TY - JOUR
T1 - Phosphorus starvation and luxury uptake in green microalgae revisited
AU - Solovchenko, Alexei
AU - Khozin-Goldberg, Inna
AU - Selyakh, I.
AU - Semenova, Larisa
AU - Ismagulova, Tatiana
AU - Lukyanov, Alexandr
AU - Mamedov, I.
AU - Vinogradova, Elizaveta
AU - Karpova, Olga
AU - Konyukhov, Ivan
AU - Vasilieva, Svetlana
AU - Mojzes, P.
AU - Dijkema, Cor
AU - Vecherskaya, Margarita
AU - Zvyagin, Ivan
AU - Nedbal, Ladislav
AU - Gorelova, Olga
N1 - Funding Information:
The financial support of BioSC funded by the Ministry of Innovation, Science, and Research of the German State of North Rhine-Westphalia is greatly appreciated (AlgalFertilizer and AlgalNutrient projects). The ultrastructural studies were carried out at the User Facilities Center of M.V. Lomonosov Moscow State University and funded by the Russian Foundation for Basic Research [grant # 18-29-25050 ]. Phosphorus biomass content was assayed with the support of RFBR [grant # 19-04-00509 ]. Partial support of the « RUDN University Program 5-100» is gratefully acknowledged. The Raman measurements were supported by the Czech Science Foundation ( GACR 17-06264S ).
Funding Information:
The authors are grateful to Dr. Olga Baulina for her invaluable help with the electron microscopy, to Mrs. Isabel Meuser, Mr. Andres Sadowsky, and Mr. Pavel Scherbakov for their dedicated technical help, and to Dr. Andrey Bychkov for his help with the ICP-MS assays. The financial support of BioSC funded by the Ministry of Innovation, Science, and Research of the German State of North Rhine-Westphalia is greatly appreciated (AlgalFertilizer and AlgalNutrient projects). The ultrastructural studies were carried out at the User Facilities Center of M.V. Lomonosov Moscow State University and funded by the Russian Foundation for Basic Research [grant # 18-29-25050]. Phosphorus biomass content was assayed with the support of RFBR [grant # 19-04-00509]. Partial support of the ?RUDN University Program 5-100? is gratefully acknowledged. The Raman measurements were supported by the Czech Science Foundation (GACR 17-06264S). AS conceived and designed the experiments, and analyzed the results. IS, LS, AL, IK and SV carried out the cultivation experiments. IKG performed the lipid class analysis and treated the data. IM and IZ performed the RNASeq experiments and treated the data. TI performed the analytical TEM measurements and DGE assessment. OG supervised the TEM imaging and carried out the conventional TEM and morphometry. EV and OK supervised the qRT-PCR experiments and treated the data. PM carried out the Raman measurements and treated the data. CD and MV measured and interpreted the NMR spectra. LN conceived of the P-depletion experiments and supervised the large-scale cultivation experiments. All authors wrote and approved the final version of the manuscript.
Publisher Copyright:
© 2019 Elsevier B.V.
PY - 2019/11/1
Y1 - 2019/11/1
N2 - Phosphorus (P) is central to storing and transferring energy and information in living cells, including those of microalgae. Many microalgal species dwelling in low P environments are naturally equipped to take up and store P whenever it becomes available through a complex phenomenon known as “luxury P uptake.” Its research is required for better understanding of the nutrient geochemical cycles in aquatic environments but also for biotechnological applications such as sequestration of nutrients from wastewater and production of algal fertilizers. Here, we report on our recent insights into luxury P uptake and polyphosphate formation originating from physiological, ultrastructural, and transcriptomic evidence. The cultures pre-starved of P and re-fed with inorganic phosphate (Pi) exhibited a bi-phasic kinetics of Pi uptake comprising fast (1–2 h after re-feeding) and slow (1–3 d after re-feeding) phases. The rate of Pi uptake in the fast phase was ca. 10 times higher than in the slow phase with an opposite trend shown for the cell division rate. The transient peak of polyphosphate accumulation was determined 2–4 h after re-feeding and coincided with the period of slow cell division and fast Pi uptake. In this phase, the microalgal cells reached the highest P content (up to 5% of dry cell weight). The P re-feeding also reversed the characteristic changes in cell lipids induced by P starvation, namely increase in the major membrane glycolipid (DGDG/MGDG) ratio and betaine lipids. These changes were reversed upon Pi re-feeding of the starved culture. Electron microscopy revealed the ordered organization of vacuolar polyphosphate indicative of the possible involvement of an enzyme (complex) in their synthesis. A candidate gene encoding a protein similar to the vacuolar transport chaperone (VTC) protein, featuring an expression pattern corresponding to polyphosphate accumulation, was revealed. Implications of the findings for efficient biocapture of phosphorus are discussed.
AB - Phosphorus (P) is central to storing and transferring energy and information in living cells, including those of microalgae. Many microalgal species dwelling in low P environments are naturally equipped to take up and store P whenever it becomes available through a complex phenomenon known as “luxury P uptake.” Its research is required for better understanding of the nutrient geochemical cycles in aquatic environments but also for biotechnological applications such as sequestration of nutrients from wastewater and production of algal fertilizers. Here, we report on our recent insights into luxury P uptake and polyphosphate formation originating from physiological, ultrastructural, and transcriptomic evidence. The cultures pre-starved of P and re-fed with inorganic phosphate (Pi) exhibited a bi-phasic kinetics of Pi uptake comprising fast (1–2 h after re-feeding) and slow (1–3 d after re-feeding) phases. The rate of Pi uptake in the fast phase was ca. 10 times higher than in the slow phase with an opposite trend shown for the cell division rate. The transient peak of polyphosphate accumulation was determined 2–4 h after re-feeding and coincided with the period of slow cell division and fast Pi uptake. In this phase, the microalgal cells reached the highest P content (up to 5% of dry cell weight). The P re-feeding also reversed the characteristic changes in cell lipids induced by P starvation, namely increase in the major membrane glycolipid (DGDG/MGDG) ratio and betaine lipids. These changes were reversed upon Pi re-feeding of the starved culture. Electron microscopy revealed the ordered organization of vacuolar polyphosphate indicative of the possible involvement of an enzyme (complex) in their synthesis. A candidate gene encoding a protein similar to the vacuolar transport chaperone (VTC) protein, featuring an expression pattern corresponding to polyphosphate accumulation, was revealed. Implications of the findings for efficient biocapture of phosphorus are discussed.
KW - Chlorella
KW - Lipids
KW - Luxury uptake
KW - Phosphorus starvation
KW - Polyphosphate
KW - Transcriptomics
UR - http://www.scopus.com/inward/record.url?scp=85071890970&partnerID=8YFLogxK
U2 - 10.1016/j.algal.2019.101651
DO - 10.1016/j.algal.2019.101651
M3 - Article
AN - SCOPUS:85071890970
SN - 2211-9264
VL - 43
JO - Algal Research
JF - Algal Research
M1 - 101651
ER -