iron :: Ocean Carbon & Biogeochemistry

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Dust-borne iron in the Southern Ocean was more bioavailable during glacial periods

Posted by mmaheigan

· Wednesday, January 23rd, 2019

The Southern Ocean is iron (Fe)-limited, and increased fluxes of dust-borne Fe to the Southern Ocean during the Last Glacial Maximum (LGM) have been associated with phytoplankton growth and CO₂ drawdown. Dust contains different mixes of Fe-bearing minerals, depending on the source region. Fe(II) silicate minerals from physical weathering are more bioavailable than Fe(III) oxyhydroxide minerals from chemical weathering. The Fe(II) silicates are dominant in dust sources that have been weathered from bedrock by glaciers in Patagonia, but the impact of glacial activity on dust-borne Fe speciation (Fe oxidation state and mineral composition) and bioavailability over the last glacial cycle has not previously been quantified.

Figure 1. The fraction of Fe(II) in dust (Fe(II)/Fetotal, dominated by Fe(II) silicates, shown as blue dots connected with dotted lines on blue axes) in marine sediment cores from (A) the South Atlantic and (B) the South Pacific plotted with the total dust flux (grey lines on grey axes).

A recent study in PNAS reconstructs the speciation of dust-borne Fe over the last glacial cycle in South Atlantic and South Pacific marine sediment cores using Fe K-edge X-ray absorption spectroscopy. The authors observed that the highly bioavailable Fe(II) silicate content of dust-borne Fe is higher in both regions during cold glacial periods, suggesting that a given flux of Fe is more bioavailable in glacial versus interglacial periods (Figure 1). Therefore, all Fe cannot be considered equal in biogeochemical models working on glacial-interglacial timescales. The bioavailability of a given flux of Fe at the LGM was likely a dominant driver of phytoplankton growth, with more bioavailable Fe driving increased phytoplankton activity and associated atmospheric CO₂ drawdown and subsequent cooling. The observed association between glacial periods and increased Fe bioavailability in the Southern Ocean may indicate an important positive feedback mechanism between glacial activity and cold glacial temperatures through Fe speciation and the efficiency of the biological pump.

Paper link: https://doi.org/10.1073/pnas.1809755115

Authors:
Elizabeth M. Shoenfelt (Lamont-Doherty Earth Observatory, Columbia University)
Gisela Winckler (Lamont-Doherty Earth Observatory, Columbia University)
Frank Lamy (Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research)
Robert F. Anderson (Lamont-Doherty Earth Observatory, Columbia University)
Benjamin C. Bostick (Lamont-Doherty Earth Observatory, Columbia University)

Constraints on glacial overturning circulation and export production lead to answers about the carbon cycle

Posted by mmaheigan

· Friday, January 4th, 2019

One of the biggest unsolved mysteries in climate science concerns the dynamics and feedbacks of the ice age carbon dioxide (CO₂) cycle.

At the height of the Pleistocene ice ages, the atmospheric CO₂ concentration was about 1/3 lower than during the warm interglacial periods. Most scientists think that the CO₂ that was missing from the atmosphere was in the deep ocean, but how and why remains unclear. In a study published in Earth and Planetary Science Letters, we compared different computer simulations of the ice age ocean with δ¹³C, radiocarbon (¹⁴C), and δ¹⁵N data from sea floor sediments.

We find that a weak and shallow Atlantic Meridional Overturning Circulation (6-9 Sv, or approximately half of today’s overturning rate) best reproduces the glacial sediment isotope data. Increasing the atmospheric soluble iron flux in the model’s Southern Ocean intensifies export production, carbon storage, and further improves agreement with glacial δ¹³C and δ¹⁵N reconstructions.

Figure Caption: Depth profiles of global mean δ13C, calculated using only grid boxes for which there exists Last Glacial Maximum data. Blue: Weak Atlantic circulation; Red: Strong Atlantic circulation; Green: Collapsed Atlantic circulation; Dashed: Extra iron in the Southern Ocean; Orange: Last Glacial Maximum Data.

Our best-fitting simulation (blue, dashed line in the figure) is a significant improvement over previous studies and suggests that both circulation and export production changes were necessary to maximize carbon storage in the glacial ocean. These findings provide an equilibrium glacial state, consistent with a combination of proxies, that can be used as a basis for simulations covering the last deglaciation time period. Understanding the different states that the global climate system can transit, and the characteristics of the transitions, is crucial to project possible outcomes of current climate change processes.

