Abstract
In this mini-review, the potential of using microorganisms to design biosensors for detecting environmental pollutants is analyzed and discussed. A distinction is made between a classical biosensor (CB) and a whole-cell biosensor (WCB), emphasizing their structural components and the possibility of using whole microorganisms as their bioreceptor elements. The advantages and disadvantages of using prokaryotic microorganisms as opposed to eukaryotic microorganisms are described. Likewise, the advantages of using protozoa (ciliates) over other eukaryotic microorganisms are also shown. We analyze the current bibliography on biosensors built on microorganisms as bioreceptors of pollutant molecules, such as inorganic (metal(loid)s) or organic (xenobiotics). New trends, such as the prokaryotic riboswitches, microbial two-component systems where the pollutant can be simultaneously detected and bioremediated, along with advances in synthetic biology, are shown as promising tools in the design of environmental biosensors.
Graphical Abstract
Similar content being viewed by others
References
Adeniran A, Sherer M, Tyo KEJ (2015) Yeast-based biosensors: design and applications. FEMS Yeast Res 15:1–15
Aksmann A, Pokora W, Bascik-Remisiewicz A et al (2014) Time-dependent changes in antioxidative enzyme expression and photosynthetic activity of Chlamydomonas reinhardtii cells under acute exposure to cadmium and anthracene. Ecotoxicol Environ Saf 110C:31–40
Amaro F, Turkewitz AP, Martin-Gonzalez A et al (2011) Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila. Microb Biotechnol 4:513–522
Amaro F, Turkewitz AP, Martin-Gonzalez A et al (2014) Functional GFP-metallothionein fusion protein from Tetrahymena thermophila: a potential whole-cell biosensor for monitoring heavy metal pollution and a cell model to study metallothionein overproduction effects. Biometals 27:195–205
Aury JM, Jaillon O, Duret L et al (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178
Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206–212
Berezhetskyy AL, Sosovska OF, Durrieu C et al (2008) Alkaline phosphatase conductometric biosensor for heavy metal ions determination. IRBM 29:136–140
Bernard E, Wang B (2017) Synthetic cell-based sensors with programmed selectivity and sensitivity. In: Rasooly A, Prickril B (eds) Biosensors and biodetection: methods and protocols. Methods in molecular biology, vol 1572. Springer, New York, pp 343–363
Beyersdorf-Radeck B, Karlson KR, Bachmann TT et al (1998) Screening of xenobiotic compounds degrading microorganisms using biosensor techniques. Microbiol Res 153:239–245
Branco R, Cristovao A, Morais PV (2013) Highly sensitive, highly specific whole-cell bioreporters for the detection of chromate in environmental samples. PLoS One 8:e54005
Caceres JO, Sanz-Mangas D, Manzoor S et al (2019) Quantification of particulate matter, tracking the origin and relationship between elements for the environmental monitoring of the Antarctic region. Sci Tot Env 665:125–132
Cerminati S, Soncini FC, Checa SK (2011) Selective detection of gold using genetically engineered bacterial reporters. Biotechnol Bioeng 108:2553–2560
Chouteau C, Dzyadevych S, Chovelon JM et al (2004) Development of novel conductometric biosensors based on immobilized whole cell Chlorella vulgaris microalgae. Biosens Bioelectron 19:1089–1096
Corbisier P, van der Lelie D, Borremans B et al (1999) Whole cell-and protein-based biosensors for the detection of bioavailable heavy metals in environmental samples. Anal Chim Acta 387:235–244
De Schamphelaere KAC, Nys C, Janssen CR (2014) Toxicity of lead (Pb) to freshwater green algae: development and validation of a bioavailability model and inter-species sensitivity comparison. Aquat Toxicol 155:348–359
