Abstract
The Antarctic continent is a reservoir of new genetic resources to the bioprospection of microorganisms adapted to the polar conditions and capable to produce molecules with differentiated properties. Biosurfactants are a promising alternative to replace synthetic surfactants due to their eco-friendly characteristics and the possibility of being produced from raw materials, such as lignocellulosic biomass. The aim of the current study was to evaluate the biosurfactants produced by Antarctic yeast strains using detoxified sugarcane straw hemicellulosic hydrolysate (DSSHH). Therefore, the biosurfactant production, using xylose as the carbon source, was first evaluated in semi-defined medium and subsequently in DSSHH. The Naganishia adellienses L95 showed the highest emulsification index (52%) and total xylose consumption (40 g.L−1) in DSSHH. The biosurfactant produced by the yeast strain L95 was partially characterized, and its emulsion remained stable under low-temperature conditions (0 and 4 °C), at high salt concentration (10%), and alkaline condition. The screening of yeasts for the attainment of natural products that have potential biotechnological applications is of great importance. The results showed the potential of L95 to produce biosurfactants in DSSHH.
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Martínez-Rosales C, Fullana N, Musto H, Castro-Sowinski S (2012) Antarctic DNA moving forward: genomic plasticity and biotechnological potential. FEMS Microbiol Lett 331:1–9
Nicolaus B, Lama MCML, Esposito E (2001) Lipid modulation by environment stress in two models of extremophiles isolated from Antarctica. Polar Biol 24:1–8
Banat IM, Satpute SK, Cameotra SS et al (2014) Cost effective technologies and renewable substrates for biosurfactants production. Front Microbiol 5:1–18
Konishi M, Morita T, Fukuoka T, Imura T, Kakugawa K, Kitamoto D (2007) Production of different types of mannosylerythritol lipids as biosurfactants by the newly isolated yeast strains belonging to the genus Pseudozyma. Appl Microbiol Biotechnol 75:521–531
Rufino RD, Sarubbo LA, Campos-Takaki GM (2008) Enhancement of stability of biosurfactant produced by Candida lipolytica using industrial residue as substrate. World J Microbiol Biotechnol 23:729–734
Luna JM, Rufino RD, Sarubbo LA (2016) Biosurfactant from Candida sphaerica UCP0995 exhibiting heavy metal remediation properties. Process Saf Environ Prot 102:558–566
Sousa TGC, Pinheiro TA, Coelho D, Tambourgi EB et al (2016) Evaluation of biosurfactant production by yeasts from Antarctica. 5th International Symposium On Industrial Biotechnology (IBIC), 49:547–552. https://doi.org/10.3303/CET1649092
Santos DKF et al (2016) Biosurfactants: multifunctional biomolecules of the 21st Century. Int J Mol Sci 17:1–30
Conab, Companhia Nacional de Abastecimento (2020) v. 7 - Safra 2020/21, n.3 - Terceiro Levantamento, December 2020. Brazil
Pippo A, Luengo W, Alonsoamador CA, Morales Alberteris L et al (2011) Energy recovery from sugarcane-trash in the light of 2nd generation biofuels. Part1: current situation and environmental aspects. Waste Biomass Valor 2:1–16
Scheiterle L, Ulmer A, Birner R, Pyka A (2018) From commodity-based value chains to biomass-based value webs: the case of sugarcane in Brazil’s bioeconomy. J Clean Prod 172:3851–3863
Carvalho JLN, Cerri CEP, Karlen DL (2019) Sustainable sugarcane straw special issue: considerations for Brazilian bioenergy production. BioEnergy Research 12:746–748
Menandro LMS, Cantarella H, Franco HCJ, Kölln OT, Pimenta MTB, Sanches GM, Rabelo SC, Carvalho JLN (2017) Comprehensive assessment of sugarcane straw: implications for biomass and bioenergy production. Biofuels Bioprod Biorefin 11:488–504
Dragone G, Kerssemakers AAJ, Driessen JLSP, Yamakawa CK, Brumano LP, Mussatto SI (2020) Innovation and strategic orientations for the development of advanced biorefineries. Bioresour Technol 302:122847
Duarte AWF, Dayo-Owoyemi I, Nobre FS, Pagnocca FC, Chaud LCS, Pessoa A, Felipe MGA, Sette LD (2013) Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles 17:1023–1035
Kitamoto D, Fuzishiro T, Yanagishita H, Nakane T (2001) Production of biosurfactants by Candida antarctica. Biochem Eng:215–217
