Estimating Biomass and Vitality of Microalgae for Monitoring Cultures: A Roadmap for Reliable Measurements
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
35954299
PubMed Central
PMC9368473
DOI
10.3390/cells11152455
PII: cells11152455
Knihovny.cz E-zdroje
- Klíčová slova
- algae, biomass, biotechnology, cultivation, fluorescence, growth,
- MeSH
- biomasa MeSH
- chlorofyl MeSH
- fluorescence MeSH
- fotosystém II (proteinový komplex) MeSH
- mikrořasy * MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chlorofyl MeSH
- fotosystém II (proteinový komplex) MeSH
Estimating algal biomass is a prerequisite for monitoring growth of microalgae. Especially for large-scale production sites, the measurements must be robust, reliable, fast and easy to obtain. We compare the relevant parameters, discuss potential hurdles and provide recommendations to tackle these issues. The focus is on optical density and in vivo autofluorescence of chlorophyll, which have proven to be ideal candidates for monitoring purposes. Beyond biomass, cell vitality is also crucial for maintaining cultures. While maximizing biomass yield is often the primary consideration, some applications require adverse growth conditions for the synthesis of high-quality compounds. The non-invasive technique of pulse-amplified modulated (PAM) fluorescence measurements provides an ideal tool and is increasingly being employed due to ever more affordable devices. We compared three devices and studied the robustness of the dark fluorescence yield of photosystem II (Fv/Fm) at various cell densities. Although the so-called inner filter effects influence the fluorescence signal, the resulting Fv/Fm remain stable and robust over a wide range of cell densities due to mutual effects.
Zobrazit více v PubMed
Reardon K.F., Scheper T.H. Determination of Cell Concentration and Characterization of Cells. In: Rehm H.J., Reed G., editors. Biotechnology Set. 2nd ed. Wiley; Hoboken, NJ, USA: 2001. pp. 179–223.
Moheimani N.R., Borowitzka M.A., Isdepsky A., Sing S.F. Standard Methods for Measuring Growth of Algae and Their Composition. In: Borowitzka M.A., Moheimani N.R., editors. Algae for Biofuels and Energy. Springer; Dordrecht, The Netherlands: 2013. pp. 265–284.
Bhattacharya S., Shivaprakash M.K. Evaluation of three Spirulina species grown under similar conditions for their growth and biochemicals. J. Sci. Food Agric. 2005;85:333–336. doi: 10.1002/jsfa.1998. DOI
Sakai N., Sakamoto Y., Kishimoto N., Chihara M., Karube I. Chlorella strains from hot springs tolerant to high temperature and high CO2. Energy Convers. Manag. 1995;36:693–696. doi: 10.1016/0196-8904(95)00100-R. DOI
Li X., Wang X., Duan C., Yi S., Gao Z., Xiao C., Agathos S.N., Wang G., Li J. Biotechnological production of astaxanthin from the microalga Haematococcus pluvialis. Biotechnol. Adv. 2020;43:107602. doi: 10.1016/j.biotechadv.2020.107602. PubMed DOI
Lu Q., Li H., Xiao Y., Liu H. A state-of-the-art review on the synthetic mechanisms, production technologies, and practical application of polyunsaturated fatty acids from microalgae. Algal Res. 2021;55:102281. doi: 10.1016/j.algal.2021.102281. DOI
Schreiber U. Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. In: Amesz J., Hoff A.J., Van Gorkum H.J., editors. Current Topics in Photosynthesis: Dedicated to Professor L.N.M. Duysens on the Occasion of His Retirement. Springer; Dordrecht, The Netherlands: 1986. pp. 259–270. PubMed
Schreiber U., Bilger W. Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. In: Tenhunen J.D., Catarino F.M., Lange O.L., Oechel W.C., editors. Proceedings of the Plant Response to Stress, held in Sesimbra, Portugal, October 1985. Springer; Berlin/Heidelberg, Germany: 1987. pp. 27–53.