Authors:
Juan Muglia (Oregon State University)
Luke C. Skinner (Godwin Laboratory for Palaeoclimate Research, University of Cambridge)
Andreas Schmittner (Oregon State University)

New BioGEOTRACES data sets: Connecting pieces of the microbial biogeochemical puzzle

Posted by mmaheigan

· Wednesday, December 19th, 2018

Microorganisms play a central role in the transfer of matter and energy in the marine food web. Microbes depend on micronutrients (e.g. iron, cobalt, zinc, and a host of other trace metals) to catalyze key biogeochemical reactions, and their metabolisms, in turn, directly affect the cycling, speciation, and bioavailability of these compounds. One might therefore expect that marine microbial community structure and the functions encoded within their genomes might be related to trace metal availability in the ocean. The overall productivity of marine ecosystems—i.e. the amount of carbon fixed through photosynthesis—could in turn be influenced by trace metal concentrations.

For over a decade, the international GEOTRACES program has been mapping the distribution and speciation of trace metals across vast ocean regions. Given the important relationship between trace metals and the function of marine ecosystems, biological oceanographers collaborate with GEOTRACES scientists to simultaneously probe the biotic communities at some sampling sites, allowing these biological data to be interpreted in the context of detailed chemical and physical measurements.

Figure 1. Locations and depths of samples. (a) Global map of sample locations. Single cell genomes are represented by miniaturized stacked dot-plots (each dot represents one single cell genome), with organism group indicated by color, and cells categorized as “undetermined” if robust placement within known phylogenetic groups failed due to low assembly completeness/quality or missing close references. Larger points correspond to stations on associated GEOTRACES sections where metagenomes were also collected. (b) Depth distribution of metagenome samples along each of the four GEOTRACES sections. Transect distances are calculated relative to the first station sampled in the indicated orientation. For clarity, the depth distribution of samples collected below 250 m are not shown to scale (ranging from 281–5601 m). Adapted from Berube et al. (2018) Sci. Data 5:180154 and Biller et al. (2018) Sci. Data 5:180176.

Two recent papers published in Scientific Data describes two new, large-scale biological data sets that will facilitate studies aimed at understanding how microbes and metals relate to one another. Collected on four different sets of GEOTRACES cruises (Figure 1), these papers report the public availability of hundreds of single cell genomes and microbial community metagenomes from the Pacific and Atlantic Oceans. The single cell genomes focus on the marine photosynthetic bacteria Prochlorococcus and Synechococcus and how they and other community members vary in different regions of the ocean. The metagenomic sequences provide snapshots of the entire microbial community found in each of these samples, yielding a broad overview of which microbes—and which genes, including those important for understanding nutrient cycling—are found in each sample. These two datasets are complementary and further enhanced by the wealth of chemical and physical data collected by GEOTRACES scientists on the same water samples. In particular, iron is of key interest, since it often limits primary productivity. These data sets can directly link iron availability with microbial community structure and gene content across ocean basins.

With these data, researchers can now ask questions such as how microbes have evolved in response to the availability or limitation of key nutrients and explore which organisms may be contributing to biogeochemical cycles in different parts of the global ocean. The extensive suite of chemical and physical measurements associated with these sequence data underscore their potential to reveal important relationships between trace metals and the microbial communities that drive biogeochemical cycles. These data sets also encourage cross-disciplinary collaborations and provide baseline information as society faces the challenges and uncertainties of a changing climate.

Authors:
Paul M. Berube (Massachusetts Institute of Technology)
Steven J. Biller (Massachusetts Institute of Technology; current affiliation: Wellesley College)
Sallie W. Chisholm (Massachusetts Institute of Technology)

Dramatic Increase in Chlorophyll-a Concentrations in Response to Spring Asian Dust Events in the Western North Pacific

Posted by mmaheigan

· Tuesday, October 23rd, 2018

According to Martin’s iron hypothesis, input of aeolian dust into the ocean environment temporarily relieves iron limitation that suppresses primary productivity. Asian dust events that originate in the Taklimakan and Gobi Deserts occur primarily in the spring and represent the second largest global source of dust to the oceans. The western North Pacific, where productivity is co-limited by nitrogen and iron, is located directly downwind of these source regions and is therefore an ideal location for determining the response of open water primary productivity to these dust input events.

