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Schwanniomyces etchellsii, acid-thermotolerant yeasts from urban city soil

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Abstract

Acid-tolerant yeasts are one of the important keys to producing ethanol from acidic substrates, especially from molasses and agricultural waste. In this study, selected cultivars of yeasts isolated from a variety of locations such as botanical gardens in Thailand urban areas, which are often found highly polluted in the air such as carbon dioxide which is a cause of acid rain. There is limited information about how tolerant yeasts, are or their functional properties related to the environment. Yeast species were determined by using the 18S rDNA sequence guide. The level of acid tolerance was evaluated by adding to the culture medium lactic acid (300–900 mM), acetic acid (100–400 mM), and propionic acid (25–100 mM). 18S rDNA analysis has shown a %similarity of the nucleotide sequence higher than 98.65% compared to the database. Schwanniomyces etchellsii strains found in urban city soil were notable for their tolerance of lactic acid up to 100 mM. There are two main types of yeasts in overall acid tolerance: S. etchellsii, which is recognized as an osmotic pressure-resistant species that is highly resistant to fermentation inhibitors and produces ethanol; and Schizosaccharomyces pombe, which cell wall has been reported to be characterized by accumulation of α-(1,3)-glucan and malic acid can be used in metabolic pathways. The results show that S. pombe, isolated from rice paddy fields, can grow efficiently in acetic and propionic acid up to 400 mM and 100 mM, respectively. This species could be cultured in ethanol at a concentration of 12.5% (v/v). Moreover, it presented high ethanol and acetic acid production of 14.5–15.9 g/L and 7–10 g/L, respectively, with or without acidic conditions. In comparison, S. etchellsii, isolated from the botanical garden soil, which is grown in acetic, propionic, and lactic acid, was also indicated to be an organic acid-tolerant species.

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References

  • Ahmadi N, Khosravi-Darani K, Mortazavian AM (2017) An overview of biotechnological production of propionic acid: from upstream to downstream processes. Electron J Biotechnol 28:67–75

    Article  CAS  Google Scholar 

  • Arous F, Azabou S, Jaouani A, Zouari-Mechichi H, Nasri M, Mechichi T (2016a) Biosynthesis of single-cell biomass from olive mill wastewater by newly isolated yeasts. Environ Sci Pollut Res 23:6783–6792

    Article  CAS  Google Scholar 

  • Arous F, Mechichi T, Nasri M, Aggelis G (2016b) Fatty acid biosynthesis during the life cycle of Debaryomyces etchellsii. Microbiology 162:1080–1090

    Article  CAS  PubMed  Google Scholar 

  • Badea GI, Radu GL (2018) Introductory chapter: carboxylic acids - key role in life sciences. In: Badea GI, Radu GL (eds) Carboxylic acid - key role in life sciences. IntechOpen, London, pp 1–5

    Chapter  Google Scholar 

  • Benito Á, Calderón F, Benito S (2017) The combined use of Schizosaccharomyces pombe and Lachancea thermotolerans-effect on the anthocyanin wine composition. Molecules 22:739

    Article  PubMed  PubMed Central  Google Scholar 

  • Biedunkiewicz A, Bielecki A (2010) Hirudo medicinalis Linnaeus, 1758–a probable vector of transmission of fungi potentially pathogenic for humans; initial studies. Pol J Environ Stud 19:43–47

    Google Scholar 

  • Branduardi P, Dato L, Porro D (2014) Molecular tools and protocols for engineering the acid-tolerant yeast Zygosaccharomyces bailii as a potential cell factory. Yeast metabolic engineering. Humana Press, New York, pp 63–85

    Chapter  Google Scholar 

  • Carneiro CVG, Silva FCDPE, Almeida JR (2019) Xylitol production: identification and comparison of new producing yeasts. Microorganisms 7:484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caspeta L, Nielsen J (2015) Thermotolerant yeast strains adapted by laboratory evolution show trade-off at ancestral temperatures and preadaptation to other stresses. Mbio 6:e00431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chahardoli A, Jalilian F, Memariani Z, Farzaei MH, Shokoohinia Y (2020) Analysis of organic acids. In: Sanches SA, Nabavi SF, Saeedi M, Nabavi SM (eds) Recent Advances in Natural Products Analysis. Elsevier, Amsterdam, pp 767–823

