Trends in

Biotechnology
Review

Plasma for aquaponics

Syamlal Sasi, 1,2 Karthika Prasad, 1,2,* Janith Weerasinghe, 1,3 Olha Bazaka, 4 Elena P. Ivanova ,4
Igor Levchenko , 5,@ and Kateryna Bazaka 2,3,*

Global environmental, social, and economic challenges call for innovative Highlights
solutions to food production. Current food production systems require advances Population growth increases the pres-
beyond traditional paradigms, acknowledging the complexity arising from sus- sure on agricultural systems, depleting
resources and causing pollution.
tainability and a present lack of awareness about technologies that may help
limit, for example, loss of nutrients from soil. Aquaponics, a closed-loop system Aquaponics systems combine aqua-
that combines aquaculture with hydroponics, is a step towards the more efficient culture with hydroponics in a single
management of scarce water, land, and nutrient resources. However, its large-scale closed-loop system, where plant
waste sustains the growth of fish food
use is currently limited by several significant challenges of maintaining desirable
(e.g., larvae and worms), and fish
water chemistry and pH, managing infections in fish and plants, and increasing waste provides nutrients to plants,
productivity efficiently, economically, and sustainably. This paper investigates thus reducing their physical, environ-
the opportunities presented by plasma technologies in meeting these challenges, mental, and economic footprint.

potentially opening new pathways for sustainability in food production. Scale-up of aquaponics systems is hin-
dered by the need to maintain a fine bal-
ance between conditions that sustain
optimal productivity in intensive fish,
Aquaponics in the modern world plant, and nitrifying bacteria populations
Agriculture is increasingly under pressure from the growing global demand for food, competition for while mitigating pathogenic infections.
resources (i.e., land, water, energy, and labour), changes in production and consumption trends,
The use of plasmas in aquaponic sys-
and climate change. Food production systems need to adapt to cope with these challenges tems may help to resolve several key
by maximising their production efficiency and minimising their need for resources and reducing challenges such as disease and water-
environmental pollution associated with the use of fertilisers, pesticides and antimicrobials [1,2]. quality management, including removal
of pathogens and pollutants, enhance-
ment of plant growth, and extension of
Traditional monocrop agriculture (see Glossary) relies on the use of large areas of arable land, an the freshness and safety of perishable
increasingly scarce resource, degrading its quality in the process. Because this system is open-loop, plant and fish products.
the tremendous volumes of water and chemicals (such as pesticides and fertilisers), are not retained,
and become pollutants for oceans and waterways [3–5]. Closed-loop intensive farming systems
offer an opportunity to retain and reuse water and nutrients [6,7], with hydroponics and aquaponics
using a mere 10–30% of the fresh water used by conventional agriculture [6,7]. They are also less
susceptible to extreme heat and rain events and climate change-related reductions in precipitation
and water availability that hamper crop productivity in conventional agriculture. Of the two systems,
hydroponics is limited by the need for a continuous supply of plant nutrients. At the same time, the 1
Product Development, BudMore Pty
process is simpler, as water chemistry is optimised for the needs of the plants. Ltd, Brisbane, QLD 4000, Australia
2
School of Engineering, College of
Engineering and Computer Science, The
In contrast, aquaponics synergistically combines aquaculture and hydroponics in a single loop, Australian National University, Canberra,
where microorganisms and plants use fish waste as a nutrient source, and in doing so maintain ACT 2600, Australia
3
School of Mechanical, Medical and
water quality at the levels suitable for healthy growth of substantial stocks of fish and crustaceans. Process Engineering, Faculty of
These productivity gains and environmental savings come at the cost of a greater system and Engineering, Queensland University of
process complexity, where optimal growth conditions have to be sustained for three very different Technology, Brisbane, QLD 4000,
Australia
groups of organisms [8–10]. 4
School of Science, RMIT University, PO
Box 2476, Melbourne, Vic 3001, Australia
5
Of the challenges that limit the use of aquaponics [11], the most critical are cost and technical com- Plasma Sources and Applications
Centre, National Institute of Education,
plexity of infrastructure needed to sustain stable pH and water chemistry, microbial and algae bloom Nanyang Technological University,
control, and problems associated with the management of disease in fish and plant crops [12]. Singapore 637616

46 Trends in Biotechnology, January 2023, Vol. 41, No. 1 https://doi.org/10.1016/j.tibtech.2022.08.001

© 2022 Elsevier Ltd. All rights reserved.
Trends in Biotechnology

Plasma: a step towards simpler aquaponics *Correspondence:

karthika.prasad@anu.edu.au (K. Prasad)
As a tool that can produce various combinations of reactive chemical species and physical and katia.bazaka@anu.edu.au
effects, plasma holds the potential to address these challenges with a single solution, significantly (K. Bazaka).
@
simplifying the logistics of running an aquaponics system (Box 1). Twitter: @SpaceAdvanced
(I. Levchenko).

In this review article we discuss the opportunities and challenges of integrating plasma systems
with aquaponics.

Figure 1 (Key figure) shows a concept architecture for a ‘smart’ aquaponics system, where
plasma is used in conjunction with automation and artificial intelligence (AI) to enable continued
water quality monitoring and delivery of plasma-generated effects optimised for a specific task.

These tasks include control of pathogen load, degradation of chemicals and waste products,
stimulation of animal and plant growth and maturation, plasma-enhanced aeration, and optimisa-
tion of water chemistry at different points within the system.

Box 1. Plasma for aquaponics

CAPs present an interesting toolbox of technologies that can be used to control and drive a wide range of processes with
immediate relevance to aquaponics [88,89]. These include degradation of excess nutrients, chemicals, and drugs, adjustment
of water chemistry and pH, stimulation of organism growth, mitigation of algal blooms and infections in plants and animals, etc.
From an integration point of view, plasmas have a number of highly attractive features. The devices used for plasma generation
can be very simple yet produce a rich assortment of physical and chemical effects. They can be scaled up or down, which
means that they can address the needs of different farmers (Figure I). They have a very small footprint, and can be powered
from the power grid as well as from solar energy, making them suitable for remote areas. They do not rely on the use of any
chemicals, and any chemical species they generate can be produced at the point of application, alleviating the need for storage.
Yet, if required, reactive species can be captured in PAW, and transported and/or stored for a period of time with limited loss of
efficacy. Importantly, the reactive species are produced from water, and, after sufficient time, revert back to water, without gen-
erating by-products that may be harmful or persist in the environment. Plasma-based treatments also combine well with other
conventional treatments, often enhancing their efficacy through synergistic effects. They are also not restricted to any particular
species of plant, animal or microorganism, and can be optimised to address the needs of virtually any system. The diversity of
well-described device configurations may further assist in this optimisation process.

Various factors affect the agricultural productivity... From agro - to aqua Aquaponic cycle
could help!
Only 37.3% is agriculture land
Water scarcity
Nitrobacteria
Filter water
NO3
37.3% AQUAPONICS
Land degradation
CYCLE
Increase NO2
in population

CO2 NH3+ NH 4
Ammonia
Carbon footprint Loss of biodiversity Nitrosomonas

Trends in Biotechnology

Figure I. From agro to aqua: plasma can enhance benefits derived from aquaculture. Left: a schematic
representation of various factors that affect agricultural productivity. Right: from agro to aqua: aquaponic systems hold
strong potential as a sustainable food production platform and an alternative to conventional agriculture. The cycle
begins when protein introduced in the form of fish feed is consumed by fish and then excreted as ammonia into the
recirculating water. In addition to being the waste product from protein metabolism excreted by fish, ammonia can also
form during microbial decomposition of organic matter. Increased feed inputs needed to sustain high fish densities lead
to greater ammonia concentrations. Ammonia nitrogen is typically present in both ammonia (NH 3) and less toxic
ammonium (NH4+) forms in a pH- and water-temperature-dependent equilibrium (NH3 + H+ = NH4+). Nitrifying bacteria
(Nitrosomonas spp.) convert NH3 to nitrite (NO2– ) as NH3 + O2 → NO2 + 3H+ + 2e–, which is in turn converted to more
stable nontoxic NO3– by Nitrobacter spp. via NO2– + H2O → NO3 + 2H+ + 2e–. This nitrate is then absorbed by plants.

