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Citrus essential oil: would it be feasible as antimicrobial in the bioethanol industry?

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Abstract

Essential oils (EOs) extracted from Citrus peels contain 85%–99% volatile components (a mixture of monoterpenes, sesquiterpenes, and their oxygenated derivatives) and 1%–15% non-volatile compounds. Citrus EOs have been long known for their antimicrobial properties, owing to which these EOs have a diverse range of applications. However, no studies have reported the applicability of Citrus EOs for the control of bacterial and yeast contaminants in the bioethanol industry. In this regard, the present review aimed to explore the feasibility of Citrus EOs in this industry. The Web of Science database was searched for reports that described the association of Citrus EOs with the most common microorganisms in the bioethanol industry to evaluate the efficacy of these EOs as antimicrobial agents in this context. The objective of the review was to suggest a novel antimicrobial that could replace sulfuric acid and antibiotics as the commonly used antimicrobial agents in the bioethanol industry. Citrus EOs exhibit antibacterial activity against Lactobacillus, which is the main bacterial genus that contaminates this fermentation process. The present report also confirms the selective action of these EOs on the contaminating yeasts and not/less on ethanol-producing yeast Saccharomyces cerevisiae, however further studies should be conducted to investigate the effects of Citrus EOs in yeast-bacterium co-culture.

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Fig. 1

Kharfan and Toledo (2014) and Pauletti and Silvestre (2018)

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References

  • Ajayi-Moses OB, Ogidi CO, Akinyele BJ (2019) Bioactivity of Citrus essential oils (CEOs) against microorganisms associated with spoilage of some fruits. Chem Biol Technol Agric 22:1–15

    Google Scholar 

  • Akarca G, Sevik R (2022) Biological activities of Citrus limon L. and Citrus sinensis L. peel essential oils. J Essent Oil-Bear Plants 24:1415–1427

    Article  Google Scholar 

  • Alderees F, Mereddy R, Were S, Netzel ME, Sultanbawa Y (2021) Anti-yeast synergistic effects and mode of action of Australian native plant essential oils. Appl Sci 11:10670

    Article  CAS  Google Scholar 

  • Ambrosio CMS, Alencar SM, Sousa RLM, Moreno AM, Gloria EM (2017) Antimicrobial activity of several essential oils on pathogenic and beneficial bacteria. Ind Crops Prod 97:128–136

    Article  CAS  Google Scholar 

  • Ambrosio CMS, Ikeda NY, Miano AC, Saldaña E, Moreno AM, Stashenko E, Contreras-Castillo CJ, Gloria EM (2019) Unraveling the selective antimicrobial activity and chemical composition of citrus essential oils. Sci Reports 9:17719

    Google Scholar 

  • Ambrosio CMS, Contreras-Castillo CJ, Gloria EM (2020) In vitro mechanism of antibacterial action of a citrus essential oil on an enterotoxigenic Escherichia coli and Lactobacillus rhamnosus. J Appl Microbiol 129:541–553

    Article  CAS  Google Scholar 

  • Amorim HV, Lopes ML, Oliveira JVC, Buckeridge MS, Goldman GH (2011) Scientific challenges of bioethanol production in Brazil. Appl Microbiol Biotechnol 91:1267–1275

    Article  CAS  Google Scholar 

  • Asikin Y, Kawahira S, Goki M, Hirose N, Kyoda S, Wada K (2018) Extended aroma extract dilution analysis profile of Shiikuwasha (Citrus depressa Hayata) pulp essential oil. J Food Drug Anal 26:268–276

    Article  CAS  Google Scholar 

  • Basso TO, Gomes FS, Lopes ML, Amorim HV, Eggleston G, Basso LC (2014) Homo-and heterofermentative lactobacilli differently affect sugarcane-based fuel ethanol fermentation. Antonie Van Leeuwenhoek 105:169–177

    Article  CAS  Google Scholar 

  • Bassolé IH, Juliani HR (2012) Essential oils in combination and their antimicrobial properties. Molecules 17:3989–4006

    Article  Google Scholar 

  • Bevilacqua A, Corbo MR, Sinigaglia M (2010) In vitro evaluation of the antimicrobial activity of eugenol, limonene, and Citrus extract against bacteria and yeasts, representative of the spoiling microflora of fruit juices. J Food Prot 73:888–894