    Chapter  Google Scholar 

  • Choi GW, Um HJ, Kim MN, Kim Y, Kang HW, Chung BW et al (2010) Isolation and characterization of ethanol-producing Schizosaccharomyces pombe CHFY0201. J Microbiol Biotechnol 20:828–834

    CAS  PubMed  Google Scholar 

  • Conte A, Speranza B, Sinigaglia M, Del Nobile MA (2007) Effect of lemon extract on foodborne microorganisms. J Food Prot 70:1896–1900

    Article  CAS  PubMed  Google Scholar 

  • Gemmill TR, Trimble RB (1998) All pyruvylated galactose in Schizosaccharomyces pombe N-glycans is present in the terminal disaccharide, 4, 6-O-[(R)-(1-carboxyethylidine)]-Galβ 1, 3Galα1. Glycobiology 8:1087–1095

    Article  CAS  PubMed  Google Scholar 

  • Guo ZP, Olsson L (2016) Physiological responses to acid stress by Saccharomyces cerevisiae when applying high initial cell density. FEMS Yeast Res 16:7

    Article  Google Scholar 

  • Halm M, Hornbaek T, Arneborg N, Sefa-Dedeh S, Jespersen L (2004) Lactic acid tolerance determined by measurement of intracellular pH of single cells of Candida krusei and Saccharomyces cerevisiae isolated from fermented maize dough. Int J Food Microbiol 94:97–103

    Article  CAS  PubMed  Google Scholar 

  • Ji RY, Ding Y, Shi TQ, Lin L, Huang H, Gao Z et al (2018) Metabolic engineering of yeast for the production of 3-hydroxypropionic acid. Front Microbiol 9:2185

    Article  PubMed  PubMed Central  Google Scholar 

  • Jindamorakot S, Ninomiya S, Limtong S, Yongmanitchai W, Tuntirungkij M, Potacharoen W et al (2009) Three new species of bipolar budding yeasts of the genus Hanseniaspora and its anamorph Kloeckera isolated in Thailand. FEMS Yeast Res 9:1327–1337

    Article  CAS  PubMed  Google Scholar 

  • Kildegaard KR, Jensen NB, Schneider K, Czarnotta E, Özdemir E, Klein T et al (2016) Engineering and systems-level analysis of Saccharomyces cerevisiae for production of 3-hydroxypropionic acid via malonyl-CoA reductase-dependent pathway. Microb Cell Factor 15:53

    Article  Google Scholar 

  • Koivistoinen OM, Kuivanen J, Barth D, Turkia H, Pitkänen JP, Penttilä M et al (2013) Glycolic acid production in the engineered yeasts Saccharomyces cerevisiae and Kluyveromyces lactis. Microb Cell Factories 12:82

    Article  Google Scholar 

  • Kuntiya A, Takenaka S, Seesuriyachan P (2013) High potential of thermotolerant Candida tropicalis no. 10 for high concentration of phenol biodegradation. Food Appl Biosci J 1:59–68

    Google Scholar 

  • Lehmann DM, Krishnakumar K, Batres MA, Hakola-Parry A, Cokcetin N, Harry E et al (2019) A cost-effective colourimetric assay for quantifying hydrogen peroxide in honey. Access Microbiol 1:10

    Article  Google Scholar 

  • Li Y, Adams J, Shi Y, Wang H, He JS, Chu H (2017) Distinct soil microbial communities in habitats of differing soil water balance on the Tibetan Plateau. Sci Rep 7:46407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lidén G (2017) Carboxylic acid production. Fermentation 3:46

