Abstract
This work proposes a method of forming a microorganism–mediator(s) receptor system, in which the rates of separate stages of mediator bioelectrocatalysis are used as the basis for the development of biosensors for the biochemical oxygen demand (BOD) rapid assay. In the presence of a ferrocene mediator, the yeast Blastobotrys adeninivorans was shown to enable oxidation of a larger range of substrates as compared with other investigated microorganisms—bacteria Escherichia coli and yeast Ogataea polymorpha. The rate constants of the interaction of the yeast B. adeninivorans with nine compounds, electron transfer mediators, were determined; the best mediator for these microorganisms was found to be neutral red (kint = 0.681 ± 0.009 dm3/g s). Neutral red possesses a high rate of interaction with the ferrocene mediator (14,200 ± 100 dm3/mol s) shown earlier to be the most promising acceptor of electrons at a carbon paste electrode (0.4 ± 0.1 cm/s). These features enabled the formation of a two-mediator ferrocene–neutral red system to be used in a biosensor. A two-mediator-based biosensor had a higher sensitivity (the lower limit of detected BOD concentrations, 0.16 mg/dm3) than that of a one-mediator system based on neutral red and ferrocene. Analysis of ten samples from surface water reservoirs showed the combination of ferrocene, neutral red and the yeast B. adeninivorans to enable the data that highly correlated (R = 0.9693) with those of the standard method.
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References
Babkina E, Chigrinova E, Ponamoreva O, Alferov V, Reshetilov A (2006) Bioelectrocatalytic oxidation of glucose by immobilized bacteria Gluconobacter oxydans. Eval Water Insoluble Mediat Effic Electroanal 18(19–20):2023–2029
Bilal M, Iqbal HMN (2019) Microbial-derived biosensors for monitoring environmental contaminants: recent advances and future outlook. Process Saf Environ Prot 124:8–17
Bischoff F, Chamas A, Litwińska K, Matthes F, Böer E, Kunze G (2017) Applications of Blastobotrys (Arxula) adeninivorans in biotechnology. Yeast diversity in human welfare. Springer, Singapore, pp 455–479
Chan C, Lehmann M, Tag K, Lung M, Kunze G, Riedeld K, Gruendige B, Renneberg R (1999) Measurement of biodegradable substances using the salt-tolerant yeast Arxula adeninivorans for a microbial sensor immobilized with poly(carbamoyl)sulfonate (PCS). Part II: application of the novel biosensor to real samples from coastal and island regions. Biosens Bioelectron 14(3):295–302
Christwardana M, Kwon Y (2017) Yeast and carbon nanotube based biocatalyst developed by synergetic effects of covalent bonding and hydrophobic interaction for performance enhancement of membraneless microbial fuel cell. Bioresour Technol 225:175–182
Ejeian F, Etedali P, Mansouri-Tehrani HA, Soozanipour A, Low ZX, Asadnia M, Taheri-Kafrani A, Razmjou A (2018) Biosensors for wastewater monitoring: a review. Biosens Bioelectron 118:66–79
Gal I, Schlesinger O, Amir L, Alfonta L (2016) Yeast surface display of dehydrogenases in microbial fuel cells. Bioelectrochemistry 112:53–60
Galler H, Feierl G, Petternel C, Reinthaler FF, Haas D, Habib J, Kittinger C, Luxner J, Zarfel G (2018) Multiresistant bacteria isolated from activated sludge in Austria. Int J Environ Res 15(3):479
Gao G, Fang D, Yu Y, Wu L, Wang Y, Zhi J (2017) A double-mediator based whole cell electrochemical biosensor for acute biotoxicity assessment of wastewater. Talanta 167:208–216
Hooi KB, Ismail AK, Ahamad R, Shahir S (2015) A redox mediated UME biosensor using immobilized Chromobacterium violaceum strain R1 for rapid biochemical oxygen demand measurement. Electrochim Acta 176:777–783
Hu J, Gao G, Xia S (2015) Development of a mediator-type bioelectrochemical sensor based on polypyrrole immobilized ferricyanide and microorganisms for biochemical oxygen demand fast detection. Int J Electrochem Sci 10:9695–9705
Hu J, Gao G, Xia S (2016) A mediated BOD microsensor based on poly (neutral red) and bacteria modified interdigited ultramicroelectrode array. Int J Electrochem Sci 11(7):6387–6402
Hu J, Li Y, Gao G, Xia S (2017) A mediated BOD biosensor based on immobilized B. subtilis on three-dimensional porous graphene-polypyrrole composite. Sensors 17(11):2594
Ikeda T, Kurosaki T, Takayama K, Kano K (1996) Measurements of oxidoreductase-like activity of intact bacterial cells by an amperometric method using a membrane-coated electrode. Anal Chem 68(1):192–198
Ino K, Onodera T, Fukuda MT, Nashimoto Y, Shiku H (2019) Combination of double-mediator system with large-scale integration-based amperometric devices for detecting NAD(P)H: quinone oxidoreductase 1 activity of cancer cell aggregates. ACS Sens 4(6):1619–1625
ISO 5815–1:2003 (2003) Water quality—determination of biochemical oxygen demand after N days (BODn), part 1: dilution and seeding method with allylthiourea addition
ISO 20665:2008 (2008) Water quality—determination of chronic toxicity to Ceriodaphnia dubia
Jordan MA, Welsh DT, Teasdale PR (2014) Ubiquity of activated sludge ferricyanide-mediated BOD methods: a comparison of sludge seeds across wastewater treatment plants. Talanta 125:293–300
Kamanina OA, Lavrova DG, Arlyapov VA, Alferov VA, Ponamoreva ON (2016) Silica sol-gel encapsulated methylotrophic yeast as filling of biofilters for the removal of methanol from industrial wastewater. Enzyme Microb Technol 92:94–98
Kasem ET, Tsujiguchi T, Nakagawa N (2013) Effect of metal modification to carbon paper anodes on the performance of yeast-based microbial fuel cells, part Ι: in the case without exogenous mediator. Key Eng Mater 534:76–81
Kharkova AS, Arlyapov VA, Turovskaya AD, Avtukh AN, Starodumova IP, Reshetilov AN (2019) Mediator BOD biosensor based on cells of microorganisms isolated from activated sludge. Appl Biochem Microbiol 55:189–197
Kharkova AS, Arlyapov VA, Turovskaya AD, Shvets VI, Reshetilov AN (2020) A mediator microbial biosensor for assaying general toxicity. Enzyme Microb Technol 132:109435
Liu L, Bai L, Yu D, Zhai J, Dong S (2015) Biochemical oxygen demand measurement by mediator method in flow system. Talanta 138:36–39
Mazloum-Ardakani M, Barazesh B, Moshtaghioun SM, Sheikhha MH (2019) Designing and optimization of an electrochemical substitute for the MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) cell viability assay. Sci Rep 9(1):1–8
Nakamura H (2018) Current status of water environment and their microbial biosensor techniques. Part II: recent trends in microbial biosensor development. Anal Bioanal Chem 410(17):1–23
Nakamura H, Abe Y, Koizumi R, Suzuki K, Mogi Y, Hirayama T, Karube I (2007a) A chemiluminescence biochemical oxygen demand measuring method. Anal Chim Acta 602(1):94–100
Nakamura H, Suzuki K, Ishikuro H, Kinoshita S, Koizumi R, Okuma S, Gotoh M, Karube I (2007b) A new BOD estimation method employing a double-mediator system by ferricyanide and menadione using the eukaryote Saccharomyces cerevisiae. Talanta 72(1):210–216
Nicholson RS, Shain I (1964) Theory of stationary electrode polarography. Single scan and cyclic methods applied to reversible, irreversible, and kinetic systems. Anal Chem 36(4):706–723
Niyomdecha S, Limbut W, Numnuam A, Asawatreratanakul P, Kanatharana P, Thavarungkula P (2017) A novel BOD biosensor based on entrapped activated sludge in a porous chitosan–albumin cryogel incorporated with graphene andmethylene blue. Sens Actuat B Chem 241:473–481
Pasco N, Hay J, Scott A, Webber J (2005) Redox coupling to microbial respiration: an evaluation of secondary mediators as binary mixtures with ferricyanide. Aust J Chem 58:288–293
Pauliukaite R, Brett CMA (2008) Poly (neutral red): electrosynthesis, characterization, and application as a redox mediator. Electroanalysis 20(12):1275–1285
Ponamoreva ON, Kamanina TV, Alferov VA, Machulin AV, Rogova TV, Arlyapov SV, Suzina VA, Alferov SV, Ivanova EP (2015) Yeast-based self-organized hybrid bio-silica sol–gels for the design of biosensors. Biosens Bioelectron 67:321–326
Rawson F, Gross A, Garrett D, Downard A, Baronian K (2012) Mediated electrochemical detection of electron transfer from the outer surface of the cell wall of Saccharomyces cerevisiae. Electrochem Commun 15(1):85–87
Trosok S, Driscoll B, Luong J (2001) Mediated microbial biosensor using a novel yeast strain for wastewater BOD measurement. Appl Microbiol Biotechnol 56(3–4):550–554
Yudina NY, Arlyapov VA, Chepurnova MA, Alferov SV, Reshetilov AN (2015) A yeast co-culture-based biosensor for determination of waste water contamination levels. Enzyme Microb Technol 78:46–53
Zaitseva AS, Arlyapov VA, Yudina NY, Alferov SV, Reshetilov AN (2017) Use of one- and two-mediator systems for developing a BOD biosensor based on the yeast Debaryomyces hansenii. Enzyme Microb Technol 98:43–51
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This study was carried out within the framework of the State Assignment of the Ministry of Science and Higher Education of the Russian Federation, No. FEWG-2020-0008.
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State Assignment of the Ministry of Science and Higher Education of the Russian Federation, No. FEWG-2020-0008.
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VAArl, ONP, VAAlf, ANR, conceptualization; ASK, ASI, VAArl, conducted the experiments; ASK, ASI, VAArl, ONP, data analysis; VAArl, ONP, VAAlf, ANR, wrote the manuscript with contribution from the other authors.
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Kharkova, A.S., Arlyapov, V.A., Ilyukhina, A.S. et al. A kinetic approach to the formation of two-mediator systems for developing microbial biosensors as exemplified by a rapid biochemical oxygen demand assay. 3 Biotech 11, 222 (2021). https://doi.org/10.1007/s13205-021-02709-8
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DOI: https://doi.org/10.1007/s13205-021-02709-8