Remoção de nutrientes de vinhaça por Klebsormidium flaccidum e produ-ção de biomassa com potencial econômico

Ronald Tarazona Delgado; Mayara dos Santos Guarieiro; Frederico Pacheco Militão; Valéria de Oliveira Fernandes

doi:10.20873/jbb.uft.cemaf.v13n1.18757

Autores/as

Ronald Tarazona Delgado Universidade Federal do Rio Grande https://orcid.org/0000-0003-1366-6269
Mayara dos Santos Guarieiro Universidad Federal de Espírito Santo https://orcid.org/0000-0002-7972-5594
Frederico Pacheco Militão Universidade Federal do Espírito Santo https://orcid.org/0000-0002-9507-8008
Valéria de Oliveira Fernandes Universidad Federal de Espírito Santo https://orcid.org/0000-0002-1968-3927

DOI:

https://doi.org/10.20873/jbb.uft.cemaf.v13n1.18757

Palabras clave:

efluente, microalga, remediação, sustentabilidade

Resumen

El etanol es una alternativa sostenible para la movilidad debido a su baja emisión de carbono. En Brasil, la producción de etanol de la caña de azúcar genera una gran cantidad de vinaza, cuyo principal uso en la fertirrigación causa impactos ambientales negativos. Este estudio tiene como objetivo cultivar la microalga Klebsormidium flaccidum utilizando vinaza como fuente de nutrientes, con el fin de remover nutrientes y producir simultáneamente biomasa de valor económico. Se probaron tres tratamientos con concentraciones de 10%, 20% y 30% de vinaza diluida, denominados T1, T2 y T3, respectivamente. Un cultivo utilizando Bold Basal Medium se consideró como control. Aunque los tratamientos resultaron en densidades celulares inferiores al control, hubo un aumento en la masa seca (MS) debido a la disponibilidad de nutrientes. Los pigmentos fotosintéticos (clorofila a y carotenoides) fueron inferiores en los tratamientos, pero las proteínas (T2 y T3: 8,72 ± 0,11% MS) aumentaron con la adición de vinaza. Los carbohidratos fueron más abundantes en la concentración más baja de vinaza (T1: 66,39% MS), mientras que los lípidos registraron el mayor valor entre los tratamientos en T1 (5,74% MS). Entre los ácidos grasos, se destacó la presencia elevada del ácido mirístico (T3: 164,4 µg g^-1 MS) y el ácido palmítico (T2: 176,4 µg g^-1 MS). K. flaccidum demostró una alta eficiencia en la eliminación de N-total y NH₄⁺ (> 90%) en los tratamientos T2 y T3. Las mayores eliminaciones de P-total, su forma iónica PO₄^-3, y K también ocurrieron en estos tratamientos. Nuestros resultados destacan el potencial de K. flaccidum en la biorremediación de aguas residuales agrícolas, promoviendo una economía sostenible.

Palabras clave: alga, efluente, remediación, sostenibilidad.

Citas

American Public Health Association (APHA). Standard Methods for the Examination for Water and Wastewater. 22th ed. Washington, D.C.: AWWA, WPCF, 2012.

Beuckels A, Smolders E, Muylaert K. Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment. Water Research, v. 77, p. 98-106, 2015.

https://doi.org/10.1016/j.watres.2015.03.018

Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, v. 37, p. 911-917, 1959.

https://doi.org/10.1139/o59-099

Budiyono IS, Sumardiono S, Sasongko SB. Production of Spirulina platensis biomass using digested vinasse as culti-vation medium. Trends in Applied Sciences Research, v. 9, p. 93-102, 2014.

https://doi.org/10.3923/tasr.2014.93.102

Calixto CD, da Silva Santana JK, de Lira EB, Sassi PGP, Rosenhaim R, da Costa Sassi CF, da Conceição MM, Sassi R. Biochemical compositions and fatty acid profiles in four species of microalgae cultivated on household sewage and agro-industrial residues. Bioresource Technology, v. 221, p. 438–446, 2016. https://doi.org/10.1016/j.biortech.2016.09.066

Candido C, Bernardo A, Lombardi AT. Optimization and qualitative comparison of two vinasse pre-treatments aiming at microalgae cultivation. Engenharia Sanitária e Ambiental, v. 26, n. 2, p. 359-367, 2021.

https://doi.org/10.1590/S1413-415220190306

Candido C, Lombardi AT. The physiology of Chlorella vul-garis grown in conventional and biodigested treated vinas-ses. Algal Research, v. 30, p. 79-85, 2018.