Ferraz A, Baeza J, Rodriguez J, Freer J (2000) Estimating the chemical composition of biodegraded pine and eucalyptus wood by drift spectroscopy and multivariate analysis. Bioresour Technol 74:201–212
Marton JM, Felipe MGA, Silva JBA, Pessoa Junior A (2006) Evaluation of theactivated charcoals and adsorption conditions used in the treatment of sugarcane bagasse hydrolysate for xylitol production. Braz J Chem Eng 23:9–21
Nitschke M, Pastore GM (2004) Biosurfactant production by B. subtilis using cassava-processing effluent. Appl Biochem Biotechnol 112:163–172
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia 35(6):1039–1042
Francy DS et al (1991) Emulsification of hydrocarbons by subsurface bacteria. J Ind Microbiol 8:237–246
Siegmund I, Fritz W (1991) New method for detecting rhamnolipids excreted by pseudomonas species during growth on mineral agar. Biotechnol Tech 5:265–268
Gunther NW, Nuñez A, Fett W, Solaiman DK (2005) Production of rhamnolipids by Pseudomonas chlororaphis, a nonpathogenic bacterium. Appl Environ Microbiol 71:2288–2293
Morikawa M, Hirata Y, Imanaka T (2000) A study on the structure function relationship of lipopeptide Biosurfactants. Biochim Biophys Acta 1488:211–218
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229
Hernández-Pérez AFH, Costa IAL, Silva DDV, Dussán KJ et al (2016) Biochemical conversion of sugarcane straw hemicellulosic hydrolysate supplemented with co-substrates for xylitol production. Bioresour Technol 200:1085–1088
Canilha L, Carvalho W, Felipe MGA, Silva JBA, Giulietti M (2010) Ethanol production from sugarcane bagasse hydrolysate using Pichia stipites. Appl Biochem Biotechnol 161(1-8):84–92
Carvalho W, Santos JC, Canilha L, Silva SS, Perego P, Converti A (2005) Xylitol production from sugarcane bagasse hydrolysate Metabolic behaviour of Candida guilliermondii cells entrapped in Ca-alginate. Biochem Eng J 25:25–31
Arruda PV et al (2017) Scale up of xylitol production from sugarcane bagasse hemicellulosic hydrolysate by Candida guilliermondii FTI 20037. J Ind Eng Chem 47:297–302
Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane bagasse hydrolysate improves etanol production by Candida shehatae NCIM 3501. Bioresour Technol 98:1947–1950
Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Brandão LR, Teixeira LCRS, Moliné M, Libkind D, Broock MV, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42(3):937–947
Duarte AWF, Passarini MRZ, Delforno TP, Pellizzari FM, Cipro CVZ, Montone RC, Petry MV, Putzek J, Rosa LH, Sette LD (2016) Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environ Microbiol Rep 8:874–885
Duarte AWF, Dos Santos JA, Vianna MV, Vieira JMF, Mallagutti VH, Inforsato FJ, Wentzel LCP, Lario LD, Rodrigues A, Pagnocca FC, Pessoa A, Sette LD (2018) Cold-adapted enzymes produced by fungi from terrestrial and marine Antarctic environments. Crit Rev Biotechnol 38:600–619
Wentzel LCP, Inforsato FJ, Montoya QV, Rossin BG, Nascimento NR, Rodrigues A, Sette LD (2019) Fungi from Admiralty Bay (King George Island, Antarctica) soils and marine sediments. Microb Ecol 77:12–24
Malavenda R, Rizzo C, Michaud L, Gerçe B, Bruni V, Syldatk C, Hausmann R, Lo Giudice A (2015) Biosurfactant production by Arctic and Antarctic bacteria growing on hydrocarbons. Polar Biol 38(10):1565–1574. https://doi.org/10.1007/s00300-015-1717-9
Jain RM, Mody K, Joshi N, Mishra A, Jha B (2013) Production and structural characterization of biosurfactant produced by an alkaliphilic bacterium, Klebsiella sp.: Evaluation of different carbon sources. Colloids Surf B: Biointerfaces 108:199–204
Joshi-Navare K, Singh PK, Prabhune AA (2014) New yeast isolate Pichia caribbica synthesizes xylolipid biosurfactant with enhanced functionality. Eur J Lipid Sci Technol 116:1070–1079
Chaud LCS, Lario LD, Bonugli-Santos RC, Sette LD, Pessoa Junior A, Felipe MGA (2016) Improvement in extracellular protease production by the marine antarctic yeast Rhodotorula mucilaginosa L7. New Biotechnol 33:807–814
Dimitrova S, Pavlova K, Lukanov L, Korotkova E et al (2013) Production of metabolites with antioxidant and emulsifying properties by antarctic strain Sporobolomyces salmonicolor AL1. Appl Biochem Biotechnol 1:301–311
