photolithotrophs incur greater DNA damage and repair, and faster protein turnover with increased rRNA requirement, needs further investigation. A related source of environmental damage is ultraviolet B (UVB) radiation (280-320 nm), whose flux at the Earth's surface decreased as oxygen (and ozone) increased in the atmosphere. This oxygenation led to the requirements of defence against ROS, and decreasing availability to organisms of combined (non-dinitrogen) nitrogen and ferrous iron, and (indirectly) phosphorus, in the oxygenated biosphere. Differential codon usage in the genome and, especially, the proteome can lead to economies in the use of potentially growth-limiting elements.
Philosophical Transactions of The Royal Society B Biological Sciences 01/2013; 368(1622):20120264. · 6.23 Impact Factor
[show abstract][hide abstract] ABSTRACT: The future biosphere on Earth (as with its past) will be made up
predominantly of unicellular microorganisms. Unicellular life was probably
present for at least 2.5 Gyr before multicellular life appeared and will likely
be the only form of life capable of surviving on the planet in the far future,
when the ageing Sun causes environmental conditions to become more hostile to
more complex forms of life. Therefore, it is statistically more likely that
habitable Earth-like exoplanets we discover will be at a stage in their
habitable lifetime more conducive to supporting unicellular, rather than
multicellular life. The end stage of habitability on Earth is the focus of this
work. A simple, latitude-based climate model incorporating eccentricity and
obliquity variations is used as a guide to the temperature evolution of the
Earth over the next 3 Gyr. This allows inferences to be made about potential
refuges for life, particularly in mountains and cold-trap (ice) caves and what
forms of life could live in these environments. Results suggest that in high
latitude regions, unicellular life could persist for up to 2.8 Gyr from
present. This begins to answer the question of how the habitability of Earth
will evolve at local scales alongside the Sun's main sequence evolution and, by
extension, how the habitability of Earth-like planets would evolve over time
with their own host stars.
International Journal of Astrobiology. 10/2012; 12(2).
[show abstract][hide abstract] ABSTRACT: Macroalgae occur in the marine benthos from the upper intertidal to depths of more than 200 m, contributing up to 1 Pg C per year to global primary productivity. Freshwater macroalgae are mainly green (Chlorophyta) with some red (Rhodophyta) and a small contribution of brown (Phaeophyceae) algae, while in the ocean all three higher taxa are important. Attempts to relate the depth distribution of three higher taxa of marine macroalgae to their photosynthetic light use through their pigmentation in relation to variations in spectral quality of photosynthetically active radiation (PAR) with depth (complementary chromatic adaptation) and optical thickness (package effect) have been relatively unsuccessful. The presence (Chlorophyta, Phaeophyceae) or absence (Rhodophyta) of a xanthophyll cycle is also not well correlated with depth distribution of marine algae. The relative absence of freshwater brown algae does not seem to be related to their photosynthetic light use. Photosynthetic inorganic carbon acquisition in some red and a few green macroalgae involves entry of CO(2) by diffusion. Other red and green macroalgae, and brown macroalgae, have CO(2) concentrating mechanisms; these frequently involve acid and alkaline zones on the surface of the alga with CO(2) (produced from HCO(3) (-)) entering in the acid zones, while some macroalgae have CCMs based on active influx of HCO(3) (-). These various mechanisms of carbon acquisition have different responses to the thickness of the diffusion boundary layer, which is determined by macroalgal morphology and water velocity. Energetic predictions that macroalgae growing at or near the lower limit of PAR for growth should rely on diffusive CO(2) entry without acid and alkaline zones, and on NH(4) (+) rather than NO(3) (-) as nitrogen source, are only partially borne out by observation. The impact of global environmental change on marine macroalgae mainly relates to ocean acidification and warming with shoaling of the thermocline and decreased nutrient flux to the upper mixed layer. Predictions of the impact on macroalgae requires further experiments on interactions among increased inorganic carbon, increased temperature and decreased nitrogen and phosphorus supply, and, when possible, studies of genetic adaptation to environmental change.
Photosynthesis Research 07/2012; 113(1-3):105-25. · 3.15 Impact Factor
[show abstract][hide abstract] ABSTRACT: Limitation of grain crop productivity by phosphorus (P) is widespread and will probably increase in the future. Enhanced P efficiency can be achieved by improved uptake of phosphate from soil (P-acquisition efficiency) and by improved productivity per unit P taken up (P-use efficiency). This review focuses on improved P-use efficiency, which can be achieved by plants that have overall lower P concentrations, and by optimal distribution and redistribution of P in the plant allowing maximum growth and biomass allocation to harvestable plant parts. Significant decreases in plant P pools may be possible, for example, through reductions of superfluous ribosomal RNA and replacement of phospholipids by sulfolipids and galactolipids. Improvements in P distribution within the plant may be possible by increased remobilization from tissues that no longer need it (e.g. senescing leaves) and reduced partitioning of P to developing grains. Such changes would prolong and enhance the productive use of P in photosynthesis and have nutritional and environmental benefits. Research considering physiological, metabolic, molecular biological, genetic and phylogenetic aspects of P-use efficiency is urgently needed to allow significant progress to be made in our understanding of this complex trait.
