Phytoplankton Ecology

Structural analysis of phytoplankton communities variation in the archipelago of La Maddalena (North Sardinian Coast): A canonical correlation approach

by Giovanni Zurlini

THESIS: 'The effect of ocean acidification upon free-living Symbiodinium spp. (Dinophyceae)'

by Patrick Brading

This is a copy of my PhD thesis which contains a little more info than the peer-reviewed papers I have published so far.

Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligo-mesotrophic lake (Lake Stechlin, Germany)

by Viktoria Uveges

authors: Viktória Üveges, Kálmán Tapolczai, Lothar Krienitz & Judit Padisák

In winter of 2009/2010, Aphanizomenon
flos-aquae bloomed in the ice and snow covered oligomesotrophic Lake... more In winter of 2009/2010, Aphanizomenon
flos-aquae bloomed in the ice and snow covered oligomesotrophic Lake Stechlin, Germany. The photosynthesis
of the natural population was measured at eight
temperatures in the range of 2–35C, at nine different
irradiance levels in the range of 0–1,320 lmol m-2 s-1
PAR at each applied temperature. The photoadaptation
parameter (Ik) and the maximum photosynthetic rate
(Pmax) correlated positively with the temperature
between 2 and 30C, and there was a remarkable drop
in both parameters at 35C. The low Ik at low
temperatures enabled the active photosynthesis of
overwintering populations at low irradiance levels
under ice and snow cover. The optimum of the
photosynthesis was above 20C at irradiances above
150 lmol m-2 s-1. At lower irradiance levels
(7.5–30 lmol m-2 s-1), the photosynthesis was the
most intensive in the temperature range of 2–5C. The
interaction between light and temperature allowed the
proliferation of A. flos-aquae in Lake Stechlin resulting
in winter water bloom in this oligo-mesotrophic lake.
The applied 2C is the lowest experimental temperature
ever in the photosynthesis/growth studies of A. flosaquae,
and the results of the P–I and P–T measurements
provide novel information about the tolerance and
physiological plasticity of this species.

Effects of temperature on growth rate, cell composition and nitrogen metabolism in the marine diatom Thalassiosira pseudonana (Bacillariophyceae)

by John Berges

Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation

by John Berges

A review of phytoplankton dynamics in tropical African lakes

by Mzime Ndebele-Murisa

Influence of irradiance and temperature on the iron content of the marine diatom Thalassiosira weissflogii (Bacillariophyceae)

by Robert Strzepek

R. F. Strzepek and N. M. Price

The marine diatom Thalassiosira weissflogii (Grun.) Fryxell et Hasle was grown over a wide range of irradiances and... more The marine diatom Thalassiosira weissflogii (Grun.) Fryxell et Hasle was grown over a wide range of irradiances and temperatures in both NO3– and NH4+-amended seawater containing high Fe. Maximum growth rates were not affected by N source, but the initial slope of the growth irradiance curve was significantly greater for the NH4+-grown cells. Light-limited phytoplankton con- tained 4 times more Fe (μmol Fe mol–1 C) than light-sufficient cells, and at intermediate irradiances had the highest chlorophyll a concentrations (g C g-1 chl a). Iron quotas increased as irradiance was reduced because growth rates declined by 20-fold, whereas steady-state Fe transport rates declined by only a factor of 6. Accumulation of Fe was apparently regulated by a light-induced physiological requirement. Similar reductions in growth rate with declining temperature elicited only minor changes in Fe quota, and the increase in Fe quota, was observed only at the 2 lowest temperatures. At irradiance levels between 37 and 150 μmol photons m–2 s–1, the relative increase in Fe quota exactly matched the relative increase predicted from the change in abundance of PSI and PSII reported to occur during photoacclimation of T. weissflogii. Subsequent increases in Fe quota at low light may represent additional changes to the photosynthetic apparatus or accumulation of Fe in a non-metabolic pool. The results demonstrate that the Fe content of phytoplankton is influenced by ambient light and imply that the extent of photoacclimation of natural populations may be con- strained by the availability of Fe.

Phytoplankton processes. Part 2: Rates of primary production and factors controlling algal growth during the Southern Ocean Iron RElease Experiment (SOIREE)

by Robert Strzepek

M.P. Gall, R. Strzepek, M. Maldonado, P.W. Boyd

The Southern Ocean Iron RElease Experiment (SOIREE) fertilised 200km of polar waters (mixed- layer depth, 65 m) south... more The Southern Ocean Iron RElease Experiment (SOIREE) fertilised 200km of polar waters (mixed- layer depth, 65 m) south of Australia in February 1999. During the 13-d SOIREE, iron enrichment stimulated primary production, algal growth and biogenic silica production rates. A #oristic shift from small to large cells resulted in a greater contribution to community production by diatoms, which contributed '60% to community production towards the end of SOIREE. Column-integrated rates of primary production increased by more than 10-fold, and community production rates (normalised to chlorophyll) had doubled by day 4, but then declined after day 6 to initial rates. Iron enrichment increased the growth rates of the algal community from 0.02 to 0.15d’ (based on changes in in-situ chlorophyll concentrations), from 0.02 to 0.2 d’ (based on algal carbon), and more than doubled initial rates (based on C) to 0.2 d’ during SOIREE. However, these iron-elevated rates were less than the maximum rates (0.69d’) predicted for waters at 2.53C. Community biogenic silica production rates increased by 6-fold, i.e. to a lesser extent than primary production rates, resulting in a 2-fold reduction in the silicic-acid:carbon uptake ratio. Shipboard perturbation experiments indicated that iron, rather than both iron and light, limited algal growth in these waters. However, a signi"cant increase in light attenuation in situ due to algal self-shading, suggested that light limitation of algal growth might become signi"cant after day 13 at this locale. Limitation of algal growth by both iron (and silicic acid and/or zinc) within iron-fertilised waters after day 8 of SOIREE was not evident from the results of a shipboard experiment.

Phytoplankton processes during a mesoscale iron enrichment in the NE subarctic Pacific: Part III--Primary productivity

by Robert Strzepek

Adrian Marchetti, Nelson D. Sherry, Philippe Juneau, Robert F. Strzepek, and Paul J. Harrison

As part of the Canadian SOLAS program, a large scale iron (Fe) enrichment experiment (Subarctic Ecosystem Response to... more As part of the Canadian SOLAS program, a large scale iron (Fe) enrichment experiment (Subarctic Ecosystem Response to Iron Enrichment Study; SERIES) was performed in the NE subarctic Pacific in July of 2002. Dissolved Fe was added to a 77km2 patch of seawater and the evolution of the subsequent phytoplankton bloom was monitored for 26 days. Particulate organic primary productivity (OPP) inside the patch began to increase in all phytoplankton size-fractions (picophytoplankton, nanophytoplankton and microphytoplankton) relative to outside the patch within 48 h. After day 10, microphytoplankton (420mm) were responsible for the vast majority of both OPP and phytoplankton biomass. Maximum OPP of ca. 15 mmol C m􏰀3 d􏰀1 was achieved on day 15, representing a 20-fold increase from average OPP measured outside the patch. Water-column integrated, biomass (chl a)-specific OPP (Pbint) of the total phytoplankton assemblage peaked twice, once following the first Fe infusion on day 4 (2.9 mmol C mg chl a-1 d-1) and then coinciding with maximum OPP on day 15 (2.6 mmol C mg chl a-1 d-1). Maximum Pbint achieved on day 4 represented a 5-fold increase relative to Pbint measured outside the patch. Water-column integrated OPP also peaked on day 15 at ca. 251 mmol C m-2 d-1, and coincided with a rapid decline in silicic acid (Si(OH4)) concentrations. At this time, microphytoplankton accounted for ca. 90% of total OPP. Patch-averaged chlorophyll a (chl a) concentrations were maximal (􏰁5 mg m􏰀3, 416 times the outside patch) on day 18, during which time microphytoplankton OPP had begun to decline. In addition to OPP, particulate inorganic primary productivity (IPP) also increased due to an elevated coccolithophore abundance, reaching a maximum of 0.25 mmol C m􏰀3 d􏰀1 achieved 9 days after the initial Fe enrichment, which then decreased back to rates similar to those measured outside of the patch. Changes in primary productivity were also assessed using pulse amplitude-modulated (PAM) fluorometry. Relative electron transport rates (ETR) obtained by PAM fluorometry were significantly correlated (po0.001, r2 1⁄4 0.82) with the 14C-based primary production rates during the Fe enrichment experiment. The increase in all measured photosynthetic parameters with Fe enrichment provides compelling evidence that primary productivity in the NE subarctic Pacific is regulated by Fe availability during the summer.

Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited …

by Robert Strzepek

Maria T. Maldonado, Robert F. Strzepek, Sylvia Sander, Phillip W. Boyd

Though it is clear that plankton in oceanic regions access iron bound to strong organic ligands, the mechanism... more Though it is clear that plankton in oceanic regions access iron bound to strong organic ligands, the mechanism mediating the release of iron from these complexes remains unresolved. In this study, we aim to elucidate the mechanisms of organic iron acquisition by plankton in subantarctic waters. In particular, we investigated the importance of photochemistry in mediating the reductive dissociation of iron from organic complexes, using naturally occurring ligands, and model iron complexes, with different iron-binding groups and photoreactivities. Our results demonstrate that iron within the model ligands is available for uptake and growth by indigenous plankton, but that photolability of these complexes does not determine iron bioavailability. In contrast, light significantly enhances iron acquisition from the in situ ligands, suggesting that the in situ iron ligands are photolabile, and that photochemistry in surface waters may play a significant role in iron uptake from the dissolved organic iron pool by oceanic plankton.

Climate-mediated changes to mixed-layer properties in the Southern Ocean: assessing the phytoplankton response

by Robert Strzepek

P. W. Boyd, S. C. Doney, R. Strzepek, J. Dusenberry, K. Lindsay, and I. Fung

Concurrent changes in ocean chemical and phys- tests/metrics that will reflect the relative plasticity of different... more Concurrent changes in ocean chemical and phys- tests/metrics that will reflect the relative plasticity of different ical properties influence phytoplankton dynamics via alter- phytoplankton functional groups and/or species to respond to ations in carbonate chemistry, nutrient and trace metal inven- changing ocean conditions.
tories and upper ocean light environment. Using a fully cou-
pled, global carbon-climate model (Climate System Model 1.4-carbon), we quantify anthropogenic climate change rela- tive to the background natural interannual variability for the Southern Ocean over the period 2000 and 2100. Model re- sults are interpreted using our understanding of the environ- mental control of phytoplankton growth rates – leading to two major findings. Firstly, comparison with results from phytoplankton perturbation experiments, in which environ- mental properties have been altered for key species (e.g., bloom formers), indicates that the predicted rates of change in oceanic properties over the next few decades are too sub- tle to be represented experimentally at present. Secondly, the rate of secular climate change will not exceed background natural variability, on seasonal to interannual time-scales, for at least several decades – which may not provide the pre- vailing conditions of change, i.e. constancy, needed for phy- toplankton adaptation. Taken together, the relatively subtle environmental changes, due to climate change, may result in adaptation by resident phytoplankton, but not for several decades due to the confounding effects of climate variabil- ity. This presents major challenges for the detection and at- tribution of climate change effects on Southern Ocean phy- toplankton. We advocate the development of multi-faceted

Deciphering diatom biochemical pathways via whole-cell proteomics

by Robert Strzepek

Nunn BL, Aker JR, Shaffer SA, Tsai S, Strzepek RF, Boyd PW, Freeman TL, Brittnacher M, Malmström L, Goodlett DR.

Diatoms play a critical role in the oceans' carbon and silicon cycles; however, a mechanistic understanding of the... more Diatoms play a critical role in the oceans' carbon and silicon cycles; however, a mechanistic understanding of the biochemical processes that contribute to their ecological success remains elusive. Completion of the Thalassiosira pseudonana genome provided 'blueprints' for the potential biochemical machinery of diatoms, but offers only a limited insight into their biology under various environmental conditions. Using high-throughput shotgun proteomics, we identified a total of 1928 proteins expressed by T pseudonana cultured under optimal growth conditions, enabling us to analyze this diatom's primary metabolic and biosynthetic pathways. Of the proteins identified, 70% are involved in cellular metabolism, while 11% are involved in the transport of molecules, We identified all of the enzymes involved in the urea cycle, thereby presenting a complete pathway to convert ammonia to urea, along with urea transporters, and the urea-degrading enzyme urease. Although metabolic exchange between these pathways remains ambiguous, their constitutive presence suggests complex intracellular nitrogen recycling. In addition, all C(4)-related enzymes for carbon fixation have been identified to be in abundance, with high protein sequence coverage. Quantification of mass spectra acquisitions demonstrated that the 20 most abundant proteins included an unexpectedly high expression of clathrin, which is the primary structural protein involved in endocytic transport. This result highlights a previously overlooked mechanism for the inter- and intra-cellular transport of nutrients and macromolecules in diatoms, potentially providing a missing link to organelle communication and metabolite exchange. Our results demonstrate the power of proteomics, and lay the groundwork for future comparative proteomic studies and directed analyses of specifically expressed proteins and biochemical pathways of oceanic diatoms.

An algal photoprotection index and vertical mixing in the Southern Ocean

by Ross Vennell

Journal of Plankton Research, Volume 32, Issue 4, April 2010, Pages 515-527
http://dx.doi.org/10.1093/plankt/fbq003

We explored the relationship between mixing dynamics in the surface mixed layer and the photoprotective response of... more We explored the relationship between mixing dynamics in the surface mixed layer and the photoprotective response of phytoplankton. The distribution of photoprotective pigments was determined at 15 stations in subantarctic waters southeast of New Zealand during austral autumn. The first-order kinetics of the phytoplankton photoprotective response to both light and dark was determined using in situ simulated (deck) incubations. The vertical mixing regime was deduced from two physical parameterizations based on CTD and ADCP profiles. A photophysiological index based on the vertical profile of de-epoxidation state (DES) of the diadinoxanthin-cycle to changes in light intensity was compared with the two physical estimates of vertical eddy diffusivity. For short time scales (<12 h) and within a similar water mass, the DES index provides within one order of magnitude an estimate of average vertical velocity representative of the bulk vertical eddy diffusivity. From the results, a conceptual model is presented of the quantitative relationship between vertical mixing and phytoplankton photoprotection in the water column. This relationship can provide additional insights into the effects of changes in vertical eddy diffusivity in the surface mixed layer on the photoprotective response of phytoplankton.

What is the role and nature of programmed cell death in phytoplankton ecology?

by John Berges

Effects of iron limitation on intracellular cadmium of cultured phytoplankton: Implications for surface dissolved cadmium to phosphate ratios

by Robert Strzepek

Erin S. Lane, David M. Semeniuk, Robert F. Strzepek, Jay T. Cullen and Maria T. Maldonado

This study compares intracellular Cd content (Cd:C) of cultured marine phytoplankton grown under various Fe levels,... more This study compares intracellular Cd content (Cd:C) of cultured marine phytoplankton grown under various Fe levels, with estimated particulate Cd:P ratios derived from regression slopes of Cd versus PO43− relationships from a global dataset. A 66-fold difference in Cd:C ratios was observed among the seven species grown under identical Fe concentrations, with oceanic diatoms having the highest Cd quotas and prymesiophytes the lowest. Interestingly, all species significantly increased their Cd:C ratios under Fe-limitation (on average 2-fold). The global data set also showed that the mean estimated Cd:P ratio of surface water particulates in HNLC (high nutrient low chlorophyll) regions were approximately 2-fold higher than non-HNLC regions. A sequence of events are proposed to explain high Cd:P ratios in HNLC waters. First, the seasonal relief from Fe-limitation in HNLC regions leads to blooms of large chain forming diatoms with high intrinsic Cd:P ratios. These large blooms may, in theory, deplete surface water CO2 and Zn concentrations, which ultimately, would result in increased Cd uptake. Eventually these blooms will run out of Fe, which has been shown to further increase intercellular Cd via growth biodilution and increased Cd uptake through non-specific Fe(II) transporters. Ultimately, Fe-limited diatoms with enhanced Cd quotas will sink out of surface waters leading to pronounced regional differences in Cd:P ratios between HNLC and non-HNLC waters in the global ocean.

Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements

by Robert Strzepek

Robert F. Strzepek, Maria T. Maldonado, Keith A. Hunter, Russell D. Frew, and Philip W. Boyd

We report results of laboratory studies examining the effect of low levels of iron (Fe) availability on the... more We report results of laboratory studies examining the effect of low levels of iron (Fe) availability on the intracellular Fe concentrations and specific growth rates in Southern Ocean diatoms (Fragilariopsis kerguelensis, Eucampia antarctica, Proboscia inermis, and Thalassiosira antarctica) and Phaeocystis antarctica. All species grew on Fe complexed to the siderophore desferrioxamine B (DFB). Concentrations of DFB up to 100-fold in excess of Fe were required to limit growth rates by ~ 50%. Southern Ocean phytoplankton also grew on Fe complexed by ~ 10-fold excess concentrations of the siderophores ferrichrome, enterobactin, or aerobactin, whereas the temperate coastal diatoms Thalassiosira weissflogii and Thalassiosira pseudonana did not. Intracellular Fe concentrations and Fe:C ratios of all Southern Ocean species were exceptionally low and decreased with decreasing Fe availability. However, large diatoms had significantly lower cell-volume–normalized Fe content and Fe : C ratios than Phaeocystis. Short-term Fe uptake and extracellular Fe(II) production measurements provided evidence that Phaeocystis possesses a reductive Fe transport pathway. Our findings demonstrate that the large- diatom Fe requirements are at least 2-fold lower than currently reported for oceanic algal species and suggest that bioreduction may enable resident phytoplankton to directly use Fe bound to strong organic ligands.

Photosynthetic architecture differs in coastal and oceanic diatoms

by Robert Strzepek

Robert F. Strzepek & Paul J. Harrison

Diatoms are a key taxon of eukaryotic phytoplankton and a major contributor to global carbon fixation1. They are... more Diatoms are a key taxon of eukaryotic phytoplankton and a major contributor to global carbon fixation1. They are ubiquitous in the marine ecosystem despite marked gradients in environmental properties, such as dissolved iron concentrations, between coastal and oceanic waters. Previous studies have shown that offshore species of diatoms and other eukaryotic algae have evolved lower iron requirements to subsist in iron-poor oceanic waters, but the biochemical mechanisms responsible for their decreased iron demand are unknown2, 3. Here we show, using laboratory-cultured model species, a fundamental difference between a coastal and an oceanic diatom in their photosynthetic architecture. Specifically, the oceanic diatom had up to fivefold lower photosystem I and up to sevenfold lower cytochrome b 6 f complex concentrations than a coastal diatom. These changes to the photosynthetic apparatus markedly decrease the cellular iron requirements of the oceanic diatom but not its photosynthetic rates. However, oceanic diatoms might have also sacrificed their ability to acclimate to rapid fluctuations in light intensity—a characteristic of dynamic and turbid coastal waters. We suggest that diatoms, and probably other eukaryotic algal taxa, exploited this difference in the underwater light climate between oceanic and coastal waters, enabling them to decrease their iron requirements without compromising photosynthetic capacity. This adaptation probably facilitated the colonization of the open ocean by diatoms, and contributes to their persistence in this iron-impoverished environment.

Photosynthetic iron requirements of marine diatoms

by Robert Strzepek

PhD Thesis, University of British Columbia, 2003

Marine diatoms play a predominant role in the global carbon cycle but their growth is often limited by iron... more Marine diatoms play a predominant role in the global carbon cycle but their growth is often limited by iron availability, especially in some oceanic regions. Diatoms from oceanic waters have lower iron requirements than coastal species, but the biochemical basis for this difference is unknown. The photosynthetic apparatus is a probable source of interspecific variability in iron requirements because it is both iron- rich and highly plastic, but it has not been examined in any oceanic diatom species.
I examined the phenotypic and genotypic variability in diatom iron requirements and measured for the first time the cellular concentrations of photosystems in a coastal and an oceanic diatom (Thalassiosira weissflogii and T. oceanica, respectively) acclimated to a range of irradiances and iron concentrations. Growth and photosynthetic rates, elemental composition, and photosynthetic pigments were measured. Photosynthetic electron transport chain complexes were quantified to construct a photosynthetic iron budget.
In iron-limited diatoms, nearly all the cellular iron was required for photosynthetic electron transport. Consequently, cellular and photosynthetic iron requirements co-varied with growth irradiance. Growth and photosynthetic measurements established that the increased iron requirement of low light acclimated cells did not appreciably heighten their susceptibility to iron limitation, or necessarily result in iron- light co-limitation, because the reduction in growth rate (Fe demand) at low light was greater than the increase in Fe requirements. The diatoms acquired comparatively more iron at low light by uncoupling rates of steady state iron uptake from growth and, in the
coastal diatom, by reducing cell volumes. Instead, diatoms were more iron-stressed growing near their maximum capacity under high irradiances.
The photosynthetic iron requirements of the oceanic diatom were substantially diminished: the cytochrome b6f complex and photosystem I, the most iron-rich complexes, were present at extraordinarily low concentrations compared to those found in coastal diatoms. The concentrations of these complexes were comparably low in Fe- replete cells, demonstrating that their abundance was not a consequence of iron deficiency. These results provide the first biochemical explanation for the low cellular iron requirements of an oceanic phytoplankton species.

Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate

by Robert Strzepek

Johann Lavaud, Robert F. Strzepek, and Peter G. Kroth

In this study, we show a fundamental difference between diatom species from different marine habitats in their ability... more In this study, we show a fundamental difference between diatom species from different marine habitats in their ability to cope with changes in irradiance. Estuarine species show a higher and more flexible capacity for photoprotection than oceanic and coastal species, and when exposed to excess light, the impairment of their photosynthetic capacity because of photoinhibition was reduced. This resulted in maintenance of growth in a fluctuating light regime, conferring the estuarine species an adaptive advantage. The ability of diatoms, and to a larger extent other phytoplankton, to occupy a wide range of ecological niches depends critically on their capacity to exploit the differences in underwater light climate. These results might explain how diatoms adapt to the challenge of maintaining optimal photosynthetic production in turbulent waters, in which the rate of light change is high.

Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae)

by Patrick Brading