    Article  Google Scholar 

  • Loira I, Morata A, Palomero F, González C, Suárez-Lepe JA (2018) Schizosaccharomyces pombe: a promising biotechnology for modulating wine composition. Fermentation 4:70

    Article  Google Scholar 

  • Loureiro V, Malfeito-Ferreira M (2003) Spoilage yeasts in the wine industry. Int J Food Microbiol 86:23–50

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Brauer MJ, Botstein D (2009) Slow growth induces heat-shock resistance in normal and respiratory-deficient yeast. Mol Biol Cell 20:891–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malainey ME (2011) Chapter 5: Organic Compounds. In: Malainey ME (ed) A Consumer’s Guide to Archaeological Science, Manuals in Archaeological Method, Theory and Technique. Springer, New York, pp 45–72

    Chapter  Google Scholar 

  • Martinez FAC, Balciunas EM, Salgado JM, González JMD, Converti A, de Souza Oliveira RP (2013) Lactic acid properties, applications and production: a review. Trends Food Sci Technol 30:70–83

    Article  CAS  Google Scholar 

  • Matsakas L, Topakas E, Christakopoulos P (2014) New trends in microbial production of 3-hydroxypropionic acid. Curr Biochem Eng 1:141–154

    Article  CAS  Google Scholar 

  • Merli G, Becci A, Amato A, Beolchini F (2021) Acetic acid bioproduction: the technological innovation change. Sci Total Environ 798:149292

    Article  CAS  PubMed  Google Scholar 

  • Mira NP, Teixeira MC, Sá-Correia I (2010) Adaptive response and tolerance to weak acids in Saccharomyces cerevisiae: a genome-wide view. OMICS J Integr Biol 14:525–540

    Article  CAS  Google Scholar 

  • Ozaki A, Konishi R, Otomo C, Kishida M, Takayama S, Matsumoto T et al (2017) Metabolic engineering of Schizosaccharomyces pombe via CRISPR-Cas9 genome editing for lactic acid production from glucose and cellobiose. Metab Eng Commun 5:60–67

    Article  PubMed  PubMed Central  Google Scholar 

  • Petersen J, Russell P (2016) Growth and the environment of Schizosaccharomyces pombe. Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.top079764

    Article  PubMed  PubMed Central  Google Scholar 

  • Phommachan K, Keo-oudone C, Nurcholis M, Vongvilaisak N, Chanhming M, Savanhnaly V et al (2022) Adaptive laboratory evolution for multistress tolerance, including fermentability at high glucose concentrations in thermotolerant Candida tropicalis. Energies 15:561

    Article  CAS  Google Scholar 

  • Phongprathet S, Vichitphan K, Han J, Vichitphan S, Swangkaew J (2018) Hanseniaspora thailandica BC9 β-glucosidase for the production of β-D-hexyl glucoside. J Microbiol Biotechnol 28:579–587

    Article  CAS  Google Scholar 

  • Relich RF, Schmitt BH, Koehlinger J, Wiederhold NP, May M (2015) Schwanniomyces etchellsii: an unusual cause of fungemia in a patient with cholecystitis. Diagn Microbiol Infect Dis 84:221–222

    Article  PubMed  Google Scholar 

  • Ribeiro RA, Bourbon-Melo N, Sá-Correia I (2022) The cell wall and the response and tolerance to stresses of biotechnological relevance in yeasts. Front Microbiol 13:953479

    Article  PubMed  PubMed Central  Google Scholar 

  • Sauer M, Porro D, Mattanovich D, Branduardi P (2010) 16 Years research on lactic acid production with yeast-ready for the market. Biotechnol Genet Eng Rev 27:229–256

    Article  CAS  PubMed  Google Scholar 

  • Song Z, Du H, Zhang M, Nie Y, Xu Y (2019) Schizosaccharomyces pombe can reduce acetic acid produced by Baijiu spontaneous fermentation microbiota. Microorganisms 7:606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA (2010) The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J Appl Microbiol 109:13–24

