Single cell carbon and nitrogen dynamics in chain forming diatoms, including their resting stage
Abstract
The oceans are a fundamental part of all life on earth, accounting for more than half of Earth’s oxygen production. The ocean is also key to long term carbon dioxide sequestration. Diatoms are a group of phytoplankton differentiated by their silica shell/frustule and account for ~20% of global primary production. Some of these diatoms form colonies/chains which are viewed as a way to reduce grazing pressure, but also effect aggregation, sedimentation, and nutrient assimilation. Exponential growth conditions during algae blooms have been well studied. Less is known about how they survive between blooms when conditions are no longer optimal. In nature, high nutrient availability in the photic zone and subsequent blooms only last a few weeks. Growth limited conditions persist for most of the year.
In chapter I and II, shifts in carbon and nitrogen assimilation dynamics were investigated in two chain forming diatoms: Chaetoceros affinis (I) and Skeletonema marinoi (II) at the beginning of nitrate limitation. C. affnis which are often larger than S. marinoi and are relatively more abundant during summer conditions with low nitrate availability. Skeletonema produce smaller cells and dominate at the beginning of blooms, where they thrive and assimilate excess nitrogen. C. affinis produced exudates of sugars and was colonized by attached bacteria that assimilated both carbon and nitrogen derived from their host. Later, diatoms were remineralised by bacteria, releasing ammonium. This ammonium could balance carbon assimilation for active diatoms. I speculate that cells in chains could benefit from remineralization of other cells in the chain and supply active cells with ammonium. S. marinoi showed no difference in carbon and nitrogen assimilation depending on chain length. The cells assimilated nitrate at a rate 25-65 times lower than the diffusive supply could provide, when compared to modelled diffusive supply from the ambient water. This indicated that cells were limited by biological uptake rates rather than diffusive supply. In chapter I and II, I demonstrated that C. affinis and S. marinoi had different ways of dealing with nitrate limitation, corresponding to the niches they fill. C. affinis recirculate the nitrogen with help of bacteria, which would allow them to keep a standing population in low nitrogen availability between blooms. S. marinoi on the other hand assimilated an excess of nitrogen during high availability, where they usually dominate.
In addition to playing a key role in primary production and nutrient turnover, diatoms also contribute to particle transport from the photic zone to the sediment. Diatoms form resting stages which can survive decades to centuries in dark and anoxic sediments. Mechanism of survival is unknown, and they have previously been considered as “dormant” in the sediment. Basic mechanisms for cell maintenance in resting stages of S. marinoi were investigated in chapter III. I showed that they were able to assimilate both nitrate and ammonium in dark and anoxic conditions. The nitrogen specific generation time varied between 23-500 years which may be enough to maintain viable cells, but not for growth. In chapter IV, I investigated if resting stages could use nitrate as an electron acceptor and assimilate organic molecules available in the sediment (acetate and urea). The resting stages performed dissimilatory nitrate reduction to ammonium (DNRA) and assimilated N from urea. They could not assimilate carbon from urea but assimilated carbon from acetate. Hence, the sediment provides resting stages with both carbon and nitrogen for assimilation and respiration. I have shown that diatom resting stages are not as dormant as previously assumed. I also showed that two common chain forming diatoms have different mechanisms of circumventing reliance on nitrate diffusion from the ambient water. The next step is to connect this to marine monitoring and prediction models taking chain formation into account. This thesis has only scratched the surface on chain forming diatoms responses to adverse conditions. Considering the large diversity of chain forming diatoms, the responses to such conditions may be equally diverse.
Parts of work
Chapter I: Stenow, R., Robertson, K. E., Whitehouse, J. M., & Ploug, H. Single cell dynamics and nitrogen transformation in diatom chains and solitary cells. ISME Journal. [In revision] Chapter II: Stenow, R., Olofsson, M., Whitehouse, J. M., & Ploug, H., Single cell carbon and nitrogen assimilation in the chain forming diatom Skeletonema marinoi. [Manuscript in preparation for Limnology and Oceanography] Chapter III: Stenow, R., Olofsson, M., Robertson, K. E., Kourtchenko, O., Whitehouse, J. M., Ploug, H., & Godhe, A. (2020) Resting stages of Skeletonema marinoi assimilate nitrogen from the ambient environment under dark, anoxic conditions. Journal of Phycology, 56(3), 699-708. https://doi.org/10.1111/jpy.12975 Chapter IV: Stenow, R., Robertson, K. E., Kourtchenko, O., Whitehouse, J. M., & Ploug, H. Resting stages of Skeletonema marinoi assimilate organic compounds and respire using dissimilatory nitrate reduction to ammonium in dark, anoxic conditions. [Manuscript in preparation for Environmental Microbiology]
Degree
Doctor of Philosophy
University
University of Gothenburg. Faculty of Science
Institution
Department of Marine Sciences ; Institutionen för marina vetenskaper
Disputation
Onsdagen den 6e, september, 2023 kl. 13:00 i Korallrevet, rumsnummer: 3401, Natrium, Institutionen för marina vetenskaper, Medicinaregatan 7B, 413 90 Göteborg
Date of defence
2023-09-06
rickard.stenow@gu.se
Date
2023-08-10Author
Stenow, Rickard
Keywords
Diatoms
Resting stages
N cycling
Chain formation
Secondary ion mass spectrometry (SIMS)
Publication type
Doctoral thesis
ISBN
978-91-8069-375-2 (PRINT)
978-91-8069-376-9 (PDF)
Language
eng