Kurtzman CP, Price NPJ, Ray KJ, Kuo TM (2010) Production of sophorolipid biosurfactants by multiple species of the Starmerella (Candida) bombicola yeast clade. FEMS Microbiol Lett 311:140–146
Silva DDV, Felipe MGA, Mancilha IM, Luchese RH, Silva SS (2004) Inhibitory effect of acetic acid on bioconversion of xylose in xylitol by Candida guilliermondii in sugarcane bagasse hydrolysate. Braz J Microbiol 35:248–254
Marcelino PRF, Peres GFD, Terán-Hilares R, Pagnocca FC, Rosa CA, Lacerda TM, dos Santos JC, da Silva SS (2019) Biosurfactants production by yeasts using sugarcane bagasse hemicellulosic hydrolysate as new sustainable alternative for lignocellulosic biorefineries. Ind Crop Prod 129:212–223. https://doi.org/10.1016/j.indcrop.2018.12.001
Hernández-Pérez AF, Arruda PV, Felipe MGA (2016) Sugarcane straw as a feedstock for xylitol production by Candida guilliermondii FTI 20037. Braz J Microbiol l.47:2
Candido RG, Mori NR, Gonçalves AR (2019) Sugarcane straw as feedstock for 2G ethanol: evaluation of pretreatments and enzymatic hydrolysis. Ind Crop Prod 142:111845
Rakeshkumar J, Kalpana M, Nidhi J, Avinash M, Bhavanath J (2013) Effect of unconventional carbon sources on biosurfactant production and its application in bioremediation. Int J Biol Macromol 62:52–58. https://doi.org/10.1016/j.ijbiomac.2013.08.030
Giro MEA, Martins JJ, Rocha MV, Melo VM, Gonçalves LR (2009) Clarified cashew apple juice as alternative raw material for biosurfactant production by Bacillus subtilis in a batch bioreactor. Biotechnol J 4(5):738–747
Nair AS, Al-Bahry S, Sivakumar N (2020) Co-production of microbial lipids and biosurfactant from waste office paper hydrolysate using a novel strain Bacillus velezensis ASN1. Biomass Convers Bior 10:383–391
Scorzetti G, Petrescu I, Yarrow D, Fell JW (2000) Cryptococcus adeliensis sp. nov., a xylanase producing basidiomycetous yeast from Antarctica. Antonie Van Leeuwenhoek 77:153–157
Chandankere R, Yaoa J, Choic MMF, Masakorala K, Chana Y (2013) An efficient biosurfactant-producing and crude-oil emulsifying bacterium Bacillus methylotrophicus USTB a isolated from petroleum reservoir. Biochem Eng J 74:46–53
Sobrinho HBS, Rufino RD, Luna JM, Salgueiro AA, Campos-Takaki GM, Leite LFC, Sarubbo LA (2008) Utilization of two agroindusfrial by-products for the productionof a surfactant by Candida sphaerica UCP0995. Process Biochem 43:912–917
Sim L, Ward OP, Li ZY (1997) Production and characterisation of a biosurfactant isolated from Pseudomonas aeruginosa UW-1. J Ind Microbiol Biotechnol 19:232–238
Sarubbo LA, Farias CB, Campos-Takaki GM (2007) Co-utilization of canola oil and glucose on the production of a surfactant by Candida lipolytica. Curr Microbiol 54:68–73
Knoblich A, Matsumoto M, Ishiguro R, Murata K, Fujiyoshi Y, Ishigami Y, Osman M (1995) Electron cryo-microscopic studies on micellar shape and size of surfactin, an anionic lipopeptide. Colloids Surf B: Biointerfaces 5:43–48
Nitschke M, Pastore GM (2002) Biossurfactantes: Propriedades e aplicações. Quím Nova 25:772–776
Calderon F, Poulin P (1999) Progress in understanding emulsion metastability and surface forces. Curr Opin Colloid Interface Sci 4:223–230
Sivapathasekaran C, Mukherjee S, Sen R (2010) Biosurfactant production and growth kinetics of bacteria in a designer marine medium: improved physiochemical properties. Biotechnol J 10:1060–1068
Kokal S (2002) Crude oil emulsions: a state-of-the-art review. In: Annual technical conference and exhibition. Proceedings. San Antonio, Texas, EUA
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The authors would like to thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grant # 2013/19486-0) for the fellowships and for the financial support.
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Chaves, F.d.S., Brumano, L.P., Franco Marcelino, P.R. et al. Biosurfactant production by Antarctic-derived yeasts in sugarcane straw hemicellulosic hydrolysate. Biomass Conv. Bioref. 13, 5295–5305 (2023). https://doi.org/10.1007/s13399-021-01578-8
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DOI: https://doi.org/10.1007/s13399-021-01578-8