Figure 1. Daily aerosol index values (black squares) and chlorophyll-a concentrations (mg m-3, circles) during the spring (a) 2010 (weak dust event), (b) 1998 (strong dust event) in the western North Pacific. Color scale represents difference between mixed layer depth (MLD) and isolume depth (Z0.054) that indicates conditions for typical spring blooms; water column structures of MLD and isolume were identical in the spring of 1998 and 2010. Dramatic increases in chlorophyll-a (pink shading, maximum of 5.3 mg m-3) occurred in spring 1998 with a lag time of ~10 days after the strong dust event (aerosol index >2.5) on approximately April 20 compared to constant chlorophyll-a values (<2 mg m-3) in the spring of 2010.

A recent study in Geophysical Research Letters included an analysis of the spatial dynamics of spring Asian dust events, from the source regions to the western North Pacific, and their impacts on ocean primary productivity from 1998 to 2014 (except for 2002–2004) using long-term satellite observations (daily aerosol index data and chlorophyll-a). Geographical aerosol index distributions revealed three different transport pathways supported by the westerly wind system: 1) Dust moving predominantly over the Siberian continent (>50°N); 2) Dust passing across the northern East/Japan Sea (40°N‒50°N); and 3) Dust moving over the entire East/Japan Sea (35°N‒55°N). The authors observed that strong dust events could increase ocean primary productivity by more than 70% (>2-fold increase in chlorophyll-a concentrations, Figure 1) compared to weak/non-dust conditions. This result suggests that spring Asian dust events, though episodic, may play a significant role in driving the biological pump, thus sequestering atmospheric CO₂ in the western North Pacific.

Another recent study reported that anthropogenic nitrogen deposition in the western North Pacific has significantly increased over the last three decades (i.e. relieving nitrogen limitation), whereas this study indicated a recent decreasing trend in the frequency of spring Asian dust events (i.e. enhancing iron limitation). Further investigation is required to fully understand the effects of contrasting behavior of iron (i.e., decreasing trend) and nitrogen (i.e., increasing trend) inputs on the ocean primary productivity in the western North Pacific, paying attention on how the marine ecosystem and biogeochemistry will respond to the changes.

Authors:
Joo-Eun Yoon (Incheon National University)
Il-Nam Kim (Incheon National University)
Alison M. Macdonald (Woods Hole Oceanographic Institution)

Widespread nutrient co-limitation discovered in the South Atlantic

Posted by mmaheigan

· Thursday, March 15th, 2018

Unicellular photosynthetic microbes—phytoplankton—are responsible for virtually all oceanic primary production, which fuels marine food webs and plays a fundamental role in the global carbon cycle. Experiments to date have suggested that the growth of phytoplankton across much of the ocean is limited by either nitrogen or iron. But simultaneously low concentrations of these and other nutrients have been measured over large areas of the open ocean, raising the question: Are phytoplankton communities only limited by a single nutrient?

Authors of a study recently published in Nature tested this by conducting nutrient addition experiments on a GEOTRACES cruise in the nutrient-deficient South Atlantic gyre. Seawater samples were amended with nitrogen, iron, and cobalt both individually and in various combinations. Concurrent nitrogen and iron addition stimulated increased phytoplankton growth, yielding a ~40-fold increase in chlorophyll a. Supplementary addition of cobalt or cobalt-containing vitamin B₁₂ further enhanced phytoplankton growth in several experiments.

Experiments conducted throughout the southeast Atlantic GEOTRACES GA08 cruise transect (left panel) demonstrated that nitrogen and iron had to be added to significantly stimulate phytoplankton growth (right panel). Supplementary addition of cobalt (or cobalt-containing vitamin B12) stimulated significant additional growth.

In addition to co-limited sites, the study identified ‘singly’ and ‘serially’ limited sites. These limitation regimes could be predicted by the measured ambient seawater nutrient concentrations, demonstrating the potential for using nutrient datasets to make confident predictions about limitation at larger spatial scales, an approach that is being more widely used in programmes like GEOTRACES,.

Finally, a complex, state-of-the-art biogeochemical ocean model suggested a much smaller extent of nutrient co-limitation than the experiments indicated. Authors attributed this to relatively restricted microbial and nutrient diversity in the model. These findings have implications for how such models are constructed if they are to represent nutrient co-limitation in the ocean and accurately project changes in ocean productivity in the future.