Trends in Biotechnology, January 2023, Vol. 41, No. 1 47

 Trends in Biotechnology

Key figure Glossary

General architecture of smart plasma-assisted aquaponic system Aquaponics: a closed-loop system
that combines the principles of
aquaponics and aquaculture for the
Automatic control and monitoring system simultaneous growth of plant and fish
produce, where waste produced by
Plants growing in aquaponics system aquaculture organisms is removed from
the water by microorganisms and plants
that use it for their nutrition.
Cold atmospheric plasma (CAP): a
Plasma enhanced
tray aeration system gas in a partially ionised state, where
many of the heavier species – such as
ions and molecules in the ground or
Growth tray excited state – remain at a lower
temperature when compared to
energetic electrons. It is rich in various
concentrations of neutral and excited
atomic, molecular, ionic, and radical
species, electrons, positive and negative
Air supply
ions, and free radicals. UV photons and
Filters
Cold plasma water treatment visible light are also emitted from species
Sensor
in an excited state.
Sensors Dielectric barrier discharge (DBD):
an electrical discharge between two
electrodes separated by an insulating
dielectric barrier that is capable of
Reservoir
ionising a neutral gas.
Pump control Hydroponics: a type of horticulture in
which plants are grown in a liquid
nutrient medium without the use of soil;
benefits include reduced water
consumption and water recycling, and a
Air pump considerably smaller land footprint.
Monocrop agriculture: a practice of
Nutrient pump Air line
growing a single crop year after year on
Nutrients RONs the same arable land, often using
Trends in Biotechnology
significant quantities of fertilisers to
replenish the diminishing reserves of
nutrients, pesticides to fight infections,
Figure 1. An automated system uses plasma to mitigate growth of harmful microorganisms, degrade drugs and chemicals, and copious volumes of fresh water for
stimulate animal and plant growth and maturation, aerate water, and maintain targeted water chemistry at different points of irrigation.
the system. Abbreviation: RONs, reactive oxygen and nitrogen species. Pathogen load: in aquaculture, the
number of microorganisms per unit
volume of water that can cause infection
in plants or fish.
Advantages include increased productivity, onsite manufacturing of active chemistries that do Planktonic state: the state of a
not persist in the environment (Box 2), immediate switching between plasma treatment modes microorganism in which they live and
grow in a free-floating manner.
that saves energy, drug-, fertiliser- and pesticide-free production, and integrated wastewater
Plasma-activated water (PAW): an
treatment. aqueous solution rich in reactive
chemical species that form as a result of
The concept builds on significant recent successes of applying plasma at different stages of the CAP treatment of water under controlled
conditions. The chemistry and
food production cycle – from disease management and growth stimulation in agriculture and concentration of these species depend
aquaculture to industrial biotechnology and food processing – and related fundamental advances on such treatment as plasma-forming
and translational studies focused on integration and scale-up. voltage, the carrier gas(es), temperature,
pulse duration, and frequency, etc.
Plasma device: a piece of equipment
Plasma-enabled water conditioning and disease management in aquaponics capable of converting a neutral gas into
Infectious diseases represent a critical challenge in aquaponics systems as they develop and an ionised gas; in this context, a partially-
spread rapidly though the closed-loop architecture, affecting all elements of the aquaponics ionised gas at room temperature and
atmospheric pressure.
system. Plasma represents unique possibilities for disease prevention and eradication in fish

48 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

Box 2. Plasma–liquid interface: possibilities for aquaponics Plasma discharge: an ionised gas
When plasma interacts with the surface of a liquid, several types of representative effects can take place. Some of these consisting of positive and negative
effects are listed here and illustrated in Figure I; however, the complexity of chemical and physical processes in the gas and charges and a large number of reactive
liquid phases and at the interface makes their deconvolution challenging. Some of the frequently observed phenomena species.
that may induce measurable effects in liquids used in aquaponics systems include [90,91]: Reactive chemical species: a term
used to collectively describe species
• Strong electric current-induced electrohydraulic shocks. with significant chemical reactivity,
• Generation and propagation of radiation of considerable intensity through liquid media. including radicals (such as superoxide
• Ultrasonically induced cavitation and related phenomena. radical anion and hydroxyl radical) and
• High-voltage pulse-induced electric breakdowns between conducting surfaces (e.g., electrodes) in liquids. nonradicals (such as hydrogen
• Reactive chemistry arising from diffusion of reactive species from bulk plasma, interactions between molecules in liquid peroxide). In the context of aquaponics,
and incident plasma-generated energetic species, and cascade chemical reactions. most of these are oxygen- and nitrogen-
• Generation of exotic excited states of molecules and atoms through interactions between molecules in gas and liquid containing species.
with strong UV and other excited species; and many others. Sessile state: a state in which
microorganisms live and grow attached
Evidently, such a rich diversity of processes that can take place simultaneously and affect and be affected by each other to a surface, often forming a biofilm that
presents a considerable challenge for detection and quantification of potentially relevant species such as exotic excited acts as a protective barrier against
states of molecules, atoms, and their attribution to specific processes. Figure I shows some of the charge-transfer physical and chemical damage.
processes that take place at plasma–liquid interfaces. Modelling efforts provide some insights into the formation and
lifetime of these species, yet gaps still exist in our understanding of these processes.

Configurations of the liquid–plasma interface also play a role in defining the dynamics of species generation, adding to the
challenges of developing a comprehensive toolbox [92]. To maximise process efficiency and tailor the plasma system to a
particular application, configurations that utilise more than one source of energy for excitation of species can be used,
giving rise to highly desired and sometimes unique synergistic effects that would be difficult to realise outside these hybrid
systems. Examples of how these synergies can be used span applications from marine antifouling technology [93],
hydrophilicity and hydrophobicity control [94] to targeted therapy [95] and cancer treatment [96].

Electrohydraulic
Plasma
shocks and many others
UV radiation Free electrons

Self-organization
at Plasma–water
Electric fields interface

Plasma-surface
sheath E Energy + liquid

Deformation Evaporation
of liquid surface
Short-living species, radicals and electrons Undersheath water layer

Diffusion
Heat transfer

Water Long-living species and radicals Slow chemical reactions

Trends in Biotechnology

Figure I. Plasma at liquid interface: an extended set of capabilities. Strongly nonequilibrium processes in liquids
driven by plasma-generated effects can be harnessed to control the properties of liquids and the behaviour of living
cells and organisms. Some of these processes are yet to be identified or their potential explored. An electric field is
present in the plasma-surface sheath between the bulk plasma and electrically charged surface of a liquid. In the under-
sheath water layer, short-living species, radicals, and electrons are present.

and plant populations, as it has been shown to effectively kill pathogens in their planktonic state
and sessile state and to remove even thick biofilms from living and artificial surfaces with minimal
harm to host species. It also stabilises water quality to prevent the growth of undesirable microbial
species.

Trends in Biotechnology, January 2023, Vol. 41, No. 1 49

 Trends in Biotechnology

Water sterilisation and preconditioning

Prior to every growth cycle, water sterilisation is a critical operation in aquaponics and aquacul-
ture, executed to minimise the pathogen load in water prior to introducing animal or plant
species into the system. Common industrial water treatments using chlorination, ozonation
and UV have drawbacks that render them unsuitable for aquaponics (Table 1). Toxic even at
minimal concentrations, residual chlorine degrades slowly and generates harmful oxidation
by-products. Ozonation depletes nitrogen levels, disrupting the nitrogen cycle and destabilising
the entire aquaponics system. Higher residual ozone levels lead to elevated mortality of fish and
poor growth rate of crops.