New Phytologist 06/2012; 195(2):306-20. · 6.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Phosphorus (P) is the proximate (immediate) limiting element for primary productivity in some habitats, and is generally the ultimate limiting element for primary productivity. Although RNA can account for over half of the non-storage P in photosynthetic organisms, some primary producers have more ribosomes than the minimum needed for the observed rate of net protein synthesis; some of this RNA may be needed for protein turnover. Two cases of protein turnover which can occur at a much faster rate than the bulk protein turnover are those of photodamaged photosystem II and O(2)-damaged nitrogenase. While RNA involved in photosystem II repair accounts for less than 1% of the non-storage P in photosynthetic organisms, a maximum, of 12% of non-storage P could occur in RNA associated with replacement of damaged nitrogenase and/or O(2) damage avoidance mechanism in diazotrophic (N(2) fixing) organisms. There is a general trend in published data towards lower P use efficiency (g dry matter gain per day per mol P in the organism) for photosynthetic diazotrophic organisms growing under P limitation with N(2) as their nitrogen source, rather than with NH(4)(+), urea or NO(3)(-). Additional work is needed to examine the generality of a statistically verified decrease in P use efficiency for diazotrophic growth relative to growth on other nitrogen sources and, if this is confirmed, further investigation of the mechanism is needed. The outcome of such work would be important for relating the global distribution of diazotrophy to P availability. There are no known P acquisition mechanisms specific to diazotrophs. Phosphorus (P) is the proximate (immediate) limiting element for primary productivity in some habitats, and is generally the ultimate limiting element for primary productivity. Although RNA can account for over half of the non-storage P in photosynthetic organisms, some primary producers have more ribosomes than the minimum needed for the observed rate of net protein synthesis; some of this RNA may be needed for protein turnover. Two cases of protein turnover which can occur at a much faster rate than the bulk protein turnover are those of photodamaged photosystem II and O(2)-damaged nitrogenase. While RNA involved in photosystem II repair accounts for less than 1% of the non-storage P in photosynthetic organisms, a maximum, of 12% of non-storage P could occur in RNA associated with replacement of damaged nitrogenase and/or O(2) damage avoidance mechanism in diazotrophic (N(2) fixing) organisms. There is a general trend in published data towards lower P use efficiency (g dry matter gain per day per mol P in the organism) for photosynthetic diazotrophic organisms growing under P limitation with N(2) as their nitrogen source, rather than with NH(4)(+), urea or NO(3)(-). Additional work is needed to examine the generality of a statistically verified decrease in P use efficiency for diazotrophic growth relative to growth on other nitrogen sources and, if this is confirmed, further investigation of the mechanism is needed. The outcome of such work would be important for relating the global distribution of diazotrophy to P availability. There are no known P acquisition mechanisms specific to diazotrophs.
[show abstract][hide abstract] ABSTRACT: Anthropogenically released CO2 is dissolving in the ocean,
causing a decrease in bulk-seawater pH (ocean acidification).
Projections indicate that the pH will drop 0.3 units from its present
value by 2100 (ref. ). However, it is unclear how the growth of plankton
is likely to respond. Using simulations we demonstrate how pH and
carbonate chemistry at the exterior surface of marine organisms deviates
increasingly from those of the bulk sea water as organism metabolic
activity and size increases. These deviations will increase in the
future as the buffering capacity of sea water decreases with decreased
pH and as metabolic activity increases with raised seawater
temperatures. We show that many marine plankton will experience pH
conditions completely outside their recent historical range. However,
ocean acidification is likely to have differing impacts on plankton
physiology as taxon-specific differences in organism size, metabolic
activity and growth rates during blooms result in very different
microenvironments around the organism. This is an important
consideration for future studies in ocean acidification as the carbonate
chemistry experienced by most planktonic organisms will probably be
considerably different from that measured in bulk-seawater samples. An
understanding of these deviations will assist interpretation of the
impacts of ocean acidification on plankton of different size and
[show abstract][hide abstract] ABSTRACT: Highly expressed proteins can exhibit relatively small material costs, in terms of the quantities of carbon (C), nitrogen (N) or sulphur (S) atoms they contain. This 'elemental sparing' probably reflects selection to reduce the quantities of potentially growth-limiting elements in abundant proteins, but the evolutionary mechanisms for adaptive elemental sparing are still poorly understood. Here, we predict that the extent of 'elemental sparing' in highly expressed proteins will vary among organisms, according to the effectiveness of selection in determining the fate of mutations. We test this hypothesis in bacteria by asking whether 'elemental sparing' is correlated with codon usage bias. Bacteria exhibit extraordinary variation in their life histories and demography and consequently in the effectiveness of selection in determining whether preferred codons are used in highly expressed genes. We find that C sparing and S sparing, but not N sparing, are significantly correlated with adaptive codon usage bias among 148 genera of bacteria, suggesting that selection for elemental sparing and codon bias are promoted by similar bacterial traits. Our study helps identify principles that determine how nutrient scarcity can shape the elemental composition of proteins.
[show abstract][hide abstract] ABSTRACT: Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco)-photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO(2) assimilation. The high CO(2) and (initially) O(2)-free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO(2) decreased and O(2) increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO(2) affinity and CO(2)/O(2) selectivity correlated with decreased CO(2)-saturated catalytic capacity and/or for CO(2)-concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco-PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO(2) episode followed by one or more lengthy high-CO(2) episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO(2) ocean. More investigations, including studies of genetic adaptation, are needed.
Philosophical Transactions of The Royal Society B Biological Sciences 02/2012; 367(1588):493-507. · 6.23 Impact Factor