Authors:
Thomas J. Browning (GEOMAR)
Eric P. Achterberg (GEOMAR)
Insa Rapp (GEOMAR)
Anja Engel (GEOMAR)
Erin M. Bertrand (Dalhousie University)
Alessandro Tagliabue (University of Liverpool)
Mark Moore (University of Southampton)

The sea surface microlayer in a future ocean

Posted by mmaheigan

· Tuesday, November 28th, 2017

The sea surface microlayer (SML) is the boundary interface between the atmosphere and ocean, spanning the uppermost ~1 mm of the ocean. Covering 70% of the Earth’s surface, the SML supports a rich diversity of life, serving as an incubator for eggs and larvae. The SML controls air-sea interactions and serves as an important hotspot of microbially mediated biochemical activity. A recent review paper by Wurl et al. highlights the important role of the SML in climate and ecosystem function and how it might change in the future.

Figure Caption: The sea surface microlayer comprises a complex biofilm and serves as a biochemical micro-reactor with distinct microbial communities and short-term carbon accumulation.

The SML is directly exposed to meteorological forces such as UV radiation, precipitation, and diurnal warming. Since these forces will be impacted by climate change, the SML is also likely to experience changes in the future. For example, projected increases in primary productivity in the upper sunlit layer of the ocean may enhance the supply of surface-active organic material to the SML with accompanying feedbacks on the molecular diffusion and conduction processes that drive exchange of heat and climate-relevant gases such as CO₂ between the ocean and atmosphere. Furthermore, changes in UV flux may enhance the SML’s role as a biochemical reactor in which unique microbial communities and photochemical reactions occur, including the transformation of deposited atmospheric particles like dust into bioavailable nutrients like iron to fuel phytoplankton production. Increasing levels of manmade pollutants such as pharmaceuticals and micro-plastics are accumulating in the SML. These and other pollutants have the potential to disrupt biochemical and photochemical processes in the SML, as well as the unique and diverse food webs it supports.

Moving forward, novel techniques and a holistic approach will be needed to improve our understanding of highly complex SML dynamics. Multidisciplinary data sets that link microbial community structure and function with biogeochemistry will be needed, and eventually, the SML should be included in computer models used to forecast future changes in climate, marine ecosystems, and biogeochemistry.

Authors:
Oliver Wurl (Carl von Ossietzky Universität Oldenburg, Institute for Chemistry and Biology of the Marine Environment)
Werner Ekau (Leibniz Centre for Tropical Marine Research, Bremen)
William M. Landing (Florida State University, Department of Earth, Ocean, and Atmospheric Science)
Christopher J. Zappa (Lamont-Doherty Earth Observatory, Columbia University)

Role for iron in controlling microbial phosphorus acquisition in the ocean

Posted by mmaheigan

· Thursday, October 12th, 2017

In the subtropical North Atlantic, dissolved inorganic phosphorus (DIP) concentrations are depleted and might co-limit N₂ fixation and microbial productivity. There are relatively large pools of dissolved organic phosphorus (DOP), but microbes need an enzyme to access this P source. One such alkaline phosphatase (APase) enzyme requires zinc (Zn) as its activating cofactor. This has been known for almost 30 years. However, recent crystallography studies revealed that two other widespread APase enzymes contain Fe. Via this requirement, Fe availability could regulate microbial access to the DOP pool.

As detailed in a recent publication in Nature Communications (Browning et al. 2017), this hypothesis was tested on a cruise across the tropical North Atlantic by adding Fe and Zn to incubated seawater and monitoring changes in bulk APase using a simple fluorescence assay. Adding Fe significantly increased APase activity in seawater samples collected in areas that were far-removed from coastal and aerosol Fe sources. Despite seawater Zn concentrations being much lower than Fe, it appeared not to be limiting.

Iron (Fe) and zinc (Zn) enrichment experiments conducted in the DIP-depleted tropical North Atlantic suggested that Fe, not Zn, could limit alkaline phosphatase activity (APA). DIP*=DIP–DIN/16, and represents excess DIP availability assuming a 16-fold higher microbial N requirement. Results in the bar chart represent a subset of treatments from one experiment (out of eight conducted).