https://doi.org/10.1016/j.algal.2018.01.005

Caporgno MP, Taleb A, Olkiewicz M, Font J, Pruvost J, Legrand J, Bengoa C. Microalgae cultivation in urban wastewater: nutrient removal and biomass production for biodiesel and methane. Algal Research, v. 10, p. 232–239, 2015.

https://doi.org/10.1016/j.algal.2015.05.011

Christofoletti CA, Escher JP, Correia JE, Marinho JF, Fonta-netti CS. Sugarcane vinasse: Environmental implications of its use. Waste Management, v. 33, n. 12, p. 2752–2761, 2013.

https://doi.org/10.1016/j.wasman.2013.09.005

Conceição GR, da Silva CS, do Vale TO, dos Santos JN, Matos JBTL, de Almeida PF, Chinalia FA. Culture opera-tional strategies for the production of methane and algal oil using ethanol vinasse effluent. Journal of Applied Phycolo-gy, v. 35, n. 5, p. 2135–2149, 2023. https://doi.org/10.1007/s10811-023-03019-7

Da Silva JC, Lombardi AT. Chlorophylls in Microalgae: Occurrence, Distribution, and Biosynthesis. In: Jacob-Lopes E, Queiroz MI, Zepka LQ (eds). Pigments from Microalgae Handbook. Springer Nature, Switzerland, p. 1-18, 2020.

https://doi.org/10.1007/978-3-030-50971-2

Delgado RT, Guarieiro MS, Antunes PW, Cassini ST, Terre-ros HM, Fernandes VO. Effect of nitrogen limitation on growth, biochemical composition, and cell ultrastructure of the microalga Picocystis salinarum. Journal of Applied Phy-cology v. 33, n. 4, p. 2083–2092, 2021.

https://doi.org/10.1007/s10811-021-02462-8

Engin IK, Cekmecelioglu D, Yücel AM, Oktem HA. Evalua-tion of heterotrophic and mixotrophic cultivation of novel Micractinium sp. ME05 on vinasse and its scale up for bio-diesel production. Bioresource Technology, v. 251, p. 128-134, 2018.

https://doi.org/10.1016/j.biortech.2017.12.023

Ferreira G, Fernandes D, Pinto LR, Tasic M, Maciel Filho R. Investigation of Desmodesmus sp. growth in photobioreac-tor using vinasse as a carbon source. Chemical Engineering Transactions, v. 65, p. 721-726, 2018.

https://doi.org/10.3303/CET1865121

Fogg GE, Thake B. Algal Cultures and Phytoplankton Ecolo-gy. The University of Wisconsin Press, London, 175p., 1987.

Franco-Morgado M, Amador-Espejo GG, Pérez-Cortés M, Gutiérrez-Uribe J.A. Microalgae and Cyanobacteria Poly-saccharides: Important Link for Nutrient Recycling and Re-valorization of Agro-Industrial Wastewater. Applied Food Research, v. 3, n. 100296, p. 1-11, 2023. https://doi.org/10.1016/j.afres.2023.100296

Fuess LT, Garcia ML, Zaiat M. Seasonal characterization of sugarcane vinasse: Assessing environmental impacts from fertirrigation and the bioenergy recovery potential through biodigestion. Science of The Total Environment, v. 634, p. 29–40, 2018.

https://doi.org/10.1016/j.scitotenv.2018.03.326

Grobbelaar JU. The microalgal cell with reference to mass cultures. Inorganic algal nutrition. In: Richmond A, Hu Q (eds). Handbook of Microalgal Culture: Biotechnology and Applied Phycology. Wiley-Blackwell, Oxford, p. 123-133, 2013.

https://doi.org/10.1002/9781118567166.ch8

Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M et al. Klebsormidium flaccidum genome reveals pri-mary factors for plant terrestrial adaptation. Nature Commu-nications, v. 5, p. 3978, 2014. https://doi.org/10.1038/ncomms4978

Jeffrey SW, Humphrey GF. New spectrophotometric equa-tions for determining chlorophylls a, b, c1 and c2 in higher plants, algae, and natural phytoplankton. Biochemie und Physiologie der Pflanzen, v. 167, p. 191-194, 1975. https://doi.org/10.1016/S0015-3796(17)30778-3

Kadioglu A, Algur OF. Tests of media with vinasse for Chla-mydomonas reinhardtii for possible reduction in vinasse pollution. Bioresource Technology, v. 42, n. 1, p. 1-5, 1992. https://doi.org/10.1016/0960-8524(92)90080-H

Karsten U, Herburger K, Holzinger A. Photosynthetic plastici-ty in the green algal species Klebsormidium flaccidum (Streptophyta) from a terrestrial and a freshwater habitat. Phycologia, v. 56, n. 2, p. 213–220, 2016. https://doi.org/10.2216/16-85.1

Kochert G. Carbohydrate determination by phenol–sulfuric acid method. In: Hellebust JA, Craigie JS (eds). Handbook of Phycological Methods: Physiological and Biochemical Methods. Cambridge University Press, Cambridge, p. 95–97, 1978.

Kumar N, Banerjee C, Chang JS, Shukla P. Valorization of wastewater through microalgae as a prospect for generation of biofuel and high-value products. Journal of Cleaner Pro-duction, v. 362, p. 132114, 2022. https://doi.org/10.1016/j.jclepro.2022.132114

Liu J, Danneels B, Vanormelingen P, Vyverman W. Nutrient removal from horticultural wastewater by benthic filamen-tous algae Klebsormidium sp., Stigeoclonium spp. and their communities: From laboratory flask to outdoor algal turf scrubber (ATS). Water Research, v. 92, p. 61-68, 2016.

https://doi.org/10.1016/j.watres.2016.01.049

Liu J, Pemberton B, Lewis J, Scales PJ, Martin GJO. Wastewater treatment using filamentous algae – A review. Bioresource Technology, v. 298, p. 122556, 2020. https://doi. org/10.1016/j.biortech.2019.122556

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. Journal of Bio-logical Chemistry, v. 193, n. 265–275, 1951. https://doi.org/10.1016/S0021-9258(19)52451-6

Lyra FH, Carneiro MTWD, Brandão GP, Pessoa HM, Castro EVR. Determination of Na, K, Ca and Mg in biodiesel sam-ples by flame atomic absorption spectrometry (F AAS) us-ing microemulsion as sample preparation. Microchemical Journal, v. 96, n. 1, p. 180-185, 2010. https://doi.org/10.1016/j.microc.2010.03.005

Markou G, Vandamme D, Muylaert K. Microalgal and cyano-bacterial cultivation: The supply of nutrients. Water Rese-arch, v. 65, p. 186–202, 2014. https://doi.org/10.1016/j.watres.2014.07.025

Marques SSI, Nascimento IA, de Almeida PF, Chinalia FA. Growth of Chlorella vulgaris on sugarcane vinasse: The ef-fect of anaerobic digestion pretreatment. Applied Biochemis-try and Biotechnology, v. 171, p. 1933-1943, 2013. https://doi.org/10.1007/s12010-013-0481-y

Mitra D, Van Leeuwen J., Lamsal B. Hetero-trophic/mixotrophic cultivation of oleaginous Chlorella vul-garis on industrial co-products. Algal Research, v. 1, n. 1, p. 40-48, 2012. https://doi.org/10.1016/j.algal.2012.03.002

Montoya T, Gómez J, Mariano M, Jara E, Carrasco N, Tara-zona R et al. Comunidades aereoterrestres de la microalga Klebsormidium (Klebsormidiophyceae, Streptophyta) en costras biológicas del desierto costero peruano. Arnaldoa, v. 26, n. 3, p. 1105-1124, 2019. https://doi.org/10.22497/arnaldoa.263.26317

Oliveira O, Gianesella S, Silva V, Mata T, Caetano N. Lipid and carbohydrate profile of a microalga isolated from was-tewater. Energy Procedia, v. 136, p. 468–473, 2017. https://doi.org/10.1016/j.egypro.2017.10.305

Patel AK, Vadrale AP, Singhania RR, Michaud P, Pandey A, Chen, SJ. et al. Algal polysaccharides: current status and future prospects. Phytochemistry Reviews, v. 22, p. 1167–1196, 2023.

doi:10.1007/s11101-021-09799-5

Ramirez NNV, Farenzena M, Trierweiler JO. Growth of microalgae Scenedesmus sp. in ethanol vinasse. Brazilian Archives of Biology and Technology, v. 57, n. 5, p. 630-635, 2014.

https://doi.org/10.1590/S1516-8913201401791

Renewable Fuels Association (RFA). Annual Ethanol Produc-tion. Washington, D.C.: RFA, 2024. Available at: https://ethanolrfa.org/markets-and-statistics/annual-ethanol-production. Accessed on: Feb. 20, 2024.

