Bioresource Technology 305 (2020) 123068

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Review

Diatom mediated heavy metal remediation: A review T

a b b,⁎
Thomas Kiran Marella , Abhishek Saxena , Archana Tiwari
a
International Crop Research Institute for Semi-arid Tropics (ICRISAT), Patancheru 502 324, Telangana State, India
b
Diatom Research Laboratory, Amity Institute of Biotechnology, Amity University, Noida, Uttar Pradesh 201 313, India

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

A R T I C LE I N FO A B S T R A C T

Keywords: Exposure to heavy metals is a major threat to aquatic bodies and is a global concern to our four main spheres of
Algae the earth viz. atmosphere, biosphere, hydrosphere, and lithosphere. The biosorption of pollutants using naturally
Diatoms inspired sources like microalgae has considerable advantages. Diatoms are the most dominant and diverse group
Biosorption of phytoplankton which accounts for 45% oceanic primary productivity. They perform a pioneer part in the
Heavy metal
biogeochemistry of metals in both fresh and marine water ecosystems. The diatoms play a significant role in
Phycoremediation
degradation, speciation, and detoxification of chemical wastes and hazardous metals from polluted sites. Herein,
an overview is presented about the ability of diatom algae to phycoremediate heavy metals by passive adsorption
and active assimilation from their aqueous environments with an emphasis on extracellular and intracellular
mechanisms involved in contaminant uptake through the frustules for preventing heavy metal toxicity.

1. Introduction ecosystem. Many anthropogenic actives lead to release and bioaccu-

The availability of clean water is an essential requirement for all
living organisms around the world. The emerging technological ad-
vancements and contemporaneous anthropogenic lifestyles are posing
great risks to the waterbodies (Martín et al., 2015; Ganeshkumar et al.,
2018). A myriad of emerging pollutants is generated day by day with
the recent products coming through various sources like municipal
waters, industrialization, fuel combustion, vehicles and smelting pro-
cesses (Geissen et al., 2015; Xiong et al., 2018). Human beings are the
primary consumers on this planet which puts severe pressure on aquatic
food webs. Anthropogenic activities like increased energy demand,
agriculture practices, habitat destruction, overfishing, hunting, defor-
estation and population growth is putting immense stress on our
mulation of heavy metals in aquatic ecosystems. Heavy metals can
cause severe damage to living beings due to their ability to remain
persistent, accumulate, and bio-magnify through the aquatic food chain
(Ouyang et al., 2018). Phytoplankton regulates trace metal ions in
water by intracellular and extracellular assimilation mechanisms. As
primary producer phytoplankton are one of the first responders which
get exposed and influenced by these pollutants. Among the phyto-
plankton, diatom algae are the dominant community in the aquatic
ecosystem contributing significantly to removing heavy metals from the
polluted environment and make them harmless to restore the polluted
environment to their previous condition. This is an environment-
friendly and cost-effective approach enroute for removing heavy metal
from the environment (Nhat et al., 2018).

⁎
Corresponding author.
E-mail address: panarchana@gmail.com (A. Tiwari).

https://doi.org/10.1016/j.biortech.2020.123068
Received 14 December 2019; Received in revised form 15 February 2020; Accepted 18 February 2020
Available online 20 February 2020
0960-8524/ © 2020 Elsevier Ltd. All rights reserved.
T. Kiran Marella, et al.
Discharge of heavy metals into water bodies can cause very high
toxicity in our drinking water leading to reduced growth and devel-
opment of body organs, initiate cancer, damage nervous system and
ultimately death. Depending on concentration, heavy metals can induce
both positive and negative effects on animal, plant and human life.
Heavy metal toxicity is severely affecting the health of not only humans
but the entire aquatic ecosystem. Heavy metals can alter the physio-
logical and biochemical properties of aquatic species since they de-
crease productivity due to danger caused by bioaccumulation and
biomagnifications inside the food chain (Kobielska et al., 2018). The
most common heavy metal found in an aquatic ecosystem are Cadmium
(Cd), Copper (Cu), Zinc (Zn), Lead (Pb), Chromium (Cr) and Mercury
(Hg). Cd compounds are routinely used as coloring agents in plastic
industry, anticorrosive coating for steel and electrical batteries (Mu
et al., 2018) It is also a naturally occurring metal in natural deposits and
metal ores. Cd can be easily absorbed into filter feeding fish which can
lead to bio-magnification through the food chain (Rizwan et al., 2019).
Cd can cause severe kidney damage and osteoporosis in humans
(Rebelo and Caldas, 2016). Cu due to its high water-soluble nature can
enter waterbodies through industrial and anthropogenic sources. Cu
poisoning can lead to vomiting, abdominal pains and other gastro-
intestinal complications and in extreme cases can cause organ failure
and even death. Zn can cause nausea, abdominal cramps and internal
bleeding. Pb poisoning can lead to renal damage, high blood pressure,
brain and nervous system damage (Utomo et al., 2016).
Unabated discharge of partially treated and untreated wastewater
may present a serious risk to the aquatic food chain. Heavy metals due
to their highly persistent nature are very toxic, that’s why there is an
urgent need to work on technologies which can minimize their use and
also for their efficient removal from the environment. Existing methods
of heavy metal removal from wastewater include adsorption using ac-
tivated carbon, membrane filtration, ion exchange, and chemical pre-
cipitation but these methods are energy intensive, expensive, and need
constant maintenance (Kumar et al., 2015). Algae based wastewater
remediation called phycoremediation has been recommended for the
elimination of heavy metals, pesticides, and other waste products
(Baghour, 2019; Marella et al., 2016, 2018; Tiwari and Marella, 2019).
Using diatom algae in phycoremediation is advantageous over con-
ventional methods since they are ubiquitous, can grow faster, highly
adaptive to the environment, non-toxic, ecofriendly, cost-effective,
sustainable system, reusable, recyclable, capable of remediating heavy
metal with low energy input because of autotrophy which has attracted
global attention among the scientists (Sunday et al., 2018).
The different algal classes Chlorophyceae, Phaeophyceae,
Xanthophyceae, Rhodophyceae, Bacillariophyceae and Dinophyceae
play a significant ecological role in maintaining water quality. Algae
possess huge prospective in generating diverse bioactive metabolites
and cellular mechanisms to inhabit a plethora of habitats including
various wastewaters (Marella et al., 2019). Diatoms are unicellular
eukaryotic microscopic plants prevalent in an aquatic ecosystem either
as single cells or attached to the substratum in the form of colonies,
filaments, ribbons (Fragilaria), fans (Meridion), zigzags (Tabellaria), or
stellate (Asterionella) with approximately 200 genera and more than
100,000 species. They belong to phylum heterokont, class Bacillar-
iophyceae, division Bacillariophyta, grouped into centric (Coscino-
discophyceae), pennate (Fragilariophyceae; no raphe), and pennate
(Bacillariophyceae; with raphe), golden brown with incredible high
photosynthetic activity containing various bioactive compounds and
valuable pigments (Fu et al., 2017; Kuczyńska et al., 2015). They are
highly adaptable to varying environmental conditions like temperature,
pH, light period and salinity and still can reach higher growth rates
compared to other algae groups. Their size ranges from 1 to 2000 µm
and are known to contribute up to 45% of net primary productivity
(NPP) in the ocean due to their higher growth rate and competitive
advantages over other groups of microalgae. Besides being explored for
food, feedstocks and biomolecule production, they are of immense
2
Bioresource Technology 305 (2020) 123068
importance in phycoremediation of heavy metals found in wastewater
aimed at sequestration of heavy metals and optimization of lipid bodies
build-up for biofuel generation (Yi et al., 2017). The silica cell wall
known as frustule is a hard-external layer made up of amorphous silica
decorated with pores that are nano to micro-sized in nature with di-
mensions in the range of 20–600 nm along with spines, hyaline area,
and other features. When diatom adsorbs heavy metals, they got ex-
change and complexed at their frustules which provide large contact
area facilitating in heavy metal adsorption (Lin et al., 2020).
Diatom algae are highly diverse and have extensive evolutionarily
variances in the metabolic pathways and cellular organization as
compared to other algal species. Diatoms can reach higher productivity
than other algae and are grown for aquaculture for decades
(Hildebrand, 2008). The diatoms are well adapted to use their efficient
cellular machinery in combating pollutants and in utilizing the waste-
water as growth medium (Marella et al., 2019; X.W. Wang et al., 2019).
Their 3-dimensional frustule nanoarchitecture can be exploited as a
means for the elimination of heavy metal contamination from waste-
water (Jamali et al., 2012). Diatoms use biotic and abiotic mechanisms
to counter contaminants and are well adapted to varying environmental
conditions to accumulate the environment pollutants (Congestri et al.,
2005; Guzzon et al., 2008). Hence, a cost-effective novel approach
needs to be planned which not only decontaminate the toxic com-
pounds but also as an effective sustainable strategy to recycle and reuse
heavy metals. Recently, Phycoremediation is accepting significantly
more consideration which includes the utilization of microalgae or
macroalgae for the remediation of heavy metal particles present in
water samples (Azimi et al., 2017). This review highlights the me-
chanism of intracellular and extracellular heavy metal remediation by
diatoms.
2. Physiological advantage of diatoms in comparison with other
algae
Diatoms are unique microalgae and based oncell wall they are-
classified into araphid pennates, raphid pennates, radial centrics, bi-
polar and multipolar centrics. These four major groups were originated
and diversified sequentially during the Mesozoic era under decreasing
carbon dioxide (CO2) level formulating an advanced carbon con-
centrating mechanism (Armbrust, 2009). This has resulted in an in-
crease in the number of diatoms species throughout the Eocene period
creating a cool environment globally with a significant drop in atmo-
spheric CO2 levels. The diatom evolution and its genome are unique
(Morozov et al., 2019), which perhaps gives them the unique metabolic
abilities (Datta et al., 2019). Whole-genome sequence data revealed
that diatoms are potential candidates for genetic manipulation and
metabolic engineering thus explored for the fabrication of chip-based
micro and nanodevices, water purification devices, biosensors, solar
cells, drug delivery, etc. with enhanced optical, electrical, mechanical
properties and biocompatibility (Uthappa et al., 2018). Due to their
large storage vacuole, the productive capability of diatoms is much
more than other class of microalgae (Raven and Beardall, 2016). This
favors diatoms to store huge amount of nutrients owing to their large
surface area to volume ratio (Eppley and Rogers, 1970) and enables
them to survive even when the availability of nutrients are limited
(Falkowski et al., 2004). The growth rate of diatoms is also higher
reaching up to 2 to 4 cell division day−1 (Furnas, 1990). The diatoms
are much more productive than other eukaryotes of similar size thus
making them very good for mass culturing under different mixing re-
gimes even under high turbulence and varying light intensities (Gao
et al., 2019; Vella et al., 2019; Wang and Seibert, 2017).
Due to their heavy silica cell wall, diatoms exhibit higher settling
rate which helps in faster deep-sea burial of nutrients and they are
known to be primary contributors to present day oil reserves due to
their high lipid content (Falkowski et al., 2004). Their silica cell wall
(biosilica) is a permeable 3-dimensional (3-D) structure known as
T. Kiran Marella, et al.
Table 1
Heavy metal tolerant and sensitive diatom species.
Type Diatom Species
Heavy metal tolerant Nitzschia palea
Cyclotella Meneghiniana
Aulacosera granulata
Cyclotella atomus
Gomphonema pseudoaugur
Nitzschia closterium
Navicula cryptocephala; Synedra acus; Synedra ulna;
Cyclotella bodanica; Cyclotella glomerata
Thalassiosira pseudonana
Nitzschia; Achnanthidium; Pinnularia; Cymbella
Eunotia exigua; Achnanthidium minutissium
Achnanthidium minutissimum; Fragilaria spp., Nitzschia
palea; Ulnaria ulna
Cymbellales, Naviculales, Bacillariales
Achnanthidium minutissium, Eunotia exigua,
Eunotia; Fragilaria; Navicula; Nitzschia; Pinnularia
Planothidium freuentissimum
Phaeodactylum tricornutum
Fragilaria spp., Nitzschia palea, Ulnaria ulna,
Heavy metal sensitive Gomphonema acuminatum
Cymbella austrica; Eunotia arcus; Eunotia pectinate;
Anomoensis serians; Tabelaria flocculosa
Ditylum birghtwellii
Thalassiosirales; Fragilariales
frustule which works as a potential pH buffer system enhancing car-
bonic anhydrase activity near cell surface leading to the enhanced
transformation of bicarbonate to carbon dioxide (CO2) (Milligan and
Morel, 2002). Diatom frustule biogenesis is accepting much con-
sideration in the field of nanoscience and innovation on account of their
potential future applications (Sai et al., 2019; Mishra et al., 2017). The
diatom ability to fix carbon is higher to other classes of algae examined
under both field and laboratory conditions (Bach et al., 2019;
Samantaray et al., 2019).
Photosynthetic activity of diatoms is much higher even under low
light conditions than green algae for example, marine diatom
Pheodactyulum tricornutum is efficient than Chlorella vulgaris in con-
verting light energy into biomass even under low irradiance (Wagner
et al., 2006). Thylakoid membranes of diatoms are arranged into three
groups without any differentiation affecting redox signaling (Berkaloff
et al., 1990). This differentiation in photosynthetic apparatus con-
tributes to diatoms unique metabolic potential. In diatoms, both pho-
toprotective and light harvesting pigments are synthesized from the
same precursors since they lack the α-carotene biosynthetic pathway
which is not the case with chlorophytes (Wagner et al., 2006;
Westermann and Rhiel, 2005). Calvin and Benson's cycle are light in-
dependent through the redox state of the groups and oxidative pentose
phosphate cycle is not there in the chloroplast (Michels et al., 2005).
Evidently, both C3 and C4 cycles are present in diatoms. The most
significant feature is the presence of the urea cycle (Armbrust et al.,
2004) which is not found in chlorophytes. Diatoms contain soluble
Chrysolaminarin stored in Chysolaminarin vacuole (CV) as storage form
of carbohydrate whereas other algae store starch in their chloroplast
(Beattie et al., 1961). Diatoms are not so much organized in carbohy-
drate storage yet the essential energy to use soluble carbohydrate to
insoluble carbohydrate stored in the chloroplast is quite lower
(Hildebrand et al., 2012). By virtue of these unique potentials, diatoms
can have exceedingly higher advantages in the wastewater remediation
and quenching of plethora of heavy metals which contributes to their
significance in phycoremediation (Marella et al., 2016; Jamali et al.,
2012). Further, the degradation of pollutants also depends on the level
of contamination in the environment. Diatoms are known to acclimatize
and sustain in varying environmental circumstances to accumulate the
Bioresource Technology 305 (2020) 123068
Reference
Chen et al., 2014
Morin et al., 2008a, 2008b
Li et al., 2011
Cattaneo et al., 2008
Gautam et al., 2017
Stauber and Florence, 1989
Austin and Munteanu, 1984
Rijstenbil et al., 1994
Van dam et al., 1994
Debenest et al., 2010
Gold et al., 2002; Morin et al., 2008a, 2008b; da Silva et al., 2009; Rimet and Bouchez, 2011;
Roubeix et al., 2011; Luís et al., 2011; Roubeix et al., 2012
Larras et al., 2014
Van dam et al., 1994, DeNicola, 2000
DeNicola, 2000; Morin et al., 2012; Pandey and Bergey; 2016
Arini et al., 2013
Torres et al., 1998
Gold et al., 2002; Morin et al., 2008a,b; da Silva et al., 2009; Debenest et al., 2010; Rimet and
Bouchez, 2011; Luís et al., 2011; Roubeix et al., 2011; Roubeix et al., 2012; Morin et al., 2012;
Pandey and Bergey, 2016
Pandey and Bergey, 2016
Torres et al., 1998
Rijstenbil et al., 1994
Larras et al., 2014
environment pollutants. Diatoms can contribute in river basin man-
agement by controlling the contaminants from low to moderate levels
(Jamali et al., 2012; Marella et al., 2016).
The world is confronting energy crisis and diatoms can be a great
rescue owing to their high lipid productivities even under challenging
physicochemical conditions (Gao et al., 2019). Diatoms help in asses-
sing the water quality of lakes, rivers, and oceans (Lobo et al., 2016).
They are more impervious to the harmful metals contrasted with other
microbial network and in the end decreasing harmful metal con-
centration in water assets and can serve as a substitute for treating
wastewater. Since diatoms are abundant photoautotrophs in fresh and
marine waters, they adopt different strategies for survival and growth
when exposed to high metal concentration. Their molecular mechanism
is quite unique which enables them to differentiate between essential
and non-essential heavy metals for their growth and development
(Doshi et al., 2008). Toxicity to heavy metals depends on algal strains
and their characteristics, metal concentration, and environmental
conditions. Microscopic organisms like bacteria, yeast, fungus and algae
biomass has been commonly utilized for the treatment of heavy metals
yet diatoms demonstrate high affinity towards heavy metal due to their
large surface area, mucilage, a simple nutrient requirement for their
growth and development (Hernández-Ávila et al., 2017).
Micronutrients such as copper (Cu), Nickel (Ni), Zinc (Zn) at a low
concentration exhibit a very important part in the metabolic process of
both prokaryotes and eukaryotes. Though, at high concentration these
elements seem to be very toxic and could lead to death. Cadmium (Cd),
Lead (Pb), and Mercury (Hg) being the other class of heavy metals are
also critical and toxic to living organisms and thus are unsuitable and
non-essential even at very low concentration (Gadd, 1993). Benthic
communities of estuarine and shallow systems are mostly dominated by
benthic diatom algae. Diatoms contribute to the food web as they
provide food forseveral higher trophic organisms and play a crucial role
in biogeochemical cycle thus contributing to total primary production.
Due to their short life cycles, benthic diatoms can reflect a rapid change
in the environment in a short period of time by changing their diversity
and density this makes them useful as bioindicators of water quality (J.
Wang et al., 2019; X.W. Wang et al., 2019).
Being an excellent biological indicator, benthic diatoms are
3
T. Kiran Marella, et al.
routinely used as bio-monitors of pollution. Several investigators have
reported their findings on diatoms algae as pollution tolerant species
which varies from one species to others in response to their habitat and
the types of metals they are exposed to (Lin et al., 2020). The advantage
of this change in community structure can be used to isolate and
identify species which are potential candidates for heavy metal removal
applications (Table 1).
Microalgae and bacterial aggregates can form biofilms which facil-
itates their synergetic coexistence. Interactions between benthic dia-
toms and bacteria on the surface biofilms of sediments can help to
modulate nutrient fluxes at benthic level fueling one of the productive
environments (Kouzuma and Watanabe, 2015). Biofilm response to
heavy metal exposure depends on a mixture of various physicochemical
stressors, initial diatom community composition and interspecies in-
teractions. A wide range of sensitivities among species results in dif-
ferent responses to various anthropogenic pressures. Primary response
of microalgae to heavy metal toxicity is to change their community
structure which results in production of toxicant-induced succession
(TIS) (Schmitt-Jansen et al., 2016). It is very hard to predict the impact
of a given toxicant as its effects can be modulated by multiple factors
such as the presence of nutrients or human derived pressures. Different
growth form and micro distribution of diatom species in a biofilm can
determine different responses of benthic communities to metals and
nutrients. In freshwater systems studies have been done to check the
stability of these benthic communities for pesticides and other organic
pollutants. In marine environments, most investigations have assessed
the response of benthic communities in a biofilm to antifouling bio-
cides. Few investigations assessed substance dependent pattern in
benthic community and modification of diatom species composition in
response to metals and nutrients present (Belando et al., 2017).
3. Diatom heavy metal remediation
Heavy metal bioremediation is a two-step process which involves
initial biosorption of heavy metal to different metal binding ligands on
cell surface followed by bioaccumulation which is an intracellular
process involving cellular machinery composed of inorganic molecules
and associated enzymes (Hernández-Ávila et al., 2017). Biosorption is a
faster process where a majority of the heavy metal is bound to the
surface and depending on the metal requirement for intracellular me-
tabolic activities some metal ions are transported in to the cells and
utilized for different metabolic functions. Diatom algae are one of the
most studied species in terms of the effect of different heavy metal ions,
their cellular and molecular responses to metal toxicity (Table 2). But
the volume of research work done on application of diatoms for heavy
metal removal is quite sparse compared to green and blue green algae
(Lin et al., 2020).
Biogeochemistry of trace metal acquisition and control in oceans
has been studied for several decades and many researchers demon-
strated that their concentrations are much below limits than expected in
a medium composition of seawater (Hernández-Ávila et al., 2017; Sbihi
et al., 2014). This implies that there exists a regulating mechanism for
concentration and distribution of metals in the aquatic system. Many
algal species especially diatoms have the capability to sorb the metals
which involves the metal binding to their cell surface or the in-
tracellular ligands. They help in the sequestration of large quantities of
nutrients and trace elements which includes heavy metals from water
environments (Hernández-Ávila et al., 2017). Diatoms have developed
various mechanisms like biotransformation, biomineralization, bioac-
cumulation and biosorption to counter heavy metal toxicity (Tiwari and
Marella, 2019; Baeyens et al., 2018). Diatoms can sequester trace me-
tals by use of high affinity metal binding surface functional groups doe
extracellular adsorption. Diatoms are efficient in metal acquisition and
storage. Diatoms can sequester upto 10% of their biomass in metals.
Heavy metals, such as Cd, Hg, Pb, and Se are not essential trace
metals for algae growth as they are not known to have any
4
Bioresource Technology 305 (2020) 123068
physiological function. But Cu, Co, Mn, Mo, Ni, and Zn as trace metal
and Fe as major nutrient is essential for algae growth and metabolism
(Sunda, 1989). The high concentration of essential and non-essential
heavy metals can hinder numerous physiological processes both at
cellular and molecular level. Co is a component of vitamin cobalamin
(B12) and it is incorporated into superoxide dismutase facilitating the
prevention of oxidative stress (Meier et al., 1994). Mn is an essential
part of enzyme pathways as enzymes use it for redox properties in
catalyzing oxygen development during photosynthesis (Raven et al.,
1999). Cd although toxic at high concentrations but it can be used as an
analogue to Zn, which plays a critical role in cellular metabolism (Lane
and Morel, 2000). Lead has strong affinity towards cell surface ligands
though which it can be transported intracellularly even though it is not
an essential nutrient. Heavy metal toxicity in microalgae can cause
inactivation of enzymes by replacing metals which act as cofactors with
non-essential but structurally similar metal ions. Production of reactive
oxygen species (ROS) is a primary response to heavy metal poisoning
which imbalances the electron transport activities at chloroplast
membranes. Oxidative stress due to reactive oxygen species (ROS) can
lead to membrane disintegration, lipid peroxidation and DNA damage
(Table 3) (Volland et al., 2014; Hernández-Ávila et al., 2017).
Diatoms use complex defense mechanisms which includes the pro-
duction of metal exclusion, detoxification, regulation of metal ligand
production, cell surface ligand modification and antioxidant molecules
production. Diatom T. weissflogii employs a phytochelatin export system
for the expulsion of metals from the cytoplasm. Morelli and Scarano
(2001) found that P.tricornutum can degrade metal chelated complexes
to reduce internal metal concentration. Diatom also produces anti-
oxidant compounds like poly unsaturated fatty acids (PUFA), terpenes
and pigments like fucoxanthin to control detoxification, uptake, trans-
port and accumulation of heavy metals (Fu et al., 2015). Photosynthetic
pigments like chlorophyll a, b, c is affected by heavy metal toxicity
which is countered by diatoms by increasing pigment production.
Pollution tolerant and sensitive diatoms respond differently to heavy
metal pollution. Heavy metal tolerant diatom Thalassiosira pseudonana
can produce high levels of antioxidants, phytochelatins in comparison
with pollution sensitive diatom Ditylum birghtwellii. Copper and zinc
toxicity can lead to oxidative stress, diatom cells respond by increasing
their surface area and roughness which helps in copper adsorption and
speciation. Due to strong oxidation potential, Cu stress was indicated by
gradual decrease in reduced glutathione (GSH) as well as elimination of
superoxide anions as indicated by high activity of superoxide dismutase
(SOD) (Rijstenbil et al., 1994). There can be changes in reproduction as
a defense mechanism to heavy metal stress. Diatom Ditylum bright-
well performs sexual reproduction in response to Cu stress. The early
warning signals for Cu toxicity are the release of toxins, increased level
of malondialdehyde production, pre-sexual cells and cell augmentation
(Rijstenbil and Gerringa, 2002).
3.1. Factors affecting heavy metal remediation
Several factors affect adsorption of heavy metals by diatoms such as
metal concentration, amount of biomass, temperature, pH etc. The in-
itial concentration of metals plays a significant role in heavy metal
removal. As metal concentration increases in wastewater, the adsorp-
tion increases and after some time becomes saturated. Since diatoms
have many functional groups on their cell surface, a low-affinity func-
tional groups adsorb metal at high concentration whereas a high-affi-
nity functional group adsorbs metal at low concentration. Therefore,
the removal of the heavy metal decreases with increases in concentra-
tion (Mehta and Gaur, 2005). Similarly, pH is also a function of heavy
metal adsorption from wastewater however, optimum pH to enhance
maximum metal removal by diatoms is still not fully studied. Studies
have shown that with an increase in pH, the metal adsorption by dia-
toms increases. Melosira sp. can effectively removes arsenic from the
aqueous environment due to the presence of thiol and amino groups,
T. Kiran Marella, et al. Bioresource Technology 305 (2020) 123068

Table 2
Mechanisms used by diatoms for biosorption and bioaccumulation of heavy metals.
Diatom species Removed heavy metal Mechanism involved Reference

Nitzschia pelliculosa Cd; Pb Loix et al., 2017; Hernández-Ávila et al., 2017

Planothidium lanceolatum Cd; Cu; Zn Surface ligand modification Sbihi et al., 2012; Loix et al., 2017; Jadoon and
Malik, 2017; Łukowski and Dec 2018
Coscinodiscus granii Cd; Zn Living / Non-living Loix et al., 2017; Łukowski and Dec 2018, Rabsch
and Elbrächter, 1980
Chetoceros costatum Hg Living / Non-living Volland et al., 2014;Deng et al., 2013;
60
Cyclotella meninigiana Co;54Mn;137Cs;110m Ag Adsorption, Cellular intake- potassium Adam and Garnier-Laplace, 2003
channel
Achnanthidium; Minutissimum; Thalassiosira weissflogii; Cd;Pb Adsorption (Carboxyl and silanol Loix et al., 2017; Hernández-Ávila et al.,
Skeletonema costatum; Navicula minima groups), ionic strength 2017;Gélabert et al., 2007
Nitzschia closterium Cd Adsorption (SiO2 influenced removal) Ma et al., 2018
Nitzschia closterium Cu; Zn; Co; Mn Adsorption Jadoon and Malik, 2017; Łukowski and Dec
2018;
Thalsssiosira oceanica Cd Absorption (Fe deficiency increased Cd Loix et al., 2017;Lane et al., 2008; Desai et al.,
intake) 2006
Nitzschia palea Cd Adsorption (Frustulin) Santos et al., 2013
Nitzschia palea Cd Absorption (Phytochelatin chelation) Loix et al., 2017;Figueira et al., 2014
Navicula subminiscula Adsorption (contact time and Cherifi et al., 2016
concentration of heavy metal)
Pheodactylum tricornutum Cd Adsorption (metal ligand) Loix et al., 2017;
Skeletonema costatum Cd; Cu Absorption (Vacuole storage) Loix et al., 2017; Jadoon and Malik, 2017
Thalassiosira weissflogii Cd Absorption (metallothionein transport Loix et al., 2017;
system)
P. tricornutum Cd; Pb; Cu Absorption (Phytochelatins and Loix et al., 2017; Hernández-Ávila et al., 2017;
antioxidant enzymes) Morelli and Scarano, 2001; 2004
Ditylum birghtwellii; Thalassiosira pseudonana Cd; Cu; Zn Adsorption (antioxidant activity, ROS Loix et al., 2017; Łukowski and Dec 2018;
scavenging) Rijstenbil et al., 1994

Table 3
Physiological toxicity of different heavy metals and response survival mechanism of diatom algae.
Heavy metal Physiological function affected Cellular response mechanism of diatoms to mitigate heavy metal
toxicity

Copper (Cu) Photosynthesis; impaired enzyme activity; DNA Antioxidant molecules production; pigment production; increased metal Jadoon and Malik, 2017
damage; cell membrane damage; Nutrient ligands; Cell surface ligand modification; feedback inhibition through
acquisition delayed metal adsorption; Metal exclusion; Internal sequestering
Cadmium (Cd) ROS; Photosynthesis; impaired enzyme activity; Loix et al., 2017; Desai et al.,
impaired RUBISCO; nutrient acquisition; cell wall 2006
elasticity
Zinc (Zn) Reduction in inorganic C acquisition; Enzyme Łukowski and Dec 2018
activity; carbonic anhydrase activity; CO2 sensing
and sequestration
Chromium (Cr) Oxidative stress; genotoxicity; Intracellular signaling Kumar and Bhardwaj, 2017;
Hernández-Ávila et al., 2017
Arsenic (As) Oxidative stress; genotoxicity; DNA damage Jaishankar et al., 2014
Lead (Pb) ROS; Cellular adhesion Hernández-Ávila et al., 2017;
Volland et al., 2014
Mercury (Hg) Enzyme activity; ROS; Cell damage Volland et al., 2014; Deng
et al., 2013

showing maximum adsorption capacity at an acidic pH of 4 (Zhang
et al., 2015). From previous studies, optimal pH for the removal of Cd,
Ni, Zn was slightly acidic whereas for the Cu and Pb it was more acidic
(Hernández-Ávila et al., 2017; Zhang et al., 2015; Romera et al., 2007).
Another factor that plays a key role in heavy metal removal is
biomass concentration. The living biomass due to the presence of active
surface ligands provides better possibilities in removal than dead bio-
mass. Adsorption of Cu and Ni was maximum even at the low biomass
concentration. Many studies have shown that increasing biomass con-
centration decreases Pb sorption. Similarly, decrease sorption of Cr, Co,
Ni, Cu, and Cd occur at high biomass concentration due to low avail-
ability of metal, increased electrostatic interactions, interference be-
tween binding sites and reduced mixing (Mehta and Gaur, 2005).
Temperature is also an influencing factor in heavy metal removal. With
the increase in temperature, the removal efficiency increases suggesting
that metal adsorption is an endothermic process, for example, increase
adsorption of Ni by Chlorella vulgaris at high temperature. However,
others studies on macroalgae Sargassum sp. have shown contrary
results, indicating the exothermic nature of metal adsorption suggesting
the adsorption of Cd2+ ions at ambient temperature. Thus, it can be
inferred that an increase in temperature increases heavy metal bio-
sorption due to bond rupture that increases the number of active sites or
provides higher affinities towards metal adsorption (Mehta and Gaur,
2005).
The presence of anions and cations in the medium can also affect
metal adsorption due to competition for active adsorption sites and
reduced heavy metal adsorption. The ions can form inner-sphere com-
plexes with heavy metal and reduce interactions between two ions
(John et al., 2018).
3.2. Mechanisms of extracellular biosorption
Biosorption is a physico-chemical method that accumulates heavy
metals from polluted water sites through uptake by physicochemical
pathway without ATP or it may bind metals mediated during metabo-
lism involving ATP. This mechanism can help in removing toxic metals

5
T. Kiran Marella, et al. Bioresource Technology 305 (2020) 123068

from wastewater discharged from industries and prove to be a cost-

effective solution for environmental remediation through filtering
techniques (J. Wang et al., 2019; X.W. Wang et al., 2019). An extra-
cellular metabolic passive process which doesn’t require energy where
the adsorption of heavy metal occurs at the cell surface and is de-
termined by equilibrium. The factors affecting the efficacy of this
method are pH, temperature, contact time, ionic strength, biomass
concentration, metal concentration, cell wall composition of desired
species and complexation with metallic ions (Ding et al., 2017). The
main advantage of this method is its low operating cost, least ratio of
sludge volume and high competence in detoxifying very less amount of
heavy metal, even in situ remediation. Microalgae cell wall is loaded
with polymers quite similar to cellulose, pectins, hemicelluloses, ara-
binogalactan proteins, extension, and lignins. The outer cell wall layer
possess many functional groups such as carboxyl, phosphoryl, and
amine thus gives a negative charge to them. Heavy metal with positive
charge attracted towards them through electrostatic interaction subse-
quently results in an effective biosorption (Hedayatkhah et al., 2018;
Ding et al., 2017; J. Wang et al., 2019; X.W. Wang et al., 2019).
Heavy metal biosorption is an emerging field with advantages like
high efficacy of removal and availability of inexpensive biosorbents.
Diatom algae especially benthic diatoms have a symbiotic relationship
with bacteria forming diatom bacterial biofilms, during the process
many diatoms produce extracellular polysaccharides (EPS) which fa-
cilitates in metal ion adhesion to cell wall (Amin et al., 2012;Koedooder
et al., 2018). Silica frustule of diatoms is formed by crystalline alu-
minum silicates of tetrahedral structure sharing oxygen atoms. Gen-
erally, complexation with heavy metals cations occurs in two ways (i)
inner sphere complexation, the interacting ligand close to the central
metal cation and (ii) outer-sphere complexation, the ions of opposite
charges attracted and approached to each other within a critical dis-
tance forming ion pair. However, in the case of microalgae, extra-
cellular complexation occurs between metal ion chelating agent and
polymer excreted by algae. The chelating agent contains electron pair
attracted electrostatically when clung to metal ion without any electron
transfer. Thus, the final structure has an electric charge which is the
sum of participant’s charges. There is the formation of coordination
bonds between metals and amino and the carboxyl group of the mi-
croalgal cell wall. The production of acids such as citric, oxalic, glu-
conic, fumaric, lactic and malic acids chelate toxic metals resulting in
the formation of metallo-organic molecules, this helps in solubilization
and leaching of metal compounds from their surface (Köhler et al.,
2017; Kumar et al., 2015).
In diatoms, functional groups like amino (–NH2), carboxyl
(–COOH), silanol (SI–O–H), phytochelatins, carboxyl, aldehyde, ketone,
ester are present in three-dimensional micro-nano-porous structure
which can be used to control surface charge properties, metal ion af-
finities and metal detoxification (Lane and Morel, 2000) (Fig. 1). For
example, diatoms when complexed with zinc, the thermodynamic
model indicating the divalent metal ion sorption onto the diatom sur-
face by –COOH located in the extracellular polysaccharide layer of the
cell wall. Binding of zinc is governed by various parameters such as pH,
zinc and biomass concentration in solution, ionic strength, and tem-
perature (Gélabert et al., 2007). Cd, an analog of Zn also plays an im-
portant role in carrying out the metabolic activity of planktonic cells
(Lane and Morel, 2000). Although, Cd at high concentration is toxic to
cells, but becomes an essential nutrient in case of Zn deficiency by re-
placing Zn in some enzymes. Pb does not demonstrate any metabolic
requirement by the cells however, it becomes much stronger than both
Cd and Zn while binding with ligands and on the solid surface.
Therefore, Zn, Cd, Pb adsorb by phytoplanktons community which
considered as first step towards metal uptake by the diatom algae. In-
deed, a more systematic and thorough investigation is required to va-
lidate the complexion of Cd and Pb with the diatom surface (Gélabert
et al., 2007).
In diatom Thalassiosira weissflogii phytochelatins biosynthesis is
Fig. 1. Organic and inorganic cell surface molecules facilitating adsorption of
heavy metal.
induced by presence of heavy metals like Cd2+, Pb2+, Ni2+, Zn2+,
Co2+, Ag+ and Hg2+ (Ahner and Morel, 1995). Phytochelatin pro-
duction in diatoms helps in metal detoxification at the cell wall and it
also helps in combating oxidative stress. Working with Phaeodactylum
tricornutum, Morelli and Scarano (2004) found that oxidized form of
phytochelatin is present in response to Cu stress and they hypothesized
that oxidized phytochelatins can help in ROS scavenging as well as play
a role in essential trace metal homeostasis (Luo et al., 2014).
3.3. Mechanisms of intracellular bioaccumulation
An intracellular active metabolic process where organisms take up
heavy metals at a faster rate which is driven by energy. In this process,
heavy metal pollutants accumulated along with growing nutrients
which ultimately remove pollution from the wastewater. Upon accu-
mulation of heavy metals, the microalgae produce reactive oxygen
species (ROS) acting as signaling molecules in order to control cellular
metabolism. Thus, forecasting programmed cell death, stomatal beha-
vior, and defense against pathogens. However, a high level of ROS may
damage cellular components such as lipids, proteins, and DNA, and an
increased rate of mutagenesis due to its high oxidative properties
(Kumar et al., 2015).
Aggregation of heavy metal by algae comprises of passive- an un-
derlying quick uptake followed by active- a moderate uptake me-
chanism. During the passive mechanism metal particles are first ad-
sorbed on the cell surface by various surface molecules (Perales-Vela
et al., 2006). In the active mechanism, the absorption of heavy metals
into the cell wall was brought about bya series of mechanisms which
includes: (1) Detoxification of heavy metals ions at the cell wall layer
through complexation both by extracellular polysaccharides and phy-
tochelatins (2) Energy driven efflux pumps at the cell wall regulate the
inflow of heavy metals into the cell by regulating their influx through
concentration dependent mechanism were extracellular metal ion
concentration influences the intracellular intake. (3) Intracellular metal
ions are further modified by changing their oxidation state by enzy-
matic action. Vaporization of heavy metals into volatile compounds
helps in their excretion from cells. Methylation of metals reduces the
risk of metal ion exposure to sensitive reaction sites intracellularly. (4)
Metal ions were transported intracellularly metal locations by metal

6
T. Kiran Marella, et al.
Fig. 2. Mechanism of intracellular heavy metal transport and assimilation.
binding ligands especially polyphosphates and polychelatins which
further deactivate metal toxicity. (5) Metal and ligand complex binds to
the cellular and organelle membranes. (6) Detoxified heavy metals are
transported into membranes. (7) Heavy metals are utilized by cellular
organelles for different metabolic activities (Fig. 2). Diatoms regulate
their enzymatic activity which enables them to detoxify of heavy metals
by dehalogenation and denitrification (Xiong et al., 2018; Kumar et al.,
2015).
In response to heavy metal exposure diatoms trigger a metal ex-
clusion mechanism to maintain equilibrium with environmental metal
concentration. Heavy metal tolerant diatoms can produce phytochela-
tins, macromolecules and exocellular polysaccharides as a barrier to
extracellular adsorption to reduce toxicity effects (Maršálek and
Rojíčková, 1996).
In diatoms, phytochelatins and metallothioneins which form metal
chelated complexes facilitate in accumulation and storage of heavy
metals in storage vacuoles and also in the cytoplasm as insoluble salts
(Perrein-Ettajani et al., 1999). Certain heavy metals like cadmium (Cd)
are transported intracellularly through manganese (Mn) and zinc (Zn)
uptake system (Sunda and Huntsman, 2000). Heavy metal chelated
complex transport and storage mechanism was observed in Skeletonema
costatum in response to cadmium (Cd) and copper (Cu) stress with in-
creased storage in the vacuole. In Skeletonema costatum, when Cd and
Cu as pollutants are introduced then detoxification was observed and it
was concluded that sequestration capacity of Cu was less than Cd in the
vacuole as confirmed in Electron energy loss spectroscopy (EELS)
(Nassiri et al., 1997).
4. Technological advantages
There are several techniques for the remediation of wastewater such
as physical methods, chemical methods, biological methods, and col-
lective methods. The physical methods involves the use of activated
carbon, graphene oxide, filtration and flocculation for the adsorption of
heavy metal contaminants whereas chemical methods implies ozona-
tion, oxidation–reduction reactions, ionizing radiations, and UV treat-
ments but these methods entails expensive equipment, toxic chemicals,
skilled manpower, time-consuming and not so cost-effective which to
some degree may remove heavy metals from wastewater but not a
sustainable solution for long term goal, hence to maintain and support
our aquatic ecosystem from pollution a prolonged technological con-
cept is high on demand which not only remediates the water from
7
Bioresource Technology 305 (2020) 123068
heavy metals but also nature-friendly. Algal based remediation is the
biological approach which degrades the contaminants from the waste-
water and smartly tackles our problem judiciously. Diatom algal
mediated technology is quite promising in biodegradation and photo-
degradation of heavy metal contamination from the wastewater thus it
is the only possible way for the phycoremediation of heavy metals from
the wastewater (Ghosh et al., 2016; Tokumura et al., 2016; Yan et al.,
2018).
Heavy metal contaminants that persist in the water bodies are toxic
to our environment and threaten living organisms even at low con-
centrations. Upon accumulation in the human body, they may infect
tissue, damage the reproduction system, inhibit cell proliferation, etc.
Existing conventional wastewater treatment does not efficiently remove
them so the upcoming accepted technology is diatom-based degrada-
tion of heavy metal pollutants via adsorption or integration into cells.
Diatoms contain chemical moieties such as hydroxyl, carboxyl, phos-
phate, and amide, which act as metal-binding sites (Tolbooma et al.,
2019; Bilal et al., 2019; Rasheed et al., 2019). Open pond bioreactors
with low aeration is utilized in agriculture and industrial wastewater
treatment. Their main advantage is low operating and investment cost
and easy handling however it is associated with disadvantages also such
as low efficacy due to contamination, high feed and high land footprint
(Meneses-Jácome et al., 2016; Cuellar-Bermudez et al., 2017). An im-
proved version of open pond bioreactor is raceway ponds i.e. high-rate
algal ponds (HRAP) for wastewater treatment where a symbiotic re-
lationship exists between diatoms and bacteria. Here, photosynthesis is
carried out by the release of oxygen by diatoms which is consumed by
bacteria to degrade heavy metal pollution without aeration (Matamoros
et al., 2015; Matamoros et al., 2016; Garcia-Rodríguez et al., 2015;
Sawant et al., 2018). Bubble column photobioreactors are closed sys-
tems designed in a vertical, horizontal and helical shape consists of
transparent tubes to allow access of natural or artificial light (Nwoba
et al., 2019). This system is advantageous over open pond bioreactor
due to better control of pH, temperature, higher volumetric efficiency,
better use of the cultivation area, better capture of radiant energy and
less loss of water. This is a very promising concept but the running cost
is very high (Gouveia et al., 2016; Zhu et al., 2014; Christenson and
Sims, 2011).
The algae biofilm-based remediation technologyis also known as
algal turf scrubber (Huang et al., 2013). This technology is en-
vironmentally friendly which uses microalgae consortium which in-
cludes green, blue green and diatom algae to assimilate nutrients and
T. Kiran Marella, et al.
heavy metals from wastewater. Nowadays, this technology is pre-
dominantly used to concentrate heavy metals into biomass (Adey et al.,
2011). In this technology, water pumped from the river, as water pulses
down the flow way, it stimulates attached algae growth as biofilm on
solid support, creating controlled algae biofilms. Due to growth of algae
as biofilm instead of suspended cultures cost of harvesting biomass can
be reduced drastically. The harvested biomass of microalgae can be
recycled through anaerobic digestion system for the renewable synth-
esis of biofuels such as biodiesel thus utilizing the energy of algae
biomass for bioenergy generation (Huang et al., 2013). However, still,
there is a lot of gap in knowledge regarding the treatment of wastewater
using diatoms. One such gap is the test of more species to remove
contaminants since no single species is found that can tolerate all heavy
metals. Finally, there is a need to test this process in full-scale bior-
eactors such as open ponds since various physical–chemical conditions
like as temperature, seasons, pH of the medium, dissolved oxygen, light
periods, consortia, etc., play a vital role in the biological degradation of
heavy metal which is hard to establish or control thus its challenging
but not impossible.
5. Commercial production of diatoms and their applications
The production and harvesting of diatoms are commercially viable
approaches since they absorb CO2 and remove excess nutrients from the
wastewater at the same time produce beneficial bioproducts. Diatoms
contain lipid bodies such as membrane-bound polar lipids, triglycer-
ides, and free fatty acids besides sterols, waxes, and acyl lipids (Wang
and Seibert, 2017). Diatoms have a high lipid fraction of 40–60% thus is
a foremost contender for biofuel production. The most dominant factor
in diatoms production is its silicate cell wall thus they exhibit higher
growth rate compared with other algae groups (Gao et al., 2019). China
and United States have started the production of diatoms as a future
goal to achieve self-sufficiency in sustainable liquid biofuel production
because the waste material left behind can be recycled and converted
into biocrude via thermal processing, remaining nutrients contain rich
protein and used as animal feed whereas frustules with nano-size hole
can be used to remove heavy metal from wastewater (Wang and
Seibert, 2017). Diatoms contain a high proportion of ecosapentaenoic
acid (EPA) as polyunsaturated fatty acid (PUFA) which plays a key role
in antimicrobial defense mechanism (Peltomaa et al., 2019). Jawkai
bioengineering R&D Center, China has achieved up to 120 MT of dry
weight per hectare per year diatom yields. In China, 99.9% of Cu found
in wastewater removed through filtration process using diatom frus-
tules (Wang 2015; Wang and Seibert, 2017). In recent times, NASA
investigated an exclusive floating algae-cultivation system which is
successful in increasing microalgae growth and treat wastewater on a
small scale however is yet to be ascertained (Wang and Seibert, 2017).
Diatoms are a prominent tool for targeted drug delivery in cancer
treatment to deliver the drug in a controlled and sustained manner
without any harm to normal cells with reduced side effects caused by
chemotherapy to the patient (Kabir et al., 2020). The scientist has re-
placed expensive synthetic silica with diatom frustules as a drug de-
livery carrier system. Professor Nico Voelcker, an expert in bio-nano
science successfully loaded diatoms with chemotherapeutic drugs and
injected to cancerous mice and obtained positive results (Tieu et al.,
2019; Delalat et al., 2015). Diatoms can manufacture frustules of var-
ious shapes and sizes thus have the ability to fabricate micro- or nano-
scale devices such as optical systems and semiconductor nanolitho-
graphy. Diatoms have been cultivated for intracellular metabolites like
eicosapentaenoic acid (EPA), essential lipids, and amino acids for
pharmaceutical and cosmetic purposes. Chaetoceros and Thalassiosir-
a species are used as larval feed (Spolaore et al., 2006), Thalassiosira
pseudonana and Skeletonema costatum as feed for bivalve molluscs
(Hemaiswarya et al., 2011; Hildebrand et al., 2012). P. tricornutu-
m and Nitzschia laevis have been cultivated for EPA production (Lebeau
and Robert, 2003). Diatomaceous earth (DE) or diatomite industrially
8
Bioresource Technology 305 (2020) 123068
utilized in polishing, liquid filtration and as a source of nanomaterial
because of their complex microscopic shells (Mishra et al., 2017). In
forensic science, diatoms help to distinguish death by submersion from
a post-morterm immersion of a body in the water because their silica
does not decay and found in the body which helps in identification and
may be good evidence of sinking as the reason of death (Zhou et al.,
2019). With the alarming population, the demand for diatoms as po-
tential environment-friendly raw material is witnessing a great rise in
various sectors be it healthcare, engineering, cosmetics, during the
forecast period. Geographically, global diatom market is segmented
into five regions which include North America, Europe, Asia Pacific,
Middle East & Africa, and Latin America wherein North America is
leading the current market share whereas Asia Pacific region is ex-
pected to be the fastest-growing regional market and is likely to grow
exponentially.
Diatoms are the renewable source of bioenergy and biofuel pro-
duction. Being natural enigma, they need to explore much more to
maximize their potential future benefits. Their mystery is yet to be
unfolded. A plethora of questions are yet to be answered such as their
phenotype, genotype, how to manipulate them without breaking their
silica cell wall and their genetic engineering. Researchers are working
day and night to find novel diatoms species to decode their frustule
structure (Levitan et al., 2014). Diatoms can be used in various appli-
cations in the field of nano-biotechnology, pharmaceutical, and en-
vironmental science (Jamali et al., 2012). Mass cultivation of diatoms
could be a prominent source of therapeutics and commercial applica-
tions. Nowadays diatoms research is getting worldwide attention be-
cause of their natural availability. In the coming future, diatomist and
nanotechnologist will find a way for more promising and challenging
applications as the research on diatoms light up (Mishra et al., 2017;
Jamali et al., 2012).
According to recent studies, living species demonstrates the high
capability of bioaccumulation and bio-adsorption of heavy metal than
the dead species because of enzymatic intracellular and extracellular
exercises. Microalgae can develop productively in wastewater by ex-
pelling essential nutrients, heavy metals, and micropollutants (Miranda
et al., 2017). Diatoms biofilms are multilayered and multi-aspects
structures which include consortia of heterotrophic and photo-
autotrophic eukaryotic organisms. Since diatoms contain many pig-
ments, they catch daylight and shields cells from harmful radiation.
This enables various species to colonize various zones inside the biofilm
structure that are most appropriate for the development of diatoms
known as consortia, a heterotrophic complex structure for the steady
production of a biological system by the extracellular polymeric sub-
stance (EPS) intended to preserve water, nutrients, acts as a barrier
against toxicity, mortality, protection against grazers, harmful chemi-
cals, and facilitates heavy metal removal (Schenk et al., 2008). Besides,
metal also bio-sorbed or complexed by carboxyl group found in the
microalgal organic layer and another organic polymer. In this way,
heavy metals can be removed by algal biomass as cation exchange
column. Wastewater remediation is the most noteworthy utilization of
algal biofilms providing simple, energy efficient technology for the
absorption of nutrients, nitrogen and phosphorous followed by easy and
robust separation of algal biomass from the bulk of wastewater. In fu-
ture, diatoms biofilm will serve as the next generation bioenergy
feedstocks which can grow robustly in wastewater, tailored designed
for the treatment of wastewater and heavy metal removal besides
generating more lipids bodies as a feedstock for biodiesel production
(Rajkumar et al., 2013).
6. Conclusion
The extent of heavy metal pollution has percolated to various en-
vironments and it is continuously worsening due to human interven-
tions which are leading to intense interest in research activities con-
cerning to identification of mechanisms and processes to deal with its
T. Kiran Marella, et al.
harmful effects. Diatoms are studied as indicator species for heavy
metal pollution in wastewater but still, they are under utilized because
of tricky isolation, culturing and mass cultivation. Several researchers
have proven their efficiency in phycoremediation however a sustain-
able economic eco-friendly technology is still to be perfected. Diatoms
are the best natural driven material for adsorption of heavy metal with
high commercial potential. Their ability to tolerate pollution and
bioaccumulate heavy metals needs further research thus makes them
potential candidates for heavy metal phycoremediation.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
Authors wish to thank Dr. Sreenath Dixit, Director, IDC, ICRISAT for
encouragement and support. We are thankful to Department of
Biotechnology, Ministry of Science and Technology for research
funding (BT/PR15650/AAQ/3/815/2016).
References
Adam, C., Garnier-Laplace, J., 2003. Bioaccumulation of silver-110m, cobalt-60, cesium-
137, and manganese-54 by the freshwater algae Scenedesmus obliquus and Cyclotella
meneghiana and by suspended matter collected during a summer bloom event.
Limnol. Oceanogr. 48, 2303–2313.
Adey, W.H., Kangas, P.C., Mulbry, W., 2011. Algal turf scrubbing: cleaning surface waters
with solar energy while producing a biofuel. Bioscience 61, 434–441.
Ahner, B.A., Morel, F.M., 1995. Phytochelatin production in marine algae. Induction by
various metals. Limnol. Oceanogr. 40, 658–665.
Amin, S.A., Parker, M.S., Armbrust, E.V., 2012. Interactions between diatoms and bac-
teria. Microbiol. Mol. Biol. Rev. 76, 667–684.
Arini, A., Durant, F., Coste, M., Delmas, F., Feurtet-Mazel, A., 2013. Cd decontamination
and reversal potential of teratological forms of the diatom Planothidium freuentis-
simum after experimental condition. J. Phycol. 49, 361–370.
Armbrust, E.V., 2009. The life of diatoms in the world's oceans. Nature 459, 185.
Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou,
S., Allen, A.E., Apt, K.E., Bechner, M., 2004. The genome of the diatom Thalassiosira
pseudonana: ecology, evolution, and metabolism. Science 306, 79–86.
Austin, A., Munteanu, N., 1984. Evaluation of changes in a large oligotrophic wilderness
park lake exposed to mine tailing effluent for 14 years: the phytoplankton. Environ.
Pollut. A. 33, 39–62.
Azimi, A., Azari, A., Rezakazemi, M., Ansarpour, M., 2017. Removal of heavy metals from
industrial wastewaters: a review. Chem. Biol. Eng. Rev. 4, 37–59.
Bach, L.T., Hernández-Hernández, N., Taucher, J., Spisla, C., Sforna, C., Riebesell, U.,
Arístegui, J., 2019. Effects of elevated CO2 on a natural diatom community in the
subtropical NE Atlantic. Front. Mar. Sci. 6, 75.
Baeyens, W., Gao, Y., Davison, W., Galceran, J., Leermakers, M., Puy, J., Superville, P.-J.,
Beguery, L., 2018. In situ measurements of micronutrient dynamics in open seawater
show that complex dissociation rates may limit diatom growth. Sci. Rep. 8, 16125.
Baghour, M., 2019. Algal degradation of organic pollutants. In: Martínez, L., Kharissova,
O., Kharisov, B. (Eds.), Handbook of Ecomaterials. Springer, Cham, pp. 1–22.
Beattie, A., Hirst, E., Percival, E., 1961. Studies on the metabolism of the Chrysophyceae.
Comparative structural investigations on leucosin (chrysolaminarin) separated from
diatoms and laminarin from the brown algae. Biochem. J. 79, 531.
Belando, M., Marín, A., Aboal, M., García-Fernández, A., Marín-Guirao, L., 2017.
Combined in situ effects of metals and nutrients on marine biofilms: shifts in the
diatom assemblage structure and biological traits. Sci. Total Environ. 574, 381–389.
Berkaloff, C., Caron, L., Rousseau, B., 1990. Subunit organization of PSI particles from
brown algae and diatoms: polypeptide and pigment analysis. Photosynth. Res. 23,
181–193.
Bilal, M., Adeel, M., Rasheed, T., Zhao, Y., Iqbal, H.M., 2019. Emerging contaminants of
high concern and their enzyme-assisted biodegradation–a review. Environ. Int. 124,
336–353.
Cattaneo, A., Couillard, Y., Wunsam, S., 2008. Sedimentary diatoms along a temporal and
spatial gradient of metal contamination. J. Paleolimnol. 40, 115–127.
Chen, X., Li, C., McGowan, S., Yang, X., 2014. Diatom response to heavy metal pollution
and nutrient enrichment in an urban lake: evidence from paleolimnology. Ann.
Limnol.-Int. J. Lim. 50, 121–130.
Cherifi, O., Sbihi, K., Bertrand, M., Cherifi, K., 2016. The removal of metals (Cd, Cu and
Zn) from the Tensift river using the diatom Navicula subminuscula Manguin: A la-
boratory study. Int. J. Adv. Res. Biol. Sci. 3, 177–187.
Christenson, L., Sims, R., 2011. Production and harvesting of microalgae for wastewater
treatment, biofuels, and bioproducts. Biotechnol. Adv. 29, 686–702.
Congestri, R., Cox, E.J., Cavacini, P., Albertano, P., 2005. Diatoms (Bacillariophyta) in
9
Bioresource Technology 305 (2020) 123068
phototrophic biofilms colonising an Italian wastewater treatment plant. Diatom Res.
20, 241–255.
Cuellar-Bermudez, S.P., Aleman-Nava, G.S., Chandra, R., Garcia-Perez, J.S., Contreras-
Angulo, J.R., Markou, G., Muylaert, K., Rittmann, B.E., Parra-Saldivar, R., 2017.
Nutrients utilization and contaminants removal. A review of two approaches of algae
and cyanobacteria in wastewater. Algal Res. 24, 438–449.
da Silva, E.F., Almeida, S.F.P., Nunes, M.L., Luís, A.T., Borg, F., Hedlund, M., de Sa, C.M.,
Patinha, C., Teixeira, P., 2009. Heavy metal pollution downstream the abandoned
Coval da M_o mine (Portugal) and associated effects on epilithic diatom communities.
Sci. Total Environ. 407, 5620–5636.
Datta, A., Marella, T.K., Tiwari, A., Wani, S.P., 2019. The diatoms: from eutrophic in-
dicators to mitigators. In: Gupta, S., Bux, F. (Eds.), Application of Microalgae in
Wastewater Treatment. Springer, Cham, pp. 19–40.
Debenest, T., Silvestre, J., Coste, M., Pinelli, E., 2010. Effects of pesticides on freshwater
diatoms. Rev. Environ. Contam. Toxicol. 203, 87–103.
Delalat, B., Sheppard, V.C., Ghaemi, S.R., Rao, S., Prestidge, C.A., McPhee, G., Rogers, M.,
Donoghue, J.F., Pillay, V., Johns, T.G., Kroger, N., Voelcker, N.H., 2015. Targeted
drug delivery using genetically engineered diatom biosilica. Nat. Commun. 6, 8791.
Deng, G.F., Zhang, T.W., Yang, L.M., Wang, Q.Q., 2013. Studies of biouptake and
transformation of mercury by a typical unicellular diatom Phaeodactylum tricornutum.
Chin. Sci. Bull. 58, 256–265.
DeNicola, D.M., 2000. A review of diatoms found in highly acidic environments.
Hydrobiologia 433, 111–122.
Desai, S.R., Verlecar, X.N., Nagarajappa, Goswami, U., 2006. Genotoxicity of cadmium in
marine diatom Chaetoceros tenuissimus using the alkaline Comet assay.
Ecotoxicology 15, 359–363.
Ding, T., Yang, M., Zhang, J., Yang, B., Lin, K., Li, J., Gan, J., 2017. Toxicity, degradation
and metabolic fate of ibuprofen on freshwater diatom Navicula sp.. J. Hazard. Mater.
330, 127–134.
Doshi, H., Seth, C., Ray, A., Kothari, I., 2008. Bioaccumulation of heavy metals by green
algae. Curr. Microbiol. 56, 246–255.
Eppley, R.W., Rogers, J.N., 1970. Inorganic nitrogen assimilation of Ditylum brightwellii, a
marine plankton diatom. J. Phycol. 6, 344–351.
Falkowski, P.G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O., Taylor, F.J.,
2004. The evolution of modern eukaryotic phytoplankton. Sci. 305, 354–360.
Figueira, E., Freitas, R., Guasch, H., Almeida, S.F., 2014. Efficiency of cadmium chelation
by phytochelatins in Nitzschia palea (Kützing) W. Smith. Ecotoxicology 23, 285–292.
Fu, W., Nelson, D., Yi, Z., Xu, M., Khraiwesh, B., Jijakli, K., Chaiboonchoe, A., Alzahmi,
A., Al-Khairy, D., Brynjolfsson, S., Salehi-Ashtiani, K., 2017. Bioactive compounds
from microalgae: current development and prospects. Studies in Natural Products
Chemistry. 54. Elsevier, pp. 199–225.
Fu, W., Wichuk, K., Brynjólfsson, S., 2015. Developing diatoms for value-added products:
challenges and opportunities. New Biotechnol. 32, 547–551.
Furnas, M.J., 1990. In situ growth rates of marine phytoplankton: approaches to mea-
surement, community and species growth rates. J. Plankton Res. 12, 1117–1151.
Gadd, G., 1993. Microbial formation and transformation of organometallic and organo-
metalloid compounds. FEMS Microbiol. Rev. 11, 297–316.
Ganeshkumar, V., Subashchandrabose, S.R., Dharmarajan, R., Venkateswarlu, K., Naidu,
R., Megharaj, M., 2018. Use of mixed wastewaters from piggery and winery for nu-
trient removal and lipid production by Chlorella sp. MM3. Bioresour. Technol. 256,
254–258.
Gao, G., Wu, M., Fu, Q., Li, X., Xu, J., 2019. A two-stage model with nitrogen and silicon
limitation enhances lipid productivity and biodiesel features of the marine bloom-
forming diatomSkeletonemacostatum. Bioresour. Technol. 289, 121717.
Garcia-Rodríguez, A., Matamoros, V., Fontàs, C., Salvado, V., 2015. The influence of
Lemna sp. and Spirogyra sp. on the removal of pharmaceuticals and endocrine dis-
ruptors in treated wastewaters. Int. J. Environ. Sci. Technol. 12, 2327–2338.
Gautam, S., Pandey, L.K., Vinayak, V., Arya, A., 2017. Morphological and physiological
alterations in the diatom Gomphonema pseudoaugur due to heavy metal stress. Ecol.
Indic. 72, 67–76.
Geissen, V., Mol, H., Klumpp, E., Umlauf, G., Nadal, M., van der Ploeg, M., van de Zee,
S.E., Ritsema, C.J., 2015. Emerging pollutants in the environment: a challenge for
water resource management. Int. Soil Water Conserv. Res. 3, 57–65.
Gélabert, A., Pokrovsky, O., Schott, J., Boudou, A., Feurtet-Mazel, A., 2007. Cadmium and
lead interaction with diatom surfaces: a combined thermodynamic and kinetic ap-
proach. Geochim. Cosmochim. Acta 71, 3698–3716 .
Ghosh, A., Khanra, S., Mondal, M., Halder, G., Tiwari, O.N., Saini, S., Bhowmick, T.K.,
Gayen, K., 2016. Progress toward isolation of strains and genetically engineered
strains of microalgae for production of biofuel and other value added chemicals: a
review. Energy Convers. Manag. 113, 104–118.
Gold, C., Feurtet-Mazel, A., Coste, M., Boudou, A., 2002. Field transfer of periphytic
diatom communities to assess short-term structural effects of metals (Cd, Zn) in
rivers. Water Res. 36, 3654–3664.
Gouveia, L., Graça, S., Sousa, C., Ambrosano, L., Ribeiro, B., Botrel, E.P., Neto, P.C.,
Ferreira, A.F., Silva, C.M., 2016. Microalgae biomass production using wastewater:
treatment and costs. Scale-up considerations. Algal Res. 16, 167–176.
Guzzon, A., Bohn, A., Diociaiuti, M., Albertano, P., 2008. Cultured phototrophic biofilms
for phosphorus removal in wastewater treatment. Water Res. 42, 4357–4367.
Hedayatkhah, A., Cretoiu, M.S., Emtiazi, G., Stal, L.J., Bolhuis, H., 2018. Bioremediation
of chromium contaminated water by diatoms with concomitant lipid accumulation
for biofuel production. J. Environ. Manage. 227, 313–320.
Hemaiswarya, S., Raja, R., Ravi Kumar, R., Ganesan, V., Anbazhagan, C., 2011.
Microalgae: a sustainable feed source for aquaculture. World J. Microb. Biot. 27,
1737–1746.
Hernández-Ávila, J., Salinas-Rodríguez, E., Cerecedo-Sáenz, E., Reyes-Valderrama, I.,
Arenas-Flores, A., Román-Gutiérrez, A.D., Rodríguez-Lugo, V., 2017. Diatoms and
T. Kiran Marella, et al.
their capability for heavy metal removal by cationic exchange. Metals 7, 169.
Hildebrand, M., 2008. Diatoms, biomineralization processes, and genomics. Chem. Rev.
108, 4855–4874.
Hildebrand, M., Davis, A.K., Smith, S.R., Traller, J.C., Abbriano, R., 2012. The place of
diatoms in the biofuels industry. Biofuels 3, 221–240.
Huang, Z., Jones, J., Gu, J., Hallerman, E., Lane, T., Song, X., Wan, R., 2013. Performance
of a recirculating aquaculture system utilizing an algal turf scrubber for scaled-up
captive rearing of freshwater mussels (Bivalvia: Unionidae). N. Am. J. Aquacult. 75,
543–547.
Jadoon, S., Malik, A., 2017. DNA damage by heavy metals in animals and human beings:
an overview. Biochem. Pharmacol. 6, 235.
Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B., Beeregowda, K.N., 2014.
Toxicity, mechanism and health effects of some heavy metals. Interdiscip.Toxicol. 7,
60–72.
Jamali, A.A., Akbari, F., Ghorakhlu, M.M., de la Guardia, M., Khosroushahi, A.Y., 2012.
Applications of diatoms as potential microalgae in nanobiotechnology. Bioimpacts 2,
83–89.
John, Y., David, V.E., Mmereki, D., 2018. A comparative study on removal of hazardous
anions from water by adsorption: a review. Int. J. Chem. Eng. 2018, 21.
Kabir, A., Nazeer, N., Bissessur, R., Ahmed, M., 2020. Diatoms embedded, self-assembled
carriers for dual delivery of chemotherapeutics in cancer cell lines. Int. J. Pharm. 573,
118887.
Kobielska, P.A., Howarth, A.J., Farha, O.K., Nayak, S., 2018. Metal–organic frameworks
for heavy metal removal from water. Coord. Chem. Rev. 358, 92–107.
Koedooder, C., Gueneugues, A., Van Geersdaële, R., Vergé, V., Bouget, F.-Y., Labreuche,
Y., Obernosterer, I., Blain, S., 2018. The role of the glyoxylate shunt in the accli-
mation to iron limitation in marine heterotrophic bacteria. Front. Mar. Sci. 5, 435.
Köhler, L., Machill, S., Werner, A., Selzer, C., Kaskel, S., Brunner, E., 2017. Are diatoms
“Green” aluminosilicate synthesis microreactors for future catalyst production?
Molecules 22, 2232.
Kouzuma, A., Watanabe, K., 2015. Exploring the potential of algae/bacteria interactions.
Curr. Opin. Biotechnol. 33, 125–129.
Kuczyńska, P., Jemiola-Rzeminska,, M., Strzalka, K., 2015. Photosynthetic pigments in
diatoms. Mar. Drugs 13, 5847–5881.
Kumar, G., Bhardwaj, M., 2017. Comparative genotoxicity of heavy metals in root mer-
istems of Cuminum cyminum L. Chromosome Bot. 12, 56–61.
Kumar, K.S., Dahms, H.-U., Won, E.-J., Lee, J.-S., Shin, K.-H., 2015. Microalgae–a pro-
mising tool for heavy metal remediation. Ecotox. Environ. Safe. 113, 329–352.
Lane, E.S., Jang, K., Cullen, J.T., Maldonado, M.T., 2008. The interaction between in-
organic iron and cadmium uptake in the marine diatom Thalassiosira oceanica.
Limnol. Oceanogr. 53, 1784–1789.
Lane, T.W., Morel, F.M., 2000. A biological function for cadmium in marine diatoms.
Proc. Natl. Acad. Sci. 97, 4627–4631.
Larras, F., Keck, F., Montuelle, B., Rimet, F., Bouchez, A., 2014. Linking diatom sensitivity
to herbicides to phylogeny: a step forward for biomonitoring? Environ. Sci. Technol.
48, 1921–1930.
Lebeau, T., Robert, J.M., 2003. Diatom cultivation and biotechnologically relevant pro-
ducts. Part I: cultivation at various scales. Appl. Microbiol. Biotechnol. 60, 612–623.
Levitan, O., Dinamarca, J., Hochman, G., Falkowski, P.G., 2014. Diatoms: a fossil fuel of
the future. Trends Biotechnol. 32, 117–124.
Li, J., Peng, F., Ding, D., Zhang, S., Li, D., Ting, Z., 2011. Characteristics of the phyto-
plankton community and bioaccumulation of heavy metals during algal blooms in
Xiangjiang River (Hunan, China). Sci. China Life Sci. 54, 931–938.
Lin, Z., Li, J., Luan, Y., Dai, W., 2020. Application of algae for heavy metal adsorption: a
20-year meta-analysis. Ecotox. Environ. Safe. 190, 110089.
Lobo, E.A., Heinrich, C.G., Schuch, M., Wetzel, C.E., Ector, L., 2016. Diatoms as bioin-
dicators in rivers. In: Necchi JR, O. (Ed.), River Algae. Springer, pp. 245–271.
Loix, C., Huybrechts, M., Vangronsveld, J., Gielen, M., Keunen, E., Cuypers, A., 2017.
Reciprocal Interactions between cadmium-induced cell wall responses and oxidative
stress in plants. Front. Plant. Sci. 31, 1867.
Luís, A.T., Teixeira, P., Almeida, S.F.P., Ector, L., Matos, J.X., Ferreira da Silva, E.A.,
2011. Environmental impact of mining activities in the Lousal area (Portugal): che-
mical and diatom characterization of metal-contaminated stream sediments and
surface water of Corona stream. Sci. Total Environ. 409, 4312–4325.
Łukowski, A., Dec, D., 2018. Influence of Zn, Cd, and Cu fractions on enzymatic activity of
arable soils. Environ. Monit. Assess. 190, 278.
Luo, C.S., Liang, J.R., Lin, Q., Li, C., Bowler, C., Anderson, D.M., Wang, P., Wang, X.W.,
Ya-Hui Gao, Y.H., et al., 2014. Cellular responses associated with ROS production and
cell fate decision in early stress response to iron limitation in the diatom Thalassiosira
pseudonana. J. Proteome Res. 13, 5510–5523.
Ma, J., Zhou, B., Duan, D., Wei, Y., Pan, K., 2018. Silicon limitation reduced the ad-
sorption of cadmium in marine diatoms. Aquat. Toxicol. 202, 136–144.
Marella, T.K., Bhaskar, M.V., and Tiwari, A., 2016. Phycoremediation of eutrophic lakes
using diatom algae. Lake Sci. Climate Change. M. Nageeb Rashed, Intech Open, DOI:
10.5772/64111.
Marella, T.K., Datta, A., Patil, M.D., Dixit, S., Tiwari, A., 2019. Biodiesel production
through algal cultivation in urban wastewater using algal floway. Bioresour. Technol.
280, 222–228.
Marella, T.K., Parine, N.R., Tiwari, A., 2018. Potential of diatom consortium developed by
nutrient enrichment for biodiesel production and simultaneous nutrient removal
from waste water. Saudi J. Biol. Sci. 25, 704–709.
Maršálek, B., Rojíčková, R., 1996. Stress factors enhancing production of algal exudates: a
potential self-protective mechanism? Z. Naturforsch. 51c, 646–650.
Martín, J.R., De Arana, C., Ramos-Miras, J., Gil, C., Boluda, R., 2015. Impact of 70 years
urban growth associated with heavy metal pollution. Environ. Pollut. 196, 156–163.
Matamoros, V., Gutiérrez, R., Ferrer, I., García, J., Bayona, J.M., 2015. Capability of
10
Bioresource Technology 305 (2020) 123068
microalgae-based wastewater treatment systems to remove emerging organic con-
taminants: a pilot-scale study. J. Hazard. Mater. 288, 34–42.
Matamoros, V., Uggetti, E., García, J., Bayona, J.M., 2016. Assessment of themechanisms
involved in the removal of emerging contaminants by microalgae from wastewater: a
laboratory scale study. J. Hazard. Mater. 301, 197–205.
Mehta, S.K., Gaur, J.P., 2005. Use of algae for removing heavy metal ions from waste-
water: progress and prospects. Crit. Rev. Biotechnol. 25, 113–152.
Meier, B., Sehn, A.P., Sette, M., Paci, M., Desideri, A., Rotilio, G., 1994. In vivo in-
corporation of cobalt into Propionibacterium shermanii superoxide dismutase. FEBS
let. 348, 283–286.
Meneses-Jácome, A., Diaz-Chavez, R., Velásquez-Arredondo, H.I., Cárdenas-Chávez, D.L.,
Parra, R., Ruiz-Colorado, A.A., 2016. Sustainable energy from agro-industrial was-
tewaters in Latin-America. Renew. Sust. Energ. Rev. 56, 1249–1262.
Michels, A.K., Wedel, N., Kroth, P.G., 2005. Diatom plastids possess a phosphor-
ibulokinase with an altered regulation and no oxidative pentose phosphate pathway.
Plant physiol. 137, 911–920.
Milligan, A.J., Morel, F.M., 2002. A proton buffering role for silica in diatoms. Science
297, 1848–1850.
Miranda, A.F., Ramkumar, N., Andriotis, C., Höltkemeier, T., Yasmin, A., Rochfort, S.,
Wlodkowic, D., Morrison, P., Roddick, F., Spangenberg, G., 2017. Applications of
microalgal biofilms for wastewater treatment and bioenergy production. Biotechnol.
Biofuels. 10, 120.
Mishra, M., Arukha, A.P., Bashir, T., Yadav, D., Prasad, G.B.K.S., 2017. All new faces of
diatoms: potential source of nanomaterials and beyond. Front. Microbiol. 8, 1239.
Morelli, E., Scarano, G., 2001. Synthesis and stability of phytochelatins induced by cad-
mium and lead in the marine diatom Phaeodactylum tricornutum. Mar. Environ. Res.
52, 383–395.
Morelli, E., Scarano, G., 2004. Copper-induced changes of non-protein thiols and anti-
oxidant enzymes in the marine microalga Phaeodactylum tricornutum. Plant Sci. 167,
289–296.
Morin, S., Cordonier, A., Lavoie, I., Arini, A., Blanco, S., Duong, T.T., Torn_es, E., Bonet,
B., Corcoll, N., Faggiano, L., Laviale, M., P_er_es, F., Becares, E., Coste, M., Feurtet-
Mazel, A., Fortin, C., Guasch, H., Sabater, S., 2012. Consistency in diatom response to
metal-contaminated environments. In: H. Guasch, A. Ginebreda, A. Geiszinger (Eds.),
Emerging and Priority Pollutants in Rivers. Springer-Verlag, Berlin, pp. 117–146.
Morin, S., Duong, T.T., Dabrin, A., Coynel, A., Herlory, O., Baudrimont, M., Delmas, F.,
Durrieu, G., Sch€afer, J., Winterton, P., Blanc, G., Coste, M., 2008a. Long-term survey
of heavy-metal pollution, biofilm contamination and diatom community structure in
the Riou Mort watershed, South-West France. Environ. Pollut. 151, 532–542.
Morin, S., Duong, T.T., Herlory, O., Feurtet-Mazel, A., Coste, M., 2008b. Cadmium toxi-
city and bioaccumulation in freshwater biofilms. Arch. Environ. Contam. Toxicol. 54,
173–186.
Morozov, A.A., Galachyants, Yuri P., 2019. Diatom genes originating from red and green
algae: implications for the secondary endosymbiosis models. Mar. Genom. 45, 72–78.
Mu, W., Chen, Y., Liu, Y., Pan, X., Fan, Y., 2018. Toxicological effects of cadmium and
lead on two freshwater diatoms. Environ. Toxicol. Phar. 59, 152–162.
Nassiri, Y., Mansot, J., Wéry, J., Ginsburger-Vogel, T., Amiard, J., 1997. Ultrastructural
and electron energy loss spectroscopy studies of sequestration mechanisms of Cd and
Cu in the marine diatom Skeletonema costatum. Arch. Environ. Con. Tox. 33, 147–155.
Nhat, P.V.H., Ngo, H.H., Guo, W.S., Chang, S.W., Nguyen, D.D., Nguyen, P.D., Bui, X.T.,
Zhang, X.B., Guo, J.B., 2018. Can algae-based technologies be an affordable green
process for biofuel production and wastewater remediation? Bioresour. Technol. 256,
491–501.
Nwoba, E.G., Parlevliet, D.A., Laird, D.W., Alameh, K., Moheimani, N.R., 2019. Light
management technologies for increasing algal photobioreactor efficiency. Algal Res.
39, 101433.
Ouyang, W., Wang, Y., Lin, C., He, M., Hao, F., Liu, H., Zhu, W., 2018. Heavy metal loss
from agricultural watershed to aquatic system: a sciento metrics review. Sci. Total
Environ. 637, 208–220.
Pandey, L.K., Bergey, E.A., 2016. Exploring the status of motility, lipid bodies, deformities
and size reduction in periphytic diatom community from chronically metal (Cu, Zn)
polluted waterbodies as a biomonitoring tool. Sci. Total Environ. 550, 372–381.
Peltomaa, E., Hallfors, H., Taipale, S.J., 2019. Comparison of diatoms and dinoflagellates
from different habitats as source of PUFAS. Mar. Drugs 17 pii, E233.
Perales-Vela, H.V., Pena-Castro, J.M., Canizares-Villanueva, R.O., 2006. Heavy metal
detoxification in eukaryotic microalgae. Chemosphere 64, 1–10.
Perrein-Ettajani, H., Amiard, J., Haure, J., Renaud, C., 1999. Effets des métaux (Ag, Cd,
Cu) sur la composition biochimique et compartimentation de ces métaux chez deux
microalgues Skeletonema costatum et Tetraselmis suecica. Can. J. Fish Aquat. Sci. 56,
1757–1765.
Rabsch, U., Elbrächter, M., 1980. Cadmium and zinc uptake, growth, and primary pro-
duction in Coscinodiscus granii cultures containing low levels of cells and dissolved
organic carbon. Helgoländer Meeresunters 33, 79.
Rajkumar, R., Yaakob, Z., Takriff, M.S., 2013. Potential of micro and macro algae for
biofuel production: a brief review. Bio. Res. 9, 1606–1633.
Rasheed, T., Bilal, M., Nabeel, F., Adeel, M., Iqbal, H.M., 2019. Environmentally-related
contaminants of high concern: potential sources and analytical modalities for de-
tection, quantification, and treatment. Environ. Int. 122, 52–66.
Raven, J.A., Beardall, J., 2016. Algal photosynthesis and physiology. In: Slocombe, S.P.,
Benemann, J.R. (Eds.), Microalgal Production for Biomass and High Value Products.
Taylor and Francis, pp. 1–19.
Raven, J.A., Evans, M.C., Korb, R.E., 1999. The role of trace metals in photosynthetic
electron transport in O 2-evolving organisms. Photosynth. Res. 60, 111–150.
Rebelo, F.M., Caldas, E.D., 2016. Arsenic, lead, mercury and cadmium: toxicity, levels in
breast milk and the risks for breastfed infants. Environ. Res. 151, 671–688.
Rijstenbil, J., Derksen, J., Gerringa, L., Poortvliet, T., Sandee, A., Van den Berg, M., Van
T. Kiran Marella, et al.
Drie, J., Wijnholds, J., 1994. Oxidative stress induced by copper: defense and damage
in the marine planktonic diatom Ditylum brightwellii, grown in continuous cultures
with high and low zinc levels. Mar. Biol. 119, 583–590.
Rijstenbil, J., Gerringa, L., 2002. Interactions of algal ligands, metal complexation and
availability, and cell responses of the diatom Ditylum brightwellii with a gradual in-
crease in copper. Aquat. Toxicol. 56, 115–131.
Rimet, F., Bouchez, A., 2011. Use of diatom life-forms and ecological guilds to assess
pesticide contamination in rivers: lotic mesocosm approaches. Ecol. Indic. 11,
489–499.
Rizwan, M., Ali, S., Rehman ur, M.Z., Maqbool, A., 2019. A critical review on the effects
of zinc at toxic levels of cadmium in plants. Environ. Sci. Pollut. Res. 26, 6279–6289.
Romera, E., González, F., Ballester, A., Blázquez, M.L., Muñoz, J.A., 2007. Comparative
study of biosorption of heavy metals using different types of algae. Bioresour.
Technol. 98, 3344–3353.
Roubeix, V., Fauvelle, V., Tison-Rosebery, J., Mazzella, N., Coste, M., Delmas, F., 2012.
Assessing the impact of chloroacetanilide herbicides and their metabolites on per-
iphyton in the Leyre River (SW France) via short term growth inhibition tests on
autochthonous diatoms. J. Environ. Monit. 14, 1655–1663.
Roubeix, V., Mazzella, N., Schouler, L., Fauvelle, V., Morin, S., Coste, M., Delmas, F.,
Margoum, C., 2011. Variations of periphytic diatom sensitivity to the herbicide
diuron and relation to species distribution in a contamination gradient: implications
for biomonitoring. J. Environ. Monit. 13, 1768–1774.
Sai, S.S., Sangeetha, V., Abhinaya, S., Ramprabhu, S., 2019. Diatom frustule-graphene
based nanomaterial for room temperature hydrogen storage. Int. J. Hydrogen Energ.
45, 764–773.
Samantaray, S.S., Sangeetha, V., Abinaya, S., Ramaprabhu, S., 2019. Diatom frustule-
graphene based nanomaterial for room temperature hydrogen storage. Int. J. H.
Energy 45, 764–773.
Santos, J., Almeida, S.F., Figueira, E., 2013. Cadmium chelation by frustulins: a novel
metal tolerance mechanism in Nitzschia palea (Kützing) W. Smith. Ecotoxicology 22,
166–173.
Sawant, S.S., Khadamkar, H.P., Mathpati, C.S., Pandit, R., Lali, A.M., 2018.
Computational and experimental studies of high depth algal raceway pond photo-
bioreactor. Renew. Energy 118, 152–159.
Sbihi, K., Cherifi, O., Bertrand, M., Gharmali, A.E., 2014. Biosorption of metals (Cd, Cu
and Zn) by the freshwater diatom Planothidium lanceolatum: a laboratory study.
Diatom Res. 13, 55–63.
Sbihi, K., Cherifi, O., El Gharmali, A., Oudra, B., Aziz, F., 2012. Accumulation and tox-
icological effects of cadmium, copper and zinc on the growth and photosynthesis of
the freshwater diatom Planothidium lanceolatum (Brébisson) Lange-Bertalot: a la-
boratory study. J. Mater. Environ. Sci. 3, 497–506.
Schenk, P.M., Thomas-Hall, S.R., Stephens, E., Marx, U.C., Mussgnug, J.H., Posten, C.,
Kruse, O., Hankamer, B., 2008. Second generation biofuels: high-efficiency micro-
algae for biodiesel production. Bioenergy Res. 1, 20–43.
Schmitt-Jansen, M., Bley, L.M., Krumbiegel, M.L., Rotter, S., 2016. Induced community
tolerance of periphyton towards combined salt and toxic stress. Freshw. Biol. 61,
2152–2161.
Spolaore, P., Joannis-Cassan, C., Duran, E., Isambert, A., 2006. Commercial applications
of microalgae. J. Biosci. Bioeng. 101, 87–96.
Stauber, J., Florence, T., 1989. The effect of culture medium on metal toxicity to the
marine diatom Nitzschia closterium and the freshwater green alga Chlorella pyr-
enoidosa. Water Res. 23, 907–911.
Sunda, W.G., 1989. Trace metal interactions with marine phytoplankton. Biol. Oceanogr.
6, 411–442.
Sunda, W.G., Huntsman, S.A., 2000. Effect of Zn, Mn, and Fe on Cd accumulation in
phytoplankton: implications for oceanic Cd cycling. Limnol. Oceanogr. 45,
1501–1516.
Sunday, E.R., Uyi, O.J., Caleb, O.O., 2018. Phycoremediation: an eco-solution to en-
vironmental protection and sustainable remediation. J. Chem. Environ. Biol. Engr.
2, 5.
Tieu, T., Alba, M., Elnathan, R., Cifuentes-Rius, A., Voelcker, N.H., 2019. Advances in
11
Bioresource Technology 305 (2020) 123068
porous silicon-based nanomaterials for diagnostic and therapeutic applications. Adv.
Ther. 2, 1800095.
Tiwari, A., Marella, T.K., 2019. Potential and application of diatoms for industry-specific
wastewater treatment. In: Gupta, S., Bux, F. (Eds.), Application of Microalgae in
Wastewater Treatment. Springer, Cham, pp. 321–339.
Tokumura, M., Sugawara, A., Raknuzzaman, M., Habibullah-Al-Mamun, M., Masunaga,
S., 2016. Comprehensive study on effects of water matrices on removal of pharma-
ceuticals by three different kinds of advanced oxidation processes. Chemosphere 159,
317–325.
Tolbooma, S.N., Carrillo-Nieves, D., Rostro-Alanis, M.J., Quiroz, R.C., Barceló, D., Iqbal,
H.M.N., Parra-Saldivar, R., 2019. Algal-based removal strategies for hazardous con-
taminants from the environment-a review. Sci. Total Environ. 665, 358–366.
Torres, E., Cid, A., Herrero, C., Abalde, J., 1998. Removal of cadmium ions by the marine
diatom Phaeodactylum tricornutum Bohlin accumulation and long-term kinetics of
uptake. Bioresour. Technol. 63, 213–220.
Uthappa, U.T., Brahmkhatri, V., Sriram, G., Jung, H.Y., Yu, J., Kurkuri, N., Aminabhavi,
T.M., Altalhi, T., Neelgund, G.M., Kurkuri, M.D., 2018. Nature engineered diatom
biosilica as drug delivery systems. J. Control. Release. 281, 70–83.
Utomo, H.D., Tan, K.X.D., Choong, Z.Y.D., Yu, J.J., Ong, J.J., Lim, Z.B., 2016. Biosorption
of heavy metal by algae biomass in surface water. J. Environ. Prot. 7, 1547.
Van dam, H., Mertens, A., Sinkeldam, J., 1994.A. A coded checklist and ecological in-
dicator values of freshwater diatoms from The Netherlands. Neth. J. Aquat. Ecol. 28,
117–133.
Vella, F.M., Sardo, A., Gallo, C., Landi, S., Fontana, A., d'Ippolito, G., 2019. Annual
outdoor cultivation of the diatom Thalassiosira weissflogii: productivity, limits and
perspectives. Algal Res. 42, 101553.
Volland, S., Bayer, E., Baumgartner, V., Andosch, A., Lütz, C., Sima, E., Lütz-Meindl, U.,
2014. Rescue of heavy metal effects on cell physiology of the algal model system
Micrasterias by divalent ions. J. Plant Physiol. 171, 154–163.
Wagner, H., Jakob, T., Wilhelm, C., 2006. Balancing the energy flow from captured light
to biomass under fluctuating light conditions. New Phytol. 169, 95–108.
Wang, J.K., 2015. An absorbent and method of application for the treatment of heavy
metal waste water. Chinese Patent 201410072325.
Wang, X.W., Huang, L., Ji, P.Y., Chen, C.P., Li, X.S., Gao, Y.H., Liang, J.R., 2019. Using a
mixture of wastewater and seawater as the growth medium for wastewater treatment
and lipid production by the marine diatom Phaeodactylum tricornutum. Bioresour.
Technol. 289, 121681.
Wang, J., Liu, Q., Zhao, X., Borthwick, A.G.L., Liu, Y., Chen, Q., Ni, J., 2019. Molecular
biogeography of planktonic and benthic diatoms in the Yangtze River. Microbiome 7,
153.
Wang, J.K., Seibert, M., 2017. Prospects for commercial production of diatoms.
Biotechnol. Biofuels 10, 16.
Westermann, M., Rhiel, E., 2005. Localisation of fucoxanthin chlorophyll a/c-binding
polypeptides of the centric diatom Cyclotella cryptica by immuno-electron micro-
scopy. Protoplasma 225, 217–223.
Xiong, J.Q., Kurade, M.B., Jeon, B.H., 2018. Can microalgae remove pharmaceutical
contaminants from water? Trends Biotechnol. 36, 30–44.
Yan, Z., Kangas, P.C., Yuan, X., Chen, Y., Zhang, Y., Li, J., Su, Y., Gao, X., Chen, N., 2018.
Flow conditions influence nutrient removal at an artificial lake and a drinking water
reservoir with an algal floway. Algal Res. 35, 245–252.
Yi, Z., Xu, M., Di, X., Brynjólfsson, S., Fu, W., 2017. Exploring valuable lipids in diatoms.
Front. Mar. Sci. 4, 17.
Zhang, J., Ding, T., Zhang, Z., Xu, L., Zhang, C., 2015. Enhanced adsorption of trivalent
arsenic from water by functionalized diatom silica shells. PLoS One 10, e0123395.
Zhou, Y., Zhang, J., Huang, J., Deng, K., Zhang, J., Qin, Z., Wang, Z., Zhang, X., Tuo, Y.,
Chen, L., Chen, Y., Huang, P., 2019. Digital whole-slide image analysis for automated
diatom test in forensic cases of drowning using a convolutional neural network al-
gorithm. Forensic Sci. Int. 302, 109922.
Zhu, L.D., Hiltunen, E., Antila, E., Zhong, J.J., Yuan, Z.H., Wang, Z.M., 2014. Microalgal
biofuels: flexible bioenergies for sustainable development. Renew. Sust. Energ. Rev.
30, 1035–1046.