    Article  CAS  Google Scholar 

  • Bevilacqua A, Speranza B, Campaniello D, Corbo MR, Sinigaglia M (2013) Inhibition of spoiling yeasts of fruit juices through Citrus extracts. J Food Prot 76:1753–1760

    Article  Google Scholar 

  • Bialon M, Krzysko-Lupicka T, Koszalkowska M, Wieczorek PP (2014) The influence of chemical composition of commercial lemon essential oils on the growth of Candida strains. Mycopathologia 177:29–39

    Article  CAS  Google Scholar 

  • Bischoff KM, Liu S, Leathers TD, Worthington RE, Rich JO (2009) Modelling bacterial contamination of fuel ethanol fermentation. Biotechnol Bioeng 103:117–122

    Article  CAS  Google Scholar 

  • Bnina EB, Daami-Remadi JHB (2020) Access to oxygenated monoterpenes via the biotransformation of (R)-limonene by Trichoderma harzianum and Saccharamyces cerevisiae. Chemistry Africa 3:647–656

    Article  Google Scholar 

  • Brennan TCR, Kromer JO, Nielsen LK (2013) Physiological and transcriptional responses of Saccharomyces cerevisiae to d-limonene show changes to the cell wall but not to the plasma membrane. Appl Environ Microbiol 79:3590–3600

    Article  CAS  Google Scholar 

  • Calo JR, Crandall PG, O’Bryan CA, Ricke SC (2015) Essential oils as antimicrobials in food systems – a review. Food Control 54:111–119

    Article  CAS  Google Scholar 

  • Campedelli I, Mathur H, Salvetti E, Clarke S, Rea MC, Torriani S, Ross RP, Hill C, O’Toole PW (2018) Genus-wide assessment of antibiotic resistance in Lactobacillus spp. Appl Environ Microbiol 85:e01738-e1818

    Google Scholar 

  • Ceccato-Antonini SR (2018) Conventional and nonconventional strategies for controlling bacterial contamination in fuel ethanol fermentations. World J Microbiol Biotechnol 34:80

    Article  Google Scholar 

  • Chouhan S, Sharma K, Guleria S (2017) Antimicrobial activity of some essential oils – present status and future perspectives. Medicines 4:58

    Article  Google Scholar 

  • Cristani MT, D’Arrigo M, Mandalari G, Castelli F, Sarprieto MG, Micieli D, Venuti V, Bisignano G, Saija A, Trombetta D (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308

    Article  CAS  Google Scholar 

  • Dellias MDTF, Borges CD, Lopes ML, Cruz SH, Amorim HV, Tsai SM (2018) Biofilm formation and antimicrobial sensitivity of Lactobacilli contaminants from sugarcane-based fuel ethanol fermentation. Antonie Van Leeuwenhoek 111:1631–1644

    Article  CAS  Google Scholar 

  • Deng W, Liu K, Cao S, Sun J, Zhong B, Chun J (2020) Chemical composition, antimicrobial, antioxidant, and antiproliferative properties of grapefruit essential oil prepared by molecular distillation. Molecules 25:217

    Article  CAS  Google Scholar 

  • Denkova-Kostova RS, Goranov BG, Teneva DG, Tomova TG, Denkova ZR, Shopska V, Mihaylova-Ivanova Y (2021) Bio-preservation of chocolate mousse with free and immobilized cells of Lactobacillus plantarum D2 and lemon (Citrus lemon L.) or grapefruit (Citrus paradise L.) zest essential oils. Acta Sci Pol Technol Aliment 20:5–16

    CAS  Google Scholar 

  • Ellouze I, Abderrabba M, Sabaou N, Mathieu F, Lebrihi A, Bouajila J (2012) Season’s variation impact on Citrus aurantium leaves essential oil: chemical composition and biological activities. J Food Sci 77:173–180

    Article  Google Scholar 

  • Ephrem E, Najjar A, Charcosset C, Greige-Gerges H (2019) Selection of nerolidol among a series of terpenic and phenolic compounds for its potent activity against Lactobacillus fermentum ATCC 9338. Process Biochem 80:146–156

    Article  CAS  Google Scholar 

  • Fancello F, Petretto GL, Zara S, Sanna ML, Addis R, Maldini M, Foddai M, Rourke JP, Chessa M, Pintore G (2016) Chemical characterization, antioxidant capacity and antimicrobial activity against food related microorganisms of Citrus limon var. pompia leaf essential oil. LWT Food Sci Technol 69:579–585