    Article  CAS  PubMed  Google Scholar 

  • Strassburg K, Walther D, Takahashi H, Kanaya S, Kopka J (2010) Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress. OMICS J Integr Biol 14:249–259

    Article  CAS  Google Scholar 

  • Sun W, Vila-Santa A, Liu N, Prozorov T, Xie D, Faria NT, Ferreira FC, Mira NP, Shao Z (2020) Metabolic engineering of an acid-tolerant yeast strain Pichia kudriavzevii for itaconic acid production. Metab Eng Commun. https://doi.org/10.1016/j.mec.2020.e00124

    Article  PubMed  PubMed Central  Google Scholar 

  • Suyama A, Higuchi Y, Urushihara M, Maeda Y, Takegawa K (2017) Production of 3-hydroxypropionic acid via the malonyl-CoA pathway using recombinant fission yeast strains. J Biosci Bioeng 124:392–399

    Article  CAS  PubMed  Google Scholar 

  • Takayama S, Ozaki A, Konishi R, Otomo C, Kishida M, Hirata Y (2018) Enhancing 3-hydroxypropionic acid production in combination with sugar supply engineering by cell surface-display and metabolic engineering of Schizosaccharomyces pombe. Microb Cell Factories 17:176

    Article  CAS  Google Scholar 

  • Thontowi A, Putra FJN, Yopi Y (2017) Evaluation of Non-Saccharomyces cerevisiae strains isolated from sea water against inhibitory compounds for ethanol production. Squalen Bull Mar Fish Postharvest Biotechnol 12:57–65

    Article  Google Scholar 

  • Tikka C, Osuru HP, Atluri N, Raghavulu PCV (2013) Isolation and characterization of ethanol tolerant yeast strains. Bioinformation 9:421–425

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker GM, Stewart GG (2016) Saccharomyces cerevisiae in the production of fermented beverages. Beverages 2:30

    Article  Google Scholar 

  • Wallecha A, Mishra S (2003) Purification and characterization of two β-glucosidases from a thermo-tolerant yeast Pichia etchellsii. Biochim Biophys Acta - Proteins Proteom 1649:74–84

    Article  CAS  Google Scholar 

  • Warnecke T, Gill RT (2005) Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microb Cell Factories 94:25

    Article  Google Scholar 

  • Yadav N, Hakkarainen M (2021) Degradable or not? Cellulose acetate as a model for complicated interplay between structure, environment and degradation. Chemosphere 265:128731

    Article  CAS  PubMed  Google Scholar 

  • Zahoor F, Sooklim C, Songdech P, Duangpakdee O, Soontorngun N (2021) Selection of potential yeast probiotics and a cell factory for xylitol or acid production from honeybee samples. Metabolites 11:312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarnowski R, Sanchez H, Andreu C, Andes D, del Olmo M (2021) Formation and characterization of biofilms formed by salt-tolerant yeast strains in seawater-based growth medium. Appl Microbiol Biotechnol 105:2411–2426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by Research and Researchers for Industries (RRI) by Thailand Research Fund [grant numbers PHD61I0031] and Innovation Institute, PTT Public Co. Ltd. Special Thanks for members of Biofuels by Biocatalysts Research Unit for support.

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Research and Researchers for Industries (RRI) by Thailand Research Fund,PHD61I0031,PHD61I0031,PHD61I0031,Innovation Institute,PTT Public Co. Ltd.

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The authors confirm contribution to the paper as follows: All authors reviewed the results and approved the final version of the manuscript. Study conception and design: NB, CG Acquisition of data: SL, CG Analysis and interpretation of data: SL, NB, CG Drafting of manuscript: SL, CG Critical revision: CG.

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Correspondence to Chompunuch Glinwong.

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Lertsriwong, S., Boonvitthya, N. & Glinwong, C. Schwanniomyces etchellsii, acid-thermotolerant yeasts from urban city soil. World J Microbiol Biotechnol 39, 159 (2023). https://doi.org/10.1007/s11274-023-03602-7

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