Microalgal photoautotrophic growth induces pH decrease in the aquatic environment by acidic metabolites secretion

Mingcan Wu1, Guimei Wu2, Feimiao Lu2, Hongxia Wang3, Anping Lei1, Jiangxin Wang1
1Shenzhen Key Laboratory of Marine Bioresource and Eco-environmental Science, Shenzhen Engineering Laboratory for Marine Algal Biotechnology, Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China
2State Key Laboratory of Marine Resource Utilization in South China Sea, College of Oceanology, Hainan University, Haikou, 570228, China
3Center for Microalgal Biotechnology and Biofuels, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China

Tóm tắt

Abstract Background

Microalgae can absorb CO2 during photosynthesis, which causes the aquatic environmental pH to rise. However, the pH is reduced when microalga Euglena gracilis (EG) is cultivated under photoautotrophic conditions. The mechanism behind this unique phenomenon is not yet elucidated.

Results

The present study evaluated the growth of EG, compared to Chlorella vulgaris (CV), as the control group; analyzed the dissolved organic matter (DOM) in the aquatic environment; finally revealed the mechanism of the decrease in the aquatic environmental pH via comparative metabolomics analysis. Although the CV cell density was 28.3-fold that of EG, the secreted-DOM content from EG cell was 49.8-fold that of CV (p-value < 0.001). The main component of EG’s DOM was rich in humic acids, which contained more DOM composed of chemical bonds such as N–H, O–H, C–H, C=O, C–O–C, and C–OH than that of CV. Essentially, the 24 candidate biomarkers metabolites secreted by EG into the aquatic environment were acidic substances, mainly lipids and lipid-like molecules, organoheterocyclic compounds, organic acids, and derivatives. Moreover, six potential critical secreted-metabolic pathways were identified.

Conclusions

This study demonstrated that EG secreted acidic metabolites, resulting in decreased aquatic environmental pH. This study provides novel insights into a new understanding of the ecological niche of EG and the rule of pH change in the microalgae aquatic environment.

Từ khóa


Tài liệu tham khảo

Shahid A, Malik S, Zhu H, Xu J, Nawaz MZ, Nawaz S, Alam MA, Mehmood MA. Cultivating microalgae in wastewater for biomass production, pollutant removal, and atmospheric carbon mitigation; a review. Sci Total Environ. 2020;704: 135303.

Deviram G, Mathimani T, Anto S, Ahamed TS, Ananth DA, Pugazhendhi A. Applications of microalgal and cyanobacterial biomass on a way to safe, cleaner and a sustainable environment. J Clean Prod. 2020;253: 119770.

Huang Q, Jiang F, Wang L, Yang C. Design of photobioreactors for mass cultivation of photosynthetic organisms. Engineering. 2017;3(3):318–29.

Zhu J, Rong F, Zong B. Factors in mass cultivation of microalgae for biodiesel. Chin J Catal. 2013;34(1):80–100.

Vadlamani A, Viamajala S, Pendyala B, Varanasi S. Cultivation of microalgae at extreme alkaline pH conditions: a novel approach for biofuel production. ACS Sutain Chem Eng. 2017;5:7284–94.

Zerveas S, Mente MS, Tsakiri D, Kotzabasis K. Microalgal photosynthesis induces alkalization of aquatic environment as a result of H+ uptake independently from CO2 concentration—new perspectives for environmental applications. J Environ Manag. 2021;289: 112546.

Gong Q, Feng Y, Kang L, Luo M, Yang J. Effects of light and pH on cell density of Chlorella vulgaris. Energy Procedia. 2014;61:2012–5.

Mackinder LCM, Chen C, Leib RD, Patena W, Blum SR, Rodman M, Ramundo S, Adams CM, Jonikas MC. A spatial interactome reveals the protein organization of the algal CO2-concentrating mechanism. Cell. 2017;171(1):133-147.e114.

Wu M, Li J, Qin H, Lei A, Zhu H, Hu Z, Wang J. Pre-concentration of microalga Euglena gracilis by alkalescent pH treatment and flocculation mechanism of Ca3 (PO4) 2, Mg3 (PO4)2, and derivatives. Biotechnol Biofuels. 2020;13:1–13.

Gissibl A, Sun A, Care A, Nevalainen H, Sunna A. Bioproducts from Euglena gracilis: synthesis and applications. Front Bioeng Biotechnol. 2019;7:108.

Hasan MT, Sun A, Mirzaei M, Te’o J, Hobba G, Sunna A, Nevalainen H. A comprehensive assessment of the biosynthetic pathways of ascorbate, α-tocopherol and free amino acids in Euglena gracilis var. saccharophila. Algal Res. 2017;27:140–51.

Suzuki K. Large-scale cultivation of Euglena. Cham: Springer; 2017. p. 285–93.

Halter D, Goulhen-Chollet F, Gallien S, Casiot C, Hamelin J, Gilard F, Bertin PN. In situ proteo metabolomics reveals metabolite secretion by the acid mine drainage bio-indicator, Euglena mutabilis. ISME J. 2012;6(7):1391–402.

Tomita Y, Takeya M, Suzuki K, Nitta N, Higuchi C, Marukawa-Hashimoto Y, Osanai T. Amino acid excretion from Euglena gracilis cells in dark and anaerobic conditions. Algal Res. 2019;37:169–77.

Tomita Y, Yoshioka K, Iijima H, Nakashima A, Iwata O, Suzuki K, Hasunuma T, Kondo A, Hirai MY, Osanai T. Succinate and lactate production from Euglena gracilis during dark, anaerobic conditions. Front Microbiol. 2016;7:2050.

Wu M, Qin H, Deng J, Liu Y, Lei A, Zhu H, Hu Z, Wang J. A new pilot-scale fermentation mode enhances Euglena gracilis biomass and paramylon (β-1, 3-glucan) production. J Clean Prod. 2021;321: 128996.

Sheng GP, Yu HQ. Characterization of extracellular polymeric substances of aerobic and anaerobic sludge using three-dimensional excitation and emission matrix fluorescence spectroscopy. Water Res. 2006;40(6):1233–9.

Wicaksono A, Hidayat S, Damayanti Y, Jin DSM, Sintya E, Retnoaji B, Alam P. The significance of pelvic fin flexibility for tree climbing fish. Zoology. 2016;119(6):511–7.

Lu Z, Sha J, Wang W, Li Y, Wang G, Chen Y, Hu Q, Zhang X. Identification of auto-inhibitors in the reused culture media of the Chlorophyta Scenedesmus acuminatus. Algal Res. 2019;44: 101665.

Sha J, Lu Z, Ye J, Wang G, Hu Q, Chen Y, Zhang X. The inhibition effect of recycled Scenedesmus acuminatus culture media: influence of growth phase, inhibitor identification and removal. Algal Res. 2019;42: 101612.

Zhang X, Lu Z, Wang Y, Wensel P, Sommerfeld M, Hu Q. Recycling Nannochloropsis oceanica culture media and growth inhibitors characterization. Algal Res. 2016;20:282–90.

Wu M, Du M, Wu G, Lu F, Li J, Lei A, Zhu H, Hu Z, Wang J. Water reuse and growth inhibition mechanisms for cultivation of microalga Euglena gracilis. Biotechnol Biofuels. 2021;14(1):1–15.

Wu M, Zhang H, Sun W, Li Y, Hu Q, Zhou H, Han D. Metabolic plasticity of the starchless mutant of Chlorella sorokiniana and mechanisms underlying its enhanced lipid production revealed by comparative metabolomics analysis. Algal Res. 2019;42: 101587.

Zeng M, Hao W, Zou Y, Shi M, Jiang Y, Xiao P, Lei A, Hu Z, Zhang W, Zhao L. Fatty acid and metabolomic profiling approaches differentiate heterotrophic and mixotrophic culture conditions in a microalgal food supplement ‘Euglena’. BMC Biotechnol. 2016;16(1):1–8.

O’Neill EC, Trick M, Henrissat B, Field RA. Euglena in time: evolution, control of central metabolic processes and multi-domain proteins in carbohydrate and natural product biochemistry. Perspect Sci. 2015;6:84–93.

Oukarroum A. Change in photosystem II photochemistry during algal growth phases of Chlorella vulgaris and Scenedesmus obliquus. Curr Microbiol. 2016;72(6):692–9.

Ebringer L. Erythromycin-induced bleaching of Euglena gracilis. J Protozool. 1962;9(3):373–4.

Shao Q, Hu L, Qin H, Liu Y, Tang X, Lei A, Wang J. Metabolomic response of Euglena gracilis and its bleached mutant strain to light. PLoS ONE. 2019;14: e0224926.

Alami AH, Alasad S, Ali M, Alshamsi M. Investigating algae for CO2 capture and accumulation and simultaneous production of biomass for biodiesel production. Sci Total Environ. 2021;759: 143529.

Movasaghi Z, Rehman S, ur Rehman DI. Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl Spectrosc Rev. 2008;43:134–79.

Yoshioka K, Suzuki K, Osanai T. Effect of pH on metabolite excretion and cell morphology of Euglena gracilis under dark, anaerobic conditions. Algal Res. 2020;51: 102084.

Goto K, Beneragama CK. Circadian clocks and antiaging: do non-aging microalgae like Euglena reveal anything? Ageing Res Rev. 2010;9:91–100.

He J, Liu C, Du M, Zhou X, Hu Z, Lei A, Wang J. Metabolic responses of a model green microalga Euglena gracilis to different environmental stresses. Front Bioeng Biotechnol. 2021;9: 662655.

Ouyang Y, Chen S, Zhao L, Song Y, Lei A, He J, Wang J. Global metabolomics reveals that vibrio natriegens enhances the growth and paramylon synthesis of Euglena gracilis. Front Bioeng Biotechnol. 2021;9: 652021.

Carmelo V, Santos H, Sá-Correia I. Effect of extracellular acidification on the activity of plasma membrane ATPase and on the cytosolic and vacuolar pH of Saccharomyces cerevisiae. BBA-Biomembranes. 1997;1325(1):63–70.

Banerjee S, Kane PM. Regulation of V-ATPase activity and organelle pH by phosphatidylinositol phosphate lipids. Front Cell Dev Biol. 2020;8:510.

Kvíderová J. Photochemical performance of the acidophilic red alga Cyanidium sp. in a pH gradient. Origins Life Evol B. 2012;42(2):223–34.

Gross W. Ecophysiology of algae living in highly acidic environments. Hydrobiologia. 2000;433(1):31–7.

Hosseinpour Tehrani H, Becker J, Bator I, Saur K, Meyer S, Rodrigues Lóia AC, Blank LM, Wierckx N. Integrated strain-and process design enable production of 220 g L−1 itaconic acid with Ustilago maydis. Biotechnol Biofuels. 2019;12(1):1–11.

Hooftman A, O’Neill LA. The immunomodulatory potential of the metabolite itaconate. Trends Immunol. 2019;40(8):687–98.

Wierckx N, Agrimi G, Lübeck PS, Steiger MG, Mira NP, Punt PJ. Metabolic specialization in itaconic acid production: a tale of two fungi. Curr Opin Biotechnol. 2020;62:153–9.

Nguyen TV, Alfaro AC, Merien F, Young T, Grandiosa R. Metabolic and immunological responses of male and female new Zealand Greenshell™ mussels (Perna canaliculus) infected with Vibrio sp. J Invertebr Pathol. 2018;157:80–9.

Michelucci A, Cordes T, Ghelfi J, Pailot A, Reiling N, Goldmann O, Binz T, Wegner A, Tallam A, Rausell A. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc Natl Acad Sci USA. 2013;110(19):7820–5.

Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology. 1979;111(1):1–61.

Yang Q, Li Y, Yang JD, Liu Y, Zhang L, Luo S, Cheng JP. Holistic prediction of the pKa in diverse solvents based on a machine-learning approach. Angew Chem Int Ed. 2020;132(43):19444–53.

Silverstein TP, Heller ST. pK a values in the undergraduate curriculum: what is the real pK a of water? J Chem Educ. 2017;94(6):690–5.