Cold atmospheric plasma (CAP) is a source of high electric fields, energetic charged particles,
ultrasound, UV light, and even shockwaves. When placed in contact with water, plasma can gen-
erate a significant amount of hydroxyl radicals and hydrogen peroxide, ozone, singlet oxygen,
nitrate radicals, and superoxides at the interface, which can then penetrate into the water [13].
In this respect, the plasma–liquid interaction is the source of the very same chemical agents
used in conventional sterilisation [14], as well as in advanced oxidation-based degradation of
organic compounds such as volatile organic compounds, pesticides, pharmaceuticals, and
care products in wastewater streams. At higher doses, CAP can decompose organic molecules
in water by a series of chemical reactions (such as abstraction and addition) and physical pro-
cesses (such as plasma-induced heating). The compounds in solution are first converted into
lower-molecular-weight molecules, and ultimately into water, carbon dioxide, and essentially
harmless mineral acids and salts. Plasma-generated species increase electrical conductivity

Table 1. Comparison of different water sterilisation methods used in aquaponics

Method Advantages
Chlorination • Effective microbial disinfection
• Avoids recontamination
• Reduces moulds and algae
Ozonation • Elimination of contaminants and
pollutants
• Leaves no odour or taste
UV disinfection • Effective microbial disinfection
• Leaves no by-products
• No effect on taste or odour
Cold atmospheric • Effective microbial disinfection
plasma or • Degradation of organic waste
plasma-activated • No effect on taste or odour
water • Increases dissolved oxygen (DO),
decreases chemical oxygen
demand (COD) and pH
• Synergistic effects with UV and
highly reactive species
• Chemical free
• Controllable mild reactions
• No adverse effect on the
environment, no residual chemicals
Disadvantages
• Chlorine residues, even at low concentrations,
are toxic to aquatic life
• Potential longer-term effects of chlorination
by-products
• Changes to taste and odour of treated water [77]
• Limited duration of protection
• High residual ozone concentrations pose risk to
cultured fish stocks, causing gross tissue
damage and stock mortalities
• Often used in conjunction with other filtration
methods
• Destabilisation of pH
• Can cause algal growth
• In some cases, water needs to be prefiltered as
high turbidity reduces efficacy
• Not effective against various contaminants in
water
• Excess hydrogen peroxide, nitrates, and nitrites
produced during plasma generation may react
to form potentially toxic compounds such as
peroxynitrous acid
• The lifespan of the reactive species is relatively
short

50 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

and levels of dissolved oxygen, decrease chemical oxygen demand (COD) and pH values, and
degrade waste molecules and eliminate foul odour to better support fish and plant growth,
making aquaponics systems more suitable for use in areas with a high population density.

These properties make CAP a promising technology to recover clean water from wastewater
streams, such as those produced by abattoirs. Wastewater generation in abattoirs is significant,
with estimated 10–11 kl per tonne of carcase weight produced in large integrated export facilities,
and 3–5 kl per tonne in small domestic facilities in Australia [15]. With increasing scarcity and demand
for fresh water supplies, and consequent increased financial costs of water, there is a growing
pressure for large industrial water users, including abattoirs, to use water more efficiently.

For this reason, abattoirs are increasingly being seen as not necessarily polluting but as a nutrient
resource that can be captured through integrating farming practices [16]. In some Asian coun-
tries, integrated livestock fish aquaculture introduces animal excreta and urine into fish ponds
to enhance the biological productivity of ponds by stimulating growth of plankton and other
microorganisms eaten by the fish [17]. In Australia, the integration of meat and livestock effluent
and aquaculture has chiefly been limited to primary algal production [18]. However, this can be
extended to polycultures using commercially valuable species such as carp and silver perch
that can feed on phytoplanktonic, zooplanktonic, and benthic food resources resulting from the
primary production [19]. At the same time, this will lead to improvement in wastewater quality, for ex-
ample, a significant reduction in nutrient load and increase in dissolved oxygen levels. However, for
the integrated system to be effective and profitable, several issues need to be resolved.

The combined wastewater output contains organic matter with high levels of nitrogen and phospho-
rus, a wide range of potentially pathogenic microorganisms, some quantities of cleaning and disinfec-
tion chemicals, and trace amounts of toxic compounds, hormones, and heavy metals [20].
Depending on the waste stream, the organic matter can vary from ‘green’ waste from manure,
paunch wastes, stockyard washing, and emptying of the animal stomachs, to ‘red’ waste with
high protein, blood and fat content from carcase washing. The temperature of wastewater can also
range from cool to hot. As such, it cannot be discharged directly into a fishpond [17,19]. First, waste-
water needs to be pretreated (e.g., via polymeric chemical coagulation and flocculation) to reduce the
level of suspended solids, fats, oils, and grease. This requires a multistep process that is expensive to
install and maintain. For example, for stickwater treatment, a membrane-based vibratory shear
enhanced process (VSEP) would require a capital investment of several hundred thousand of dollars
to install a system capable of processing 30 kl per day, with processing costs per kl of >$4.00
[15,16,19,21]. Yet this system would not be able to remove either microorganisms or pollutants,
and its efficacy would be affected by the temperature and volume of the effluent.

Biological and chemical treatment of abattoir wastewater is also challenging due to its unique
composition, where the amount of dissolved oxygen needed by chemical reactions or aerobic
biological organisms to break down organic material (expressed as the COD or biological oxygen
demand, BOD) is high. Even after pretreatment, suspended solids from the wastewater can
cause high water turbidity (200−400 nephelometric turbidity units, NTU) and thus prevent sunlight
needed for algal photosynthesis from penetrating deep into the water [15,16,21]. The growth of
algal species, Chlorella and Chlamydomonas species, is needed to absorb CO2 produced by
bacterial breakdown of organic matter in the effluent and to produce oxygen to meet the respira-
tion needs of those bacteria.

Furthermore, the pretreated wastewater still contains high levels of N and P (up to 150 mg/l
ammonia and around 5 mg/l phosphate) that need to be managed in order to prevent their

Trends in Biotechnology, January 2023, Vol. 41, No. 1 51

 Trends in Biotechnology

accumulation in the matter settling on the bottom of ponds that can lead to toxic blue-green algal
(cyanobacterial) blooms [19]. Until the pond is stabilised and the balance between algae (e.g., a
commercially significant Chlorella vulgaris) and bacterial populations are attained, the levels of
ammonia (100–150 mg/l) and water pH in the pretreated water will in most cases exceed the
upper tolerance limits of most fish species, affecting fish survival and growth [19]. However,
pond stabilisation is time- and resource-consuming. Moreover, in order for aerobic biological
organisms to break down organic material present in wastewater, significant amounts of
dissolved oxygen have to be introduced into the water. This is addressed by aeration to promote
carbon assimilation, ammonification, and nitrification by the aerobic bacterial community, and to
maintain a pH that favours the growth of desired microbial communities.

Unlike conventional methods that rely on sequential removal of expected groups of hazards from
abattoir wastewaters – microbiological (pathogens such as Escherichia coli, and spoilage organisms),
chemical (‘micropollutants’ such as disinfection by-products and hormones), and physical
(macrocontaminants) – CAP systems have the capacity to achieve this goal more efficiently,
especially if renewable energy (e.g., solar energy directly from solar panels or via a battery) to
create and sustain an electric discharge is used.

Effectively, this means that plasma treatment can be used to efficiently decontaminate wastewater,
as well as to convert concentrated stickwater into a mixture of higher-value compounds that can be
used as precursors for biofuels, growth media for industrial fermentation, and other uses.

Infection mitigation
Infection mitigation in a dynamic complex system comprising species from multiple kingdoms is
not trivial. Plants and animals in an aquaponics system can be infected by a broad spectrum of
pathogens [22,23]. However, the available treatment options are limited as the recirculating
water is shared by plants, fish, and beneficial microorganisms. Where in conventional aquaculture
chlorination or ozonation may be suitable, these can only be used in between growth cycles in
aquaponics, with administration of organism-specific drugs and antibiotics as the only viable op-
tion during the growth cycle [11]. However, prolonged use of antibiotics leads to the emergence
of antibiotic-resistant microorganisms of greater concern for the health of their host and poten-
tially the human consumer. Furthermore, antibiotics from commercial aquaculture persist in the
environment, with traces often found in water bodies [24]. Most fertilisers, pesticide and insecti-
cides used to manage airborne and waterborne plant infections are toxic to aquatic life. Isolation
of causal agents, efficient detection/monitoring of the disease, controlled application of chemicals
(pesticides) or use of natural pesticides, and so on, are some of the currently adopted practices
for infection management in aquaponics systems [22].