Rodrigues DB, Flores EMM, Barin JS, Mercadante AZ, Jacob-Lopes E, Zepka LQ. Production of carotenoids from microalgae cultivated using agroindustrial wastes. Food Re-search International, v. 65, p. 144–148, 2014. https://doi.org/10.1016/j.foodres.2014.06.037

Santana H, Cereijo CR, Teles VC, Nascimento RC, Fernandes MS, Brunale P. et al. Microalgae cultivation in surgacane vinasse: Selection, growth and biochemical characterization. Bioresource Technology, v. 228, p. 133-140, 2017.

https://doi.org/10.1016/j.biortech.2016.12.075

Santos RR, Araújo ODQF, Medeiros JL, Chaloub RM. Culti-vation of Spirulina maxima in medium supplemented with sugarcane vinasse. Bioresource Technology, v. 204, p. 38-48, 2016.

https://doi. org/10.1016/j.biortech.2015.12.077

Sathasivam R, Radhakrishnan R, Hashem A, Abd Allah EF. Microalgae metabolites: A rich source for food and medi-cine. Saudi Journal of Biological Sciences, v. 26, n. 4, p. 709–722, 2019.

https://doi.org/10.1016/j.sjbs.2017.11.003

Silva AS, Griebeler NP, Borges LC. Uso de vinhaça e impac-tos nas propriedades do solo e lençol freático. Revista Brasi-leira de Engenharia Agrícola e Ambiental, v.11, n.1, p. 108-114, 2007.

https://doi.org/10.1590/S1415-43662007000100014

Singh AK, Sharma N, Farooqi H, Abdin MZ, Mock T, Kumar S. Phycoremediation of municipal wastewater by microalgae to produce biofuel. International Journal of Phytoremedia-tion, v. 19, n. 9, p. 805-812, 2017. https://doi.org/10.1080/15226514.2017.1284758

Siqueira JC, Braga MQ, Ázara MS, Garcia KJ, Alencar SNM, Ramos TS, Siniscalchi LAB, Assemany PP, Ensinas AV. Recovery of vinasse with combined microalgae cultivation in a conceptual energy-efficient industrial plant: Analysis of related process considerations. Renewable and Sustainable Energy Reviews, v. 155, p. 111904, 2022. https://doi.org/10.1016/j.rser.2021.111904

Spolaore P, Joannis-Cassan C, Duran E, Isambert A. Com-mercial application of microalgae. Journal of Bioscience and Bioengineering, v. 101, n. 2, p. 87–96, 2006. https://doi.org/10.1263/jbb.101.87

Stein J. Handbook of Phycological methods. Culture methods and growth measurements. Cambridge University Press, 448 p., 1973.

Strickland JDH, Parsons TR. A practical handbook of sea-water analysis. Bulletin of the Fisheries Research Board of Canada, Ottawa, 310p., 1972.

Syaichurrozi I, Jayanudin J. Effect of tofu wastewater addition on the growth and carbohydrate-protein-lipid content of Spirulina platensis. International Journal of Engineering, v. 30, n. 11, p. 1631–1638, 2017. https://doi.org/10.5829/ije.2017.30.11b.02

Tawfik A, Ismail S, Elsayed M, Qyyum MA, Rehan M. Sus-tainable microalgal biomass valorization to bioenergy: key challenges and future perspectives. Chemosphere, v. 296, p. 133812, 2022.

https://doi.org/10.1016/j.chemosphere.2022.133812

Valderrama LT, Del Campo CM, Rodriguez CM, de Bashan LE, Bashan Y. Treatment of recalcitrant wastewater from ethanol and citric acid production using the microalga Chlo-rella vulgaris and the macrophyte Lemna minuscula. Water Research, v. 36, n. 17, p. 4185-4192, 2002. https://doi.org/10.1016/S0043-1354(02)00143-4

Wang Y, Guo W, Yen HW, Ho SH, Lo YC, Cheng CL, Ren N, Chang JS. Cultivation of Chlorella vulgaris JSC-6 with swine wastewater for simultaneous nutrient/COD removal and carbohydrate production. Bioresource Technology, v. 198, p. 619-625, 2015. https://doi.org/10.1016/j.biortech.2015.09.067

Zhang L, Cheng J, Pei H, Pan J, Jiang L, Hou Q et al. Cultiva-tion of microalgae using anaerobically digested effluent from kitchen waste as a nutrient source for biodiesel production. Renewable Energy, v. 115, p. 276-287, 2018. https://doi.org/10.1016/j.renene.2017.08.034

Zheng S, He M, Jiang J, Zou S, Yang W, Zhang Y et al. Effect of kelp waste extracts on the growth and lipid accu-mulation of microalgae. Bioresource Technology, v. 201, p. 80–88, 2016. https://doi.org/10.1016/j.biortech.2015.11.038

Znad H, Al Ketife AMD, Judd S, AlMomani F, Vuthaluru, HB. Bioremediation and nutrient removal from wastewater by Chlorella vulgaris. Ecological Engineering, v. 110, p. 1-7, 2018.

https://doi.org/10.1016/j.ecoleng.2017.10.008