Diaz S, Martin-Gonzalez A, Cubas L et al (2016) High resistance of Tetrahymena thermophila to paraquat: mitochondrial alterations, oxidative stress and antioxidant genes expression. Chemosphere 144:909–917
Diels L, Van Roy S, Taghavi S et al (2009) From industrial sites to environmental applications with Cupriavidus metallidurans. A Leeuwenhoek 96:247–258
Edwards AL, Batey RT (2010) Riboswitches: a common RNA regulatory element. Nat Educ 3(9):9
Eisen JA, Coyne RS, Wu M et al (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4:e286
Erbe JL, Adams AC, Taylor KB et al (1996) Cyanobacteria carrying an smt-lux transcriptional fusion as biosensors for the detection of heavy metal cations. J Ind Microbiol 17:80–83
Findei BS, Etzel M, Will S et al (2017) Design of artificial riboswitches as biosensors. Sensors 17:1–28. https://doi.org/10.3390/s17091990
Guascito MR, Malitesta C, Mazzotta E et al (2008) Inhibitive determination of metal ions by an amperometric glucose oxidase biosensor: study of the effect of hydrogen peroxide decomposition. Sens Actuators B Chem 131:394–402
Gutierrez JC, Martin-Gonzalez A, Diaz S et al (2003) Ciliate as potential source of cellular and molecular biomarker/biosensors for heavy metal pollution. Eur J Protistol 39:461–467
Gutierrez JC, Martin-Gonzalez A, Diaz S et al (2008) Ciliates as cellular tools to study the eukaryotic cell-heavy metal interactions. In: Brown SE, Welton WC (eds) Heavy metal pollution. Nova Science Publishers, New York, pp 1–44
Gutierrez JC, Amaro F, Diaz S et al (2011) Ciliate metallothioneins: unique microbial eukaryotic heavy-metal-binder molecules. J Biol Inorg Chem 16:1025–1034
Gutierrez JC, Amaro F, Martin-Gonzalez A (2015) Heavy metal whole-cell biosensors using eukaryotic microorganisms: an updated critical review. Front Microbiol 6:1–8
Gutierrez JC, Amaro F, Martin-Gonzalez A (2017) Microbial biosensors for metal(loid)s. In: Cravo-Laureau C et al (eds) Microbial ecotoxicology. Springer International Publishing AG, Cham, pp 313–336
Hill MK (2004) Understanding environmental pollution. A primer. Cambridge University Press, Cambridge
Hou Q, Ma A, Wang T et al (2015) Detection of bioavailable cadmium, lead and arsenic in polluted soil by tailored multiple Escherichia coli whole-cell sensor set. Anal Bioanal Chem 407:6865–6871
Hu Q, Li L, Wang Y et al (2010) Construction of WCB-11: a novel phiYFP arsenic-resistant whole-cell biosensor. J Environ Sci 22:1469–1474
Huang CW, Yang SH, Sun MW et al (2015) Development of a set of bacterial biosensors for simultaneously detecting arsenic and mercury in groundwater. Environ Sci Pollut Res Int 22:10206–10213
Huse SM, Welch DM, Morrison HG et al (2010) Ironing out the wrinkles in the rare biosphere through improved OUT clustering. Environ Microbiol 12:1889–1898
Ilangovan R, Daniel D, Krastanov A et al (2006) Enzyme based biosensor for heavy metal ions determination. Biotechnol Equip 20:184–189
Ivask A, Rolova T, Kahru A (2009) A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotechnol 9:41. https://doi.org/10.1186/1472-6750-9-41
Jia X, Bur R, Zhao T et al (2019) Development of a sensitive and specific whole-cell biosensor for arsenic detection. Appl Environ Microbiol 85:e00694
Jouanneau S, Durand MJ, Assaf A et al (2017) Bacterial bioreporter applications in ecotoxicology: concepts and practical approach. In: Cravo-Laureau C et al (eds) Microbial ecotoxicology. Springer International Publishing AG, Cham, pp 283–311
Jung Y, Park C-B, Kim Y et al (2015) Application of multi-species microbial bioassay to assess the effects of engineered nanoparticles in the aquatic environment; potential of a luminous microbial array for toxicity risk assessment (LumiRAMA) on testing for surface-coated silver nanoparticles. Int J Environ Res Public Health 12:8172–8186
