Physiological and ecological aspects of Chlorella sorokiniana (Trebouxiophyceae) under photoautotrophic and mixotrophic conditions
Abstract
Mixotrophy is a metabolic strategy in which an organism is autotrophic and heterotrophic simultaneously. Considering that the aquatic environment provides several organic sources of carbon, it is probably common for microalgae to perform mixotrophy and not only photoautotrophy, but little is known about microalgae mixotrophy. The present work aimed at investigating the growth, photosynthetic activity, morphology, and biochemical composition of the microalga Chlorella sorokiniana in mixotrophic and photo-mixotrophic conditions, comparing it with photoautotrophy. The results showed pH changes after glucose addition, reaching pH 11.62 in mixotrophic and 10.47 in sequential photo-mixotrophic cultures, which limited the microalgal growth. Highest biomass was obtained in the mixotrophic culture in comparison with the sequential photo-mixotrophic one. Rapid light saturation curves showed that α (photosynthetic efficiency, 1.69) and relative electron transport rate (rETR; 565.61) were higher in the mixotrophic cultures, whereas the highest I k (irradiance saturation, 386.68) was obtained in the photoautotrophic ones. In the sequential photo-mixotrophic cultures, photosynthetic activity varied during glucose consumption, decreasing the maximum quantum yield F v/F m after glucose addition, indicating change in metabolism, from photoautotrophy to mixotrophy by the microalga. The results showed that the mixotrophic cultures had higher production of chlorophyll a (6.26 mg mL-1), cell density (6.62 × 10 7 cell mL-1), and lipids (0.06 pg μm-3). Sequential photo-mixotrophic cultures showed the highest biovolume (360.5 μm 3 cell-1) and total carbohydrates (0.026 pg μm-3). The protein concentration was 3.2 and 2.4 times higher in photoautotrophy and photo-mixotrophic growth, respectively, than in mixotrophy, but lipids were three times higher under mixotrophy. The biochemical changes we observed indicate that the microalga's plasticity in face of new environmental characteristics, such as the presence of organic carbon, can change the flow of energy through natural ecosystems.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
At the end of the experiment, no differences in cell densities among the three cultures were observed.
“At the end of the experiment, no differences in cell densities among the three cultures were observed.”
From Challenges and Opportunities to Increase Economic Feasibility and Sustainability of Mixotrophic Cultivation of Green Microalgae of the Genus Chlorella (2022) · cites this paper as [106]
Sequential photo-mixotrophic cultures of C. sorokiniana showed the highest total carbohydrate concentration (0.026 pg μm−3) compared with mixotrophic (0.009 pg μm−3) and photoautotrophic cultures (0.007 pg μm−3) after 5 days.
“It was found that the sequential photo-mixotrophic cultures showed the highest total carbohydrate concentration (0.026 pg μm -3 ) when compared to the mixotrophic (0.009 pg μm -3 ) and photoautotrophic cultures (0.007 pg μm -3 ) after 5 days.”
From Challenges and Opportunities to Increase Economic Feasibility and Sustainability of Mixotrophic Cultivation of Green Microalgae of the Genus Chlorella (2022) · cites this paper as [106]
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria
Rippka, R., Stanier, R. Y., Deruelles, J., Herdman, M., & Waterbury, J. B. (1979) · Microbiology · doi:10.1099/00221287-111-1-1 · Cited by 7,606 · see citing works
The Ecological Role of Water-Column Microbes in the Sea
Azam, F., Fenchel, T., Field, J., Gray, J. S., Meyer-Reil, L., & Thingstad, T. F. (1983) · Marine Ecology Progress Series · doi:10.3354/meps010257 · Cited by 5,398 · see citing works
Non-Photochemical Quenching. A Response to Excess Light Energy
Müller, P., Li, X.-P., & Niyogi, K. K. (2001) · Plant Physiology · doi:10.1104/pp.125.4.1558 · Cited by 2,840 · see citing works
Falkowski, P. G., & Raven, J. A. (2007) · Princeton University Press eBooks · doi:10.1515/9781400849727 · Cited by 1,958 · see citing works
Algal Physiology and Biochemistry.