DIP is depleted in surface waters of the tropical North Atlantic because inputs of North African aerosol Fe stimulates N₂ fixation and leads to microbial drawdown of DIP. If the modern ocean is a good analog for the past, the lack of APase stimulation following experimental Zn addition could reflect limited evolutionary selection for Zn-containing APase. In general, DIP is only substantially depleted where there is enhanced Fe input fueling N₂ fixation; it therefore follows that any significant requirement for APases might be restricted to these relatively high-Fe, low-Zn waters.

On a shorter timescale, growing anthropogenic nitrogen input to the ocean relative to phosphorus could result in more prevalent oceanic phosphorus deficiency. Corresponding iron inputs might then serve as an important control on phosphorus availability for microbes in these regions.

Authors:

Tom Browning (GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany)
Eric Achterberg (GEOMAR)
Jaw Chuen Yong (GEOMAR)
Insa Rapp (GEOMAR)
Caroline Utermann (GEOMAR)
Anja Engel (GEOMAR)
Mark Moore (Ocean and Earth Science, University of Southampton, Southampton, UK)

Sinking particles as biogeochemical hubs for trace metal cycling and release

Posted by mmaheigan

· Thursday, September 14th, 2017

The extent to which the return of major and minor elements to the dissolved phase in the deep ocean (termed remineralization) is decoupled plays a major role in setting patterns of nutrient limitation in the global ocean. It is well established that major elements such as phosphorus, silicon, and carbon are released at different rates from sinking particles, with major implications for nutrient recycling. Is this also the case for trace metals?

A recent publication by Boyd et al. in Nature Geoscience provides new insights into the biotic and abiotic processes that drive remineralization of metals in the ocean. Particle composition changes rapidly with depth with both physical (disaggregation) and biogeochemical (grazing; desorption) processes leading to a marked decrease in the total surface area of the particle population. The proportion of lithogenic metals in sinking particles also appears to increase with depth, as the biogenic metals may be more labile and hence more readily removed.

Findings from GEOTRACES process studies revealed that release rates for trace elements such as iron, nickel, and zinc vary from each other. Microbes play a key role in determining the turnover rates for nutrients and trace elements. Decoupling of trace metal recycling in the surface ocean and below may result from their preferential removal by microbes to satisfy their nutritional requirements. In addition, the chemistry operating on particle surfaces plays a pivotal role in determining the specific fates of each trace metal. Teasing apart these factors will take time, as there is a complex interplay between chemical and biological processes. Improving our understanding is crucial, as these processes are not currently well represented by state-of-the-art ocean biogeochemical models.

Figure caption: Rapid changes in the characteristics of sinking particles over the upper 200 m as evidenced by: a) differential release of trace metals from sinking diatoms; b) changes in proportion of lithogenic versus biogenic materials; and c) ten-fold decrease in total particle surface area.

Authors:
Philip Boyd (IMAS, Australia)
Michael Ellwood (ANU, Australia)
Alessandro Tagliabue (Liverpool, UK)
Ben Twining (Bigelow, USA)

Relevant links:
GEOTRACES Digest: Iron Superstar

Joint workshop with GEOTRACES in August 2016: Biogeochemical Cycling of Trace Elements within the Ocean

Using GEOTRACES data to appraise iron cycling as represented within global ocean models

Posted by mmaheigan

· Thursday, June 23rd, 2016

We rely on global ocean models to predict how climate change might affect the evolution of ocean productivity, acidification, and deoxygenation (1). Such platforms are also used to test hypotheses regarding the controls on ocean biogeochemical cycling and to understand past change (both on historical and geologic timescales). Ocean biogeochemistry models began with relatively simple formulations of a carbon export flux that involved restoring to observed phosphate distributions, but have more recently evolved into complex multi-element representations of the ocean. In line with our understanding that the trace micronutrient iron (Fe) limits phytoplankton productivity over large areas of the world ocean (2), most global models that aim to project future change also explicitly represent the Fe cycle.

Datasets regarding the major limiting nutrients (nitrate, phosphate, and silicate) have been available as gridded ‘climatologies’ since the early 1990s (3). This has greatly facilitated the development and evaluation of modelled distributions over the past two decades. However, over this period there has been little comprehensive evaluation of how different models represent the ocean Fe cycle. Over recent years, there has been a marked increase in the availability of iron measurements in the ocean (4), largely driven by the international GEOTRACES effort to conduct full depth, basin-scale surveys. This led us to initiate the first-ever attempt to critically compare a range of global ocean iron models against the largest global datasets, as well as against the newly emerging ocean section data (5).