CAP is emerging as a feasible option to control infectious diseases in terrestrial and aquatic species.
Certain plant defence responses to biotic and abiotic stresses are coordinated by endogenous
reactive oxygen and nitrogen species (RONS) [25]. The mechanism by which CAP induces death
in pathogens is also largely mediated by RONS. Plasma-generated RONS may also stimulate
oxidative and nitrosative signalling and the production of defence hormones (e.g., salicylic acid
and jasmonic acid) in plants [26]. Coupling of the plants’ self-defence mechanisms with that of
CAP-generated RONS may thus improve outcomes for disease control in plants [27,28].

On surfaces [29,30], inactivation of disease-causing bacteria, viruses, and fungi may involve
direct reactive species-induced damage of cell membrane and erosion of protective extracellular
polymeric substances, oxidative stress, and damage to intracellular proteins and lipids [31,32].
RONS induce DNA breaks and interfere with critical repair processes in cells [33]. The influx of

52 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

RONS across cell membranes causes fluctuation in the intracellular pH, damaging cells which are
unable to maintain pH homeostasis [34]. The accumulation of charged particles on the surface of
bacteria can lead to cellular damage due to electrostatic interactions. Plasma-generated UV
photons can hinder replication via dimerisation of the thymine base, and via bacterial spore
inactivation (Figure 2A) [35].

Excited singlet oxygen atom O(1D) has an important role in the inactivation of fungi by causing wrinkles
in the spores of the fungal hyphae [36]. Cell leakage and viability loss through cell membrane damage,
and degradation of vesicles and conidiophores of fungi also takes place (Figure 2B).

When in contact with water, plasma (CAP) generates what is known as plasma-activated
water (PAW), also commonly referred to as plasma-treated water (PTW). PAW is enriched
with RONS, and its physicochemical properties (such as pH and conductivity) can be varied by
controlling the type and duration of plasma treatment. PAW can also inhibit germination of fungal
spores (Figure 2C) and cause apoptosis-inducing physiological changes in fungi [37].

A significant decrease in the biofilm burden on skin was demonstrated in fish grown in a plasma-
enhanced tank [38]. Figure 2D illustrates that even a brief daily treatment was sufficient to reduce
the size of the infected area. Viral proteins were also shown to be sensitive to RONS, with rapid
denaturation of bacteriophage lambda proteins causing phage inactivation (Figure 2E) [39,40].

Plasma-enabled water quality management in aquaponics

Water in fish-holding facilities progressively accumulates minerals and nutrients, altering water
chemistry and creating favourable conditions for increased phytoplankton productivity. Algal
blooms and their subsequent degradation by bacteria significantly deplete oxygen, with the
resulting anoxic environment being harmful to fish and invertebrates.

pH stabilisation and nitrogen cycle management

pH is a critical water quality characteristic determining the survival and growth of all organisms in
an aquaponics system [41]. A pH tolerance range specific to the cultured species is thus carefully
maintained, as large fluctuations in pH inhibit growth rate, reproduction, and metabolic activity,
and can distort the balance in the system and cause die-outs of subpopulations [42]. The ideal
pH range for each species in the system is different. pH values between 6 and 7 are optimal for
plants, whereas fishes have a higher threshold tolerance of 4–10 and an optimal pH requirement
of 7–9 for enhanced growth. Nitrifying bacteria, which play a key role in converting fish waste to
plant nutrients, exhibit peak ammonia oxidising activity at pH 8.2 [43].

Although pH depends on a multitude of factors, its fluctuations are mainly attributed to fish
excreta and the activity of microbes living in the system. Fish excrete ammonia which increases
the pH of the water, potentially harming fish (by denaturing proteins in the their cell walls),
retarding plant growth, and also inhibiting the survival of preferred bacterial species. Ammonia-
oxidising Nitrosomonas spp. and nitrite-oxidising Nitrobacter spp. convert NH3 into NO2 and
subsequently into plant-available NO3, also releasing H+ ions to lower the pH. In addition to the
natural mechanisms, nutrient supplementation (where carbonate, bicarbonate or hydroxide is
added) and fluidised lime-bed reactors that release dissolved limestone into the water are used to
help manage ammonia, yet these may increase water alkalinity [44]. Minor loss of ammonia can
also take place in heavily aerated ponds. Although CAP may reduce the number of nitrifying bacteria,
it may have a positive effect on the ammonia neutralisation cycle via water acidification, facilitating the
reduction of NH3 into NH4+ that takes place at lower pH. This drop in pH traps NH3 and adds a mol-
ecule of NO3, thus increasing the availability of an immediately accessible nitrogen source for plants.

Trends in Biotechnology, January 2023, Vol. 41, No. 1 53

 Trends in Biotechnology

Trends in Biotechnology

Figure 2. Antibacterial, antifungal, and antiviral mechanisms of cold atmospheric plasma (CAP) and plasma-activated water (PAW). (A) CAP can damage
virtually every component of a bacterial cell. (B) Schematic representation of the antifungal mechanism of CAP. (C) Exposure of water to CAP results in PAW rich in reactive
species that can be used to hinder conidial germination of Colletotrichum alienum, a pathogen known to cause postharvest anthracnose and rot in apple, banana, and
avocado fruit [37]. (D) Healing of bacterial skin infection in blood parrot cichlid fish housed in a plasma-enhanced fish tank [38]. (E) Transmission electron microscopy
(TEM) images of viral T4 bacteriophages treated with CAP and PAW [39]. Aggregation of T4 bacteriophages is attributed to oxidation of their cysteine-rich domains.
Prolonged CAP/PAW exposure completely degraded the envelope that enclosed the nucleic acid, and significantly modified RNA sequences via damage from reactive
oxygen and nitrogen species (RONS) and UV (in the case of CAP). Damage to spike proteins and genetic material may prevent the fusion of the virus with its host cells,
or may trigger apoptosis of infected cells. All images reprinted, with permission, from [37–39]. Abbreviations: PDA, potato dextrose agar; CP, cold plasma.

CAP is very effective in controlling the pH of a system through chemical reactions between
plasma-generated electrons, free radicals, photons, excites molecules, positive and negative
ions with water [45]. Prolonged plasma treatment often leads to the formation of strong acids

54 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

[46] (e.g., nitric and peroxynitrous acid) and hydrogen peroxide [47], and a reduction in pH [48]. It
has also been shown that the combination of both nonthermal and thermal plasma can create a
controlled pH from 0 to 7 in treated liquids. By generating plasma using different systems (e.g.,
atmospheric pressure micro-arc discharge or micro-jet device configurations), and by varying
gas chemistry, treatment duration and treated volume, size of plasma–liquid interface, and dis-
tance from the plume, different values of pH can be attained. In general, a greater concentration
of reactive oxygen species (ROS)was found for water samples treated using argon discharges,
whereas treatment air discharges produced water with greater levels of reactive nitrogen species
(RNS) and greater changes in pH and electrical conductivity. Importantly, water thus treated
showed relatively good stability with respect to pH, electrical conductivity, and levels of hydrogen
peroxide and nitric acid [49]. Furthermore, acidic pH is beneficial for reactive species transport
across microbial cell walls. Plasma-generated RONS also decrease the resistance of microorgan-
isms to acidic conditions [50,51].

Breakdown of organic waste during growth cycles

CAP can effectively decompose organic waste in contaminated water, including recalcitrant mat-
ter, during the operation part of the fish growth cycle. Primary sources of waste here include
excess fish feed, excreta from aquatic organism, and products of dead organism breakdown.
These pollutants adversely affect water quality and fish health, retard growth rate of plants and
fish, compromise the quality (colour, texture, taste, and safety) of produce, and contribute to
the increased adsorption of organic material and complex heavy metals. CAP can also initiate
the degradation of the pharmaceutical drugs (e.g., antibiotics) the persistence of which can be
harmful to fish stocks and, ultimately, to the consumer [52,53], as well as leading to antibiotics
resistance.

Management of aquaponics waste using CAP may offer a simpler, energy- and cost-efficient,
eco-friendly alternative to conventional methods, as it does not require the use of any chemical
agents. Pulsed electrical discharges can be particularly efficient for organic waste decomposition
in water. Being a source of strong electric fields, reactive particles such as UV light, oxidative spe-
cies, reductive species, ultrasound, etc., plasma can decompose waste materials more efficiently
than traditional methods. The mechanism of degradation by plasma may include electron collision
as well as photolysis or pyrolysis involving plasma-generated molecular and ionic species [54]. In
some systems, during plasma discharge a significant increase in temperature may take place,
and with a finite volume of water hindering the spread of plasma, high pressure may be gener-
ated. In an incompressible medium, the generated high pressure leads to shockwaves. Recent
developments in plasma technology specifically designed to efficiently eradicate or cause com-
plete demineralisation of pollutants has been gaining increased attention [55]. As an example,
Figure 3A illustrates a multielectrode system developed for the decomposition of pollutants in
water, using the gliding arc discharge (GAD) technology. In the gliding arc system, divergent elec-
trodes are mounted orthogonally to a plane, and processing gases used for plasma generation
are injected through a port under the symmetry axis of electrodes. Once initiated, the arc glides
in the direction of the gas flow, elongating to a point when is no longer sufficient to maintain the
self-sustained discharge. Once that critical length of the arc is reached, it will become
extinguished, interrupting the current and at the same time forming a new arc [56].

Other benefits of plasma in aquaponics

In addition to the benefits already described, plasma can be applied to many processes that
could be beneficial to the efficiency and performance of aquaponic systems. For example,
plasma treatment can promote faster germination of seeds in the growth beds, enhance plant
growth and productivity, and extend the useful shelf-life of products post-harvest.

Trends in Biotechnology, January 2023, Vol. 41, No. 1 55

 Trends in Biotechnology

Trends in Biotechnology

Figure 3. Plasma for the decomposition of contaminants, stimulation of seed germination, and improved food storage and safety. (A) Schematic diagram
of a gliding arc discharge system for plasma-based decomposition of pollutants in water [56]. (B) Plasma-generated reactive oxygen species (ROS) can promote seed
germination by acting as a signal molecule to interfere with seed dormancy. Specifically, hydrogen peroxide activates and upregulates the catalase (CAT) genes. (C)
Schematic representation of production of plasma-activated water (PAW) ice for storing seafood. Ice produced from PAW is free from microbes, which prolongs the
shelf life of the shrimp, whereas ice produced using tap water (TW) can result in the early spoilage of the shrimp [69]. (D) Washing process of raw foodstuff using
plasma-treated water (PTW) or TW as a reference with the aim to extend useful shelf-life and retain quality (colour and texture) in the prewashed produce [73].
(E) Prawns stored in TW ice (A) and PAW ice (B) for 9 days [69]. All images reprinted, with permission, from [56,69,73].

Seed germination and enhancement of plant growth

The effectiveness of CAP in assisting seed germination is being extensively studied (e.g., Figure 3B),
with efficiency reported to depend on seed type, environmental factors, etc., and optimum treatment
time [57,58]. The most sensitive phases in a plant life cycle are germination and seedling growth,
when seeds are vulnerable to several environmental stresses that can cause variation in germination,
ultimately resulting in reduced seedling growth, crop quality, and yield. CAP can etch the seed coat,

56 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

increasing its wettability, promoting subsequent water uptake, which in turn helps to trigger the
processes associated with germination.

PAW/PTW contains high levels of RONS, such as hydrogen peroxide, hydroxyl radicals, ozone,
nitric oxide, superoxide, etc. [59]. PAW can potentially double seed germination and promote
subsequent stages of seedling growth. RONS (e.g., hydroxyl radical, superoxide, hydrogen per-
oxide, and atomic oxygen) and UV can assist seed germination by inactivating seed diseases and
enhancing antioxidant defence mechanisms in plants [60]. Germination- and growth-stimulating
ROS are generated by the mitochondria in cells. The interaction between these natural reactive
species and the additional ROS produced in PAW promotes quicker seed germination [61]
by breaking down seed dormancy and activating catalase genes [62]. H2O2 in PAW can help
to control transcription processes, such as the production of antioxidants and gibberellic acid,
brassinosteroids, ethylene, auxin, and abscisic acid, hormones responsible for seed dormancy
and seed germination [63]. Moreover, RNS in PAW affects the phytochrome activity of seeds,
changing light requirements for seed germination. ROS in PAW can act as intracellular chemical
signals in seeds and seedlings, positively affecting their growth [64], and engage in thiol oxidation
or protein carbonylation.

At later growth stages, exposing plants at seed and seedling stages to RONS stimulation may
induce a wide range of stress responses by upregulating the transcription of defence and repair
molecules in their cells. Modulation of growth parameters is also likely, with changes in the phys-
ical dimensions of leaves, shoots, and roots, and the transition between distinct growth stages
reported in plants in response to PAW. Here, balancing ROS molecules (e.g., H2O2 and O2–) is crit-
ical for promoting desirable processes such as root growth and root hair development [65], leaf
development, and pollen tube growth, as excessive RONS stress may trigger deformities,
senescence, and death in plants. Nitrates generated in PAW through oxidation and reduction
of N2 may provide an alternative nitrogen source for plant growth, although this should be man-
aged carefully to maintain the nitrogen cycle and reduce the formation of toxic nitrogen species.
Importantly, PAW-mediated reduction in the disease burden may be one of the most critical
contributions to healthy plant development. In short, PAW holds great promise for improving
plant growth and crop yield while reducing harvest time.

Food storage and quality

Food safety and storage are critical aspects of food security. Both CAP and PAW treatment of
harvested produce can extend freshness and safety of perishable plant and fish products without
compromising their quality. The antimicrobial properties of CAP prevent proliferation of food-
spoilage-causing bacteria and fungi [66], and pathogens harmful to humans. The ROS present
in plasma can at times bleach the produce; however, a large variety of vegetables – including
carrots, lettuce, and tomatoes – exhibited insignificant colour change upon treatment with CAP
or PAW [67]. Furthermore, deactivation of polyphenol oxidase and peroxidase using CAP can
prevent fruit and vegetable browning [68]. Ice produced from PAW is efficient in preventing
growth of microorganisms on shrimp, extending storage life without compromising quality
(Figure 3C) [69–71].

Food quality and safety can be further improved using CAP, as it is capable of breaking down
surface contaminants on foods that may be harmful to human health (e.g., pesticides and other
agrochemicals), allowing for their controlled application to eradicate plant and fish diseases that
cannot be managed by CAP/PAW alone. Residues of pesticides (e.g., water-soluble hexachlorocy-
clohexane and endosulfan) may persist on surfaces after washing, whereas thermal or chemical
treatment may produce toxic degradation by-products and reduce food quality. ROS (particularly

Trends in Biotechnology, January 2023, Vol. 41, No. 1 57

 Trends in Biotechnology

O2–, OH, and O3), N2, and UV are particularly important in oxidation of P=S bonds and cleavage of Outstanding questions
P–S and S–C bonds [72]. Figure 3D and E illustrate the application of PAW for the quality- Can the multiple factors generated by
retaining food processing and storage [73]. plasma at scale be controlled with the
necessary precision and efficacy to
deliver the desired effects in such a
Concluding remarks and future perspectives complex, multiorganism dynamic
Aquaponics is a very effective farming method that uses 90% less water and other resources system?
when compared to the traditional farming approaches, promising economic, social, and environ-
Can sustained and/or repeated
mental sustainability, diverse food products where space is restricted, more efficient utilisation of
exposure of fish, plant and microbial
resources, and reduced pollution. (both desirable nitrifying and
pathogenic) populations to plasma-
Applied at different stages and points in the aquaculture system, CAP can facilitate the delivery generated effects lead to short- and/
or long-term changes in their pheno-
of these benefits through rapid and efficient (in terms of rates of produce generation, kg/m3) type or genotype?
on-demand production of transient chemical and physical effects for chemical-free disinfection,
water quality management, organic waste disintegration, ammonia neutralisation, and drug- Can the at-scale plasma systems be
free growth stimulation [40]. sufficiently competitive to replace
traditional chemical and physical
methods of mitigation currently used
In doing so, it may help overcome current challenges of commercial scaling, particularly providing in aquaponics?
a compact system to replace currently used complex processes and infrastructure for pathogen
Can renewable sources provide a
load management, ammonia removal via biofilters, and solid waste management with filters.
reliable source of energy for initiating
and sustaining plasma, and what are
Leaving no residue and removing traces of pesticides and agrichemicals, CAP and PAW may the cost, infrastructure and footprint,
extend the useful life of food with zero chemicals. and environmental implications of
renewables-driven plasma?

Certain types of treatment may even induce genetic or phenotypic changes in fish, increasing
productivity [74].

Yet, for the practical realisation of such plasma-enhanced aquaponics architectures, several
questions need to be answered (see Outstanding questions). Among them is a cost/benefit anal-
ysis of using plasma instead of conventional chemicals and filtration, scaling up while maintaining
energy efficiency, and in-depth understanding of dosing in a complex system.

Potential challenges
As an emerging technology for aquaponics, CAP is still rapidly evolving, with only a limited num-
ber of early adopters attempting to understand the most feasible way to implement plasma
technology in aquaponics. In part, the diversity of available plasma systems and complexity
of physical and chemical processes that may take place in a plasma/liquid/organism system
makes comparison, optimisation, and integration of CAP into aquaponics set-ups more
challenging. Additionally, it is still not clear to what extent plasma-generated reactive
species – individually and in combination with other species and chemicals – bring in desired
degradation effects before they reach levels at which the health of organisms in an industrial system
become affected. Indeed, it is critical to make a comprehensive assessment of all aspects of
plasma interactions with living organisms at a molecular, cellular, tissue, and systems level to
understand necessary plasma doses, toxicity of plasma-generated species to fish, invertebrates,
and plants, and the relationship between the plasma source and those parameters across
the system.

While a comprehensive outline of published literature (e.g., [75]) is outside the scope of this
review, a summary of relevant examples that demonstrate capabilities of different types of plasma
system can be found in Table 2, offering a general idea of their characteristic powers, doses, and
other key parameters.

58 Trends in Biotechnology, January 2023, Vol. 41, No. 1

Trends in Biotechnology

Table 2. Parameters of plasma and effects on various types of plants and animals which can be grown in an aquaponics system
Product Plasma typea Plasma parameters Treatment outcomes Refs
Zebra fish (Danio rerio) NAP 100 V, 60 Hz, 30 s, argon Evaluated the in vivo safety of plasma devices [78]
White shrimps DBD 40 kV, 500 Hz, 10 min, air Improved physicochemical properties during [79]
(Litopenaeus vannamei) storage; improved shelf life
Blood parrot cichlid fish (Cichlasoma synspilum × Microbubble/DBD 4 kV, 40 W, 15 min Reduced biofilm formation and improved health [38]
Cichlasoma citrinellum) (40 s daily) status of fish
Peas (Pisum sativum ‘Salamanca’) DBD 6–12 kV, 20 MHz, 5 min, air Germination, growth, photosynthesis of sprouts [80]
and seedlings
Blueberries (Vaccinium sect. Cyanococcus) APP 47 kHz, 549 W, 30–60 s, air Reduced native microflora on fresh blueberries [81]
Cherry tomatoes (Solanum lycopersicum) DBD 100 kV, 150 s, air Microbial reduction by 3.5 log units [82]
Romaine lettuce (Lactuca sativa var. longifolia) DBD 42.6 kV, 1.5 A, 10 min, air Microbial reduction by 0.4–0.8 log [83]
Strawberries (Fragaria × ananassa) DBD 60 kV, 50 Hz, 5 min air Microbial reduction by 2.4–3.3 log [84]
Spinach (Spinacia oleracea) HVPP 6 kV, 0.7 kA, 1–5 shots Improved seed germination [85]
Tomato (Solanum lycopersicum) FRD 80 W, 13.56 MHz, 15 s, Microbial inactivation and improved plant growth [86]
helium
Nile tilapia (Oreochromis niloticus) DBD 60 kV, 20.52–46.17 W, Microbial reduction; improved shelf life [87]
4 min, air

a
Abbreviations: NAP, nonthermal argon plasma; DBD, dielectric barrier discharge; APP, atmospheric pressure plasma; HVPP, high-voltage pulsed plasma; RFD, radio
frequency discharge.

Given the complex, poorly understood role that RONS play in natural systems, the effect of
repeated exposure to CAP or PAW for every element of this complex system needs to be better
understood. Long-term effects of food exposure to RONS on the health of human workers and
consumers, microorganisms, plants, and animals also require further exploration.

Energy efficiency of plasma systems in controlled on-demand generation of desired reactive

species in an economically feasible manner also remains a challenge. Critical parameters such
as type of discharge, power, activation time, working gas, and position of the plasma electrode
will affect scale-up, integration, and running costs.

The scale-up of aquaponics systems to commercial production is currently limited by both high
infrastructure outlay cost and high operating cost. It is worth noting that a recent survey on the
use of aquaponics in Europe found that even the traditional aquaponics systems are at their initial
stage of development, with research (at 75%) and education (41%) being the primary uses for
often custom-made systems [76]. Replacing large biofilters used for ammonia neutralisation,
and cost and labour used for chemical management of infections and water quality with a single
automated plasma system – even a relatively expensive one – will reduce both outlay and
operating costs as well as the physical footprint and complexity of the system. The engineering
challenges of scaled-up systems may differ substantially from that for the systems already in
use for small-scale PAW production.

It is not clear whether solar or other forms of renewable energy will be able to support a larger-scale
plasma system. In addition to solar-powered plasma devices that have already been demonstrated
on a laboratory scale, biomass-derived energy may be another promising alternative due to the abun-
dance of organic waste in many agricultural systems. These types of energy sources can substantially
reduce the cost and increase environmental and economic credentials of industrial CAP, with PAW
used as a vehicle to deliver desired chemistry when solar energy may not be available.

Trends in Biotechnology, January 2023, Vol. 41, No. 1 59


The complexity of control mechanisms required to tailor the chemistry of plasma species (e.g., the
need for specific gases and gas control units) and of instruments or assays currently used to
confirm CAP and PAW chemistry will need to be addressed. The processing of data from
these assays and the identification of specific operating parameters needed for the plasma
system to produce the necessary combination of chemical and physical effects will need to be
conducted using AI.
Declaration of interests
No interests are declared.
References
1. Singh, R. et al. (2019). Human overpopulation and food security:
challenges for the agriculture sustainability. In Urban Agriculture
and Food Systems: Breakthroughs in Research and Practice
(Information Resources Management Association, Ed.),
pp. 439–467, IGI Global
2. Radwan, T.M. et al. (2019) Dramatic loss of agricultural land due
to urban expansion threatens food security in the Nile Delta,
Egypt. Remote Sens. 11, 332
3. Finke, C.E. et al. (2021) Economically advantageous pathways
for reducing greenhouse gas emissions from industrial hydrogen
under common, current economic conditions. Energy Environ.
Sci. 14, 1517–1529
4. Bazaka, K. et al. (2016) Sustainable life cycles of natural-
precursor-derived nanocarbons. Chem. Rev. 116, 163–214
5. Terlouw, T. et al. (2021) Life cycle assessment of carbon dioxide
removal technologies: a critical review. Energy Environ. Sci. 14,
1701–1721
6. Eyhorn, F. et al. (2019) Sustainability in global agriculture driven
by organic farming. Nat. Sust. 2, 253–255
7. Mondal, S. and Palit, D. (2021) Agroecology for sustainable food
system and footprint mitigation. In Agroecological Footprints
Management for Sustainable Food System (Banerjee, A. et al.,
eds), pp. 69–114, Springer
8. Asadullah, M. et al. (2020) Sustainability and development of
aquaponics system: a review. Earth Sci. Pak. (ESP) 4, 78–80
9. Dos Santos, M.J.P.L. (2016) Smart cities and urban areas –
aquaponics as innovative urban agriculture. Urban For. Urban
Green. 20, 402–406
10. Junge, R. et al. (2017) Strategic points in aquaponics. Water 9, 182
11. Goddek, S. et al. (2015) Challenges of sustainable and commercial
aquaponics. Sustainability 7, 4199–4224
12. Turnsek, M. et al. (2020) Challenges of commercial aquaponics
in Europe: beyond the hype. Water 12, 306
13. Nguyen, D.V. et al. (2019) Treatment of surface water using cold
plasma for domestic water supply. Environ. Eng. Res. 24,
412–417
14. Zeghioud, H. et al. (2020) Review on discharge plasma for water
treatment: mechanism, reactor geometries, active species and
combined processes. J. Water Proc. Eng. 38, 101664
15. Warnecke, M. et al. (2008) Review of Abattoir Water Usage
Reduction, Recycling and Reuse (A.PIA.0086). Meat & Livestock
Australia Limited, North Sydney NSW 2059, June 2008
16. UniQuest Pty Limited (2003) A Nitrogen Management Strategy
for Meat Processing Plants (PRENV.012), Meat & Livestock
Australia Ltd.
17. Das, A. et al. (2021) Livelihood security of small holder farmers in
eastern Himalayas, India: pond based integrated farming system
a sustainable approach. Curr. Res. Environ. Sust. 3, 100076
18. Evans, R.A. et al. (2005) Performance of a pilot-scale high rate
algal pond system treating abattoir wastewater in rural South
Australia: nitrification and denitrification. Water Sci. Technol. 51,
117–124
19. South Australian Research and Development Institute (2006)
Feasibility Study on using Integrated Aquaculture to Treat Waste-
water from the Meat Processing Industry (PRENV.042), Meat
and Livestock Australia Ltd.
20. Oyeniran, D.O. et al. (2021) Antibiotics, algal evaluations and
subacute effects of abattoir wastewater on liver function enzymes,
60 Trends in Biotechnology, January 2023, Vol. 41, No. 1
Trends in Biotechnology
genetic and haematologic biomarkers in the freshwater fish, Clarias
gariepinus. Ecotox. Environ. Safe. 212, 111982
21. Fane, A.G. et al. (2005) Membrane Technologies for Meat
Processing Waste Streams (PRENV.028). Meat & Livestock
Australia, North Sydney, NSW 2059, April 2005
22. Stouvenakers, G. et al. (2019) Plant pathogens and control strat-
egies in aquaponics. In Aquaponics Food Production Systems,
pp. 353–378, Springer
23. Yildiz, H.Y. et al. (2019) Insight into risks in aquatic animal health
in aquaponics. In Aquaponics Food Production Systems: Combined
Aquaculture and Hydroponic Production Technologies for the Future
(Goddek, S. et al., eds), pp. 435–452, Springer
24. Assefa, A. and Abunna, F. (2018) Maintenance of fish health in
aquaculture: review of epidemiological approaches for preven-
tion and control of infectious disease of fish. J. Vet. Med. Int.
2018, 5432497
25. Lushchak, V.I. and Lushchak, O. (2021) Interplay between reac-
tive oxygen and nitrogen species in living organisms. Chem. Biol.
Interact. 349, 109680
26. Zambon, Y. et al. (2020) Plasma activated water triggers plant
defence responses. Sci. Rep. 10, 19211
27. Adhikari, B. et al. (2019) Cold atmospheric plasma-activated
water irrigation induces defense hormone and gene expression
in tomato seedlings. Sci. Rep. 9, 16080
28. Perez, S.M. et al. (2019) Plasma activated water as resistance inducer
against bacterial leaf spot of tomato. PLoS ONE 14, e0217788
29. Brun, P. et al. (2018) Antibacterial efficacy and mechanisms of
action of low power atmospheric pressure cold plasma: membrane
permeability, biofilm penetration and antimicrobial sensitization.
J. Appl. Microbiol. 125, 398–408
30. Olatunde, O.O. et al. (2019) High voltage cold atmospheric
plasma: antibacterial properties and its effect on quality of Asian
sea bass slices. Innov. Food Sci. Emerg. Technol. 52, 305–312
31. Bourke, P. et al. (2017) Microbiological interactions with cold
plasma. J. Appl. Microbiol. 123, 308–324
32. López, M. et al. (2019) A review on non-thermal atmospheric
plasma for food preservation: mode of action, determinants of
effectiveness, and applications. Front. Microbiol. 10, 622
33. Gaur, N. et al. (2020) On cold atmospheric-pressure plasma jet
induced DNA damage in cells. J. Phys. D. Appl. Phys. 54, 035203
34. Patange, A. et al. (2019) The effect of atmospheric cold plasma
on bacterial stress responses and virulence using Listeria
monocytogenes knockout mutants. Front. Microbiol. 10, 2841
35. Arjunan, K.P. et al. (2015) Effects of atmospheric pressure
plasmas on isolated and cellular DNA – a review. Int. J. Mol.
Sci. 16, 2971–3016
36. Sohbatzadeh, F. et al. (2016) Inactivation of Aspergillus flavus
spores in a sealed package by cold plasma streamers. J. Theor.
Appl. Phys. 10, 99–106
37. Siddique, S.S. et al. (2021) Plasma-activated water inhibits
in vitro conidial germination of Colletotrichum alienum, a posthar-
vest pathogen of avocado. Plant Pathol. 70, 367–376
38. Zhou, R. et al. (2019) Microplasma bubbles: reactive vehicles
for biofilm dispersal. ACS Appl. Mater. Interfaces 11,
20660–20669
39. Guo, L. et al. (2018) Mechanism of virus inactivation by cold
atmospheric-pressure plasma and plasma-activated water.
Appl. Environ. Microbiol. 84, e00726-18
Trends in Biotechnology
40. Filipić, A. et al. (2020) Cold plasma, a new hope in the field of
virus inactivation. Trends Biotechnol. 38, 11
41. Yildiz, H.Y. et al. (2017) Fish welfare in aquaponic systems: its
relation to water quality with an emphasis on feed and faeces –
a review. Water 9, 13
42. Lennard, W. and Goddek, S. (2019) Aquaponics: the basics. In
Aquaponics Food Production Systems (Goddek, S. et al., eds),
pp. 113–143, Springer
43. Goddek, S. et al. (2019) Aquaponics and global food challenges.
In Aquaponics Food Production Systems (Goddek, S. et al.,
eds), pp. 3–17, Springer
44. Yep, B. and Zheng, Y. (2019) Aquaponic trends and challenges –
a review. J. Clean. Prod. 228, 1586–1599
45. Murugesan, P. et al. (2020) Water decontamination using non-
thermal plasma: concepts, applications, and prospects. J. Environ.
Chem. Eng. 8, 104377
46. Abuzairi, T. et al. (2018) Investigation on physicochemical prop-
erties of plasma-activated water for the application of medical
device sterilization. AIP Conf. Proc. 1933, 040017
47. Šimečková, J. et al. (2020) Influence of plasma-activated water
on physical and physical–chemical soil properties. Water 12,
2357
48. Kinandana, A.W. et al. (2018) Analysis of pH on plasma activated
medium in aqueous solution in cold atmospheric pressure
plasma jets. Int. J. Innov. Res. Adv. Eng. 5, 22–25
49. Vlad, I.-E. and Anghel, S.D. (2017) Time stability of water acti-
vated by different on-liquid atmospheric pressure plasmas.
J. Electrost. 87, 284–292
50. Tsoukou, E. et al. (2020) Temperature stability and effectiveness of
plasma-activated liquids over an 18 months period. Water 12, 3021
51. Kinandana, A.W. et al. (2018) Analysis of plasma-activated
medium (PAM) in aqueous solution by an atmospheric pressure
plasma jet (APPJ), MATEC Web of Conferences 197. EDP Sciences,
p. 02013
52. Fang, S. et al. (2020) Study on pyrolysis products characteristics
of medical waste and fractional condensation of the pyrolysis oil.
Energy 195, 116969
53. Cai, X. and Du, C. (2021) Thermal plasma treatment of medical
waste. Plasma Chem. Plasma Proc. 41, 1–46
54. Tijani, J.O. et al. (2014) A review of combined advanced oxidation
technologies for the removal of organic pollutants from water.
Water Air Soil Pollut. 225, 1–30
55. Sakudo, A. et al. (2019) Disinfection and sterilization using
plasma technology: fundamentals and future perspectives for
biological applications. Int. J. Mol. Sci. 20, 5216
56. Slamani, S. et al. (2018) Initiation of Fenton process by plasma
gliding arc discharge for the degradation of paracetamol in
water. J. Photochem. Photobiol. A Chem. 359, 1–10
57. Zahoranová, A. et al. (2016) Effect of cold atmospheric pressure
plasma on the wheat seedlings vigor and on the inactivation of
microorganisms on the seeds surface. Plasma Chem. Plasma
Proc. 36, 397–414
58. Nishime, T.M.C. et al. (2020) A coaxial dielectric barrier dis-
charge reactor for treatment of winter wheat seeds. Appl.
Sci. 10, 7133
59. Mai-Prochnow, A. et al. (2021) Interactions of plasma-activated
water with biofilms: inactivation, dispersal effects and mecha-
nisms of action. NPJ Biofilms Microbiomes 7, 1–12
60. Ohta, T. (2016) Plasma in agriculture. In Cold Plasma in Food and
Agriculture (Misra, N.N. et al., eds), pp. 205–221, Academic Press
61. Adhikari, B. et al. (2020) The effects of plasma on plant growth,
development, and sustainability. Appl. Sci. 10, 6045
62. Attri, P. et al. (2021) Impact of atmospheric pressure plasma
treated seeds on germination, morphology, gene expression
and biochemical responses. Jap. J. Appl. Phys. 60, 040502
63. Kumar, S.P.J. et al. (2021) Implications of reactive oxygen and
nitrogen species in seed physiology for sustainable crop productivity
under changing climate conditions. Curr. Plant Biol. 26, 100197
64. Thirumdas, R. et al. (2018) Plasma activated water (PAW):
chemistry, physico-chemical properties, applications in food
and agriculture. Trends Food Sci. Technol. 77, 21–31
65. Tsukagoshi, H. (2016) Control of root growth and development
by reactive oxygen species. Curr. Opin. Plant Biol. 29, 57–63
66. Choi, S. et al. (2017) Effect of corona discharge plasma on micro-
bial decontamination of dried squid shreds including physico-
chemical and sensory evaluation. LWT Food Sci. Technol. 75,
323–328
67. Ma, R. et al. (2015) Non-thermal plasma-activated water inactiva-
tion of food-borne pathogen on fresh produce. J. Hazard. Mater.
300, 643–651
68. Surowsky, B. et al. (2013) Cold plasma effects on enzyme activity
in a model food system. Innov. Food Sci. Emerg. Technol. 19,
146–152
69. Liao, X. et al. (2018) Application of atmospheric cold plasma-
activated water (PAW) ice for preservation of shrimps
(Metapenaeus ensis). Food Control 94, 307–314
70. Munekata, P.E.S. et al. (2020) Influence of plasma treatment on
the polyphenols of food products – a review. Foods 9, 929
71. Pankaj, S.K. et al. (2018) Effects of cold plasma on food quality: a
review. Foods 7, 4
72. Gavahian, M. et al. (2021) Cold plasma for mitigating agrochem-
ical and pesticide residue in food and water: similarities with
ozone and ultraviolet technologies. Food Res. Int. 141, 110138
73. Schnabel, U. et al. (2021) The effect of plasma treated water unit
processes on the food quality characteristics of fresh-cut endive.
Front. Nutr. 7, 627483
74. Ji-Lun, H. et al. (2019) Novel breeding approach for Japanese
flounder using atmosphere and room temperature plasma muta-
genesis tool. BMC Genomics 20, 323
75. Gandhirajan, R.K. et al. (2021) Zebrafish larvae as a toxicity model
in plasma medicine. Plasma Process. Polym. 18, e2000188
76. Villarroel, M. et al. (2016) Survey of aquaponics in Europe. Water
8, 468
77. Al-Abri, M. et al. (2019) Chlorination disadvantages and alterna-
tive routes for biofouling control in reverse osmosis desalination.
NPJ Clean Water 2, 1–16
78. Nam, M.-K. et al. (2017) Harmless effects of argon plasma on cau-
dal fin regeneration and embryogenesis of zebrafish: novel biological
approaches for safe medical applications of bioplasma. Exp. Mol.
Med. 49, e355
79. de Souza Silva, D.A. et al. (2019) Use of cold atmospheric
plasma to preserve the quality of white shrimp (Litopenaeus
vannamei). J. Food Protect. 82, 1217–1223
80. Varilla, C. et al. (2020) Potential of cold plasma technology in en-
suring the safety of foods and agricultural produce: a review.
Foods 9, 1435
81. Lacombe, A. et al. (2015) Atmospheric cold plasma inactivation
of aerobic microorganisms on blueberries and effects on quality
attributes. Food Microbiol. 46, 479–484
82. Ziuzina, D. et al. (2016) Demonstrating the potential of industrial
scale in-package atmospheric cold plasma for decontamination
of cherry tomatoes. Plasma Med. 6, 397–412
83. Min, S.C. et al. (2017) In-package inhibition of E. coli O157: H7
on bulk romaine lettuce using cold plasma. Food Microbiol. 65,
1–6
84. Misra, N. (2014) In-package atmospheric pressure cold plasma
treatment of strawberries. J. Food Eng. 125, 131–138
85. Ji, S.H. et al. (2018) Characterization of physical and biochemical
changes in plasma treated spinach seed during germination.
J. Phys. D Appl.Phys. 51, 145205
86. Jiang, J. et al. (2014) Effect of seed treatment by cold plasma on
the resistance of tomato to Ralstonia solanacearum (bacterial
wilt). PLoS ONE 9, e97753
87. Mohamed, E.E. et al. (2021) Impact of atmospheric cold plasma
(ACP) on maintaining bolti fish (Tilapia nilotica) freshness and
quality criteria during cold storing. J. Food Proc. Preserv. 45,
e15442
88. Baranov, O. et al. (2018) From nanometre to millimetre: a range
of capabilities for plasma-enabled surface functionalization and
nanostructuring. Mater. Horiz. 5, 765–798
89. Tamilselvi, R. et al. (2022) NiFe2O4/rGO nanocomposites pro-
duced by soft bubble assembly for energy storage and environ-
mental remediation. Renew. Energy 181, 1386–1401
90. Levchenko, I. et al. (2018) Lightning under water: diverse
reactive environments and evidence of synergistic effects
for material treatment and activation. Appl. Phys. Rev. 5,
021103
91. Adamovich, I. et al. (2017) The 2017 plasma roadmap: low tem-
perature plasma science and technology. J. Phys. D. Appl. Phys.
50, 323001
Trends in Biotechnology, January 2023, Vol. 41, No. 1 61

92. Levchenko, I. et al. (2022) Functional nanomaterials from waste and
low-value natural products: A technological approach level. Adv.
Mater. Technol. Published online June 28, 2022. https://doi.org/
10.1002/admt.202101471
93. Kumar, A. et al. (2021) Functional nanomaterials, synergism and
biomimicry for environmentally benign marine antifouling technology.
Mater. Horiz. 8, 3201–3238
62 Trends in Biotechnology, January 2023, Vol. 41, No. 1
Trends in Biotechnology
94. Piferi, C. et al. (2021) Hydrophilicity and hydrophobicity control of
plasma-treated surfaces via fractal parameters. Adv. Mater.
Interfaces 8, 2100724
95. Luo, H. et al. (2017) Mutually synergistic nanoparticles for effective
thermo-molecularly targeted therapy. Adv. Funct. Mater. 27, 1702834
96. Keidar, M. et al. (2018) Plasmas for treating cancer: opportunities for
adaptive and self-adaptive approaches. Trends Biotech 36, 586–593