Baalen, C. V., & Stewart, W. P. D. (1975) · Bulletin of the Torrey Botanical Club · doi:10.2307/2484419 · Cited by 1,494 · see citing works
One Juliet and four Romeos: VeA and its methyltransferases
Sarikaya-Bayram, Ã., Palmer, J. M., Keller, N. P., Braus, G. H., & Bayram, Ö. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00001 · Cited by 1,148 · see citing works
A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton
Eilers, P. H. C., & Peeters, J. C. H. (1988) · Ecological Modelling · doi:10.1016/0304-3800(88)90057-9 · Cited by 1,112 · see citing works
Trophic Structure and Productivity of Silver Springs, Florida
Odum, H. T. (1957) · Ecological Monographs · doi:10.2307/1948571 · Cited by 835 · see citing works
The endosymbiotic origin, diversification and fate of plastids
Keeling, P. J. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0103 · Cited by 753 · see citing works
Albalasmeh, A. A., Berhe, A. A., & Ghezzehei, T. A. (2013) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2013.04.072 · Cited by 740 · see citing works
Roháček, K. (2002) · Photosynthetica · doi:10.1023/a:1020125719386 · Cited by 724 · see citing works
Weitere Studien über das Wärmegleichgewicht unter Gasmolekülen
Boltzmann, L. (1970) · Vieweg+Teubner eBooks · doi:10.1007/978-3-322-84986-1_3 · Cited by 522 · see citing works
Hendrickson, L., Furbank, R. T., & Chow, W. S. (2004) · Photosynthesis Research · doi:10.1023/b:pres.0000040446.87305.f4 · Cited by 462 · see citing works
Determination of Total Lipid, Lipid Classes, and Fatty Acids in Aquatic Samples
Parrish, C. C. (1999) · Springer eBooks · doi:10.1007/978-1-4612-0547-0_2 · Cited by 431 · see citing works
Yang, C., Hua, Q., & Shimizu, K. (2000) · Biochemical Engineering Journal · doi:10.1016/s1369-703x(00)00080-2 · Cited by 428 · see citing works
Stoecker, D. K. (1998) · European Journal of Protistology · doi:10.1016/s0932-4739(98)80055-2 · Cited by 328 · see citing works
Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes
Müller‐Navarra, D. C., Brett, M. T., Park, S., Chandra, S., Ballantyne, A. P., Zorita, E., & Goldman, C. R. (2003) · Nature · doi:10.1038/nature02210 · Cited by 326 · see citing works
Micro-algae come of age as a platform for recombinant protein production
Specht, E. A., Miyake-Stoner, S. J., & Mayfield, S. P. (2010) · Biotechnology Letters · doi:10.1007/s10529-010-0326-5 · Cited by 304 · see citing works
Wan, M., Liu, P., Xia, J., Rosenberg, J. N., Oyler, G. A., Betenbaugh, M. J., Nie, Z., & Qiu, G. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-011-3399-8 · Cited by 300 · see citing works
Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence
Kumar, K. S., Dahms, H.-U., Lee, J., Kim, H., Lee, W. C., & Shin, K. (2014) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2014.01.042 · Cited by 282 · see citing works
Lehninger, A. L. (1984) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 261 · see citing works
Mixotrophic cultivation of a Chlorella sorokiniana strain for enhanced biomass and lipid production
Li, T., Zheng, Y., Yu, L., & Chen, S. (2014) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2014.04.010 · Cited by 258 · see citing works
Goodson, C. M., Roth, R. A., Wang, Z. T., & Goodenough, U. W. (2011) · Eukaryotic Cell · doi:10.1128/ec.05242-11 · Cited by 252 · see citing works
Oil accumulation via heterotrophic/mixotrophic Chlorella protothecoides
Heredia-Arroyo, T., Wei, W., & Hu, B. (2010) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-010-8974-4 · Cited by 243 · see citing works
Rausch, T. (1981) · Hydrobiologia · doi:10.1007/bf00008520 · Cited by 228 · see citing works
PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids
White, S., Anandraj, A., & Bux, F. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.09.097 · Cited by 219 · see citing works
Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs
Tittel, J., Bissinger, V., Zippel, B., Gaedke, U., Bell, E., Lorke, A., & Kamjunke, N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2130696100 · Cited by 218 · see citing works
Gimpel, J. A., Henríquez, V., & Mayfield, S. P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01376 · Cited by 207 · see citing works
Liu, X., Duan, S., Li, A., Xu, N., Cai, Z., & Hu, Z. (2008) · Journal of Applied Phycology · doi:10.1007/s10811-008-9355-z · Cited by 195 · see citing works
Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus
Kilham, S. S., Kreeger, D. A., Goulden, C. E., & Lynn, S. G. (1997) · Freshwater Biology · doi:10.1046/j.1365-2427.1997.00231.x · Cited by 181 · see citing works
Komor, E., & Tanner, W. (1976) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1976.tb10970.x · Cited by 154 · see citing works
Regulation of starch and lipid accumulation in a microalga Chlorella sorokiniana
Li, T., Gargouri, M., Feng, J., Park, J.-J., Gao, D., Miao, C., Dong, T., Gang, D. R., & Chen, S. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.01.005 · Cited by 151 · see citing works
Droop, M. R. (1974) · Medical Entomology and Zoology · Cited by 150 · see citing works
Mixotrophy in planktonic protists as a spectrum of nutritional strategies.
