Investigations of phytoplankton responses to iron stress in seawater are complicated by the fact that iron concentrations do not necessarily reflect bioavailability. Most studies to date have been based on single species or field samples and are problematic to interpret. Here, we report results from an experimental cocultivation model system that enabled us to evaluate interspecific competition as a function of iron content and form, and to study the effect of nutritional conditions on the proteomic profiles of individual species. Our study revealed that the dinoflagellate Amphidinium carterae was able to utilize iron from a hydroxamate siderophore, a strategy that could provide an ecological advantage in environments where siderophores present an important source of iron. Additionally, proteomic analysis allowed us to identify a potential candidate protein involved in iron acquisition from hydroxamate siderophores, a strategy that is largely unknown in eukaryotic phytoplankton.

Department of Parasitology Faculty of Science Charles University BIOCEV Vestec Czech

Department of Zoology Faculty of Science Charles University BIOCEV Vestec Czech

Institute of Microbiology Academy of Sciences Centrum Algatech Trebon Czech

Zobrazit více v PubMed

Martin J.H., Gordon R.M., Fitzwater S.E. Iron Limitation. Limnol Oceanogr. 1991;36:1793–1802.

Sunda W.G., Huntsman S.A. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem. 1995;50(1-4):189–206.

Lis H., Shaked Y., Kranzler C., Keren N., Morel F.M.M. Iron bioavailability to phytoplankton: an empirical approach. ISME J. 2015;9(4):1003–1013. PubMed PMC

Kazamia E., Sutak R., Paz-Yepes J., Dorrell R.G., Vieira F.R.J., Mach J., et al. Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci Adv. 2018;4(5) doi: 10.1126/sciadv.aar4536. PubMed DOI PMC

Lampe R.H., Mann E.L., Cohen N.R., Till C.P., Thamatrakoln K., Brzezinski M.A., et al. Different iron storage strategies among bloom-forming diatoms. Proc Natl Acad Sci U S A. 2018;115(52):E12275–E12284. PubMed PMC

Hutchins D.A., Boyd P.W. Marine phytoplankton and the changing ocean iron cycle. Nat Clim Chang. 2016;6(12):1072–1079.

Du Z.Y., Zienkiewicz K., Vande P.N., et al. Algal-fungal symbiosis leads to photosynthetic mycelium. Elife. 2019;8:1–22. PubMed PMC

Fisher B.S., Estraño C.E., Cole J.A., Talamas-Rohana P. Modeling long-term host cell-Giardia lamblia interactions in an in vitro co-culture system. PLoS ONE. 2013;8(12):e81104. doi: 10.1371/journal.pone.0081104. PubMed DOI PMC

Haines K.C., Guillard R.R.L. Growth of vitamin B12-requiring marine diatoms in mixed laboratory cultures with vitamin b12-producing marine bacteria. J Phycol. 1974;10:245–252.

Croft M.T., Lawrence A.D., Raux-Deery E., Warren M.J., Smith A.G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438(7064):90–93. PubMed

Amin S.A., Green D.H., Hart M.C., et al. Photolysis of ion – siderophore chelates promotes bacteria – algal mutualism Photolysis of iron – siderophore chelates promotes bacterial – algal mutualism. Environ Sci. 2017;106:2–7. PubMed PMC

Kotabova E., Malych R., Pierella Karlusich J.J., Kazamia E., Eichner M., Mach J., et al. Complex response of the chlorarachniophyte bigelowiella natans to iron availability. mSystems. 2021;6(1) doi: 10.1128/mSystems.00738-20. PubMed DOI PMC

Mach J., Bíla J., Ženíšková K., Arbon D., Malych R., Glavanakovová M., et al. Iron economy in Naegleria gruberi reflects its metabolic flexibility. Int J Parasitol. 2018;48(9-10):719–727. PubMed

Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185–193. PubMed

Lê Cao KA, Boitard S, Besse P. Sparse PLS discriminant analysis: Biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinformatics 2011;12, DOI: 10.1186/1471-2105-12-253. PubMed PMC

Scheiber IF, Pilátová J, Malych R et al. Copper and iron metabolism in: Ostreococcus tauri -the role of phytotransferrin, plastocyanin and a chloroplast copper-transporting ATPase. Metallomics 2019;11:1657–66. PubMed