    Article  CAS  Google Scholar 

  • Fisher K, Phillips C (2008) Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends in Food Sci Technol 19:156–164

    Article  CAS  Google Scholar 

  • Fisher K, Phillips C (2009) The mechanism of action of a citrus oil blend against Enterococcus faecium and Enterococcus faecalis. J Appl Microbiol 106:1343–1349

    Article  CAS  Google Scholar 

  • Frost I, Smith WPJ, Mitri S, Millan AS, Davit Y, Osborne JM, Pitt-Francis JM, MacLean CR, Foster KR (2018) Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J 12:1582–1593

    Article  CAS  Google Scholar 

  • Gao Z, Zhong W, Chen K, Tang P, Guo J (2020) Chemical composition and anti-biofilm activity of essential oil from Citrus medica L. var. sarcodactylis Swingle against Listeria monocytogenes. Ind Crops Prod 144:02036

    Article  Google Scholar 

  • Guo JJ, Gao ZP, Xia JL, Ritenour MA, Li GY, Shan Y (2018) Comparative analysis of chemical composition, antimicrobial and antioxidant activity of citrus essential oils from the main cultivated varieties in China. LWT Food Sci Technol 97:825–839

    Article  Google Scholar 

  • Hamdan D, El-Readi MZ, Nibret E, Sporer F, Farrag N, El-Shazly A, Wink M (2010) Chemical composition of the essential oils of two Citrus species and their biological activities. Pharmazie 65:141–147

    CAS  Google Scholar 

  • Hamdan D, Ashour ML, Mulyaningsih S, El-Shazly A, Wink M (2013) Chemical composition of the essential oils of variegated pink-fleshed lemon (Citrus x limon L. Burm. f.) and their anti-inflammatory and antimicrobial activities. Z Naturforsch C J Biosci 68:275–284

    Article  CAS  Google Scholar 

  • Hsouna AB, Hamdi N, Halima NB, Abdelkafi S (2013) Characterization of essential oil from Citrus aurantium L. flowers: antimicrobial and antioxidant activity. J Oleo Sci 62:763–772

    Article  Google Scholar 

  • Hyldgaard M, Mygind T, Meyer RL (2012) Essential oils in food preservation: mode of action, synergism, and interaction with food matrix components. Front Microbiol 3:1–24

    Article  Google Scholar 

  • Kharfan D, Toledo JC (2014) Proposta de método para avaliação do desempenho técnico do processo de extração de sucos cítricos. Rev Espacios 35:1–11

    Google Scholar 

  • Khorsandi A, Ziaee E, Shad E, Razmjooei M, Eskandari MH, Aminlari M (2018) Antibacterial effect of essential oils against spoilage bacteriafrom vacuum-packed cooked cured sausages. J Food Prot 81:1386–1393

    Article  Google Scholar 

  • Konuk HB, Erguden B (2017) Antifungal activity of various essential oils against Saccharomyces cerevisiae depends on disruption of cell membrane integrity. Biocell 41:13–18

    Article  CAS  Google Scholar 

  • Konuk HB, Erguden B (2019) Spindle pole body duplication defective yeast cells are more prone to membrane damage. Mycologia 111:895–903

    Article  CAS  Google Scholar 

  • Kunicka-Styczyńska A (2011) Activity of essential oils against food-spoiling yeast. A Review. Flavour Fragr J 26:326–328

    Article  Google Scholar 

  • Leite MCA, Bezerra APB, Sousa JP, Guerra FQS, Lima EO (2014) Evaluation of antifungal activity and mechanism of action of citral against Candida albicans. Evid Based Complement Alternat Med 2014:378280

    Article  Google Scholar 

  • Lemes RS, Alves CCF, Estevam EBB, Santiago MB, Martins CHG, Santos TCL, Crotti AEM, Miranda MLD (2018) Chemical composition and antibacterial activity of essential oils from Citrus aurantifolia leaves and fruit peel against oral pathogenic bacteria. An Acad Bras Cienc 90:1285–1292

    Article  CAS  Google Scholar 

  • Liu J, Zhu Y, Du G, Zhou J, Chen J (2012) Exogenous ergosterol protects Saccharomyces cerevisiae from D-limonene stress. J Appl Microbiol 114:482–491

    Article  Google Scholar 

  • Lourencetti NMS, Wolf IR, Lacerda MPF, Valente GT, Zanelli CF, Santoni MM, Mendes-Giannini EFJ, Fusco-Almeida AM (2018) Transcriptional profile of a bioethanol production contaminant Candida tropicalis. AMB Express 8:166

