Bioresource Technology 339 (2021) 125589

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

Review

Bioremediation of heavy metals from industrial effluents by endophytes

and their metabolic activity: Recent advances
Pooja Sharma , Sunil Kumar *
CSIR-National Environmental and Engineering Research Institute (CSIR-NEERI), Nagpur 440 020, India

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

• Bioremediation of toxic metals by en­

dophytes was reviewed in-depth.
• Potentiality and feasibility of metabo­
lites of endophytes are summarized.
• Future perspectives & advancement of
endophytes technology are also
discussed.

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

Keywords: Worldwide, heavy metals pollution is mostly caused by rapid population growth and industrial development
Metal pollutants which is accumulated in food webs causing a serious public health risk. Endophytic microorganisms have a
Endophytes variety of mechanisms for metal sequestration having metal biosorption capacities. Endophytic organisms like
Detoxification
bacteria and fungi provide beneficial qualities that help plants to improve their health, reduce stress, and
Effluent treatment
Metabolic activity
detoxify metals. Endophytes have a higher proclivity for improving metal and mineral solubility by cells that
secrete low-molecular-weight organic acids and metal-specific ligands like siderophores, which change the pH of
the soil and improve binding activity. Protein-related approaches like chromatin immunoprecipitation
sequencing (ChIP-Seq) and modified enzyme-linked immunosorbent assay (ELISA test) can represent endophytic
bacterial community and DNA-protein interactions during metal reduction. This review explored the role of
endophytes in bioremediation approaches that can help in analyzing the potential and prospects in response to
industrial effluents’ detoxification.

1. Introduction
Industrial effluents are a major source of heavy metal pollution in
water, soil, and atmosphere. Heavy metal pollution in the environment
has become a severe concern to the ecosystem and aquatic life (Su, 2014;
Okolo et al., 2016). Because of its non-biodegradable nature and ability
of bioaccumulation, metal toxicity is a major environmental issue
(Gautam et al., 2015; Sharma et al., 2020a, b). Several inorganic metals,
such as zinc (Zn), chromium (Cr3+), manganese (Mn), copper (Cu),
calcium (Ca), nickel (Ni), magnesium (Mg), and sodium (Na), are
essential for metabolic and redox processes in trace amounts. Mercury
(Hg), silver (Ag), cadmium (Cd), lead (Pb), aluminum (Al), and gold
(Au) are heavy metals that have no role in biochemical functions and are
very harmful to the living organisms (Lakherwal, 2014; Sharma et al.,

* Corresponding Author.
E-mail address: s_kumar@neeri.res.in (S. Kumar).

https://doi.org/10.1016/j.biortech.2021.125589
Received 27 May 2021; Received in revised form 10 July 2021; Accepted 13 July 2021
Available online 14 July 2021
0960-8524/© 2021 Elsevier Ltd. All rights reserved.
P. Sharma and S. Kumar
2021a; Sharma et al., 2020b). The term “endophyte” refers to organism
that colonizes the internal organs of their plant hosts during a specific
period of their lives. Endophytic microorganisms are one of the most
diverse groups with an estimate of one million species (Rashmi et al.,
2019; An et al., 2015). Based on more than a decade of research, billions
of live plant species in natural ecosystems are hosts for various endo­
phytic microbes. It makes this group of microbes as one of the most
significant untapped natural resources for biosynthetic enzymes and
secondary metabolites bioprospecting (Manganyi and Ateba, 2020).
Bioremediation is a technique for cleaning up polluted environment
by transforming enzymes during the biosorption of different toxic metals
(Okoduwa et al., 2017; Tripathi et al., 2021a, b). The methodology is
both ecologically benign and innovative for ecological restoration to
enhance and boost their remediation performance for the use of mi­
crobes with distinct characteristics of catabolic ability and their prod­
ucts, such as biosurfactants and enzymes (Ma et al., 2016; Le et al.,
2017). Various options were also proposed to broaden the use of
microbial approaches for decontamination of heavy metals. Microbial
fuel cells (MFCs) have the efficiency to decrease the resistance of metals.
Bioremediation mediated by biofilm is also applied to detoxify heavy
metal polluted ecosystem. The interaction between endophytes and
plants break down complex molecules into simple molecules like nu­
trients, mobilizes metal ions, promotes pollution uptake by plants, and
improves bioremediation. The environmental pollution caused by
metals is a very serious issue that reduces crop yield and quality of food
due to overuse of agricultural pesticides and fertilizers, and mulching,
which have led to heavy metal pollution of soils (Su, 2014).
The current state of water resources demonstrates the dominance of
pollution produced by industrial effluent containing large quantities of
hazardous heavy metal or metalloids. These are of major concern
because of their persistence and non-degradability (Iloms et al., 2020).
Physical and chemical treatment techniques used for industrial effluent
treatment are more time-consuming, costly, and ineffective. Bioreme­
diation is a technique for reducing pollution emissions and ameliorating
the effects of contaminants that are mediated by endophytic microbes
(Conesa et al., 2012). This has been identified as a good strategy for
controlling pollution and a novel technique for the treatment of toxins
using biological systems. This can be a technique that uses bacteria,
fungus, metabolites, enzymes, or green plants to restore the habitat of
the ecosystem after it has been polluted (Chakraborty et al., 2012).
Bacteria that synthesize different hormonal activities, such as 1-amino­
cyclopropane-1-carboxylate (ACC), siderophores, indole acetic acid
(IAA), and deaminase can accelerate plant development and decrease
the ethylene concentration in the plant. Heavy metal has low movement
in soil and is difficult to be absorbed directly by plant roots. The inter­
action of plant roots and soil microorganisms can boost metal absorption
in the root system (Saravanan et al., 2007). Plant-linked microbes play
an important part in a host’s ability to adapt environmental alterations.
The application of appropriate remedial measures to damaged soils,
which can lower the risk of toxic metals, is very beneficial. Traditional
remediation treatments like landfilling and leaching, excavation and
disposal, or soil cleaning can be attempted (Vesely et al., 2012). A large
amount of leachate has been generated as a result of the use of wide­
spread municipal and industrial effluents of landfills for disposal, as well
as the use of agrochemicals, which cause water contamination. The risk
of leachate contaminating groundwater has emphasized development of
new landfill engineering design (Sivakumar, 2013). Plant endophytic
bacteria have received a lot of interest because of their capacity to
improve plant response to a range of stressors. Plant-microbe in­
teractions are characterized by protein secretion and binding peptide.
The transfer of effector proteins help bacteria in maintaining their
parasitic lifestyle by reducing host defense, but the host stimulates
effector-triggered immune responses whenever it detects the effector
proteins (Mengistu, 2020). Numerous studies have shown that endo­
phytes improve the plant’s ability to survive with dryness, salt, nitrogen
deficit, infections, and recently confirmed by a meta-analysis although
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Bioresource Technology 339 (2021) 125589
such an impact has substantial biotechnological implications in the
bioremediation of heavy metal (Franco-Franklin et al., 2021). The
overall chemical forms of the metals, metal ion concentrations, and
other parameters potential influenced by heavy metal are stimulatory or
inhibitory to microbes. Environmental parameters, such as low molec­
ular weight organic acids, pH, temperature, and humic acids can affect
heavy metal processing, balanced state, transit, and bioavailability to
microbes. At acidic pH level, heavy metal tends to form free ionic spe­
cies, with more protons available to saturate metal-binding sites (Kapahi
and Sachdeva, 2019). The adsorbent surface becomes increasingly
positively charged as hydrogen ion concentrations rise, lowering the
attraction between adsorbent and metal cations and thereby increased
toxicity. From the viewpoint of application, it can be concluded that
endophytic microorganisms play an essential role in degradation or
detoxification of metal pollution from industrial effluents. This review
covers current research and future applications of endophytic bacteria
for the detoxification of industrial effluents; with a focus on heavy metal
bioremediation and simultaneously it addresses wide technological and
scientific fields to solve the issue of environmental remediation at a
fundamental level.
2. Endophytes community in the environment
Endophytic microbes are recommended as an environment-friendly
way to boost plant species development and disease resistance. This
type of bacteria is distinguished by the fact that it spends the majority of
the asymptomatic life cycle within the tissue of plants, causing harm to
its host. Endophytic bacteria appear to make tiny accumulates scattered
in plant organs where nutrients are transferred, promoting the micro­
organism’s metabolic activity as well as the host plant’s metabolic re­
sponses (Perez et al., 2013; Nanda et al., 2019). Such microbes can be
related to a host of plants in a very particular or generic fashion, and
they can be passed down through in groups (Johnston and Raizada,
2011). Microbes play a key role in agriculture, medicine, and industry
development of microbial engineering (Gouda et al., 2016(Khan et al.,
2017)). The various functions of microbes can improve environmental
health as well as crop productivity (Nair and Padmavathy, 2014). En­
dophytes have fascinated the curiosity of several scientists due to their
important roles in the growth of the plants as well as aiding plant sur­
vival in stressed environment (Shen et al., 2019; Andreozzi et al., 2019).
Endophytic bacteria has the ability to utilize the exudes emitted by plant
roots as a source of energy in a critical situation during the interaction
with plants (Kandel et al., 2017; Yadav, 2018). Endophytic microor­
ganisms have been employed in the bulk production of industrially
important goods including antibiotics, enzymes, and riboflavin, etc.
(Latz et al., 2018). Microbe-based techniques for the detoxification of
metal contamination are advanced approaches where metabolites like
butanol and ethanol are also produced as by-products. Biotransforma­
tion of a wide range of chemicals lessens the impact of pollution like
degradation and bioremediation. Since last few decades, different kinds
of drugs have been synthesized from plants and microbes (Gouda et al.,
2016). These products generated from natural sources are less hazardous
and affordable. Endophytic microbes have the potential for secreting
various bioactive and metabolic compounds, such as polyphenol and
anthocyanin which are phytonutrients or metabolites and help in pre­
venting cancer and heart disease (Nair, 2014).
Endophytes are diazotrophic, which means they are nitrogen (N2)
fixers, and converts atmospheric N2 into ammonium ions to be absorbed
by host plants (Hernandez-Rodríguez et al., 2017). Endophyte bacteria
can increase plant development, increase stress response, disease resis­
tance through a variety of pathways, including phytohormone synthesis,
mineral solubilization, and siderophores production to nitrogen fixation
(Ahemad and Khan, 2012). Microbial communities are of particular
interest since they are somewhat sheltered from the soil’s hostile
ecosystem. Endophytic organisms have the potential to inhibit diseases,
boost plant development and growth under adverse environment
P. Sharma and S. Kumar
(Sánchez-López et al., 2018). The development of successful bioreme­
diation of metal requires a thorough understanding of the properties of
metal tolerance by the endophytic microbiome. Endophytes found in
various plant species have been shown to promote plant growth in
previous studies (Yan et al., 2018; Zhu and She, 2018). Under salt or
heavy metals stress, these microbes have been proven to boost plant
growth and preserve metabolic function (Tirry et al., 2018; Soldan et al.,
2019). It was discovered that the plant-bacteria connection increased
the appearance of a genetic factor related to the stress of aluminum in
Arabidopsis thaliana and implying that the plant-bacteria association
improves the plant’s tolerance mechanisms (Farh et al., 2017). The use
of these microbes in agriculture and bioremediation is gaining popu­
larity. There has been a lot of research done recently on the benefits of
endophytic bacteria on plant tolerance to multiple stresses. Armatimo­
nadetes, Cyanobacteria, Planctomycetes, Nitrospirae, Verrucomicrobia, and
Chloroflexi are among the other bacterial phyla found in the root of
endospheres in the community (Edwards et al., 2015).
Endophytic bacteria-mediated stress tolerance is considered to be the
most successful technique for bioremediation because this is environ­
mentally acceptable, economically sound, and technically feasible
(Singh et al., 2016). Endophytes have evolved successfully to the heavy
metal contaminated environment, and they have developed immune
responses like biomagnification and decrease in enzymatic activity
(Tiwari and Lata, 2018). Beside these processes, many microorganisms
have been stated to promote metal storage and increase the expression
of genes (Srivastava et al., 2013). Furthermore, the control of ethylene
concentration in plants by different endophytic microbes can affect
tolerance of different heavy metal directly by altering levels of stress.
Metagenomic sequence analysis of microbes involved in endophytic root
system has revealed potential mobility functions, viz., plant polymer
breakdown, iron uptake and storage, quorum sensing, and generation of
reactive oxygen species in the roots microbiome (Kaushal et al., 2020).
3. Industrial effluents and their toxicity
The accumulation of different heavy metal in the ecosystem has
come from continuous anthropogenic activities and the development of
industries (Ashraf et al., 2018; Rogowska et al., 2020). Heavy metal
absorbed into the human body and animals through the food chain can
cause serious harm to the animal and human health due to their high
solubility, long-term persistence, potential androgenic, mutagenic, and
carcinogenic consequences (Rehman et al., 2018(Tripathi et al., 2021a,
b)). In developing countries like India, agro-processing industries
including tanneries, pulp-paper mills, olive mills, and distilleries have
become a major source of heavy metal pollution (Juel et al., 2017;
Sharma et al., 2021b,d,f). The localization of a large number of heavy
metal in tissues and cell organelles causes increased toxicity. Non-
essential metals, such as Cr, Pb, Ni, Cd, etc., play no significant role in
humans, but they can induce toxicity by affecting the absorption of el­
ements in the body (Briffa et al., 2020). Heavy metals have been found to
impact cellular organelles and components, including lysosomes, cell
membranes, enzymes, mitochondria, and nuclei. Metal ions have been
found to interact with nuclear proteins and DNA, which caused DNA
damage, cell cycle regulation, apoptosis, and carcinogenesis (Tchoun­
wou et al., 2012). One of the most vulnerable organisms is fish which is
extremely sensitive to pollution throughout their lifecycle (Beyersmann
and Hartwig, 2008). Disturbances during the early stage of growth can
have a deleterious impact on fish later (Zhang et al., 2016). Zulfahmi
et al., 2014, and Groner et al., 2017 have reported that Nile tilapia
(Oreochromis niloticus), which is a widely dispersed fish species in
Indonesian waters, have got endangered due to metal toxicity. Heavy
metal causes two types of damages which can be classified as “direct”
and “indirect” damage. “Direct” damage refers to conformational
changes in the biomolecules due to heavy metal exposure while “indi­
rect” damage refers to production of reactive oxygen species/ nitrogen
species, such as superoxide radicals, hydrogen peroxide, nitric oxide,
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Bioresource Technology 339 (2021) 125589
and other endogenous oxidants. Signaling pathways have been observed
to be activated by heavy metals. Metal toxicity produces free radicals,
which induce DNA damage, sulphydryl homeostasis disruption, and
lipid peroxidation (Valko et al., 2005).
The mechanism of chromium toxicity and carcinogenicity is a com­
plex process (DesMarias and Costa, 2019). The intermediates produced
during the intracellular reduction of Cr6+ and Cr3+, as well as the
oxidative reaction, mediates the mechanism. The trivalent form is
generated by hexavalent form with essential target macromolecules.
DNA lesions like Cr-DNA adducts, DNA-protein crosslinks, changes in
cellular signaling pathways, DNA-DNA crosslinks, and DNA strand
breaks are caused by complexes made up of Cr3+ and peptides, DNA, and
proteins inside the cell, all of which may be a factor in chromium
compounds’ toxicity and carcinogenicity. Cr6+ is more hazardous than
the trivalent oxidative state because it has a larger redox potential and
can enter cells more easily (Klages-Mundt and Li 2017). Cr6+ exists as a
tetrahedral chromate anion at physiological pH with a structure com­
parable to that of other natural anions, such as phosphate and sulphate,
which are permeable through non-selective membrane channels. Heavy
metals like other endocrine-disrupting chemicals can influence aquatic
species’ endocrine system (Carnevali et al., 2018). Heavy metal is
common endocrine disruptor that can interfere with hormone produc­
tion and secretion. Endocrine disruptors can interfere with the produc­
tion of hormones and induce endocrine disruptive toxicity conditions
and are one of the causes of heavy metal exposure that leads to meta­
bolic illnesses like hypertension and diabetes. For example, Cd, Mn, and
Cr are heavy metal that may increase the risk of metabolic disorders.
Furthermore, metal endocrine disruptors have been linked to an
increased risk of mitochondrial dysfunction and oxidative stress
(Kovacik, A., 2017). When exposed to sublethal quantities of lead and
cadmium, adult Micropogonias undulatus demonstrated significant in­
crease or decrease in blood steroid concentrations, ovarian steroid
secretory activity, and ovarian development. The corticotropin-
releasing thyroglobulin, hormones, and gene expressions of thyroid re­
ceptors were drastically increased after minnow larvae were exposed to
mercury for four days (Rotroff, 2013). The levels of thyroxine T3 and T4
have also been shown to have increased. Toxicity can be caused by
heavy metal in aquatic species, such as animals, plants, and microor­
ganisms. For lengthy periods, some aquatic organisms exist in habitats
contaminated with heavy metal. To lessen discomfort and enhance
tolerance to heavy metal, many species can change their physiological
and biochemical signals. Heat shock proteins (HSP), transferrins (TF),
metallothionein (MT), glutathione transferase (GT), catalase (CAT), and
superoxide dismutase (SOD) are produced by fish that live in heavy
metal-polluted water for an extended period but decreasing the cell
damage caused by heavy metal (Cheuk et al., 2008). Furthermore, this
overview outlines the sources of metals in various industrial effluents as
well as their toxicity to humans and aquatic life.
4. Accumulation of metals in endophytes
Pollutants contamination is currently a global issue and hence novel,
sustainable and green technologies for the repair of environmental
pollutants are urgently needed. The bioremediation technique has been
regarded as one of the most successful, low-cost, and long-term ap­
proaches for the management of chemical contaminants in the envi­
ronment. Using or inoculating endophytic microbial strains for the
remediation of environmental substances has been done regularly for
the management of various contaminants, such as heavy metal during
the last few decades (Fe, Cd, Pb, Ni, Mn, Mg, As, and Cu). Microbial
endophytes assist in the mobilization of pollutants as well as plant
growth promotion and tolerance development against various biotic and
abiotic stresses over the extended course of the host plant and endophyte
relationship at the contaminated site. An in-depth study of the plant-
endophyte relationship might aid in the effective remediation of
polluted sites (Gupta et al., 2020).
P. Sharma and S. Kumar Bioresource Technology 339 (2021) 125589

Endophytic bacteria live underneath the epidermal cell layers in
plant tissues in which they can invade interior tissues and create sym­
biotic, mutually beneficial, commensalism, and trophobiotic relations
with their host (Schulz and Boyle, 2006). It is located in a broad variety
of plants and makes a colony in specific host plants with the maximum
densities in the roots and decreasing density as they progress from leaves
to stem. The majority of endophytic microbes come from epiphytic
bacterial populations in the root system as well as tissues of other plants;
although, a few can be transferred by seeds or tissues of broken foliar
(Dong et al., 2019). Plant stress tolerance mediated by endophytes plays
an important part in the study of microbe-plant interactions. Although
this so far in the initial stages, host stress tolerance by endophyte-
mediated interaction has recently been adequately documented, like
salinity, high-temperature stressors, drought, and infections of patho­
gens. Plant stress gene stimulation and reactive oxygen species regula­
tion are two molecular mechanisms that govern the endophyte-
mediated stress response (Nanda et al., 2019). Metal-resistant strains
were used for heavy metal removal in single or consortium, and
immobilized forms, potentially having more chemosorption sites for
biosorbed heavy metal. Bioremediation is a technique of eliminating
toxins from soils or other sources by using plants and microbial enzymes
(Suja et al., 2014; Kurniati et al., 2014; Li et al., 2018). Endophytic
microbes are effective tools for removing metals from the environment
or assisting host benefactors in bioremediation. Endophytes’ resistance
to a range of metals, like lead, zinc, chromium, cadmium, cobalt, and
manganese can be linked with plant species found in polluted areas,
implying that these microbes get the ability to bioremediate metals
(Zahoor et al., 2017). Plants that thrive in polluted lands can frequently
resist adverse rising circumstances, owing to endophytic fungus colo­
nization, which decreases the toxic effects of pollutants on the host
plants and thus encourages their development (Pietro-Souza et al.,
2017). Endophytes regulate the host plant’s metabolic and morpholog­
ical processes as well as its metal resistance by providing a variety of
detoxification routes, including, binding to fungus cell walls, extracel­
lular scavenging and precipitation, intracellular scavenging, complexa­
tion, vaporization, and compartmentalization.
Fungal endophytes showed resilience to abiotic conditions, such as
salt, temperature, nutrient deficiency, and heavy metal, which can be
used as bio-fertilizers or bio-agents to construct a balanced yield (Ripa
et al., 2019; Sharma and Rath, 2021; Sharma and Singh, 2021). Endo­
phytic bacteria have co-evolved for a long time, an ecosystem that helps
plants survive in both stresses, such as biotic and abiotic situations like
pathogen contamination, drought, and salt even while enhancing the
ecological equilibrium of the biological process. Several investigations
have also shown that heavy metal has a detrimental effect on innovation
biodiversity and plant interactions in contaminated soils (Sharma,
2021). Furthermore, significant researches are yet to be carried out, such
as selection of strains, colonization, distribution, survival, and endo­
phytic bacterial behavior in plant hosts for the success of endophytes
function and bioremediation of heavy metal. The symbiotic system of
Pseudomonas sp. J4AJ, Scirpus triqueter oil-degrading endophytes
increased S.triqueter height and stem biomass and boosted oil degrada­
tion rates compared with individual plants (Table 1) (Zhang et al.,
2014).
5. Bioremediation by endophytes
Plants can get important vitamins and growth conditions from
endophytic bacteria that assist with nutrient availability and enhance
metabolic activities (Sharma et al., 2020c; Sharma et al., 2021c, d).
Plant hormones can improve soil quality intake by influencing root
development dynamics. Endophytic colonization frequently promotes
nutrient enhancement, plant biomass, and absorption. According to the
latest findings, the plant hormones help in safeguarding plants
(Phetcharat and Duangpaeng, 2012). In the presence of inorganic
metals, microbes use a variety of mechanisms to interact and live.
Biotransformation, extrusion, enzyme usage, production of exopoly­
saccharide (EPS), and metallothionein synthesis are some of the tech­
niques utilized by microorganisms to resist metal toxicity (Sharma et al.,
2021e, (Sharma et al., 2021f)). Microbes have evolved indigenous metal
resistance and detoxifying systems in response to compounds (Dixit
et al., 2015; Yang et al., 2015). Accumulation of toxin can be removed by
microbes through extracellular chemical precipitation and volatiliza­
tion. With the presence of anionic structures that enable germs to attach
to metal cations, microbes have a negative charge on their cell surface.
Negative charge receptors in microorganisms involved in adsorbent
include the phosphoryl, hydroxyl, sulfonate, sulfhydryl, amine, alcohol,
ester, carboxyl, thiol groups, and thioether. Fig. 1 shows the description
of bioremediation by using endophytes.
The remediation or detoxification of heavy metals from industrial
effluent using natural microbial life for the prevention of river pollution
is an economically sound technology. Natural attenuation refers to
bioremediation that occurs on its own; biostimulation refers to biore­
mediation that involves microorganisms and added fertilizers; rhizode­
gradation refers to degradation that occurs in the rhizosphere;
phytovolatilization refers to plants extracting metals and releasing by
volatilization process in the environment, and rhizodegradation refers to
degradation that occurs in the rhizosphere. Rhizoremediation refers to

Table 1
Bioremediation of metal pollutants using endophytes and abilities of remediation promotion.
Host Endophytes Pollutants References

Lupinus luteus Consortia of bacteria Organic pollutants and metals Leroy et al., 2017
Brassica napus Alternaria sp. CBSF68, Penicillium sp. CBRF65, Pb and Cd Chen et al., 2016
Fusarium sp. CBRF44,
Brassica juncea Genetically engineered Enterobacter sp. CBSB1 Pb and Cd Persoh, 2015
Rumex acetosa Pseudomonas sp., Microbacterium sp., Mixed heavy metals Gaiero et al., 2013
Lolium perenne Microbacterium sp Petroleum hydrocarbons Ijaz et al., 2016
Oryza sativa L., Phomopsis liquidamba Phenanthrene, phenolic acids Wang et al., 2017; Burges et al., 2016;
Sánchez et al., 2018
Leptochloa fusca (L.) Kunth Enterobacter sp. HU38, U and Pb Lemaire et al., 2012
Brassica campestris L. Mucor sp. MHR-7 Zn2+, Mn2+,Cr6+, Cu2+, Co2+ Wang et al., 2018
Alnus firma Bacillus thuringiensis GDB-1 As, Cu, Pb, Ni, and Zn Bilal et al., 2017
Populus deltoides Burkholderia fungorum DBT1 Naphthalene, phenanthrene, fluorene, and Mahmud, 2003
dibenzothiophene
Sedum plumbizincicola Achromobacter piechaudii E6S Cd, Zn, and Pb Germaine et al., 2006
Brassica napus L. Acinetobacter calcoaceticus Sasm3 Nitrate and heavy metal Ben et al., 2017
Pteris vittata Serratia marcescens PRE01 Cd(II), Cr(VI), and V(V) Kaul et al., 2016
Trifolium arvense Pseudomonas azotoformans ASS1 Cu, Zn, and Ni Toju et al., 2018
Zea mays L. Piriformospora indica Petroleum hydrocarbons Ben Said and Or, 2017
Lotus corniculatus, Oenothera Stenotrophomonas sp., and Rhodococcus sp. Hydrocarbons Kaul et al., 2016
biennis

4
P. Sharma and S. Kumar
Fig. 1. Schematic illustration of interaction between endophytic bacteria and heavy metals.
the combination of rhizospheric processes that contribute to environ­
mental remediation (Dhankher et al., 2011). Co-metabolism is the
simultaneous use of multiple contaminants with the microbial commu­
nity due to their flexible degradative capacity. Acclimatization is a phase
that has been added to the treatment of effluents in treatment plants
(Paliwal et al., 2012). Bacterial endophytes can be transferred and
distributed across different plant tissues that help in increase of
biomolecule production (García-Suárez et al., 2017). Endophytes use a
range of different techniques for the detoxification of metal polluted
effluents at the same time. Furthermore, plant growth-promoting bac­
teria can survive independently in the rhizosphere and bulk soil after
migrating from plant tissues (Feng et al., 2017). Endophytes can also be
transferred vertically to roots and play key roles in Sedum alfredii, like
improving biomass of plant, assembling the microbiome associated with
the root, and hyper-accumulation of Cd/Zn (Luo et al., 2019). Endo­
phytes boost plant development and remediation efficiency when they
co-exist within plant growth-promoting bacteria. More than one million
taxa of endophytes has been found in plants, greatly exceeding the
number of strains with phytoremediation-promoting features already
identified (Nisa et al., 2015).
6. Metabolites of endophytes
Endophytes produce enzymes and chemicals that are environmen­
tally favorable, toxic to plant infections, and do not affect humans or
other living species, either alone or in combination with the host plants.
In addition to promoting plant growth, endophytes influence the syn­
thesis of bioactive molecules with high medicinal potential. In cultivable
endophytic fungus, a substantial number of potentially high-value
bioactive chemicals with medicinal significance have been identified
(Manganyi and Ateba, 2020). This review investigated the recent
advanced approaches of endophytic microbes in industrial effluent
treatment. This section provides descriptive information about enzymes
produced by diverse microorganisms that are involved in the biodeg­
radation of a wide range of pollutants, as well as applications and rec­
ommendations for overcoming the constraints of their efficient usage.
Endophytic bacteria include Acinetobacter, Achromobacter, Bacillus,
Agrobacterium, Brevibacterium, Pseudomonas, Microbacterium, and Xan­
thomonas, among other gram-positive and gram-negative bacteria (Sun
et al., 2013). Bacterial endophytes are complex in nature, having a range
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Bioresource Technology 339 (2021) 125589
of bioactive metabolites that function as antibacterial and anticancer
chemicals, with 76% of them identified from the Streptomyces species.
Endophytes have been shown to produce a variety of bioactive metab­
olites in a single plant or microbe, making them a good source of
pharmaceuticals for treating a variety of ailments and having potential
applications in agriculture, medicine, food, and cosmetics. Steroids,
tannins, alkaloids, tetralones, xanthones, benzopyranones, chinones,
quinones, flavonoids, saponins, phenolic acids, terpenoids, and many
other secondary metabolites were classified into various functional
groups (Fig. 2) (Godstime Omojate et al., 2014).
6.1. Secretion of enzymes
Several microbes have the potential to produce lytic enzymes for the
hydrolysis of different polymeric compounds from effluents (Gao et al.,
2010). Cellulose, proteins, hemicellulose, DNA, and chitin are among
the 1,350 substances secreted by endophytic microorganisms (Tripathi
et al., 2008). Endophytes produce a variety of enzymes that assist in the
cell wall hydrolysis of the plants, allowing them to colonize the surface
of plants. Such enzymes assist in the indirect reduction of phytopatho­
gens as well as the breakdown of cell walls. Hemicellulase, chitinases,
cellulases, and 1, 3-glucanases are only a few of the several types of
enzymes. Mutagenesis of genes encoding 1, 3-glucanase in a Lysobacter
enzymogenes strain lowered biocontrol effectiveness against Pythium-
caused sugar beet tall fescue leafspot disease and damping-off disease
(Gao et al., 2010). Streptomyces produces lytic enzymes that have a
powerful anti-cacao witch’s broom disease effect (Macagnan et al.,
2008). Enzymes may not be effective as antagonizing agents on their
own, but when paired with other mechanisms, they can boost antago­
nistic activity. Pectinase has also been shown to help reduce patho­
genesis in plants (Babalola, 2007). The biodegradation of toxic
pollutants is thought to involve a large number of enzymes from bac­
teria, fungus, and plants. Microbial enzymes enable bioremediation,
which is a cost-effective and ecologically sound technology. The
research in this field can aid in the development of improved bioprocess
technology to reduce industrial effluent toxicity for decreasing soil and
water pollution (Table 2).
P. Sharma and S. Kumar
Fig. 2. Schematic diagram of endophytes interaction with plant and their role in metal detoxification.
6.2. Phytohormones production
Endophytes release phytohormones, which promote plant growth
and change the plant’s morphology and structure. The method by which
endophytes produce plant hormones is similar to the pathways by which
rhizobacteria promote plant growth. It secretes gibberellic acid, auxins,
indole acetic acid, and ethylene, which aid in plant growth (Dutta et al.,
2014). Indole acetic acid hormones stimulates seed germination, root
length, xylem growth, lateral initiation, adventitious root formation,
metabolite biosynthesis, and regulates the rate of plant development
(Gao et al., 2010). In addition, endophytic microbes produce indole
acetic acid which can enhance root length and surface area, permitting
the plant to have easy accessibility to soil nutrients. Indole acetic acid
synthesis also extends bacterium cell walls and enhances exudate
release, as well as providing additional nutrients. Indole acetic acid
formed by endophytic bacteria is identified as the major effector mole­
cule in pathogenesis, phytostimulation, and interactions between
plant–microbe (Gao and Tao, 2012). Endophytic actinomycetes produce
plant growth-promoting compounds like indole acetic acid , which has
been proven to increase the formation and elongation of plant adven­
titious roots in different studies (Shimizu, 2011).
6.3. Production of antibiotics
Endophytes have been identified to produce secondary metabolites,
some of which have antibacterial and antifungal properties that inhibit
the growth of phytopathogenic microbes (Gunatilaka, 2006). Several
studies are still being conducted to identify endophyte metabolites for
commercial use (Fadiji and Babalola, 2020). Bioactive compounds
protect plants against pathogens (Daguerre et al., 2017). Flavonoids,
peptides, quinones, alkaloids, phenols, steroids, terpenoids, and poly­
ketides have all been identified in endophytes as antimicrobial metab­
olites (Lugtenberg et al., 2016). When a large number of microbial
species co-exist in the same plant, the endophytes or the host secrete
compounds restricts the growth of harmful microbes (Kusari et al.,
2012). In some cases, the endophytes and the host plant use different
routes to boost metabolite production; others use induced metabolism to
help in metabolizing the product of the others (Ludwig-Müller, 2015).
Many endophytic strains were eventually discovered to be unable to
6
Bioresource Technology 339 (2021) 125589
produce the chemicals on their own (Heinig et al., 2013). Phomopis
cassia, an endophyte isolated from Cassia spectabilis, was able to syn­
thesize five substances that were similar to 3, 11, 12-trihydroxycada­
lene, and Cadinane sesquiterpenes, one of which produced the most
active antifungal metabolite against Cladosporium cladsporioides and
Cladosporium sphaerospermum (Silva et al., 2006).
Alkaloids have been shown to have a high antibacterial impact
against many pathogenic gram-positive bacteria. For example, alter­
setin, a new alkaloid derived from the endophyte Alternaria sp., dis­
played a strong antibacterial action against many pathogenic gram-
positive bacteria (Hellwig et al., 2002). The volatile oil is another
metabolite that has shown antibiosis. Many volatile organic compounds
were created by an endophytic fungus from tropical trees known as
Muscodor albus, including aciphyllene, 2-butanone, and 2-methyl furan,
which were claimed to have antibacterial capabilities (Atmosukarto
et al., 2005). Furthermore, fungal endophytes isolated in vitro from
Artemisia annua can suppress the growth of most phytopathogenic or­
ganisms by generating antifungal compounds, such as n-butanol and
ethyl acetate (Liu et al., 2001). Tian et al., (2017) investigated the role of
Epichlo festucae’s anti-fungal protein in the control of Sclerotinia
homoeocarpa in Festuca rubra. The strategy of plant protection used by
Paraconiothyrium strain SSM001 against harmful wood-decaying fungus
was explored and it was linked to the generation of taxol from yew trees
(Taxus spp.) (Soliman et al., 2015).
7. Perspective and challenges
Endophytic microbes are symbiotic organisms that live inside plant
tissues without causing disease symptoms in their hosts. Plant growth-
promoting features and useful functions linked with plants under
abiotic stress conditions have been examined using endophytic mi­
crobes. This analysis is highly successful in eliminating pollutants from
the industrial effluents in an environment friendly manner. Microbial
endophytes can behave as plant development promoters by supplying
plant hormones and siderophores as well as solubilizing minerals like
phosphate, potassium, and zinc. They can help plants development in
polluted soil by breaking down toxic chemicals. Through several
methods, endophytes stimulate plant growth under abiotic conditions
like salt, dehydration, heat, heavy metal stress, and nutritional stress.
P. Sharma and S. Kumar Bioresource Technology 339 (2021) 125589

Table 2 ethylene (ET), and jasmonic acid (JA). Endophytes, on the other hand,
Some endophytic microbes and their metabolic compounds to tolerate abiotic can cause resistance to disease by increasing amino acid synthesis.
stress during bioremediation process. Consequently, endophytes are considered incredibly valuable plant as­
S. Source Endophytes Metabolites References sociates having the ability to reduce yield loss by improving the host’s
No. stress tolerance in an environmentally benign manner, hence increasing
Medi- cago Phoma medicaginis Brefeldine A Weber et al., agricultural production. Endophytes are valuable bioremediation tools
lupulina, Antibacterial 2004 having a wide range of metabolic pathways. They can be used for
Medicago methane assimilation, nitrogen fixation, bioremediation of metals, and
sativa
biotransformation of chemicals, such as propylene to epoxypropane, and
2. Edenia Chaetomium Naphthoquinone Macias-
gomezpompae acuminata spiroketal Rubalcava the production of chiral alcohols. This review was aimed to show how
et al., 2008 the endophytes system may be used in the bioremediation of metals
3. Excoecaria Penicillium Polyphenols, Lu et al., from industrial effluent as a way to mitigate environmental problems
agallocha expansum expansols A & B 2010 without removing polluted soil and dispose it of elsewhere.
4. Niphates Curvularia lunata Cytoskyrins Brady et al.,
olemda 2000,
Jadulco 8. Conclusions
et al., 2002
5. Paullinia Muscodor vitigenus Naphthalene Strobel et al., This review summarises the current scientific advances in using
paullinioides 2007
biotechnological methods for the detoxification of industrial effluents
6. Cinnamomum Muscodor albus Colatile organic Ezra et al.,
zeylanicum compounds 2004 employing endophyte-assisted bioremediation for the prevention of
7. Medi- cago Phoma medicaginis Brefeldine A Weber et al., environmental pollution. Although highly effective microbes are re­
lupulina, 2004 ported for several applications, the beneficial potential of endophytes
Medicago
bacteria in the field of bioremediation remains untouched. Emerging
sativa
8. – Streptomyces laceyi Fatty acid Singh and bioremediation strategies using endophytic bacteria, biological thera­
MS53 derivatives Dubey, 2018 pies to pollutants, rhizome interaction, and heavy metal detoxification
9. Mangifera Aspergillus Dihydropyran and Nuraini are proven to be viable ways for cleaning up the polluted environment.
casturi Kosterm minisclerotigens 4H-Pyran-4-one, et al., 2019
AKF1 and 5-hydroxy-2-
Aspergillus oryzae (hydroxymethyl- CRediT authorship contribution statement
DK7 (CAS) Kojic acid
10. Tragia Penicillium L-ascorbic acid Danagoudar Pooja Sharma: Conceptualization, Methodology, Writing – original
involucrata citrinum CGJ-C1, et al., 2018 draft. Sunil Kumar: Writing – review & editing, Supervision.
Linn P. citrinum CGJ-
C2, Cladosporium
sp. CGJ-D1, and Declaration of Competing Interest
Cryptendoxyla
hypophloia CGJ-D2
11. Adiantum Chaetomium Phenolic Selim et al., The authors declare that they have no known competing financial
capillus EtOAc globosum compound 2018 interests or personal relationships that could have appeared to influence
extract the work reported in this paper.
12. Combretum Methylobacterium EtOAc extract, Photolo
erythrophyllum radiotolerans Chloroform et al., 2020
MAMP 4754 extract Acknowledgments

The authors acknowledge the support extended by the Director,

Endophytes enhance clean-up through mutual interactions that benefit
both the organisms when used on a large basis. This method has been
recently proven to be more effective than the plant on its own for
remediation activities. Under the protection of plants, endophytes
participate in the deposition or degradation of toxic substances.
Endophytes-assisted bioremediation has various advantages, such as the
ability to counteract abiotic stressors, particularly soil pollutants,
resulting in increased global crop production and organic farming.
Endophytic bacteria have received a lot of interest because of their ca­
pacity to improve plant response to stressors. Various studies have
shown that endophytes improve plant resistance to salinity, salt,
nutrient deficiency, diseases, and this evidence was subsequently inte­
grated into a meta-analysis of available research. Mineralization of
organic phosphorus compounds are immobilized like potassium and
phosphorus minerals using endophytes. Nitrogen fixation is a type of
nutrient uptake method in which two or more endophytic microbial
communities live together. Some of the phytohormones like auxins,
cytokinins, and gibberellins aminocyclopropane-1-carboxylic acid
deaminase synthesized by endophytes.
Endophytes were shown to affect host efficiency during stress by
modifying the soil’s reaction to changes in the environment. It can
function as a boundary to harmful germs and also interact with them.
Induced systemic resistance can help to sustain plant health while also
assisting in the enhancement of growth and yields. Endophyte-mediated
enhanced resistance necessitates the signaling of salicylic acid (SA),
CSIR-NEERI, Nagpur (India) to perform this review. The authors grate­
fully acknowledge all the anonymous reviewers and Editor-in-Chief for
their valuable comments and suggestion on the earlier version of this
paper.
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