The Fe Model Intercomparison Project (FeMIP) sought to be as inclusive as possible in this first step and therefore did not seek to standardize the underlying ocean circulation or external inputs. Instead, we simply asked each of the thirteen models to provide their best representation of dissolved iron in three dimensions at monthly resolution. We then compared these models against each other, a global iron database of over 20,000 observations and against five unique basin-scale sections from the GEOTRACES intermediate data product 2014 (IDP2014) (6).

Firstly, it is apparent that even when the underlying iron cycles of the different models are evaluated, a substantial degree of inter-model discord exists. The total iron input varies from around 2 to 200 Gmol yr-1 across the thirteen models (Fig. 1a). Even for ‘well known’ sources like atmospheric deposition, the inter-model variability is around an order of magnitude. On the other hand, the average concentrations of dissolved Fe between the models is much less variable and ranges from 0.35 to 0.81 nmol L-1 (Fig. 1b), or an average of 0.58±0.14 nmol L-1. This apparent constancy reflects an initial view of the ocean Fe cycle in which interior Fe concentrations were held at a quasi-constant value of 0.6 nmol L-1 assuming a constant concentration of Fe-binding ligands (7). Thus the FeMIP models are balancing widely varying Fe input fluxes against relatively constant overall Fe concentrations by tuning the Fe scavenging rate, which is a crucial but poorly known parameter. This results in residence times for Fe that range from <5 to >500 years across the FeMIP models (Fig 1c). This difference is important, as it represents substantial inter-model deviation concerning the timescales over which the different models respond to a perturbation in Fe supply.

When compared statistically against the global dataset, similar levels of variability arise. Some models display correlation coefficients of >0.5, whereas others are slightly anti-correlated. When the FeMIP models are compared against the five GEOTRACES sections, it becomes apparent that those models that represent the newly emerging features of the iron cycle perform much better. For instance, having Fe scavenging rates that vary in space and time, including variable Fe:carbon (C) stoichiometry, multiple Fe sources, and representing ligand concentrations in a dynamic manner, all act to improve the representation of different observed features in the models. Importantly, the IDP2014 provided the opportunity to demonstrate that the issues at hand were specific to Fe, since the models could represent the observed distributions of major nutrients with a much greater degree of skill (5).

The next stage of FeMIP will be a deeper comparison of the processes themselves. Of particular interest is whether GEOTRACES datasets can provide broader assessments of the rates of Fe scavenging – e.g., using other particle-reactive, non-biological tracers such as thorium (8, 9). Equally, the emerging database of GEOTRACES process studies provides an important opportunity to appraise the way different models represent biological iron cycling and in particular, the often-observed importance of recycled and remineralized sources of Fe (10, 11). Finally, the new GEOTRACES intermediate data product 2017 will also facilitate further evaluation of models, providing new section data from the Atlantic, Pacific and Arctic Oceans.

Author

Alessandro Tagliabue (Dept. of Earth, Ocean and Ecological Sciences, School of Environmental Sciences, University of Liverpool)

References

1. L. Bopp et al., Biogeosci. 10(10), 6225-6245, doi:10.5194/bg-10-6225-2013 (2013).
2. C. M. Moore et al., Nature Geosci., doi:10.1038/ngeo1765 (2013).
3. S. Levitus et al., Prog. Oceanogr. 31(3), 245-273, doi:10.1016/0079-6611(93)90003-v (1993).
4. A. Tagliabue et al., Biogeosci. 9(6), 2333-2349, doi:10.5194/bg-9-2333-2012 (2012).
5. A. Tagliabue, A. et al., Glob. Biogeochem. Cycles, doi:10.1002/2015gb005289 (2016).
6. E. Mawji et al., Marine Chem. 177, 1-8. doi:10.1016/j. marchem.2015.04.005 (2015).
7. K. S. Johnson, R. M. Gordon, K. H. Coale, Marine Chem. 57(3-4), 137-161, doi:10.1016/s0304-4203(97)00043-1 (1997).
8. C. T. Hayes et al., Geochim. Cosmochim. Acta 169, 1-16, doi:10.1016/j.gca.2015.07.019 (2015).
9. N. Rogan et al., Geophys. Res. Lett. 43(6), 2732-2740. doi:10.1002/2016gl067905 (2016).
10. P. W. Boyd et al., Glob. Biogeochem. Cycles 29(7), 1028-1043, doi:10.1002/2014gb005014 (2015).
11. R. F. Strzepek et al., Glob. Biogeochem. Cycles 19(4), GB4S26, doi:10.1029/2005gb002490 (2005).

Exploring molecular methods for assessing trace element bioavailability in phytoplankton

Posted by mmaheigan

· Saturday, June 4th, 2016

This summer OCB and GEOTRACES are co-sponsoring a synthesis workshop on the biogeochemical cycling of trace elements in the ocean. The overall goal of the workshop is to bring together expertise from across the field of oceanography to take advantage of the growing datasets of trace elements in the ocean and explore biological-chemical-physical underpinnings of trace element cycling within the ocean. One of the three main themes that will be addressed at the workshop is “biological uptake and trace element bioavailability.” Part of this theme will include a discussion of how molecular markers have been used to address questions of trace element bioavailability in the past and the exciting future for continued efforts in this area given the growing molecular toolkit.

As a starting point to open the door to this broad discussion topic, let us turn our attention to how molecular methods have been used to evaluate iron (Fe) bioavailability to certain phytoplankton groups. Marine phytoplankton play a key role in the global carbon cycle by performing a significant fraction of global primary production (1). Since John Martin’s groundbreaking work introduced the concept that Fe is a limiting nutrient for phytoplankton growth (2), numerous studies have shown that insufficient Fe limits primary productivity in the major high-nitrate, low-chlorophyll (HNLC) regions of the ocean, and that Fe availability can regulate phytoplankton processes in many other oceanic settings (3, 4). Fe is a critical micronutrient required by phytoplankton for a Exploring molecular methods for assessing trace element bioavailability in phytoplankton Dreux Chappell (Old Dominion Univ.) multitude of cellular tasks, including electron transfer in photosynthesis and respiration, as well as macronutrient acquisition and assimilation (5). Studies of Fe limitation in marine environments beyond the traditional HNLC regions suggest that Fe limitation may be driven not simply by low Fe concentrations, but a combination of low Fe bioavailability coupled with high macronutrient supply (e.g., 6, 7). In an admittedly overly simplified summary, the different pools of Fe present in the ocean are defined based on filter pore-size cut-offs and chemical interactions with organic compounds (3). Knowledge of the distribution of these various forms of Fe in the oceans has increased dramatically in recent years thanks to coordinated sampling efforts like GEOTRACES.

While the bioavailability of Fe to phytoplankton is believed to be different for the various Fe pools, there is still no clear consensus as to which, if any, pools of Fe are always bioavailable and which, if any, are completely unavailable (8, 9). Additionally, it is known that all phytoplankton are not created equal with respect to their ability to persist under low-Fe conditions (10) and access different Fe pools (9). These factors make it difficult to accurately predict how changing concentrations of the different pools of Fe may impact phytoplankton productivity in a changing ocean. One way to address questions about biological availability is to use phytoplankton themselves as in situ indicators of Fe stress. An approach that appears promising in addressing these questions of bioavailability of Fe to individual phytoplankton species is the development of species-specific molecular markers of Fe limitation such as those that have been developed for the oceanic diatom Thalassiosira oceanica (11), and for the two main groups of the nitrogen-fixing cyanobacterial genus Trichodesmium (12). These assays in particular follow the expression of genes that encode flavodoxin, a non-Fe-containing protein that phytoplankton are known to substitute for the Fe-containing ferrodoxin protein to maintain photosynthetic electron transport under Fe-limiting conditions (13). They focus on gene expression analysis rather than protein analysis, as many phytoplankton have multiple genes that encode for flavodoxin proteins and, at least in diatoms, not all gene copies are sensitive to Fe (14).