    Article  Google Scholar 

  • Machado TF, Nogueira NAP, Pereira RCA, Sousa CT, Batista VCV (2014) The antimicrobial efficacy of Lippia alba essential oil and its interaction with food ingredients. Braz J Microbiol 45:699–705

    Article  CAS  Google Scholar 

  • Mani-López E, Cortés-Zavaleta L-M (2021) A review of the methods used to determine the target site or the mechanism of action of essential oils and their components against fungi. SN Appl Sci 3:44

    Article  Google Scholar 

  • Marchese E, D’Onofrio N, Balestrieri ML, Castaldo D, Ferrari G, Donsi F (2020) Bergamot essential oil nanoemulsions: antimicrobial and cytotoxic activity. Z Naturforsch 75:279–290

    Article  CAS  Google Scholar 

  • Martins AP, Nogueira MT, Costa MC, Salgueiro L (2011) Requisitos de qualidade em óleos essenciais: a importância das monografias da Farmacopeia Europeia e das Normas ISO. Rev Fitoterapia 11:133–145

    Google Scholar 

  • Miller AB, Cates RG, Lawrence M, Soria JAF, Espinoza LV, Martinez JV, Arbizú DA (2015) The antibacterial and antifungal activity of essential oils extracted from Guatemalan medicinal plants. Pharm Biol 53:548–554

    Article  CAS  Google Scholar 

  • Mitropoulou G, Fitsiou E, Spyridopoulou T-K, Bardouki H, Vamvakias M, Panas P, Chlichlia K, Pappa A, Kourkoutas Y (2017) Citrus medica essential oil exhibits significant antimicrobial and antiproliferative activity. LWT Food Sci Technol 84:344–352

    Article  CAS  Google Scholar 

  • Narendranath NV, Hynes SH, Thomas KC, Ingledew WM (1997) Effects of Lactobacilli on yeast-catalyzed ethanol fermentations. Appl Environ Microbiol 63:4158–4163

    Article  CAS  Google Scholar 

  • Nazzaro F, Fratianni F, de Martino L, Coppola R, de Feo V (2013) Effect of essential oils on pathogenic bacteria. Pharmaceuticals 6:1451–1474

    Article  Google Scholar 

  • Okunowo WO, Oyedeji O, Afolabi LO, Matanmi E (2013) Essential oil of grapefruit (Citrus paradisi) peels and its antimicrobial activities. Am J Plant Sci 4:1–9

    Article  Google Scholar 

  • Orchard A, van Vuuren S (2017) Commercial essential oils as potential antimicrobials to treat skin diseases. Evid Based Complement Alternat Med 2017:4517971

    Article  Google Scholar 

  • Palazzolo E, Laudicina VA, Germanà MA (2013) Current and potential use of citrus essential oils. Curr Org Chem 17:3042–3049

    Article  CAS  Google Scholar 

  • Pauletti GF, Silvestre WP (2018) Óleo essencial cítrico: produção, composição e fracionamento. In: Efrom CF, Souza PVD (eds) Citricultura do Rio Grande do Sul: indicações técnicas. Porto Alegre, SEAPI, pp 245–268

    Google Scholar 

  • Pedrosa GTS, Carvalho RJ, Berdejo D, Souza EL, Pagán R, Magnani M (2019) Control of autochthonous spoilage lactic acid bacteria in apple and orange juices by sensorially accepted doses of Citrus spp. Essential oils combined with mild heat treatments. J Food Sci 84:848–858

    Article  Google Scholar 

  • Peric M, Rajkovic K, Lemic AM, Zivkovic R, Arsenijevic VA (2019) Development and validation of mathematical models for testing antifungal activity of different essential oils against Candida species. Arch Oral Biol 98:258–264

    Article  CAS  Google Scholar 

  • Queiroz LL, Costa MS, Pereira AA, Aila MP, Costa PS, Nascimento AMA, Lacorte GA (2020) Dynamics of microbial contaminants is driven by selection during ethanol production. Braz J Microbiol 51:303–312

    Article  CAS  Google Scholar 

  • Raspo MA, Vignola MB, Andreatta AE, Juliani HR (2020) Antioxidant and antimicrobial activities of citrus essential oils from Argentina and the United States. Food Biosci 36:100561