Jones, R. I. (1994) · Lancaster EPrints (Lancaster University) · Cited by 143 · see citing works
Proton‐coupled hexose transport in Chlorella vulgaris
Komor, E. (1973) · FEBS Letters · doi:10.1016/0014-5793(73)80501-0 · Cited by 139 · see citing works
The Hexose‐Proton Symport System of Chlorella vulgaris
Komor, E., & Tanner, W. (1974) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1974.tb03476.x · Cited by 136 · see citing works
Proton channels in algae: reasons to be excited
Taylor, A. R., Brownlee, C., & Wheeler, G. L. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.06.009 · Cited by 118 · see citing works
Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria†
Oesterhelt, C., Schmälzlin, E., Schmitt, J. M., & Lokstein, H. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2007.03159.x · Cited by 108 · see citing works
Hildebrand, M., Abbriano, R. M., Polle, J. E. W., Traller, J. C., Trentacoste, E. M., Smith, S. R., & Davis, A. K. (2013) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2013.02.027 · Cited by 96 · see citing works
The effects of copper on the photosynthetic response of Phaeocystis cordata
Lombardi, A. T., & Maldonado, M. T. (2011) · Photosynthesis Research · doi:10.1007/s11120-011-9655-z · Cited by 89 · see citing works
Self-citationKong, W., Song, H., Cao, Y.-T., Yang, H. F., Hua, S., & Xia, C. (2011) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb.9000478 · Cited by 88 · see citing works
Martínez, M. E., Camacho, F., Jiménez, J. M., & Espínola, J. B. (1997) · Process Biochemistry · doi:10.1016/s0032-9592(96)00045-3 · Cited by 88 · see citing works
Hartmann, M., Zubkov, M. V., Scanlan, D. J., & Lepère, C. (2013) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12084 · Cited by 83 · see citing works
Characterization of the active hexose transport system of chlorella vulgaris
Komor, E., & Tanner, W. (1971) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(71)90314-2 · Cited by 73 · see citing works
Light- induced electron transfer and ATP synthesis in a carotene synthesizing insect
Valmalette, J.-., Dombrovsky, A., Brat, P., Mertz, C., Capovilla, M., & Robichon, A. (2012) · Scientific Reports · doi:10.1038/srep00579 · Cited by 64 · see citing works
Effects of microzooplankton and mixotrophy in an experimental planktonic food web
Ptáčník, R., Sommer, U. J., Hansen, T., & Martens, V. (2004) · Limnology and Oceanography · doi:10.4319/lo.2004.49.4_part_2.1435 · Cited by 63 · see citing works
Giovanardi, M., Ferroni, L., Baldisserotto, C., Tedeschi, P., Maietti, A., Pantaleoni, L., & Pancaldi, S. (2012) · PROTOPLASMA · doi:10.1007/s00709-012-0390-x · Cited by 58 · see citing works
ALGAE AS COMPETITORS FOR GLUCOSE WITH HETEROTROPHIC BACTERIA <sup>1</sup>
Kamjunke, N., Köhler, B., Wannicke, N., & Tittel, J. (2008) · Journal of Phycology · doi:10.1111/j.1529-8817.2008.00520.x · Cited by 56 · see citing works
Alkhamis, Y. A., & Qin, J. G. (2015) · Journal of Applied Phycology · doi:10.1007/s10811-015-0599-0 · Cited by 52 · see citing works
Respiratory increase and active hexose uptake of Chlorella vulgaris
DECKER, M. (1972) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(72)90009-1 · Cited by 50 · see citing works
Juntila, D. J., Bautista, M. A. M., & Monotilla, W. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.03.098 · Cited by 48 · see citing works
Active hexose uptake in Lemna gibba G1
Ullrich-Eberius, C. I., Novacky, A. J., & L�ttge, U. (1978) · Planta · doi:10.1007/bf00387140 · Cited by 46 · see citing works
A biochemical explanation for the success of mixotrophy in the flagellate Ochromonas sp.