The Trichodesmium assays were calibrated using cultures grown with six different concentrations of Fe in the media. In laboratory cultivation experiments, gene expression was shown to be inversely proportional to Fe present in the media and expression was downregulated when Fe was fed back to Fe-limited cultures (12). The Trichodesmium thiebautii assay was further used to evaluate field populations from open ocean samples collected globally (15), providing insights into Fe bioavailability to wild populations of Trichodesmium. Overall, there was an inverse correlation between gene expression and total dissolved Fe concentrations (Fig. 1). Comparing the results with the laboratory calibration led to the conclusion that most of the dissolved Fe, including organically bound Fe, was available to T. thiebautii. An intriguing result from this study was that one sample collected in the plume of the Amazon River had significantly higher gene expression than would be expected based on the measured dissolved Fe at that site (Fig. 1; 15). These findings suggest that there is a fraction of the dissolved Fe in the Amazon River plume that is not bioavailable to T. thiebautii, the clade of Trichodesmium that is more abundant and active in the open ocean (15, 16).

The T. oceanica assay is also highly sensitive to Fe with high gene expression in cultures that were Fe-limited, a rapid reduction of gene expression following an Fe pulse to Fe-limited cultures, and no induction of expression by macronutrient limitation (11). Using this method on field samples from the northeast Pacific Ocean, T. oceanica flavodoxin expression was found to be highest in samples with low measured dissolve Fe and vice versa (11). Two notable exceptions to this trend were samples collected along the shallow shelf of Haida Gwaii, stations 26 and 27, which showed anomalously high expression of both genes despite high measured dissolved Fe (Fig. 2), suggesting that something about the dissolved Fe in these shallow coastal stations made it unavailable to the T. oceanica in these waters. It should be noted that T. oceanica is an oceanic diatom species, so both sets of findings suggest that there is a fraction of dissolved Fe from a terrestrially influenced water sample that was not bioavailable to a species of oceanic phytoplankton.

While these two datasets are intriguing, they are limited in scope and admittedly raise more questions than they answer. There are a variety of questions that stem from these results, including what, if anything, is different about the dissolved Fe at these stations? Was this coastal/terrestrially sourced Fe unavailable because only oceanic phytoplankton, which rarely encounter dissolved Fe from terrestrial sources, were queried? Did coastal phytoplankton simply outcompete the oceanic phytoplankton for access to the dissolved Fe perhaps because they have different or more efficient Fe uptake mechanisms? Would an assay targeting coastal phytoplankton reveal the same results? We know that coastal diatoms have significantly higher Fe requirements (10). What if coastal and oceanic phytoplankton also differ in their abilities to access Fe from different sources? A recent study in the Sea of Okhotsk yielded a significant correlation between a bulk diatom community indicator of Fe stress and dissolved Fe with increasing distance from the mouth of the Amur River, suggesting that the riverine Fe was bioavailable to the community that was dominated by coastal diatoms (17).

A number of recent advances in molecular microbial oceanography are making it increasingly possible to start answering these types of questions on a broader scale. A major sequencing effort that was completed in 2014, the Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP), added a wealth of data on the functional genetic diversity of marine microeukaryotes (18). The project resulted in over 650 publicly available transcriptomes from over 250 genera of marine microeukaryotes. Even before all the transcriptomes from the project were released, data mining of a limited portion of the MMETSP publically available dataset yielded valuable information as to the varied Fe management strategies utilized by different species of marine diatoms, creating a list of additional potential molecular markers for evaluating Fe nutritional status of diatoms in the field (19). Another data mining technique that has proven useful in identifying coordinated transcriptional responses in diatoms has involved the application of clustering algorithms to evaluate publically available microarray data for two of the more commonly studied diatom species, Phaeodactylum tricornutum and Thalassiosira pseudonana, grown under a wide variety of conditions (20). New insights into the diatom Fe stress response and Fe uptake mechanisms have also been gained through combining physiological experiments with genetic knockdowns of previously uncharacterized Fe responsive genes (21). These new molecular advances are providing a suite of new potential targets for querying the physiological status of phytoplankton present throughout the global ocean. At the OCB/GEOTRACES synthesis workshop on the biogeochemical cycling of trace elements in the ocean, the conversation will include a discussion of how to effectively combine these new analyses with the growing datasets of bioactive trace elements to answer questions regarding the biological availability of different trace element pools. While this mini-review has focused on Fe, additional trace elements will be discussed at the meeting in August.

Author

Dreux Chappell (Old Dominion University)

References

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Funding for the Ocean Carbon & Biogeochemistry Project Office is provided by the National Science Foundation (NSF) and the National Aeronautics and Space Administration (NASA). The OCB Project Office is housed at the Woods Hole Oceanographic Institution.

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