Iron speciation in the microenvironment surrounding phytoplankton cells and the consequences for Fe bioavailability

Project Information

Phycosphere Fe

Grant agreement ID: 891418

DOI

10.3030/891418

Project closed

EC signature date 20 April 2020

Start date 1 November 2020

End date 31 October 2023

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 174 806,40

EU contribution

€ 174 806,40

Coordinated by

HELMHOLTZ-ZENTRUM FUR OZEANFORSCHUNG KIEL (GEOMAR)
Germany

Periodic Reporting for period 1 - Phycosphere Fe (Iron speciation in the microenvironment surrounding phytoplankton cells and the consequences for Fe bioavailability)

Reporting period: 2020-11-01 to 2022-10-31

Summary of the context and overall objectives of the project

More than a half of atmospheric CO2 on earth is taken up by phytoplankton, but iron (Fe) limits their growth in large regions of the oceans. Ongoing ocean acidification and global warming would influence Fe-stress in marine phytoplankton and hence the biological carbon fixation. Key existing knowledge gaps are the pathways by which phytoplankton take up Fe, and influences of chemical conditions in the microenvironment surrounding algal cells (i.e. phycosphere) on Fe speciation and bioavailability. This knowledge represents an impediment to understanding the complex effects of climate change on Fe uptake and oceanic carbon fixation.

The overall objective of the project is to understand the relationship between Fe speciation in the phycosphere and Fe bioavailability to phytoplankton under different ocean conditions. The data are key to the assessment of Fe availability to phytoplankton in current and future oceans, and it would improve our ability to model phytoplankton dynamics and predict biological carbon fixation in a changing ocean.

Data from this project show that even in the algae cells of ~5 µm diameter, the pH in the phycosphere is consistently different from bulk seawater. For the first time, it shows that the thickness of the pH boundary layer around phytoplankton cells is largely amplified by ocean acidification. Moreover, the modelling results suggest that the local pH alters Fe speciation in this microenvironment, and in a future more acidic ocean, a much thicker boundary layer would result in a larger deviation of the Fe speciation in the phycosphere from bulk seawater. Overall, this project suggests that precise quantification of chemical conditions in the phycosphere is crucial for better understanding how phytoplankton will respond to environmental changes.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

Work: via the application of a newly developed pH-sensing nano-probe, which allowing high spatial and temporal resolution quantification (down to 50 nm spatial resolution and 2 ms response time), we investigated whether the phycosphere pH of small cells differs from bulk seawater. By determining the phycosphere pH of model marine diatoms, green algae and coccolithophores under different environmental conditions, via changing light, seawater pH and buffering capacity, we studied the underlying mechanisms of phycosphere pH regulation and its responses to ambient environmental changes. Moreover, using newly derived proton and Fe binding constants for marine dissolved organic matter, we investigated the influences of the phycosphere on Fe speciation and its availability to phytoplankton. Finally, we investigated the influences of phycosphere pH, reacitive oxygen species and associated microbes on Fe availability to in situ plankton assemblages.

Main results: under 140 μmol photons·m-2·s-1 the phycosphere pH of Chlamydomonas concordia (5 µm diameter), Emiliania huxleyi (5 µm), Coscinodiscus radiatus (50 µm) and C. wailesii (100 µm) are 0.11 ±0.07 0.20 ±0.09 0.41 ±0.04 and 0.15 ±0.20 (mean ±SD) higher than bulk seawater (pH 8.00) respectively. Thickness of the pH boundary layer of C. wailesii increases from 18 ±4 to 122 ±17 µm when bulk seawater pH decreases from 8.00 to 7.78. Phycosphere pH is regulated by photosynthesis and extracellular enzymatic transformation of bicarbonate, as well as being influenced by light intensity and seawater pH and buffering capacity. The pH change alters Fe speciation in the phycosphere, and hence Fe availability to phytoplankton is better predicted by the phycosphere, rather than bulk seawater. The field data indicate the phycosphere might have little effect on the Fe bio-uptake.

Main dissemination: One research paper has been published in an international leading journal ISME J (i.e. nature.com/articles/s41396-022-01280-1) and the new findings were presented at several international conferences including The Association for the Sciences of Limnology and Oceanography, the Royal Society meeting as well as world-leading universities including Imperial College London.

Data availability and for further exploitation:
The datasets from this project are available in the Figshare repository via the link https://doi.org/10.6084/m9.figshare.19576477.v1.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Originality & Progress:
Much of the attention over past decades has focused on the influence of bulk seawater chemistry on metal biogeochemical cycling, phytoplankton dynamics and functions of oceanic ecosystem. Precise prediction of Fe bioavailability via speciation analyses of bulk seawater remains challenging, and the nature of Fe acquisition from the ambient environment by phytoplankton is poorly understood. The project focused on chemical and biological conditions in the micro-scale phycosphere, within which phytoplankton take up Fe and other nutrients. New knowledges produced from this project are: (1) the pH in the phycosphere of unicellular nano- and micro- phytoplankton cells is consistently different from bulk seawater. (2) the thickness of the pH boundary layer around phytoplankton cells is largely amplified by ocean acidification. (3) the modelling results suggest that the local pH alters Fe speciation in this microenvironment, and in a future more acidic ocean there might be a larger deviation of the Fe speciation in the phycosphere from bulk seawater. (4) bio-uptake of metals including Fe by phytoplankton is better predicted by taking its speciation in the phycosphere into account.

Potential impacts:
Iron bioavailability and dynamics influence phytoplankton community and primary productivity, which are important factors considered by Ecosystem modellers. The insights from this project are likely useful for modelling phytoplankton dynamics and predicting biological carbon fixation in a changing ocean.

a marine diatom