Schreiber U., Endo T., Mi H., Asada K. Quenching Analysis of Chlorophyll Fluorescence by the Saturation Pulse Method: Particular Aspects Relating to the Study of Eukaryotic Algae and Cyanobacteria. Plant Cell Physiol. 1995;36:873–882. doi: 10.1093/oxfordjournals.pcp.a078833. DOI
Baker N.R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 2008;59:89–113. doi: 10.1146/annurev.arplant.59.032607.092759. PubMed DOI
Kalaji H.M., Schansker G., Ladle R.J., Goltsev V., Bosa K., Allakhverdiev S.I., Brestic M., Bussotti F., Calatayud A., Dąbrowski P., et al. Frequently asked questions about in vivo chlorophyll fluorescence: Practical issues. Photosynth. Res. 2014;122:121–158. doi: 10.1007/s11120-014-0024-6. PubMed DOI PMC
Malapascua J.R.F., Jerez C., Sergejevová M., Lopez Figueroa F., Masojídek J. Photosynthesis monitoring to optimize growth of microalgal mass cultures: Application of chlorophyll fluorescence techniques. Aquat. Biol. 2014;22:123–140. doi: 10.3354/ab00597. DOI
Masojídek J., Torzillo G., Koblížek M. Photosynthesis in Microalgae. In: Richmond A., Hu Q., editors. Handbook of Microalgal Culture. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2013. pp. 21–36.
Masojídek J., Vonshak A., Torzillo G. Chlorophyll Fluorescence Applications in Microalgal Mass Cultures. In: Suggett D.J., Prášil O., Borowitzka M.A., editors. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer; Dordrecht, The Netherlands: 2010. pp. 277–292.
Sukenik A., Beardall J., Kromkamp J.C., Kopecký J., Masojídek J., Bergeijk S.A.v., Gabai S., Shaham E., Yamshon A. Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquat. Microb. Ecol. 2009;56:297–308. doi: 10.3354/ame01309. DOI
Butterwick C., Heaney S.I., Talling J.F. A comparison of eight methods for estimating the biomass and growth of planktonic algae. Br. Phycol. J. 1982;17:69–79. doi: 10.1080/00071618200650091. DOI
Bespalov A., Steckler T., Skolnick P. Be positive about negatives–recommendations for the publication of negative (or null) results. Eur. Neuropsychopharmacol. 2019;29:1312–1320. doi: 10.1016/j.euroneuro.2019.10.007. PubMed DOI
Fanelli D. Negative results are disappearing from most disciplines and countries. Scientometrics. 2012;90:891–904. doi: 10.1007/s11192-011-0494-7. DOI
Matosin N., Frank E., Engel M., Lum J.S., Newell K.A. Negativity towards negative results: A discussion of the disconnect between scientific worth and scientific culture. Dis. Model Mech. 2014;7:171–173. doi: 10.1242/dmm.015123. PubMed DOI PMC
Senger H. Charakterisierung einer Synchronkultur von Scenedesmus obliquus, ihrer potentiellen Photosyntheseleistung und des Photosynthese-Quotienten während des Entwicklungscyclus. Planta. 1970;90:243–266. doi: 10.1007/BF00387177. PubMed DOI
Stepanov S.S., Zolotareva E.K. Methanol-induced stimulation of growth, intracellular amino acids, and protein content in Chlamydomonas reinhardtii. J. Appl. Phycol. 2015;27:1509–1516. doi: 10.1007/s10811-014-0445-9. DOI
Wetzel R.G., Linkens G.E. Limnological Analysis. Springer; New York, NY, USA: 1991.