    Article  Google Scholar 

  • Sharma K, Mahato N, Cho MH, Lee YR (2017) Converting citrus wastes into value-added products: economic and environmentally friendly approaches. Nutrition 34:29–46

    Article  CAS  Google Scholar 

  • Shehata AS, Abdeldaym EA, Ali MR, Mohamed RM, Bob RI, Abdelgawad KF (2020) Effect of some citrus essential oils on post-harvest shelf life and physicochemical quality of strawberries during cold storage. Agronomy 10:1466

    Article  CAS  Google Scholar 

  • Souza-Liberal AT, Basilio ACM, Monte Resende A, Brasileiro BTV, Silva-Filho EA, Morais JOF, Simões DA, Morais Junior MA (2007) Identification of Dekkera bruxellensis as a major contaminant yeast in continuous fuel etanol fermentation. J Appl Microbiol 102:538–547

    Article  Google Scholar 

  • Teneva D, Denkova-Kostova R, Goranov B, Hristova-Ivanova Y, Slavchev A, Denkova Z, Kostov G (2019) Chemical composition, antioxidant activity and antimicrobial activity of essential oil from Citrus aurantium L zest against some pathogenic microorganisms. Z Naturforsch 74:105–111

    Article  CAS  Google Scholar 

  • USDA (2022) Citrus: world markets and trades. https://apps.fas.usda.gov/psdonline/circulars/citrus.pdf. Accessed 25 Jul 2022

  • Varano A, Shirahigue LD, Azevedo FA, Altenhofen da Silva M, Ceccato-Antonini SR (2022) Mandarin essential oil as an antimicrobial in ethanolic fermentation: effects on Limosilactobacillus fermentum and Saccharomyces cerevisiae. Lett Appl Microbiol 74:981–991

    Article  CAS  Google Scholar 

  • Vito MD, Bellardi MG, Sanguinetti M, Mondello F, Girolamo A, Barbanti L, Garzoli S, Sabatino M, Ragno R, Vitali A, Palucci I, Posteraro B, Gasbarrini A, Prati GM, Aragona G, Mattarelli P, Bugli F (2020) Potent in vitro activity of Citrus aurantium essential oils and Vitis vinifera hydrolate against gut yeast isolates from irritable bowel syndrome patients – the right mix for potential therapeutic use. Nutrients 12:1329

    Article  CAS  Google Scholar 

  • Wilkins MR, Suryawati L, Maness NO, Chrz D (2007) Ethanol production by Saccharomyces cerevisiae and Kluyveromyces marxianus in the presence of orange-peel oil. World J Microbiol Biotechnol 23:1161–1168

    Article  CAS  Google Scholar 

  • Wiwattanarattanabut K, Choonharuangdej S, Srithavaj T (2017) In vitro anti-cariogenic plaque effects of essential oils extracted from culinary herbs. J Clin Diagn Res 11:DC30–DC35

    CAS  Google Scholar 

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Funding

This work was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP process 2018/19139–2, research grant), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process 309688/2018–3, fellowship to SRCA) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Finance Code 001, fellowships to AV and LDS).

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  1. Dept Tecnologia Agroindustrial e Socio-Economia Rural, Centro de Ciências Agrárias, Universidade Federal de São Carlos, Campus de Araras, Via Anhanguera Km 174, Araras, SP, 13600-970, Brasil

    Sandra Regina Ceccato-Antonini, Ligianne Din Shirahigue, Amanda Varano, Bianca Novaes da Silva & Carina Sawaya Brianti

  2. Centro de Citricultura Sylvio Moreira, Instituto Agronômico (IAC), Via Anhanguera Km 158, Cordeirópolis, SP, 13490-970, Brasil

    Fernando Alves de Azevedo

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  1. Sandra Regina Ceccato-Antonini
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  2. Ligianne Din Shirahigue
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  3. Amanda Varano
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  4. Bianca Novaes da Silva
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  5. Carina Sawaya Brianti
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SRCA conceived, designed, wrote, and revised the manuscript. AA, FAA, LDS, BNS, and CSB wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Sandra Regina Ceccato-Antonini.

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Ceccato-Antonini, S.R., Shirahigue, L.D., Varano, A. et al. Citrus essential oil: would it be feasible as antimicrobial in the bioethanol industry?. Biotechnol Lett 45, 1–12 (2023). https://doi.org/10.1007/s10529-022-03320-4

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