Boëchat, I. G., Weithoff, G., Krüger, A., Gücker, B., & Adrian, R. (2007) · Limnology and Oceanography · doi:10.4319/lo.2007.52.4.1624 · Cited by 46 · see citing works
Respiratory increase and active hexose uptake of Chlorella vulgaris
Decker, M., & Tanner, W. (1972) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(72)90362-8 · Cited by 45 · see citing works
Endo, H., Nakajima, K., Chino, R., & Shirota, M. (1974) · Agricultural and Biological Chemistry · doi:10.1080/00021369.1974.10861121 · Cited by 43 · see citing works
Microalgae population dynamics in photobioreactors with secondary sewage effluent as culture medium
Marchello, A. E., Lombardi, A. T., Dellamano-Oliveira, M. J., et al. (2015) · Brazilian Journal of Microbiology · doi:10.1590/s1517-838246120131225 · Cited by 42 · see citing works
Self-citationBaldisserotto, C., Giovanardi, M., Ferroni, L., & Pancaldi, S. (2013) · Acta Physiologiae Plantarum · doi:10.1007/s11738-013-1426-3 · Cited by 42 · see citing works
Gacia, E., Littler, M. M., & Littler, D. S. (1996) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(96)02585-3 · Cited by 41 · see citing works
EXPERIMENTAL EVOLUTION OF HETEROTROPHY IN A GREEN ALGA
Bell, G. (2012) · Evolution · doi:10.1111/j.1558-5646.2012.01782.x · Cited by 40 · see citing works
Giovanardi, M., Baldisserotto, C., Ferroni, L., Longoni, P., Cella, R., & Pancaldi, S. (2013) · PROTOPLASMA · doi:10.1007/s00709-013-0531-x · Cited by 37 · see citing works
Photochemical and photoelectrochemical quenching of chlorophyll fluorescence in photosystem II
Vredenberg, W. J., Durchan, M., & Prášil, O. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.06.008 · Cited by 36 · see citing works
Wilken, S., Verspagen, J. M. H., Naus‐Wiezer, S. M. H., van Donk, E., & Huisman, J. (2013) · Ecological Applications · doi:10.1890/13-0218.1 · Cited by 33 · see citing works
Microbial glucose uptake and growth along a horizontal nutrient gradient in the North Pacific
Skoog, A., Whitehead, K., Sperling, F., et al. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.6.1676 · Cited by 33 · see citing works
Baldisserotto, C., Ferroni, L., Giovanardi, M., Boccaletti, L., Pantaleoni, L., & Pancaldi, S. (2012) · Phycologia · doi:10.2216/11-099.1 · Cited by 26 · see citing works
Utilization of Sugars by Chlorella under Various Conditions
Rodríguez-López, M. (1966) · Journal of General Microbiology · doi:10.1099/00221287-43-1-139 · Cited by 23 · see citing works
Peerapornpisal, Y., Dittamart, D., Pumas, C., & Pekkoh, J. (2014) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.14456/mijst.2014.28 · Cited by 19 · see citing works
Komor, E., Cho, B., Schricker, S., et al. (1989) · Planta · doi:10.1007/bf00392149 · Cited by 17 · see citing works
Mixotrophy: the missing link in consumer-resource-based ecologies
Cropp, R., & Norbury, J. (2015) · Theoretical Ecology · doi:10.1007/s12080-014-0248-2 · Cited by 13 · see citing works
The Effect of Glucose on Potassium Transport by Chlorella fusca
Tromballa, H. W. (1981) · Zeitschrift für Pflanzenphysiologie · doi:10.1016/s0044-328x(81)80002-5 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dragone, G. (2022) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2022.112284 · Cited by 84 · see citing works
Chieti, M. G., Petrucciani, A., Mollo, L., Gerotto, C., Eusebi, A. L., Fatone, F., Norici, A., & González-Camejo, J. (2024) · Science of The Total Environment · doi:10.1016/j.scitotenv.2024.174056 · Cited by 25 · see citing works
Stablein, M. J., Baracho, D. H., Watson, J. T., Silva, J. C., Zhang, Y., & Lombardi, A. T. (2021) · Algal Research · doi:10.1016/j.algal.2021.102548 · Cited by 14 · see citing works
Self-citation
- Authors
- Marchello, A. E., dos Santos, A. C., Lombardi, A. T., de Souza, C. W. O., & Montanhim, G. C.
- Affiliations
- Universidade Federal de São Carlos (BR)
- Corresponding author
- Marchello, Adriano Evandir
- Venue
- Microbial Ecology
- Published
- 2018-03-08
- Volume
- 76
- Issue
- 3
- Pages
- 791-800
- ISSN
- 0095-3628 (ISSN-L)
- 1432-184X
- OpenAlex
- W2790173529
- Cited by
- 27
- References
- 70
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 3 · 2023: 7 · 2022: 3 · 2021: 4 · 2020: 1 · 2018: 1
- FWCI
- 0.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Microbial Ecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo (2014/15894-0)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (302175/2015-6)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
- Keywords
- Chlorella sorokiniana, mixotrophy, photoautotrophy, microalgae growth, photosynthetic activity, chlorophyll a, lipid accumulation, protein accumulation, cell morphology, pH change, glucose supplementation, metabolic plasticity
- MeSH terms
- Chlorophyll A, Chlorella, Chlorophyll, Glucose, Light, Nitrogen, Photosynthesis, Biomass, Autotrophic Processes, Heterotrophic Processes, Microalgae
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review