Ouchetto H., Dias M., Mornet R., Lesuisse E., Camadro J.-M. A new route to trihydroxamate-containing artificial siderophores and synthesis of a new fluorescent probe. Bioorganic Med Chem. 2005;13(5):1799–1803. PubMed

Peers G., Price N.M. Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature. 2006;441(7091):341–344. PubMed

Blaby-Haas C.E., Merchant S.S. Regulating cellular trace metal economy in algae. Curr Opin Plant Biol. 2017;39:88–96. PubMed PMC

Caputi L., Carradec Q., Eveillard D., Kirilovsky A., Pelletier E., Pierella Karlusich J.J., et al. Community-level responses to iron availability in open ocean plankton ecosystems. Global Biogeochem Cycles. 2019;33(3):391–419.

Marchetti A., Schruth D.M., Durkin C.A., Parker M.S., Kodner R.B., Berthiaume C.T., et al. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci USA. 2012;109(6):E317–E325. doi: 10.1073/pnas.1118408109. PubMed DOI PMC

Taddei L., Stella G.R., Rogato A., Bailleul B., Fortunato A.E., Annunziata R., et al. Multisignal control of expression of the LHCX protein family in the marine diatom Phaeodactylum tricornutum. J Exp Bot. 2016;67(13):3939–3951. PubMed PMC

Zhou L., Wu S., Gu W., et al. Photosynthesis acclimation under severely fluctuating light conditions allows faster growth of diatoms compared with dinoflagellates. BMC Plant Biol. 2021;21:1–14. PubMed PMC

Samuelsson G., Richardson K. Photoinhibition at low quantum flux densities in a marine dinoflagellate (Amphidinium carterae) Mar Biol. 1982;70(1):21–26.

Lacour T., Babin M., Lavaud J., Kroth P. Diversity in xanthophyll cycle pigments content and related nonphotochemical quenching (NPQ) among microalgae: implications for growth strategy and ecology. J Phycol. 2020;56(2):245–263. PubMed

Coale T.H., Moosburner M., Horák A., Oborník M., Barbeau K.A., Allen A.E. Reduction-dependent siderophore assimilation in a model pennate diatom. Proc Natl Acad Sci U S A. 2019;116(47):23609–23617. PubMed PMC

Behnke J., LaRoche J. Iron uptake proteins in algae and the role of Iron Starvation-Induced Proteins (ISIPs) Eur J Phycol. 2020;55(3):339–360.

Allen A.E., LaRoche J., Maheswari U., Lommer M., Schauer N., Lopez P.J., et al. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci U S A. 2008;105(30):10438–10443. PubMed PMC

Poulson-Ellestad K.L., Jones C.M., Roy J., Viant M.R., Fernandez F.M., Kubanek J., et al. Metabolomics and proteomics reveal impacts of chemically mediated competition on marine plankton. Proc Natl Acad Sci U S A. 2014;111(24):9009–9014. PubMed PMC

Frey B.E., Small L.F. Recycling of metabolized iron by the marine dinoflagellate amphidinium carterae. J Phycol. 1979;15:405–409.

Maldonado M.T., Price N.M. Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae) J Phycol. 2001;37(2):298–310.

Strzepek R.F., Maldonado M.T., Hunter K.A., Frew R.D., Boyd P.W. Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr. 2011;56(6):1983–2002.

Boiteau R.M., Mende D.R., Hawco N.J., McIlvin M.R., Fitzsimmons J.N., Saito M.A., et al. Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proc Natl Acad Sci U S A. 2016;113(50):14237–14242. PubMed PMC

Park B.S., Erdner D.L., Bacosa H.P., Liu Z., Buskey E.J. Potential effects of bacterial communities on the formation of blooms of the harmful dinoflagellate Prorocentrum after the 2014 Texas City “Y” oil spill (USA) Harmful Algae. 2020;95:101802. doi: 10.1016/j.hal.2020.101802. PubMed DOI

Sutak R., Camadro J.M., Lesuisse E. Iron Uptake Mechanisms in Marine Phytoplankton. Front Microbiol. 2020;11:1–14. PubMed PMC

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis