Chemosphere 306 (2022) 135515

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Recent advances in the analytical strategies of microbial biosensor for

detection of pollutants
Zengling Ma a, **, 1, Catarina Meliana b, 1, Heli Siti Halimatul Munawaroh c, Ceren Karaman d,
Hassan Karimi-Maleh e, f, Sze Shin Low g, ***, Pau Loke Show a, h, *
a
Zhejiang Provincial Key Laboratory for Subtropical Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou, 325035, China
b
Department of Food Science and Nutrition, Faculty of Life Science, Indonesia International Institute of Life Sciences, Jakarta, 13210, Indonesia
c
Study Program of Chemistry, Department of Chemistry Education, Universitas Pendidikan Indonesia, Jalan Dr. Setiabudhi 229, Bandung, 40154, Indonesia
d
Akdeniz University, Department of Electricity and Energy, Antalya, 07070, Turkey
e
School of Resources and Environment, University of Electronic Science and Technology of China, P.O. Box 611731, Xiyuan Ave, Chengdu, PR China
f
Department of Chemical Engineering and Energy, Quchan University of Technology, Quchan, 9477177870, Iran
g
Research Centre of Life Science and Healthcare, China Beacons Institute, University of Nottingham Ningbo China, 199 Taikang East Road, Ningbo, 315100, Zhejiang,
China
h
Department of Chemical and Environmental Engineering, Faculty of Science and Engineering, University of Nottingham Malaysia, Jalan Broga, 43500 Semenyih,
Selangor Darul Ehsan, Malaysia

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Microbial biosensors are simple, rapid,

robust compared to conventional
methods.
• Wide applications have been discov­
ered, e.g., environmental, food
monitoring.
• Engineered microbes have great poten­
tial for high-throughput and portable
analysis.
• Microbial biosensors are advantageous
in ethical issues perspective.
• The challenges and future perspectives
of microbial biosensor are discussed.

A R T I C L E I N F O A B S T R A C T

Handling Editor: Derek Muir Microbial biosensor which integrates different types of microorganisms, such as bacteria, microalgae, fungi, and
virus have become suitable technologies to address limitations of conventional analytical methods. The main
applications of biosensors include the detection of environmental pollutants, pathogenic bacteria and compounds
related to illness, and food quality. Each type of microorganisms possesses advantages and disadvantages with
Keywords:
different mechanisms to detect the analytes of interest. Furthermore, there is an increasing trend in genetic
Microbial biosensor
Genetic engineering
modifications for the development of microbial biosensors due to potential for high-throughput analysis and
Environmental monitoring portability. Many review articles have discussed the applications of microbial biosensor, but many of them

* Corresponding author.
** Corresponding author.
*** Corresponding author.
E-mail addresses: [email protected] (Z. Ma), [email protected] (S.S. Low), [email protected], [email protected]
(P.L. Show).
1
Equal contribution as first author.

https://doi.org/10.1016/j.chemosphere.2022.135515
Received 24 February 2022; Received in revised form 10 May 2022; Accepted 25 June 2022
Available online 27 June 2022
0045-6535/© 2022 Published by Elsevier Ltd.
Z. Ma et al. Chemosphere 306 (2022) 135515

Biomedical applications focusing only about bacterial-based biosensor although other microbes also possess many advantages. Addi­
Pollutant detection tionally, reviews on the applications of all microbes as biosensor especially viral and microbial fuel cell bio­
sensors are also still limited. Therefore, this review summarizes all the current applications of bacterial-,
microalgal-, fungal-, viral-based biosensor in regard to environmental, food, and medical-related applications.
The underlying mechanism of each microbes to detect the analytes are also discussed. Additionally, microbial
fuel cell biosensors which have great potential in the future are also discussed. Although many advantageous
microbial-based biosensors have been discovered, other areas such as forensic detection, early detection of
bacteria or virus species that can lead to pandemics, and others still need further investigation. With that said,
microbial-based biosensors have promising potential for vast applications where the biosensing performance of
various microorganisms are presented in this review along with future perspectives to resolve problems related
on microbial biosensors.

Nomenclature IL Ionic Liquid

IR Inhibition Ratio
LIST OF ABBREVIATIONS JD Johne’s disease
Ace-k Acesulfame Potassium-k Li Lithium
ADP1 Acinetobacter baylyi LOD Limit of Detection
Al Aluminium MAP Mycobacterium avium subsp. Paratuberculosis
APX Ascorbate Peroxidase MAPK Mitogen-Activated Protein Kinase
BET Best Estimate Threshold MOF Metal-Organic Framework
BOD Biological Oxygen Demand MWNT Multi-Walled Carbon Nanotube
Cd Cadmium N Nitrogen
CFU Colony Forming Unit Na Natrium
CHO Chinese Hamster Ovary OCS One-component system
COD Chemical Oxygen Demand P Phosphorus
CRISPR Clustered Regularly Interspaced Short Palindromic Pb Lead
Repeats PDR Pleiotropic Drug Resistance
CRISPR-Cas9 CRISPR-associated protein 9 PEDOT Poly(3,4 Ethylenedioxy Thiophene)
Cu Copper PEI Polyethyleneimine
DES Deep Eutic Solvent PFOA Perfluorooctanoic Acid
DNA Deoxyribonucleic Acid PFOS Perfluorooctane Sulfonic Acid
DNT 2,4-dinitrotoluene PPB Part Per Billion
EDC Endocrine-Disrupting Compound PSII Photosystem II
EET Extracellular Electron Transfer PVA-SbQ Polyvinyl Alcoholstyrylpyridinium
ELLTA Enzyme-Linked Lactoferrin Assay SMCFA Short- and Medium-Chain Fatty Acids
ER Estrogen Receptor Alpha SOB Sulfur Oxidizing Bacteria
FQN Fluoroquinolone SOD Superoxide Dismutase
GA Glucoamylase SPCE Screen-Printed Carbon Electrode
GCE Glassy Carbon Electrode STEC Shiga Toxin-producing Escherichia coli serogroups
GDH Glucose Dehydrogenase TCS Two-component system
GFP Green Fluorescence Protein TN Total Nitrogen
GMB Genetically Modified Bioluminescent Bacteria TNT 2,4,6-trinitrotoluene
GPCR G-Protein Coupled Receptors TOC Total Organic Compound
GPX Gluthathione Peroxidase VOC Volatile Organic Compound
HAS Human Serum Albumin

activity of a new compound), environmental monitoring (e.g., contin­

uous monitoring of BOD, acidity, pesticides, fertilizers, industrial
1. Introduction
wastes, and domestic wastes), biodefence (e.g., identify organisms
posing a threat in virtually real-time called biowarfare agents like bac­
Biosensor is an analytical device consist of a bioreceptor, a trans­
teria, toxin, and virus), food industry (e.g., determine the quality and
ducer, and a signal-processor to detect, transmit, and record any phys­
safety of food products, monitor the fermentation process, etc.), and
iological or biochemical changes of the analytes. The main principle is
many others (Amaro et al., 2011; Arora et al., 2011; Inda and Lu, 2020;
by combining the biological recognition element (i.e., bioreceptor) with
Scognamiglio et al., 2014).
a transducer to generate a measurable signal proportional to the con­
Many bioreceptors have been used, such as enzymes, antibodies,
centration of the analytes (Fig. 1). Biosensors have been used for the past
microorganisms, plant and animal cells or tissues, and others. The
few decades to replace the conventional analytical techniques (e.g.,
importance of the biological component that is used is based on its
immunoassays, biochemical assays, etc.) as they are reusable, specific,
interaction with the analytes (i.e., need to be highly specific to minimize
sensitive, and allow rapid and multiple analyses (Goode et al., 2015;
the interferences from other substances). Although enzymes are most
Justino et al., 2017; Low et al., 2021b; Mehrotra, 2016). The applica­
commonly used due to their specificity, sensitivity, and reliability; they
tions of biosensors include in the medical and health care area (e.g.,
are very expensive, time-consuming, tend to deactivate after a short
rapid measurement of blood, gases, ions, and metabolites to determine a
period of time, and not suitable for in vitro operation environment. Thus,
person’s metabolic state), pharmaceutical (e.g., evaluate the biological

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interest in microbes (e.g., bacteria, microalgae, fungi, yeast, and virus) biosensor mechanism and applications from previous studies and
as bioreceptor have increased due to their advantages of low cost, rapid research conducted in the past five years are provided. In addition, the
response, portability, and able to detect a variety of chemical substances advantages and disadvantages of each microbial biosensor, future
due to its numerous enzymes content (D’Souza, 2001; Dai and Choi, prospects, and challenges of microbial biosensor are also discussed.
2013; Lei et al., 2006; Wasito et al., 2019). Furthermore, microbes have
broad pH and temperature range, approved for genetic modification, 2. Bacterial-based biosensor
can tremendously produce by cell culture and has better viability and
stability in vitro which can enhance and simplify the performance of Bacteria has been known for its ability to possess a wide variety of
biosensor. The key takeaway of microbes as a biosensor is due to their stress-response mechanisms (e.g., heat-shock, antioxidation, nutrient
great ability to adapt and respond to the environment by developing starvation, membrane-damage), rapid and constant detection of envi­
their ability to degrade new molecules with time (i.e., evolvability, ronmental changes, and rapid proliferation rate both in aerobic and
robustness) and short life cycles. anaerobic conditions using a relatively inexpensive media. By this,
In the present, interest in microbial biosensors has increased due to bacteria has its advantages to be used as an easy, rapid, and cheap al­
their advantages and wide application areas. Microbial biosensors have ternatives methods to detect a specific signal (i.e., analytes) of interest
been used widely to detect organic and inorganic toxicants in the which results in more accurate analysis. The bacterial-based biosensor
environment (e.g., detection of heavy metal in wastewater), assess the also gives a more practical on-line, in vitro, and dose-response analysis
nutritional quality of food products, monitor the materials (i.e., ethanol) (Checa et al., 2012; Li et al., 2015).
required in the fermentation process, detection of food contaminants, Many bacterial biosensors have been developed based on the phys­
and several clinical diagnoses (e.g., hormones, pathogens, and DNA) due iological response of bacteria immobilization in a membrane or gel
to its rapid, and easiness to conduct. The detection method of most matrix that is transmitted to a sensing device (e.g., oxygen electrode
microbial biosensors to detect inputs (i.e., toxicants, environmental used to detect organic compounds in a sample). However, recently,
cues, autoinducers, other metabolites) includes electrochemical and bacterial biosensors have been engineered by combining a reporter gene
optical detection. Electrochemical biosensor is mostly used due to its with the contaminant-sensing component to conduct quicker, more
simplicity to operate, high sensitivity, and rapid detection (Low et al., sensitive, and selective analysis. Reporter genes play the role as signal
2017, 2021c). It relies on the mechanism of toxicants to inhibit meta­ transducer to produce a detectable signal; thus, it determines the
bolic activity of the microbes. The toxicants itself will be estimated by sensitivity and detection limit of a biosensor. Meanwhile, the sensing
the oxidation current of electron mediators (electron transfer) (Yang component that plays a role in responding to the analytes will determine
et al., 2018). In addition, the biochemical responses received by the the specificity of the biosensor. Several reporter genes that are
sensing elements of microbial biosensors will also be transferred to the commonly used include lacZ (encoding beta-galactosidase of E. coli), lux
transducers by intimate and stable immobilization of microorganisms (encoding bacterial luciferase), luc (encoding insect luciferase), and gfp
either by chemical (e.g., covalent binding and cross-linking) or physical (encoding the green fluorescent protein of jellyfish) (Bjerketorp et al.,
methods (e.g., adsorption and entrapment) (Dai and Choi, 2013). 2006; Jansson, 2003; Strosnider, 2003; Tecon and Van Der Meer, 2008).
Many review articles focusing on the application of microbial bio­ Other reporter genes found to be incorporated into biosensors are also
sensors have been published with most of them discussing about the listed in Table 1, along with their advantages and disadvantages.
usage of bacterial-based biosensor (Bilal and Iqbal, 2019; Moraskie In bacteria-based biosensors, the sensor-reporter circuit is demon­
et al., 2021; Park et al., 2013; Su et al., 2011). Although, there are strated by the DNA parts where it includes regulator and reporter genes
several articles that discussed about other types of microbial biosensors, for the sensing and system output function, and promoter, operator(s),
it is nearly none to found articles that combine the applications of all terminators, ribosome binding sites, etc. for controlling the gene
microbes as biosensors, especially those discussing about viral-based expression. The mechanism of a bacterial biosensor to detect analytes is
biosensor. Therefore, this review aims to complement earlier review mostly provided by the transcription factors via internal effector binding
articles and to discuss on the recent advances in analytical strategies of domain or sensory protein that either directly repress or induce the re­
microbial biosensors for detection of pollutants. There will be four types porter gene expression of the DNA promoter’s site (Fig. 2). Afterward,
of biosensors discussed in this review, including bacterial-, microalgal-, the output of the sensing events will be translated and amplified in the
fungal-, and viral-based biosensors. Information regarding each form of reporter protein synthesis, which can be measured in the assay

Fig. 1. General Schematic layout of a biosensor.

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Table 1
Reporter and promoter genes used for bacterial-based biosensor.
Gene Protein Detection Method Wavelength Advantages Disadvantages Ref
(emission)

luc Insect luciferase Luminescence 560 nm High sensitivity, broad dynamic range, great Requires exogenous Köhler et al.
versatility, multianalyte assay substrate and ATP, (2000)
aerobic
gfp Green fluorescent Fluorescence 535 nm Real time detection without exogenous Low sensitivity Hakkila et al.
protein (GFP) substrate and cell’s metabolism disruption, (2002)
thermostability, and autofluorescence
lux Bacterial luciferase Luminescence 490 nm No exogenous substrate requirement, rapid Heat labile, aerobic Köhler et al.
response (2000)
lacZ -Galactosidase Colorimetric Electrochemical 620 nm Various detection method Requires exogenous Zhang et al.
Fluorescence (Fluorescence) substrate (2017)
Chemiluminescence
crtA Spheroidene Colorimetric – No exogenous substrate requirement, can be Substrate dependent Aynalem and
detected by naked eyes Muleta (2021)
bla β-Lactamase Colorimetric – No exogenous substrate requirement, can be Substrate dependent Köhler et al.
detected by naked eyes (2000)
ars ArsR Luminescence 600 nm High specificity and sensitivity, rapid Absence of substrate (Prévéral
response, stable during long term storage will lead to leakage et al., 2017)
cfp Cyan fluorescent Fluorescence 480 nm Simultaneous detection of multianalytes Low absorption and Biran et al.
protein (CFP) assay low quantum efficiency (2003)
yfp Yellow fluorescent Fluorescence 528 nm Simultaneous detection of multianalytes Low absorption and Potzkei et al.
protein (YFP) assay low quantum efficiency (2012)
rfp Red fluorescent Fluorescence 580 nm Real time detection, no exogenous substrate Substrate dependent Mandap et al.
protein (RFP) requirements (2006)

Fig. 2. Mechanism of bacterial sensor-reporter cell. (a) DNA parts included in sensor-reporter circuit (regulatory and reporter gene acts to sense and system output
function, respectively, while others to control gene expression). (b) Sensor function by single regulatory protein mechanism (regulator protein binds to target
compound, to induce the transcription factor of a reporter gene, thus, leading to signal amplification). (c) Separated sensor and regulator function mechanism
(receiver protein sense the target compound, activating the regulator proteins via signaling cascade, leading to the induce gene expression). Reprinted from (Tecon
and Van Der Meer, 2008) with permission from MDPI AG (CC BY 4.0 license).

(fluorescence, luminescence, coloration) (Tecon and Van Der Meer, 2.1. Applications
2008).
There are a lot of applications of bacterial biosensor with most of 2.1.1. Environmental monitoring
them focusing on environmental monitoring. In general, the principle of Pollution or contaminant coming from industry and agriculture have
bacterial biosensor is similar for all bacteria strains with only differences become major public health and environmental problem if consume and
in induction time and substrate addition (Strosnider, 2003). Table 2 presence above the safe limit (i.e., lead to existence of health problems,
summarizes the application of bacterial-based biosensor along with and death of beneficial organisms in the environments). Major con­
some of the important sensing performance indicators. taminants found includes heavy metals, herbicides, volatile compounds,
etc. Therefore, it is of utmost importance to perform environmental
monitoring to prevent those toxicants being released into air, soil, and

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Table 2
Applications of bacterial-based biosensor.
Bacteria Substrate Type (Reporter Gene) Detection Limit Ref

Acinetobacter baylyi Antibacteria compounds (ethanol, Bioluminescence Poikulainen et al. (2020)

naphthoquinones, and flavonoid)
Acinetobacter baylyi ADP1 Hg2+ Bioluminescence (lux) 0.02 mg/L Cui et al. (2018)
Zn2+ 1 mg/L
Cu2+ 0.2 mg/L
Cd2+ 0.05 mg/L
Escherichia coli Benzene Colorimetry 0.01 mM Di Gennaro et al. (2011)
Arsenite Bioluminescence (lux) 0.2 μM (Prévéral et al., 2017)
Arsenic Fluorescence (gfp) 10 g Elcin and Öktem (2020)
Copper Fluorescence (egfp) 0.08 μM Kang et al. (2018)
Silver Fluorescence (gfp) 40 μM Martinez et al. (2019)
Copper 20 μM
2,4-dinitrotoluene (DNT) Fluorescence (gfp) and (Kabessa et al., 2016;
2,4,6-trinitrotoluene (TNT) bioluminescence (lux) Shemer et al., 2021)
Fluoroquinolones (FQNs) Bioluminescence (lux) 12.5 μg/kg Cheng et al. (2014)
Sucralose Bioluminescence (lux) 1 mg/mL Harpaz et al. (2018)
Neotame 2 mg/mL
Saccharin 5 mg/mL
Aspartame 4 mg/mL
Acesulfame potassium-k (ace-k) 10 mg/mL
VOC and Penicillium digitatum infection Bioluminescence (lux) Chalupowicz et al. (2020)
Estradiol Electrochemical Furst et al. (2017)
Bisphenol A
Tyrosine Fluorescence (rfp and gfp) 4.7 and 6.8 μM, Lin et al. (2019)
respectively
Heme Bioluminescence 5 × 104 RBC/mL Barger et al. (2021)
Heme Bioluminescence (lux) Mimee et al. (2018)
Nitrate Fluorescence 4.9 μM Woo et al. (2020)
Antibacteria compounds (ethanol, Bioluminescence Poikulainen et al. (2020)
naphthoquinones, and flavonoid)
Escherichia coli and Bacillus subtilis co-culture p-coumaric acid Fluorescence (yfp) 0.03 mM Siedler et al. (2017)
Glucoamylase-displayed (GA) bacteria and Glucose Electrochemical 0.04 mM Liu et al. (2017)
glucose dehydrogenase-displayed (GDH) Maltose Electrochemical 0.1 mM
bacteria
Pseudomonas aeruginosa Perfluorooctanoic acid (PFOA) Fluorescence (gfp) 10 ng/L Sunantha and Vasudevan
Perfluorooctane sulfonate (PFOS) Fluorescence (gfp) 10 ng/L (2021)
Pseudomonas putida Antibacteria compounds (ethanol, Bioluminescence Poikulainen et al. (2020)
naphthoquinones, and flavonoid)
Pseudomonas sp. Phenols Conductometry 2 μM Kolahchi et al. (2018)
Shewanella loihica BOD Electrochemical Yi et al. (2020)
Nitrate Electrochemical 0.75 mg/L
Staphylococcus aureus Antibacteria compounds (ethanol, Bioluminescence Poikulainen et al. (2020)
naphthoquinones, and flavonoid)
Sulfur oxidizing bacteria (SOB) Chromium (Cr6+) Electrochemical 50 ppb Hassan et al. (2013)
Vibrio campbellii Chromium (Cr6+) Luminescence Thacharodi et al. (2019)

water. Bacteria species that have been used as biosensors mostly is Hamster Ovary (CHO) cells for biomonitoring in water (Manivannan
Escherichia coli due to the ease of manipulation. E. coli in combination et al., 2020). Additionally, E. coli strain coupled with reporter gfp gene
with lux and lac reporter genes have been frequently used to detect and promoter copA gene was developed as copper ion fluorescence
arsenic, benzene, toluene, xylene, and tetracyclines with good detection biosensors (Kang et al., 2018).
limit and relatively short detection period (Di Gennaro et al., 2011; Gui Another fluorescence biosensor based on E. coli containing silver/
et al., 2017; Prévéral et al., 2017). Besides, E. coli engineered with arsR copper resistance operon and a gfp gene was also studied for detection of
and gfp gene also exhibit potential as fluorescence biosensors to detect silver and copper (Martinez et al., 2019). Detection of perfluorinated
arsenic at safe drinking water limit based on the immobilization in agar compounds (i.e., PFOA and PFOS) known as pollutants containing
hydrogel and alginate bead (Elcin and Öktem, 2020). endocrine disruptors was developed using a genetically engineered
Many other bacteria strains also have been applied as biosensors Pseudomonas aeruginosa fluorescence biosensor. The bacterial strain was
based on the main mechanism that toxic compounds will interfere the synthesized with defluorinated gene and green fluorescence gene (gfp)
bacteria metabolic reactions. As an example, biosensor based on Aci­ as regulatory and reporter gene, respectively, resulted in rapid and low
netobacter baylyi ADP1 was studied to detect heavy metals (Hg2+, Zn2+, detection limit analysis (Sunantha and Vasudevan, 2021). Shewanella
Cu2+, and Cd2+) in seawater by correlating the luminescence inhibition loihica having bidirectional extracellular electron transfer (EET) has
ratio (IR) with the heavy metals concentration (Cui et al., 2018). Sulfur showed its potential as BOD and nitrate detector with the characteristics
oxidizing bacteria (SOB) were also found out to be capable of detecting of high accuracy (>80%) and rapid analysis (<1 h) (Yi et al., 2020).
toxic chemicals (e.g., Cr6+) in stream water at low concentrations by Pseudomonas sp. bacteria immobilized on gold interdigitated micro­
changing their electrical conductivity and pH (Hassan et al., 2013). electrodes surface was also developed as sensitive phenol detectors
Likewise, a bioluminescence bacterium (Vibrio campbellii) obtained from based on the conductometric measurement (Kolahchi et al., 2018).
sea urchin indicates its ability to detect chromium in water as well Lastly, bacteria-based biosensors using engineered E. coli are capable of
(Thacharodi et al., 2019). This is supported by a comparison study detecting 2,4-dinitrotoluene (DNT) vapors and buried landmines con­
conducted where genetically modified bioluminescent bacteria (GMB) taining 2,4,6-trinitrotoluene (TNT) within micromolar detection level
were shown to provide more mechanism-specific tool than Chinese (Kabessa et al., 2016; Shemer et al., 2021).

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2.1.2. Food quality control toxicity and low environmental impacts (Antonacci and Scognamiglio,
In food industries, the safety and quality of the food produced are 2020; Eom et al., 2021). The development of microalgal nanoparticles
very crucial to both the producer and consumer as it can lead to major nowadays have also been used to remove bacteria coliform and heavy
profit loss and cause health issues, respectively. The usage of bacteria- metals, as well to reduce biological and chemical oxygen demand (BOD
based biosensors has increased in the past few decades due to its ad­ and COD), nitrogen (N), and phosphorus (P) which are closely related to
vantages of being portable and able to provide biological activity of the wastewaters (Chai et al., 2021). In addition, biotreatment of inor­
analytes for food screening (e.g., detections of allergens, toxins, food­ ganic nutrients and contaminants in wastewater using microalgal can
borne pathogens) (Ye et al., 2019). For instance, p-coumaric acid, result in valuable biomass (phospholipids and carotenoids), which can
known as a phenolic acid that possesses a wide variety of biological be used for animal feed, composting, and source of biofuel (Agarwal
activity such as antioxidant, anti-inflammatory, antimutagenic, et al., 2019; Low et al., 2021a). Therefore, interest in microalgae bio­
anti-ulcer, antiplatelet, and anti-cancer, is important to be monitored sensors has increased rapidly for monitoring of water and food herbi­
(Pei et al., 2016). A p-coumaric acid-responsive biosensor was developed cide, marine pollution, volatile organic compounds (VOC), heavy
based on E. coli and Bacillus subtilis co-culture to monitor yeast p-cou­ metals, etc. Several advantages of microalgal-based biosensors include
maric acid production (Siedler et al., 2017). Maltose is a disaccharide simple, low cost, high sensitivity, sustainability, versatility, and ease of
used in food industries to provide sweetness along with its high ther­ genetic modification (Brayner et al., 2011; Jacob et al., 2021).
mostability and low hygroscopicity and viscosity, which is also impor­ The detection method of microalgal biosensors for the target com­
tant to be monitored as it is very crucial to the quality of food produced. pound is usually based on the metabolic activity of the algae in a dose-
Therefore, an electrochemical biosensor was fabricated by combining effective manner. Several endpoints such as growth rate, photosynthetic
Glucoamylase-displayed bacteria (GA-bacteria) with glucose activity, fluorescence induction, and metabolism in regard to the
dehydrogenase-displayed bacteria (GDH-bacteria) on a multi-walled inhibitory effects of the analytes are measured either electrochemically
carbon nanotube (MWNT) modified glassy carbon electrode (GCE) or optically (Han et al., 2019). Among them, optical method provides
(Liu et al., 2017). higher sensitivity level (up to picomolar concentration), while electro­
In another study, a bioluminescent biosensor based on the combi­ chemical method allows more complex and turbid matrices (Boron et al.,
nation of E. coli, Staphylococcus aureus, Acinetobacter baylyi, and Pseu­ 2020). Thus, it is important to determine the method used based on the
domonas putida was developed to screen the concentration of types of analytes. Table 3 summarized the examples of microalgae-based
antibacterial agents (ethanol, naphthoquinones, and flavonoid) in sun­ biosensors.
dew extracts (Poikulainen et al., 2020). Screening of fluoroquinolones
(FQNs), antibacterial agents used in animal, agriculture and aquacul­ 3.1. Detection based on changes in growth related parameters
ture, were studied by genetically modified E. coli pK12 containing
plasmid pRecAlux3 biosensor (Cheng et al., 2014). Aside from that, a Several factors that can affect the efficiency of microalgal biosensors
sensing system of E. coli strain was developed to screen the toxicity level include abiotic (temperature, light, pH, oxygen, carbon dioxide,
of artificial sweeteners (aspartame, sucralose, saccharine, neotame, salinity), biotic (presence of pathogens), operational factors (dilution
advantame, and acesulfame potassium-k (ace-k)) as they have been rate, aeration and mixing, frequency of harvesting), and presence of
linked to various adverse health effects (Harpaz et al., 2018). Lastly, a other inhibitory substances. Therefore, the detection of microalgal bio­
biosensor based on four different strains of E. coli sensitive to stress sensors based on changes in their growth-related parameters can be
conditions (cytotoxicity, genotoxicity, oxidative stress, and closely correlated with their optimal conditions. In general, the optimal
quorum-sensing stress) was used to detect changes in volatile organic conditions for microalgae growth are at temperature <16 ◦ C and
compounds concentration after Penicillium digitatum infection (Chalu­ >35 ◦ C, neutral pH, and low saturation yet high-intensity light (Gata­
powicz et al., 2020). maneni et al., 2018). Furthermore, the presence of inorganic nutrients
(e.g., carbon, nitrogen, and phosphorus) and heavy metals also showed a
2.1.3. Medical application significant effect to the growth of microalgae for protein synthesis and
In the discipline of medical area, applications of bacterial biosensors source of micronutrients, respectively. It is supported by Otondo et al.
also showed an increasing trend. Many biosensors have been used as a (2018) where the growth of microalgae biomass increases along with
new alternative method by being rapid, portable, and simple to conduct. higher carbon and other nutrients concentrations (Otondo et al., 2018).
As an example, assays to detect the presence of hormone disruptors (i.e., Gao et al. (2019) also further explained if increased in organic carbon to
endocrine) compounds known to have potent health effects were nitrogen (TOC/TN) ratio in wastewater can increase the growth and
developed based on the fabrication of a native estrogen receptor alpha biomass production of C. vulgaris as carbon and nitrogen are essential
(ER) on E. coli surface (Furst et al., 2017). A simple, accurate, rapid, and nutrients for microalgal growth (Gao et al., 2019). However, further
low-cost E. coli biosensor to screen tyrosine in urine was also examined increase of the TOC/TN ratio (>30) will no longer increase the growth
to detect health disorders-related tyrosine metabolism (e.g., liver dis­ rate.
ease, alkaptonuria, tyrosinemia) (Lin et al., 2019). In regard to the microalgal biosensors based on growth-related pa­
Early detection of blood in the urine (haematuria) using bacterial rameters, it is mostly used to conduct toxicity tests in wastewater.
biosensor containing E. coli cells integrated with luciferase (luxCDABE) Several microalgae species that have been used as biosensors include
reporter gene also resulted in a promising analysis (LOD within μM Chlorella, Chlamydomonas, Arthrospira, Nannochloropsis, and Scene­
range) (Barger et al., 2021). Likewise, a bioluminescence E. coli desmus sp. due to their robustness and adaptability to extreme conditions
biosensor was developed for detecting gastrointestinal biomolecules (Maryjoseph and Ketheesan, 2020; Wollmann et al., 2019). Among
related to health problems (i.e., gastrointestinal bleeding) (Mimee et al., these, Chlorella sp. has been used mostly to detects heavy metals in water
2018; Woo et al., 2020). This was further studied using engineered as it is able to give a rapid response and is suitable for the detection of
bacteria biosensors to report gut health (Tanna et al., 2021) (Fig. 3). many types of metals (Wong et al., 2018). The mechanism of microalgae
as biosensors is similar to other microbial biosensors, where a decline in
3. Microalgal-based biosensor sensor response to the presence of inhibitors or toxicants indicates
possible contamination of the surrounding environment (Fig. 4) (Zer­
In comparison with other microorganisms, microalgae have great aatkar et al., 2016). The mechanism of heavy metals toxicity towards
adaptability to a wide variety of environmental conditions, making them microalgae is by chelating proteins and affecting various physiological
less vulnerable to physiochemical changes. Besides, microalgae are and biochemical process of the algae. Firstly, heavy metals will enter the
abundant in nature, have high sensitivity to toxicants, possess less algal cells either through active transport or endocytosis; thus, resulting

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7

Fig. 3. (a) Scheme of bacterial-based biosensor for screening gut health. (1) Two sensing elements: One-component systems (OCS), which activate downstream gene expression upon ligand binding, and Two-component
systems (TCSs), which sense extracellular through transmembrane histidine kinases. (2) Processing circuits for transducing inputs to outputs. (3) Actuator elements for utilizing reporter protein into deployable digital
readouts. (b) and (c) are CRISPR spacer acquisition-based DNA recorders for detection in clinical fecal samples and external stimuli, respectively. Reprinted from (Tanna et al., 2021) with permission from Elsevier.

Chemosphere 306 (2022) 135515

Z. Ma et al. Chemosphere 306 (2022) 135515

Table 3
Applications of microalgal-based biosensor.
Microalgae Substrate Detection Detection limit Ref

Chlamydomonas Diuron Fluorescence Gosset et al. (2018)

reinhardtii Diuron Electrochemical and 0.1 M Tsopela et al. (2016)
Fluorescence
DCMU and atrazine Fluorescence 0.1 M Ferro et al. (2012)
Chlorella sp. Atrazine and imazapic Fluorescence 0.70 mg/L and 0.01 mg/L, Stone et al. (2019)
respectively
Copper Fluorescence 50 nM Roxby et al. (2020)
Chlorella vulgaris Metals Luminescence 0.001 nm/L Wong et al. (2018)
Gasoline Electrochemical 0.04% v/v Nandimandalam and Gude
(2019)
Diuron Fluorescence Gosset et al. (2018)
Simazine, atrazine and diuron Fluorescence 1.35, 0.44, and 0.25 μg/L, Turemis et al. (2018)
respectively
DCMU and atrazine Fluorescence 0.1 M Ferro et al. (2012)
Monoraphidium arcuatum Atrazine and imazapic Fluorescence 0.70 mg/L and 0.01 mg/L, Stone et al. (2019)
respectively
Nannochloropsis-like sp. Atrazine and imazapic Fluorescence 0.70 mg/L and 0.01 mg/L,
respectively
Nitzschia closterium Lead Fluorescence Gan et al. (2019)
Pediastrum duplex Atrazine and imazapic Fluorescence 0.70 mg/L and 0.01 mg/L, Stone et al. (2019)
respectively
Platymonas subcordiformis Copper Fluorescence 0.65 mol/L Han et al. (2019)
Lead Fluorescence 1.90 mol/L
Phenol Fluorescence 2.85 mmol/L
Nonylphenol (NP) Fluorescence 5.22 mol/L
Pseudokirchneriella Diuron Fluorescence Gosset et al. (2018)
subcapitata Diuron Fluorescence 1 ppb Kashem et al. (2019)
Simetryn, simazine, and atrazine Fluorescence 10 ppb
DCMU and atrazine Fluorescence 0.1 M Ferro et al. (2012)
Rhodomonas salina Herbicides (diuron, metribuzin, hexazinone, tebuthiuron, Fluorescence Thomas et al. (2020)
bromacil, simazine, propazine)

Fig. 4. Inhibitory effects of heavy metals concentration towards growth of microalgae. Adapted from (Zeraatkar et al., 2016) with permission from Elsevier.

in binding to the sulfhydryl groups in proteins, disruption of the protein (APX)). Furthermore, this oxidized proteins and lipids will then in­
structure, and displacement of essential elements. Besides, heavy metals dicates the toxicity level of heavy metals towards algae (Arunakumara
can also disrupt the oxidative balance of the algae, leading to the and Zhang, 2008).
accumulation of antioxidant enzymes (e.g., superoxide dismutase In a recent study, C. vulgaris was utilized in a bioelectrochemical
(SOD), gluthathione peroxidase (GPX), and ascorbate peroxidase platform to monitor oil spills (gasoline) in aquatic and marine

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Z. Ma et al. Chemosphere 306 (2022) 135515

environments (Nandimandalam and Gude, 2019). It was shown that the subcapitata was also designed to detect diuron (LOD of 1 ppb) and
growth of C. vulgaris was significantly reduced when gasoline concen­ simetryn, simazine, and atrazine (LOD of 10 ppb) (Kashem et al., 2019).
tration increased, followed by inhibition of oxygen produced. The ef­ Lastly, an optical biosensor based on the symbiotic association of
fects of atrazine and imazapic to multispecies freshwater microalgal C. vulgaris and ciliate Tetrahymena pyriformis was used to examine the
(Pediastrum duplex, Monoraphidium arcuatum, Nannochloropsis-like sp., presence of simazine, atrazine, and diuron (LOD of 1.35, 0.44, and 0.25
and Chlorella sp.) were evaluated and results showed that microalgae are μg/L respectively) (Turemis et al., 2018).
highly intolerant to atrazine while tolerant at high level of imazapic As microalgae have the ability to change their bioluminescent in­
(>1100 mg/L) due to the nature of sensitivity of algal species to tensity (light-emitting system) in the presence of pollutants, Wong et al.
photosystem II (PSII)-inhibiting herbicides (Stone et al., 2019). This was (2018) developed a C. vulgaris-based bioluminescent biosensor at the
also supported by others, where exposure of Rhodomonas salina to spectrum of 350–650 nm to detect metals heavy metals (Cu, Pb, Cd) and
imazapic caused low or nontoxic responses to the growth rate (Thomas light metals (Na, Al, Li) in water (LOD of 0.001–10.000 nm/L) (Wong
et al., 2020). et al., 2018). Similar experiment was conducted where a
microalgal-based biosensor using Chlorella sp. coupled with copper
nanocavities (LOD of 50 nM) (Roxby et al., 2020). Nitzschia Closterium
3.2. Detection based on changes in photosynthetic efficiency biosensor based on chlorophyll fluorescence parameters (e.g., the rela­
tive electron transfer rate of PSII, the effective quantum yield of PSII
Toxicity in water can also affects other biological processes such as photochemical energy conversion) also discovered to detect lead
detoxification, photosynthesis, and respiration (Yang et al., 2018). toxicity in the marine ecosystem (Gan et al., 2019).
Microalgae as photosynthetic microorganisms have been used to detect
toxic chemicals in water due to their high sensitivity, not laborious, and 4. Fungal-based biosensor
rapid response (2–4 h) compared to detection based on growth rate
(48–96 h) (Han et al., 2019). The concept of bioreporting using micro­ Regarding cell-based biosensors, fungal biosensor is also gaining
algae is based on the measurement of photosynthetic activity of attention as it provides other advantages compared with bacterial-based
photosystem II (PSII), where it is highly disturbed by the presence of or other microbial biosensors. Firstly, it is because the metabolic activ­
toxicants (Turemis et al., 2018). By this, microalgae are important as a ities of yeast can determine the concentration of hardly detectable
biosensor to detect any PSII inhibitors, including herbicides and heavy molecules (e.g., sugars, alcohol, lactate) by converting them into simpler
metals. PSII inhibitors are responsible for blocking the light-induced molecules (e.g., dissolved oxygen (BOD), redox potential, etc.) (Ade­
electron transfer chain in PSII by blocking the PSII quinone binding niran et al., 2015). Secondly, as a eukaryotic organism, yeast has the
site; thus, reducing the photosynthetic activity to produce oxygen advantage of mimicking the metabolic activity of higher eukaryotes. The
(chlorophyll fluorescence) (Fig. 5) (Kumar et al., 2014). This inhibition underlying reason is that most eukaryotes bind to specific receptors or
of oxygen production rate is linearly correlated with the concentration disturb a particular signal pathway (MAPKs) (Chamas et al., 2017).
of the inhibitors present in the environments. For instance, Chlorella Other than that, in comparison with bacteria, yeast has greater tolerance
vulgaris, Pseudokirchneriella subcapitata, and Chlamydomonas reinhardtii to a wide range of pH, temperature, osmolarity/ionic strength, and
coupled with fluorimeter and microfluidic chips were developed to physical robustness while rapidly growing and easy to be modified as
detect diuron (Gosset et al., 2018). A similar experiment to detect diuron well. Yeast also provides higher time- and cost-effectiveness, sensitive,
using Chlamydomonas reinhardtii was also developed by integrating reproducible, and adaptable to high-throughput formats as well to
electrochemical and optical biosensors (Tsopela et al., 2016). Rhodo­ portable devices for in-field testing (Jarque et al., 2016). Additionally,
monas salina has also been used to detect seven individual Photosystem filamentous fungi have several photosensory systems capable of
II (PSII) inhibitor herbicides (diuron, metribuzin, hexazinone, tebu­ responding to different light intensities and wavelengths to obtain
thiuron, bromacil, simazine, propazine) in the marine ecosystem crucial information about their surrounding environments (Yu and
(Thomas et al., 2020). A biosensor chip based on Pseudokirchneriella

Fig. 5. Schematic representation of the mechanism PSII inhibitor (herbicide) to block electron transfer of microalgae. Reprinted from (Kumar et al., 2014) with
permission from Elsevier.

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Z. Ma et al. Chemosphere 306 (2022) 135515

Fischer, 2019). Thus, interest in yeast and filamentous fungi has Table 4
developed in the past recent years as a sensor component. Applications of fungal-based biosensors.
Organism Substrate Detection Detection Ref
4.1. Application of fungal-based biosensors principle limit

Alternaria Formaldehyde Growth rate Seo et al.

Yeast and filamentous fungi can be found in most environments and alternata (2008)
can metabolize a wide range of organic compounds. Due to this, they Arxula BOD Amperometry 2.4 mg/L Yudina
adeninivorans et al.
have been used mainly to detect heavy metals and toxicants in envi­
(2015)
ronments or food industries and medical areas. The detection method of Aspergillus Estradiol Spectroscopy 1 ng/L Zutz et al.
yeast biosensors includes fluorescence, luminescence, colorimetry, nidulans (2017)
electrical, and growth rate variation (Adeniran et al., 2015). Recent Aspergillus Formaldehyde Growth rate Seo et al.
applications of fungal-based biosensors are shown in Table 4. For penicillioides (2008)
Blastobotrys BOD Amperometry 0.7 mg Arlyapov
instance, fungal growth of Alternaria alternata, Eurotium herbariorum,
adeninivorans О2/L et al.
and Aspergillus penicillioides were studied to detect formaldehyde in the (2021)
air at the concentration of 700–4000 g m− 3 or higher (Seo et al., 2008). Botryosphaeria Dopamine Electrochemical 0.127 Coelho
Likewise, a co-culture of yeasts Pichia angusta, Arxula adeninivorans, and rhodina mol/L et al.
Spironolactone Electrochemical 0.94 mol/ (2019)
Debaryomyces hansenii was used for the assessment of biological oxygen
L
demand (BOD) based on immobilization in N-vinylpyrrolidone-modified Candida L-Ascorbic acid Amperometric 62 M Akyilmaz
poly (vinyl alcohol) (Yudina et al., 2015). Similar recent work done on tropicalis L-Ascorbic acid Differential 59 M et al.
amperometric BOD biosensors based on D. hansenii was studied with the pulse (2020)
ferrocene-methylene blue two-mediator system, providing longer-time voltammetry
Debaryomyces BOD Amperometry 2.4 mg/L Yudina
stability (43 vs. 17 days) with a nearly similar LOD value (2.5 mg/L
hansenii et al.
vs. 2.4 mg/L) (Zaitseva et al., 2017). An optical biosensor prepared by (2015)
immobilizing baker’s yeast (Saccharomyces cerevisiae) with polyvinyl BOD Amperometry 2.5 mg/L Zaitseva
alcoholstyrylpyridinium (PVA-SbQ) matrix was also performed for rapid et al.
(2017)
BOD monitoring (Kashem and Suzuki, 2015). Despite the immobiliza­
BOD Amperometry 0.7 mg Arlyapov
tion technique itself improving biosensors’ sensitivity, the combination О2/L et al.
of multilayer films exhibits more advantages due to less competition (2021)
among the substrate within the layer and greater ability to each of the Eurotium Formaldehyde Growth rate Seo et al.
cell layers (Arlyapov et al., 2021). Furthermore, a bioassay of a micro­ herbariorum (2008)
Ogataea angusta BOD Amperometry 0.7 mg Arlyapov
fluidic chemiluminescence system based on the redox reaction between
О2/L et al.
ferricyanide-quinone and S. cerevisiae was also developed to detect BOD (2021)
of ionic liquid (ILs) and deep eutic solvents (DESs) (Costa et al., 2018). Pichia angusta BOD Amperometry 2.4 mg/L Yudina
Aside from BOD, detection of heavy metals is also essential due to its et al.
hazardous effect on the environment and human health. For instance, (2015)
Saccharomyces BOD Fluorescence 14.6 mg/L Kashem
filamentous fungi (Trichoderma asperellum), known to have binding ca­ cerevisiae and Suzuki
pacity of metals, were used to detect lead (II) and cadmium (II). The (2015)
detection method is based on the development of a modified glassy BOD Luminescence Costa et al.
carbon electrode (GCE) functionalized with nano-tubes (SWCNTs- (2018)
Copper Fermentation Capece
COOH) (Dali et al., 2018). Additionally, endophytic fungi with potential
activity et al.
beneficial capabilities of metal uptakes were also combined with (2018)
different types of nanoparticles in biosensors (Khanam et al., 2020). Acetic acid Fluorescence 5 mM Hahne
The immobilization of Pichia angusta in a bimodal silica sol-gel ma­ et al.
trix containing different amounts of hydrophobic additives was studied (2021)
Estradiol Fluorescence 1 nM Lobsiger
to investigate whether yeast cells activity can be maintained in the et al.
presence of alcohol (Ponamoreva et al., 2015). Thus, it can be used to (2019)
determine methanol concentration. On the other side, baker’s yeast Estradiol Luminescence 0.08 nM Cevenini
(S. cerevisiae) that are important to conduct fermentation activity are et al.
(2018)
known to be copper-sensitive; thus, high copper content in wine can be
Pathogenic Fluorescence Ostrov
detected by them (Capece et al., 2018). S. cerevisiae also has been fungal et al.
examined to monitor acetic acid through its transcription factors (Hahne (2017)
et al., 2021). Candida tropicalis with ascorbate oxidase enzyme activity Hexanoic acid Fluorescence 0.01 mM Baumann
was also used to detect L-Ascorbic acid. The mechanism is immobilizing Heptanoic acid Fluorescence 0.01 mM et al.
Octanoic acid Fluorescence 0.01 mM (2018)
C. tropicalis with o-aminophenol and forming a film layer on the plat­ Doxycycline Fluorescence 0.3 g/mL Miller
inum electrode surface using the electropolymerization method (Akyil­ et al.
maz et al., 2020). (2020)
Endocrine-disrupting compounds (EDCs) known to cause adverse Trichoderma Lead (II) Voltammetry Dali et al.
asperellum Cadmium (II) Voltammetry (2018)
effects in organisms have increased researcher’s interest to develop
rapid and simple technology such as biosensors for monitoring and
detecting its presence. For example, a field-portable fluorescence showed a comparable ability to detect estrogen activity by integrating
biosensor based on the integration of cell cultivation, sensor function, human estrogen receptor and -galactoside (Zutz et al., 2017). Some
and signal detection of S. cerevisiae for the detection of estradiol was other applications of fungal biosensors that have been developed include
developed (Lobsiger et al., 2019). Likewise, a portable bioluminescent the S. cerevisiae-based biosensor to detect pathogenic fungi, food
biosensor using engineered S. cerevisiae can rapidly and quantitatively spoilage, and agricultural damage (Ostrov et al., 2017). Additionally,
evaluate total estrogenic activity in small sample volumes (Cevenini Botryosphaeria rhodina, known to produce laccase (glycoproteins
et al., 2018). Fungal-based biosensors using Aspergillus nidulans also

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containing copper atoms involved in redox potential), was used as an 5. Viral-based biosensor
electrochemical biosensor to detect dopamine and spironolactone
(Coelho et al., 2019). Viruses have also been shown to be promising bioreceptors other
than the microorganisms mentioned above. Most of the virus-based
4.2. Genetic modification/engineering biosensors are based on bacteriophages (i.e., phages) as it does not
contain any mammalian promoter making it less harmful to human
Similar to the bacterial-based biosensor, genetically engineered yeast health (i.e., quiescent in the absence of host bacterium) (Oh and Han,
biosensor also showed an increasing trend by coupling the reporter gene 2020). In particular, bacteriophages are classes of virus which specif­
with an inducible promoter. However, as the promoter itself is highly ically infect bacteria making it suitable as a sensor system to detect
selective, it can only be activated in the presence of a ligand of interest pathogenic bacteria especially that cause foodborne illnesses (e.g.,
via signaling cascade or direct receptor dimer mechanism (Gonchar E. coli, Staphylococcus, Campylobacter, Bacillus, Salmonella, etc.) (Singh,
et al., 2017). For the signaling cascade, many yeast biosensors rely on 2018). Bacteriophages exist in many different types depending on the
the capabilities of G-protein coupled receptors (GPCRs) due to its ability classification, they are also one of the most abundant microbes where it
to select a wide range of molecules, rapid intracellular response towards can be found in a wide range of living environment (e.g., soil, water, and
extracellular signals, similarities between yeast mating pathway and food). Moreover, phages as biosensor could provide real-time and
mammalian cell signaling, and dependent signal transduction on MAPK live-cell detection, cost-effective, high specificity, high affinity,
cascade. For example, yeast coupled with heterologous GPCRs were laborious-free, can be engineered either genetically or chemically, more
used to deorphanization of G-protein coupled receptors, metabolic en­ stable towards various environmental factors (pH, temperature, ion
gineering of yeast to produce bioactive compounds, pathogen detection, concentrations), and compatible as monodisperse nanoparticles for
and drug discovery in the medical area (Lengger and Jensen, 2020). preparation of novel materials (Janczuk-Richter et al., 2018; Singh et al.,
Although GPCR-based biosensors may pose many advantages, devel­ 2020).
oping yeast-based biosensors using S. cerevisiae to detect short- and Several phage-based sensor mechanisms to detect bacteria include
medium-chain fatty acids (SMCFAs) requires complicated yeast strain bacterial lysis, immobilization on a transducer surface, fluorescently
construction and needs of other heterologous plasma labeled phages, recombinant reporter phages, and others monitored
membrane-localized receptors for the detection (Baumann et al., 2018). through optical and electrochemical transducer systems (Fig. 6) (Richter
Therefore, S. cerevisiae-based biosensor using PDR12 promoter coupled et al., 2018). Many earlier articles have reviewed the applications of
with enhanced GFP was developed to detect hexanoic, heptanoic, and bacteriophage-based biosensors for detecting bacteria in food, human,
octanoic acid over mM range. and environmental samples (Ahovan et al., 2020; Hussain et al., 2021;
Engineered S. cerevisiae containing plasmid pCM176-yEmRFP was Richter et al., 2018).
also used to conduct a simple and low-cost paper test strip biosensor to
detect the physiological concentration of doxycycline in both human 5.1. Applications
and raw bovine serum (Miller et al., 2020). Similarly, S. cerevisiae con­
taining ATF1 reporter gene was examined to construct a yeast biosensor As a multi-drug resistant bacterium, Salmonella, E. coli, and other
that can produce a unique scent as a readout. The best estimate pathogenic bacteria have increased public health threats, leading to the
threshold (BET) for detecting hormone estradiol in humans is 39 nM, rapid growth of research to discover novel approaches to combat this
which is sensitive enough to detect estradiol in dosage forms as a urgency. Concerning this, many bacteriophage-based biosensors have
pharmaceutical monitoring tool (Goodson et al., 2020). been discovered as one of the most promising approach for rapid and
effective detection and monitoring of these pathogens especially in food
(Wei et al., 2019). Table 5 summarize the application of phage-based

Fig. 6. General Mechanism of phage-based biosensor to detect bacteria. Reprinted from (Richter et al., 2018) with permission from Elsevier.

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Table 5
Applications of phage-based biosensor.
Phage Target Method Detection Limit Ref
2
S16 LTF-bacteriophage Salmonella Spectroscopy <10 CFU/mL (Denyes et al., 2017; Dunne and Loessner,
2019)
M13 virus particles Human serum albumin (HSA) Spectroscopy 100 nM Ogata et al. (2017)
Phage JG004 Pseudomonas aeruginosa Luminescence Harada et al. (2021)
Phage NRGp5 Escherichia coli Luminescence <20 CFU/100 mL Hinkley et al. (2020)
Siphoviridae and Myoviridae phages Shiga toxin-producing Escherichia coli Electrochemical 10–102 CFU/mL (A. Quintela and H. Wu, 2020)
family (STEC)
Siphoviridae phage family Staphylococcus aureus Fluorescence 31 CFU/mL Bhardwaj et al. (2017)
T2-bacteriophage Escherichia coli Spectroscopy 103 CFU/mL Zhou et al. (2017)
T4-bacteriophage Escherichia coli Fluorescence 104 CFU/mL Janczuk et al. (2016)
Escherichia coli Spectroscopy 103 CFU/mL Halkare et al. (2021)
T7-bacteriophage Escherichia coli Fluorescence 100 bacteria/g Wisuthiphaet et al. (2019)

biosensors. Engineered phage S16 LTF (S16 LTF) involved in foodborne bacteria in food industries. In a specific way, this review
enzyme-linked LTF assay (ELLTA) showed rapid and specific detection showed many current research of microbial biosensors that has been
of Salmonella (Denyes et al., 2017; Dunne and Loessner, 2019). Another developed and showed many advantages (simple, rapid, robust, highly
bacteriophage-based biosensor was developed for detecting sensitive and selective, etc.), proposing its great potential to keep
antibiotic-resistant bacteria, Pseudomonas aeruginosa using three developed in the future. However, several disadvantages of using
different lytic phage immobilized within functionalized porous bio­ microorganism as a sensor system include ethical issues due to the needs
polymeric and bio-reactive alginate matrices (Harada et al., 2021). In of genetic modifications and requirements of additional exogenous
addition, a Bacteriophage interfaced with a hydrophilic stable substrate (i.e., substrate dependent) for the biosensor to improve the
metal-organic framework (MOF) and NH2-MIL-53(Fe) using glutaral­ sensitivity (Table 6).
dehyde as cross-linker also showed to be a sensitive biosensor to detect
Staphylococcus aureus with a limit detection of 31 CFU/mL based on its 7. Future perspectives
photoluminescence intensity (Bhardwaj et al., 2017).
Rapid detection of biosensor to screen the presence of E. coli in Although there have been many advantages of microbial-based
drinking water is an increasing trend nowadays. As an example, biosensors have been discussed in this review, further investigation of
bacteriophage-based biosensor is able to exhibit detection limit similar
to those of traditional methods within less a quarter of time (20 CFU/
100 mL in 5 h) (Hinkley et al., 2020). T2-bacteriophage immobilized on Table 6
polyethyleneimine (PEI) carbon nanotubes on glassy carbon electrode Advantages and disadvantages of the microorganism as biosensor.
were successfully tested to electrochemically detect E. coli (LoD of 103 Microorganism Advantages Disadvantages
CFU/mL) (Zhou et al., 2017). T4-bacteriophage coupled with bifunc­ Bacteria Adaptable to wide range of Some ethical issues by using
tional magnetic-fluorescent microparticles used to detect E. coli based on environments genetic modifications
flow cytometry method was capable of exhibiting limit detection around Rapid proliferation rate Some requires additional
104 CFU/mL (Janczuk et al., 2016). A portable sandwich-type ampero­ Easy, cheap, and rapid exogenous substrate for genetic
analysis modifications
metric biosensor based on bacteriophage immobilized onto a Adaptable to high- Less relevance to eukaryotes
streptavidin-coated screen-printed carbon electrode (SPCE) was also throughput formats and
constructed to specifically detect various Shiga toxin-producing E. coli portable devices
serogroups (STEC) (LoD of 10–102 CFU/mL) (A. Quintela and H. Wu, Microalgae Abundant in nature Requires specific environmental
High sensitivity condition to live (e.g.,
2020). A genetically engineered T7-bacteriophage-based fluorescence
Less toxicity and low temperature <16 ◦ C and >35 ◦ C,
biosensor was used to rapidly detect E. coli in beverages samples with a environmental impact neutral pH, and low saturation yet
reasonable detection limit (100 bacteria/g) within less than 6 h analysis Simple, cheap, sustainable, high intensity light)
period (Wisuthiphaet et al., 2019). Lastly, a recently conducted research versatile
also showed if T4-bacteriophage bioreceptor can rapidly and precisely Ease of genetic
modification
detect E. coli on a fiber-optic platform as low as 1000 CFU/mL (Halkare Fungal Eukaryotes Some ethical issues by using
et al., 2021). Adaptable to wide range of genetic modifications
In terms of medical application, a simple, monolithic, two-electrode environments
electrochemical biosensor coated with a thin layer of a composite con­ Able to detect hardly
detectable molecules
taining chemically engineered M13 virus particles with PEDOT (poly
Rapid growing rate
(3,4 ethylenedioxy thiophene)) were constructed to bind human serum Ease of genetic
albumin (HSA) selectively. The detection limit of this biosensor showed modification
to successfully detect as low as 100 nM HSA concentration in synthetic Adaptable to high-
urine solutions (Ogata et al., 2017). throughput formats and
portable devices
Virus Adaptable to wide range of Mainly specific to detect
6. Conclusion environments pathogenic bacteria only
Specifically infect bacteria
This review has highlighted a great prospect of microbial biosensor Real-time, cheap, highly
specific and sensitive,
as an analytical device that has been used in many areas due to its ability
simple analysis
to reduce many disadvantages of conventional analytical methods (e.g., Adaptable to high-
immunoassays, biochemical assays). Several applications on the past throughput formats and
five years have been summarized within this review. The applications of portable devices
microbial biosensors discussed mainly include to detect heavy metals, Can be genetically or
chemically modified
herbicides, and BOD in the environment, as well as the detection of

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The authors declare that they have no known competing financial 10.1007/S00216-017-0661-7.
interests or personal relationships that could have appeared to influence Chai, W.S., Tan, W.G., Halimatul Munawaroh, H.S., Gupta, V.K., Ho, S.-H., Show, P.L.,
the work reported in this paper. 2021. Multifaceted roles of microalgae in the application of wastewater
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