Utermöhl H. Zur Vervollkommnung der quantitativen Phytoplankton Methodik. Int. Ver. Theor. Angew. Limnol. Mitt. 1958;9:1–38. doi: 10.1080/05384680.1958.11904091. DOI
Rott E. Some results from phytoplankton counting intercalibrations. Schweiz. Z. Hydrol. 1981;43:34–62. doi: 10.1007/BF02502471. DOI
Hillebrand H., Dürselen C.-D., Kirschtel D., Pollingher U., Zohary T. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 1999;35:403–424. doi: 10.1046/j.1529-8817.1999.3520403.x. DOI
Jeffrey S.W., Humphrey G.F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 1975;167:191–194. doi: 10.1016/S0015-3796(17)30778-3. DOI
Lorenzen C.J. A method for the continuous measurement of in vivo chlorophyll concentration. Deep. Sea Res. Oceanogr. Abstr. 1966;13:223–227. doi: 10.1016/0011-7471(66)91102-8. DOI
Schuurmans R.M., van Alphen P., Schuurmans J.M., Matthijs H.C.P., Hellingwerf K.J. Comparison of the Photosynthetic Yield of Cyanobacteria and Green Algae: Different Methods Give Different Answers. PLoS ONE. 2015;10:e0139061. doi: 10.1371/journal.pone.0139061. PubMed DOI PMC
Misumi M., Katoh H., Tomo T., Sonoike K. Relationship Between Photochemical Quenching and Non-Photochemical Quenching in Six Species of Cyanobacteria Reveals Species Difference in Redox State and Species Commonality in Energy Dissipation. Plant Cell Physiol. 2016;57:1510–1517. doi: 10.1093/pcp/pcv185. PubMed DOI PMC
Campbell D., Hurry V., Clarke A.K., Gustafsson P., Oquist G. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol. Mol. Biol. Rev. 1998;62:667–683. doi: 10.1128/MMBR.62.3.667-683.1998. PubMed DOI PMC
Ogawa T., Misumi M., Sonoike K. Estimation of photosynthesis in cyanobacteria by pulse-amplitude modulation chlorophyll fluorescence: Problems and solutions. Photosynth. Res. 2017;133:63–73. doi: 10.1007/s11120-017-0367-x. PubMed DOI
Rippka R., Deruelles J., Waterbury J.B., Herdman M., Stanier R.Y. Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology. 1979;111:1–61. doi: 10.1099/00221287-111-1-1. DOI
Zarrouk C. Ph.D. Thesis. Universit´e De Paris; Paris, France: 1966. Contribution a l’etude d’une Cyanophycee. Influence de Divers’ Facteurs Physiques et Chimiques Sur La Croissance et La Photosynthese de Spirulina maxima (Setch et Gardner) Geitler.
Nalewajko C. Dry Weight, Ash, and Volume Data for Some Freshwater Planktonic Algae. J. Fish. Res. Board Can. 1966;23:1285–1288. doi: 10.1139/f66-119. DOI
Weil J., Trudel M., Tucker S., Brodeur R.D., Juanes F. Percent ash-free dry weight as a robust method to estimate energy density across taxa. Ecol. Evol. 2019;9:13244–13254. doi: 10.1002/ece3.5775. PubMed DOI PMC
Apha . Standard Methods for the Examination of Water. 22nd ed. American Public Health Association; Albany, NY, USA: 2012.
Schagerl M., Angel R., Donabaum U., Gschwandner A., Woebken D. Limnospira fusiformis harbors dinitrogenase reductase (nifH)-like genes, but does not show N2 fixation activity. Algal Res. 2022;66:102771. doi: 10.1016/j.algal.2022.102771. DOI
Gosselain V., Hamilton P.B., Descy J.-P. Estimating phytoplankton carbon from microscopic counts: An application for riverine systems. Hydrobiologia. 2000;438:75–90. doi: 10.1023/A:1004161928957. DOI
Montagnes D.J.S., Berges J.A., Harrison P.J., Taylor F.J.R. Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton. Limnol. Oceanogr. 1994;39:1044–1060. doi: 10.4319/lo.1994.39.5.1044. DOI
Rocha O., Duncan A. The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. J. Plankton Res. 1985;7:279–294. doi: 10.1093/plankt/7.2.279. DOI
Menden-Deuer S., Lessard E.J. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 2000;45:569–579. doi: 10.4319/lo.2000.45.3.0569. DOI
Carvalho A.P., Monteiro C.M., Malcata F.X. Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavlova lutheri. J. Appl. Phycol. 2009;21:543–552. doi: 10.1007/s10811-009-9415-z. DOI
da Silva Ferreira V., Sant’Anna C. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J. Microbiol. Biotechnol. 2016;33:20. doi: 10.1007/s11274-016-2181-6. PubMed DOI
Canfield D.E., Jr., Linda S.B., Hodgson L.M. Chlorophyll-biomass-nutrient relationships for natural assemblages of Florida phytoplankton. JAWRA J. Am. Water Resour. Assoc. 1985;21:381–391. doi: 10.1111/j.1752-1688.1985.tb00148.x. DOI
Kasprzak P., Padisák J., Koschel R., Krienitz L., Gervais F. Chlorophyll a concentration across a trophic gradient of lakes: An estimator of phytoplankton biomass? Limnologica. 2008;38:327–338. doi: 10.1016/j.limno.2008.07.002. DOI
Schagerl M., Künzl G. Chlorophyll a extraction from freshwater algae—A reevaluation. Biologia. 2007;62:270–275. doi: 10.2478/s11756-007-0048-x. DOI
Pinckney J., Papa R., Zingmark R. Comparison of high-performance liquid chromatographic, spectrophotometric, and fluorometric methods for determining chlorophyll a concentrations in estaurine sediments. J. Microbiol. Methods. 1994;19:59–66. doi: 10.1016/0167-7012(94)90026-4. DOI
Simon D., Helliwell S. Extraction and quantification of chlorophyll a from freshwater green algae. Water Res. 1998;32:2220–2223. doi: 10.1016/S0043-1354(97)00452-1. DOI
Parsons T.R., Maita Y., Lalli C.M. 4.1—Determination of Chlorophylls and Total Carotenoids: Spectrophotometric Method. In: Parsons T.R., Maita Y., Lalli C.M., editors. A Manual of Chemical & Biological Methods for Seawater Analysis. Pergamon; Amsterdam, The Netherlands: 1984. pp. 101–104.
Poikāne S., Alves M.H., Argillier C., van den Berg M., Buzzi F., Hoehn E., de Hoyos C., Karottki I., Laplace-Treyture C., Solheim A.L., et al. Defining Chlorophyll-a Reference Conditions in European Lakes. Environ. Manag. 2010;45:1286–1298. doi: 10.1007/s00267-010-9484-4. PubMed DOI PMC
Mountourakis F., Papazi A., Kotzabasis K. The Microalga Chlorella vulgaris as a Natural Bioenergetic System for Effective CO2 Mitigation—New Perspectives against Global Warming. Symmetry. 2021;13:997. doi: 10.3390/sym13060997. DOI
Takeda H., Hirokawa T. Cell-Wall Chemistry, Structure and Components. In: Linskens H.-F., Jackson J.F., editors. Cell Components. Springer; Berlin/Heidelberg, Germany: 1985. pp. 31–53.
Tsuzuki M., Ohnuma E., Sato N., Takaku T., Kawaguchi A. Effects of CO(2) Concentration during Growth on Fatty Acid Composition in Microalgae. Plant Physiol. 1990;93:851–856. doi: 10.1104/pp.93.3.851. PubMed DOI PMC
Jahnke J., Mahlmann D.M., Jacobs P., Priefer U.B. The influence of growth conditions on the cell dry weight per unit biovolume of Klebsormidium flaccidum (Charophyta), a typical ubiquitous soil alga. J. Appl. Phycol. 2011;23:655–664. doi: 10.1007/s10811-010-9557-z. DOI
Jahnke J., Mahlmann D.M. Differences in the cellular dry weight per unit biovolume of Phormidium autumnale (Cyanobacteria) dependent on growth conditions. J. Appl. Phycol. 2010;22:117–122. doi: 10.1007/s10811-009-9430-0. DOI
Vonshak A. Microalgae: Laboratory growth techniques and the biotechnology of biomass production. In: Hall D.O., Scurlock J.M.O., Bolhàr-Nordenkampf H.R., Leegood R.C., Long S.P., editors. Photosynthesis and Production in a Changing Environment: A Field and Laboratory Manual. Springer; Dordrecht, The Netherlands: 1993. pp. 337–355.
Hyka P., Lickova S., Přibyl P., Melzoch K., Kovar K. Flow cytometry for the development of biotechnological processes with microalgae. Biotechnol. Adv. 2013;31:2–16. doi: 10.1016/j.biotechadv.2012.04.007. PubMed DOI
Chioccioli M., Hankamer B., Ross I.L. Flow Cytometry Pulse Width Data Enables Rapid and Sensitive Estimation of Biomass Dry Weight in the Microalgae Chlamydomonas reinhardtii and Chlorella vulgaris. PLoS ONE. 2014;9:e97269. doi: 10.1371/journal.pone.0097269. PubMed DOI PMC
Takahashi T. Routine Management of Microalgae Using Autofluorescence from Chlorophyll. Molecules. 2019;24:4441. doi: 10.3390/molecules24244441. PubMed DOI PMC
Griffiths M.J., Garcin C., van Hille R.P., Harrison S.T.L. Interference by pigment in the estimation of microalgal biomass concentration by optical density. J. Microbiol. Methods. 2011;85:119–123. doi: 10.1016/j.mimet.2011.02.005. PubMed DOI
Santos-Ballardo D.U., Rossi S., Hernández V., Gómez R.V., del Carmen Rendón-Unceta M., Caro-Corrales J., Valdez-Ortiz A. A simple spectrophotometric method for biomass measurement of important microalgae species in aquaculture. Aquaculture. 2015;448:87–92. doi: 10.1016/j.aquaculture.2015.05.044. DOI
Srinivas S.P., Mutharasan R. Inner filter effects and their interferences in the interpretation of culture fluorescence. Biotechnol. Bioeng. 1987;30:769–774. doi: 10.1002/bit.260300609. PubMed DOI
Zhang C., Liu M.-S., Han B., Xing X.-H. Correcting for the inner filter effect in measurements of fluorescent proteins in high-cell-density cultures. Anal. Biochem. 2009;390:197–202. doi: 10.1016/j.ab.2009.04.029. PubMed DOI
Panigrahi S.K., Mishra A.K. Study on the dependence of fluorescence intensity on optical density of solutions: The use of fluorescence observation field for inner filter effect corrections. Photochem. Photobiol. Sci. 2019;18:583–591. doi: 10.1039/C8PP00498F. PubMed DOI
Falkowski P., Kiefer D.A. Chlorophyll a fluorescence in phytoplankton: Relationship to photosynthesis and biomass. J. Plankton Res. 1985;7:715–731. doi: 10.1093/plankt/7.5.715. DOI
Catherine A., Escoffier N., Belhocine A., Nasri A.B., Hamlaoui S., Yéprémian C., Bernard C., Troussellier M. On the use of the FluoroProbe®, a phytoplankton quantification method based on fluorescence excitation spectra for large-scale surveys of lakes and reservoirs. Water Res. 2012;46:1771–1784. doi: 10.1016/j.watres.2011.12.056. PubMed DOI
Kruskopf M., Flynn K.J. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 2006;169:525–536. doi: 10.1111/j.1469-8137.2005.01601.x. PubMed DOI
Rolton A., McCullough A., Tuckey N.P.L., Finnie B., Cooper I., Packer M.A., Vignier J. Early biomarker indicators of health in two commercially produced microalgal species important for aquaculture. Aquaculture. 2020;521:735053. doi: 10.1016/j.aquaculture.2020.735053. DOI
Spilling K., Seppälä J. Measurement of Fluorescence for Monitoring Algal Growth and Health. In: Spilling K., editor. Biofuels from Algae: Methods and Protocols. Springer; New York, NY, USA: 2020. pp. 41–45. PubMed
Bemejo-Padilla E., Kinsou H., Filali R., Perez-Bibbins B., Taidi B. Rapid indicators for monitoring the health of Chlamydomonas nivalis biomass during preservation. J. Appl. Phycol. 2021;33:2723–2732. doi: 10.1007/s10811-021-02517-w. DOI