Kallmeyer J, Pockalny R, Adhikari RR et al (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. PNAS 109:16213–16216
Kang Y, Lee W, Kim S (2018) Enhancing the Cu-sensing capability of E. coli-based WCB by genetic engineering. Appl Microbiol Biotechnol 102:1513–1521
Kim HJ, Lim JW, Jeong H et al (2016) Development of a highly specific and sensitive cadmium and lead microbial biosensor using synthetic CadC-T7 genetic circuitry. Biosens Bioelectron 79:701–708
Kröger S, Law RJ (2005) Biosensors for marine applications. We all need the sea, but does the sea need biosensors? Biosens Bioelectron 20:1903–1913
Kumar J, D’souza SF (2010) An optical microbial for detection of methyl parathion using Sphingomonas sp. immobilized on microplate as a reusable biocomponent. Biosens Bioelectron 26:1292–1296
Lee S, Sode K, Nakanishi K et al (1992) A novel microbial sensor using luminous bacteria. Biosens Bioelectron 7:273–277
Lehmann M, Riedel K, Adler K et al (2000) Amperometric measurement of copper ions with a deputy substrate using a novel Saccharomyces cerevisiae sensor. Biosens Bioelectron 15:211–219
Lei Y, Mulchandani P, Chen W et al (2007) Biosensor for direct determination of Fenitrothion and EPN using recombinant Pseudomonas putida js444 with surface-expressed organophosphorous hydrolase. 2. Modified carbon paste electrode. Appl Biochem Biotechnol 136:243–250
Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 37(12):1921–1942
Leth S, Maltoni S, Simkus R et al (2002) Engineered bacteria based biosensors for monitoring bioavailable heavy metals. Electroanalysis 14:35–42
Li L, Liang J, Hong W et al (2015) Evolved bacterial biosensor for arsenite detection in environmental water. Environ Sci Technol 49:6149–6155
Lünse CE, Schmidt MS, Wittmann V (2011) Carba-sugars activate the glmS-riboswitch of Staphylococcus aureus. ACS Chem Biol 6:675–678
Machtel P, Bakowska-Zywicka K, Zywicki M (2016) Emerging applications of riboswitches-from antibacterial targets to molecular tools. J Appl Genet 57:531–541
Magrisso S, Erel Y, Belkin S (2008) Microbial reporter of metal bioavailability. Microb Biotechnol 1:320–330
Martin-Betancor K, Rodea-Palomares I, Muñoz-Martín MA (2015) Construction of a self-luminescent cyanobacterial bioreporter that detects a broad range of bioavailable heavy metals in aquatic environment. Front Microbiol 6:186. https://doi.org/10.3389/fmicb.2015.00186
Martin-Gonzalez A, Diaz S, Jareño C et al (1999) The use of protists in ecotoxicology. Recent Res Dev Microbiol 3:93–111
McCown PJ, Corbino KA, Stav S (2017) Riboswitch diversity and distribution. RNA 23:995–1011
Mergeay M, Monchy S, Vallaeys T et al (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27:385–410
Merulla D, van der Meer JR (2016) Regulatable and modulable background expression control in prokaryotic synthetic circuits by auxiliary repressor binding sites. ACS Synth Biol 5:36–45
Metha J, Bhardwaj SK, Bhardwaj N et al (2016) Progress in the biosensing techniques for trace – level heavy metals. Biotechnol Adv 34:47–60
Nguyen-Ngoc H, Durrieu C, Tran-Minh C (2009) Synchronous-scan fluorescence of algal cells for toxicology of heavy metals and herbicides. Ecotoxicol Environ Saf 72:316–320
Niazi JH, Kim BC, Ahn J-M et al (2008) A novel bioluminescent bacterial biosensor using the highly specific oxidative stress-inducible pgi gene. Biosens Bioelectron 24:670–675
Park JN, Sohn MJ, Oh DB (2007) Identification of the cadmium-inducible Hansenula polymorpha SEO1 gene promoter by transcriptome analysis and its application to whole-cell heavy-metal detection systems. Appl Environ Microbiol 73:5990–6000
Peña-Vazquez E, Perez-Conde C, Costas E et al (2010) Development of a microalgal PAM test method for Cu(II) in waters: comparison of using spectrofluorometry. Ecotoxicology 19:1059–1065
Peñuelas J, Fillela I (2002) Metal pollution in Spanish terrestrial ecosystems during the twentieth century. Chemosphere 46:501–505
Prathap MUA, Chaurasia AK, Sawant SN et al (2012) Polyaniline-based highly sensitive biosensor for selective detection of lindane. Anal Chem 15:6672–6678
Preveral S, Brutesco C, Descamps EC et al (2017) A bioluminescent arsenite biosensor designed for inline water analyzer. Environ Sci Pollut Res Int 24:25–32
Radhika V, Milkevitch M, Audigé V et al (2005) Engineered Saccharomyces cerevisiae strain BioS-1, for the detection of water-borne toxic metal contaminants. Biotechnol Bioeng 90:29–35
Ravikumar S, Yoo IK, Lee SY et al (2011) Construction of cooper removing bacteria through the integration of two-component system and cell surface display. Appl Biochem Biotechnol 165:1674–1681
Ravikumar S, Baylon MG, Park SJ (2017) Engineered microbial biosensors based on bacterial two-component systems as synthetic biotechnology platforms in bioremediation and biorefinery. Microb Cell Factories 16:62. https://doi.org/10.1186/s12934-017-0675-z
Roda A, Roda B, Cevenini L (2011) Analytical strategies for improving the robustness and reproducibility of bioluminescent microbial bioreporters. Anal Bioanal Chem 401:201–211
Samphao A, Rerkchai H, Jitcharoen J et al (2012) Indirect determination of mercury by inhibition of glucose oxidase immobilizated on carbon paste electrode. Int J Electrochem 7:1001–1010
Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152:17–24
Shahsavari E, Aburto-Medina A, Khudur LD et al (2017) From microbial ecology to microbial ecotoxicology. In: Cravo-Laureau C et al (eds) Microbial ecotoxicology. Springer International Publishing AG, Cham, pp 17–38
Sharma P, Asad S, Ali A (2013) Bioluminescent bioreporter for assessment of arsenic contamination in water samples of India. J Biosci 38:251–258
Shetty RS, Deo SK, Liu Y et al (2004) Fluorescence-based sensing system for copper using genetically engineered living yeast cells. Biotechnol Bioeng 88:664–670
Shing WL, Surif S, Heng LY (2008) Toxicity biosensor for the evaluation of cadmium toxicity based on photosynthetic behavior of cyanobacteria Anabaena torulosa. Asian J Biochem 3:162–168
Shitanda I, Takada K, Sakai Y et al (2005) Amperometric biosensing systems based on motility and gravitaxis of flagellate algae for aquatic risk assessment. Anal Chem 77:6715–6718
Sperling L, Dessen P, Zagulski M et al (2002) Random sequencing of paramecium somatic DNA. Eukaryot Cell 1:341–352
Tag K, Riedel K, Bauer HJ et al (2007) Amperometric detection of Cu2+ by yeast biosensors using flow injection analysis (FIA). Sens Act B Chem 122:403–409
Tauriainen S, Karp M, Chang W et al (1998) Luminescent bacterial sensor for cadmium and lead. Biosens Bioelectron 13:931–938
Terziyska A, Waltschewa L, Venkov P (2000) A new sensitive test based on yeast cells for studying environmental pollution. Environ Pollut 109:43–52
Tibazarwa C, Wuertz S, Mergeay M et al (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182:1399–1409
Tibazarwa C, Corbisier P, Mench M et al (2001) A microbial biosensor to predict bioavailable nickel in soil and its transfer to plants. Environ Pollut 113:19–26
Tseng H-W, Tsai Y-J, Yen J-H, Chen P-H et al (2014) A fluorescence-based microbial sensor for the selective detection of gold. Chem Commun 50:1735–1737
Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208
Van der Meer JR, Belkin S (2010) Where microbiology meets microengineering: design and application of reporter bacteria. Nat Rev Microbiol 8:511–522
Verma N, Singh M (2005) Biosensors for heavy metals. Biometals 18:121–129
Vopálenská I, Váchová L, Palková Z (2015) New biosensor for detection of copper ions in water based on immobilized genetically modified yeast cells. Biosens Bioelectron 72:160–167
Walmsley RM, Keenan P (2000) The eukaryotic alternative: advantages of using yeasts in place of bacteria in microbial biosensor development. Biotechnol Bioprocess Eng 5:387–394
Wan X, Ho T, Wang B (2019a) Engineering prokaryote synthetic biology biosensors. In: Handbook of cell biosensors. Springer Nature. https://doi.org/10-1007/978-3-319-47405-2_131-1
Wan X, Volpetti F, Petrova E, French C, Maerkl SJ, Wang B (2019b) Cascaded amplifying circuits enable ultrasensitive cellular sensors for toxic metals. Nat Chem Biol 15:540–548
Wang B, Buck M (2014) Rapid engineering of versatile molecular logic gates using heterologous genetic transcriptional modules. Chem Commun 50:11642–11644
Wang B, Barahona N, Buck M (2013) A modular cell-based biosensor using engineered genetic logic circuits to detect and integrate multiple environmental signals. Biosens Bioelectron 40:368–376
Wang B, Barahona N, Buck M (2014) Engineering modular and tunable genetic amplifiers for scaling transcriptional signals in cascaded gene networks. Nucleic Acids Res 42:9484–9492
Wang B, Barahona N, Buck M (2015) Amplification of small molecule-inducible gene expression via tuning of intracellular receptor densities. Nucleic Acids Res 43:1955–1964
Webster DP, TerAvest MA, Doud DF et al (2014) An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system. Biosens Bioelectron 62:320–324
Wedekind JE, Dutta D, Belashov IA et al (2017) Metalloriboswitches: RNA-based inorganic ion sensors that regulate genes. J Biol Chem 292:9441–9450
Wong LS, Lee YH, Surif S (2013) Whole cell biosensor using Anabaena torulosa with optical transduction for environmental toxicity evaluation. J Sens 567272:1. https://doi.org/10.1155/2013/567272
Yagi K (2007) Applications of whole-cell bacterial sensors in biotechnology and environmental science. Appl Microbiol Biotechnol 73:1251–1258
Yoon KP, Misra TK, Silver S (1991) Regulation of the cadA cadmium resistance determinant of Staphylococcus aureus plasmid pI258. J Bacteriol 173:7643–7649
Yoon Y, Kim S, Chae Y (2016a) Simultaneous detection of bioavailable As and Cd in contamined soils using dual-sensing bioreporters. Appl Microbiol Biotechnol 100:3713–3722
Yoon Y, Kim S, Chae Y (2016b) Evaluation of bioavailable Ar and remediation performance using a WCB. Sci Total Environ 547:125–131
Zhou T, Han H, Liu P et al (2017) Microbial fuels cell-based biosensor for toxicity detection: a review. Sensors 17:2230. https://doi.org/10.3390/s17102230
Zorawski M, Shaffer J, Velasquez E et al (2016) Creating a riboswitch-based whole-cell biosensor for bisphenol A. FASEB. https://doi.org/10.1096/fasebj.30.1.supplement.805.3
Zylstra GJ, McCombie WR, Gibson DT et al (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon. Appl Environ Microbiol 54:1498–1503
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Section Editor information
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this entry
Cite this entry
Gutiérrez, JC., Amaro, F., Díaz, S., Martín-González, A. (2020). Environmental Biosensors: A Microbiological View. In: Thouand, G. (eds) Handbook of Cell Biosensors. Springer, Cham. https://doi.org/10.1007/978-3-319-47405-2_191-1
Download citation
DOI: https://doi.org/10.1007/978-3-319-47405-2_191-1
Received:
Accepted:
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-47405-2
Online ISBN: 978-3-319-47405-2
eBook Packages: Springer Reference Chemistry and Mat. ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics