Pedosphere 28(2): 170–189, 2018

doi:10.1016/S1002-0160(18)60018-9
ISSN 1002-0160/CN 32-1315/P
⃝c 2018 Soil Science Society of China
Published by Elsevier B.V. and Science Press

Biosurfactants as a Biological Tool to Increase Micronutrient

Availability in Soil: A Review

Ratan SINGH1 , Bernard R. GLICK2 and Dheeraj RATHORE1,∗

1 School of Environment and Sustainable Development, Central University of Gujarat, Gandhinagar 382030 (India)
2 Department of Biology, University of Waterloo, Ontario N2L 3G1 (Canada)
(Received November 12, 2017; revised January 7, 2018)

ABSTRACT
Addressing micronutrient deficiencies in agricultural soils to meet the growing demands of crops is a matter of great concern
worldwide. The use of biosurfactant, a multifunctional microbial metabolite, to enhance nutrient availability may be a sustainable
way of enhancing agricultural productivity. Biosurfactants are generally less toxic than synthetic surfactants. The application of
biosurfactants in agricultural soils is anticipated to improve nutrient status, increase wettability, and achieve a more even dissemination
of complex nutrients. Numerous studies have evaluated the influence of biosurfactants on bioremediation, antimicrobial activity, and
soil flushing efficiency. This manuscript reviews the possibility of employing biosurfactants to mobilize and solubilize soil nutrients
and make them available to plants through the formation of metal-biosurfactant complexes. Although significant progress regarding
an explanation of the mechanisms behind many biosurfactant-induced effects has been made, there are still many aspects of this area
that are not sufficiently elucidated, such as differences in specificity for nutrients (e.g., Cu, Fe, Mn, and Zn) and toxins (e.g., Cd and
Pb). Biosurfactants from various isolates have been considered for their potential role in plant growth promotion and other applications
related to improving the effectiveness of agricultural soils.
Key Words: critical micelle concentration, micelle formation, microbial metabolite, microbial isolate, micronutrient deficiency, soil
metal bioavailability

Citation: Singh R, Glick B R, Rathore D. 2018. Biosurfactants as a biological tool to increase micronutrient availability in soil: A
review. Pedosphere. 28(2): 170–189.

INTRODUCTION
Micronutrients are essential substances that are re-
quired in small amounts for human and plant health
(Miller and Welch, 2013). Micronutrients are also
known as minor components or trace elements, but the
term micronutrient is supported by the American Soci-
ety of Agronomy and the Soil Science Society of Ame-
rica (Dubey, 2011). The micronutrients include boron
(B), copper (Cu), iron (Fe), chloride (Cl), manganese
(Mn), molybdenum (Mo), nickel (Ni), and zinc (Zn)
(Hänsch and Mendel, 2009).
Micronutrient deficiencies are a major global pro-
blem for soils/plants that affects both food production
and human health. Typically, deficiencies of Fe, Mn,
and Cu are less extensive than that of Zn (Imtiaz et
al., 2010). In an examination of soils from several In-
dian states, Fe deficiency was observed to be the grea-
test in Haryana (26%) followed by Tamil Nadu (18%),
Punjab (12%), Gujarat (8%), and Uttar Pradesh (9%)
(Rajamani, 2014). In addition to India, other coun-
tries such as Australia and China are also facing a soil
micronutrient deficiency problem. This widespread mi-
cronutrient deficiency problem increases the challenge
that worldwide agriculture is facing of adequately fee-
ding and supplying healthy food for people of over 7
billion, a number which is expected to reach over 9
billion by 2050 (FAO, 2011). Such an expansion in
the human population intensifies the pressure for in-
creased food production (Baligar and Fageria, 2015;
Glick, 2015). If the essential nutrients required for
agriculture cannot be supplied in sufficient amounts,
this will result in the development of widespread hu-
man malnutrition (Miller and Welch, 2013). Micronu-
trients are used by plant physiological process in very
small amounts, but are nevertheless important in plant
growth and development and crop production (Shukla
et al., 2014). These nutrients support biological pro-
cesses such as protein synthesis, gene expression, au-
xin metabolism, maintenance of biological membranes,
and protection against photooxidative damage, heat
stress and disease. Thus, insufficient nutrients negati-

∗ Corresponding author. Email: dheeraj.rathore@cug.ac.in.

BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY
vely affect crop yield, food quality, and human health
(Alloway, 2004; Yang et al., 2007; Das and Green,
2013). The abilities of different plants to take up in-
dividual micronutrients from the soil vary, notwith-
standing micronutrient concentrations in plants re-
flect the nutrient status of the soils where the plant
are grown (Knez and Graham, 2013). Successful agri-
culture therefore requires that soils contain suffici-
ent levels of key micronutrients (Knez and Graham,
2013). Inadequate levels of soil micronutrients have re-
cently increased significantly in many localities due to
the use of continuous cropping systems and decreased
applications of organic matter (such as bioslurry and
farmyard manure) in favor of chemical fertilizers, which
can degrade the physical, chemical, and biological sta-
tus of top soils (Fageria et al., 2003, 2007).
The presence of micronutrients in soil does not
mean that plants will grow and develop well because
some of the micronutrients may be tightly bound to
soil particles and therefore unavailable to the plants
(Knez and Graham, 2013). Manufactured chemical fer-
tilizers are typically soluble and fast acting. They con-
tain high-analysis materials, have a high level of plant
nutrients with few impurities, have a quick response
in the field, and are typically highly soluble in water
(Siegel et al., 1962; Silva, 2000). However, manufac-
tured fertilizers can become inactive in alkaline soil
and therefore unable to be absorbed by plants (Os-
man, 2013). In an effort to overcome this problem,
many chemical solutions have been tested for the a-
bility to decrease the binding of ionic micronutrients
to soil particles and thereby enhance their availability
to plants. In this regard, the solubility and disintegra-
tion energy of soil particles rely upon their surface area
(Milani et al., 2015). The availability of micronutrients
in soil depends on their solubility and their ability to be
mobilized (Chatzistathis, 2014). In this regard, there
are many soil factors affecting the solubility of mi-
cronutrients and their accessibility for plants, including
soil type, texture, moisture, temperature, pH, organic
matter, calcium carbonate, cation exchange capacity
(CEC), and structure (Schoonover and Crim, 2015).
Chelates or chemically synthesized surfactants are
typically used in soil washing; they are often a chemical
complex that is lipid in nature in which the metals are
held so tightly that it is easily taken up by plant roots
(Sahoo, 2007). Unfortunately, chemically synthesized
surfactants/chelators are often toxic, and many are
able to persist in the environment for a long time (Jes-
sop et al., 2015). On the other hand, there are many
naturally occurring chelating/complexion/solubilizing
agents that are produced by living organisms (plants
171
and microbes), e.g., biosurfactant, a multifunctional
microbial metabolite, and have been described as green
surfactants owing to the perception of them being en-
vironmentally friendly and biodegradable (Sinha et al.,
2008). Biosurfactants have the potential to enhance
metal bioavailability in soils (Mulligan et al., 2001),
and compared to synthetic surfactants, they can have
higher foaming, higher selectivity, and higher speci-
fic activity at elevated temperatures, pH, and salinity
(Desai and Banat, 1997; Makkar and Cameotra, 1997;
Brennan and Shelley, 1999). At the critical micelle con-
centration (CMC), biosurfactants decrease the surface
tension, increase the solubility and mobility of ionic
metals, and enhance the micronutrient availability in
soil (Pacwa-Plociniczak et al., 2011). There are very
few published reports on the use of biosurfactants in
agriculture, and therefore more detailed study is re-
quired to evaluate their potential. This review exa-
mines the role, application, and effects of biosurfac-
tants on micronutrient solubility, availability, and up-
take in plants and their potential to resolve the prob-
lems of micronutrient deficiency in soil.
SOURCES OF MICRONUTRIENTS IN SOIL
Methods of providing micronutrients to plants typi-
cally include the use of organic matters such as grass
clippings, tree leaves, and green manure (Welch et al.,
1991; Sekhon, 2003) (http://www.ncagr.gov). Howe-
ver, a more complete list of sources is as follows.
Natural sources
Geologic parent material or rock outcroppings
(Morales, 1974), volcanoes (Seaward and Richardson,
1989), and forest and prairie fires are natural sources
of micronutrients in soil. The micronutrients in the soil
and their availability to plants are determined by the
minerals contained in the original parent material and
by the weathering processes that have taken place over
the years (Wuana and Okieimen, 2011).
Agricultural sources
Manures are a common source of micronutrients
in soil (Wuana and Okieimen, 2011). Incorporation
of the following amendments enhance the macro/mi-
cronutrient supplement contents in soil: compost, crop
residues, silage juice, ruined remains of crops and
plants, wash water, beddings, spent mushroom media,
spent soilless media, and spent supplement solutions
(https://www.bcac.bc.ca) (Zu et al., 2005).
Industrial sources
In India, land around the cities receives sewage wa-
172
ters containing both domestic and industrial wastes.
These wastes can be suitable for crops that are to be
cooked, provided that the content of major plant nutri-
ents is high, that the content of toxic elements is low,
and importantly, that any sewage has been treated to
reduce pathogen load-associated risks to human health
(Subramani et al., 2014). Sewage effluents are typically
rich in plant nutrients. However, the buildup of heavy
metals, particularly Zn, Cu and Ni, in sewage-irrigated
soils needs to be monitored periodically in view of their
significant accumulation in bioavailable pool associated
with decline in pH (Rattan et al., 2005).
Domestic effluents
Effluents from domestic waste/municipal sewage
treatment plants often contain high levels of nutrients
that potentially could be used for plant growth (Ta-
ble I). Agricultural processing of effluents could pro-
vide water and nutrients for crop production (Cham-
bers et al., 2002); the nutrient-enriched sewage ef-
fluent could substantially reduce the use of chemi-
cal fertilizers (Wang and Tao, 1998; Ladwani et al.,
2012). Sewage effluent, in addition to being a source
of irrigation water, is a potential source of micronutri-
ents for plants; consequently effluent application can
increase the concentration of micro- and macronutri-
ents in soil (Asgharipour and Reza Azizmoghaddam,
2012).
DEFICIENCY STATUS OF MICRONUTRIENTS IN
SOIL AND ITS IMPACTS
It is estimated that the more than 3 billion peo-
ple worldwide suffer from nutrient deficiency (Monre-
al et al., 2015). Deficiencies of micronutrients in soil
and plant are a global nutritional problem and are
prevalent in many countries (Cakmak, 2002; Imtiaz et
al., 2010). Iron deficiency generally occurs in citrus or-
chards and sugarcane plants grown on calcareous soils,
and Mn deficiency is generally observed in plantation
crops such as cardamom and tobacco. These deficien-
cies occur due to specific soil and climatic conditions
existing at the time of crop growth, substantially af-
fecting the crop yield.
Despite adequate soil preparation, watering, and
mulching, if plants fail to grow or multiply, it can be
a sign of multiple nutrient deficiencies in soil/plant.
Jyothi (2014) compile the data for survey and analysis
of more than 250 000 soil samples in 20 Indian states
(Table II). Micronutrient deficiencies in humans result
in anemia, decrease immunity, decrease resistance to
infection, impede growth and development of the ner-
R. SINGH et al.
vous system, and increase susceptibility to other disea-
ses which slow the growth of children (Swaminathan et
al., 2013).
It is well known that micronutrient deficiencies in
agriculture soil affect the growth of plants and the nu-
trient levels of crops. Micronutrients related to agricu-
lture not only are essential for crops, but also affect
livestock (Knez and Graham, 2013). Micronutrient de-
ficiencies in agricultural soils have become a major con-
straint to the soil efficiency, stability, and sustainabili-
ty (Bell and Dell, 2008; Kumar and Babel, 2011). The
percentages of agricultural soils suffering nutrient de-
ficiencies have been estimated at 49% for Zn, 31% for
B, 15% for Mo, 14% for Cu, 10% for Mn, and 3% for Fe
(Cakmak, 2002; Alloway, 2004; Graham, 2008). In this
regard, nearly 50% of the world’s cultivated area sup-
ports suboptimal growth because of the lack of plant-
available Zn in the soil. Calcareous soils or high-pH
soils are prone to Zn sequestration, while sandy or ot-
her coarse soils are prone to Zn leaching (Adams and
Sun, 1971; Marschner, 2011). These basic soil charac-
teristics have been found throughout India in Bihar
(calcareous soils), Andhra Pradesh (Vertisols), Tamil
Nadu (Inceptisols), Karnataka (Alfisols), Maharashtra
(Lateritic soils), and Haryana (Aridisols), where low
crop yields have also been observed (Subba Rao et
al., 1996). High pH reduces the solubility and mobili-
ty of Zn in soils by stimulating its absorption to soil
constituents and limiting its diffusion to plant roots
(Sherene, 2010).
Systematic survey and analysis of more than 2.5
million soil samples in 20 Indian states by the All India
Coordinated Research Project indicates a deficiency to
the extent of 49% for Zn and 33% for B, with 13%,
7%, and 4% of the samples rating low in Fe, Mo, and
Mn, respectively (Shukla et al., 2015). These data re-
veal nutrient deficiencies in many soils, the seriousness
and extent of which varies over agro-ecological zones,
soil types, and, most importantly, management prac-
tices, crop yields, and cropping systems. Micronutrient
deficiencies in soil affect different living systems as de-
scribed in detail below.
Deficiency effects on plants
The deficiency of any single micronutrient in soil
can constrain plant growth and reduce yield, notwith-
standing the sufficient availability of other essential
micro- and macronutrients (Hodges, 1996). All nu-
trients have specific and essential functions in plant
metabolism (Maathuis and Diatloff, 2013). Micronutri-
ent deficiencies in soil tend to be harder to reliably de-
tect than macronutrient deficiencies, but they enhan-
TABLE I
Various industrial effluents which can be used for irrigation as sources of nutrients/micronutrients in soil

Effluent used Selected crop(s) Study Nutrients/micronutrients provided Reference

Domestic wastewater Wheat, gram, palak, Laboratory pot study N, P, K, micronutrients Singh et al. (2012)
methi, berseem
Olive mill wastewater Tomato, pea Greenhouse pot study N, P, K, Mg, Ca, organic matter Mseddi et al. (2016)
Wastewater from wastewater Mung Pot study in wire house N, P, K, Zn, Cr, Cu, Ni Yasmeen et al. (2014)
treatment facility
Drainage effluent Melon Field study N, P, K, Ca, Mg, Na, organic matter, etc. Miranda et al. (2008)
Domestic sewage effluent Sunflower, celosia Field study N, P, K, Mg, Ca, Zn, Fe, Mn, Cu Friedman et al. (2007)
Fishpond effluent Cherry tomato Field study N, P, K, Ca, Mg Castro et al. (2006)
Anaerobic baffled reactor effluent Maize Greenhouse pot study N, P, K, Na, Al, Cd, Cu, Fe, Mn, Mo, Ni, Zn, B, etc. Bame et al. (2014)
Sewage effluent Sugarcane Field study N, P, K, Mg, Ca dos Santos et al. (2016)
Wastewater from urban wastewater Winter melon Field study N, P, K, Zn, Cu, Mn, Fe, etc. Masciandaro et al. (2014)
treatment plant
Sugar mill effluent French bean Farm field study N, P, K, Na, Ca, Mg, Fe, Z, Mn, etc. Kumar and Chopra (2014)
Molasses-based distillery effluent Sugarcane Field study Na, K, N, P Srivastava et al. (2012)
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY

Distillery effluent Sugarcane ratoon Field study N, P, K, Na Kumar (2016)

Sugar mill effluent
Distillery effluent
Textile industrial wastewater
Distillery effluent
Textile sludge effluent
Textile effluent
Sugar mill effluent
Cassava-processing mill effluent
Textile dyeing effluent
Textile dyeing effluent
Agro-residue-based paper mill effluent Spinach
Sweet sorghum Field study K, Na, Ca, Mg, Cr, Mn, Cu, Zn, Fe Kumar and Chopra (2013)
Fenugreek Field study N, K, Ca, Mg, Fe, Zn, Cu, Cr, etc. Kumar and Chopra (2012)
Rice Field study N, P, K, Na, Mg, Zn, Fe, Cu, Ni, etc. Begum et al. (2011)
Cucumber, chili, onion, Laboratory germination test N, P, K, S, Cl Ramana et al. (2002)
bottle gourd, tomato in petri dishes
Soybean, cowpea Greenhouse pot study N, P, K, Zn, Fe, Co, Ni, Mn, Cr, etc. Araújo et al. (2007)
Wheat Petri plate germination and N, P, Ca, Mg, S, Cl Kaushik et al. (2005)
pot culture experiments
Radish Greenhouse pot study P, Mg, Ca, Cl, S, Fe Vijayaragavan et al. (2011)
Onion bulb Experiment in the dark Ca, Mg, Z, Fe, Mn, Cu, Ni, etc. Olorunfemi and Lolodi (2011)
at room temperature
Soybean Greenhouse pot study N, P, K, Na, Ca, S, Cl Ravi et al. (2014)
Country bean Pot experiment N, P, S, Cl, Cu, Co, Zn, Ni, Cr, etc. Hassan et al. (2013)
Field study N, P, K, Ca, Mg, Cl Kumar and Chopra (2015)
173
174
TABLE II
Extents of deficiencies of nutrients in soil for crop production
(source: Jyothi, 2014)
Nutrient Extent of deficiency
%
N 26–63
P 38–42
K 13–37
S 35–40
Zn 49
Fe 13
B 33
ce the strong development of crops, delivering hig-
her yields and harvest quality. An adequate supply
of micronutrients also increases hereditary potential of
plants. More specifically, sufficiency or deficiency of mi-
cronutrients has a significant effect on root and shoot
growth, seed viability, and food quality. Their toxicity
or insufficiency can bring about hindered development,
low yield, and even plant death.
Deficiency effects on food supply
As described previously, soil micronutrient defi-
ciencies can lead to lower crop yields (Rehm and
Schmitt, 2002; PAIS, 2012). During the past decade,
micronutrient status has been ascertained primarily
for Zn and to a lesser extent for B and Mo (Nar-
wal et al., 2013; Bailey et al., 2015). Deficiency of
Zn is widespread in Asia (Turkey, India, China, and
Indonesia), sub-Saharan Africa, and the northwestern
region of South America (Cakmak, 2002; PAIS, 2012)
(https://www.iatp.org). Modern, highly productive,
pathogen-resistant crops that also demonstrate tolera-
nce against environmental stresses such as drought and
ultraviolet (UV) rays have, since the green revolution,
dominated the food supply (WHO, 2005). Insufficien-
cies of micronutrients in soils have now turned into a
limiting factor for yield and productivity in most agri-
cultural fields around the world. Furthermore, many
food systems in developing countries cannot provide
sufficient micronutrients to meet the demands of their
citizens, especially low-income families (Khoshgoftar-
manesh et al., 2010).
Impacts of micronutrient deficiency in human
Malnutrition in human develops when micronu-
trients are not supplied through food in sufficient
amounts (Miller and Welch, 2013). Worldwide, more
than two billion people suffer from one or more mi-
cronutrient deficiencies (Popkin et al., 2012). In deve-
loping countries, micronutrient deficiencies in human
are now a massive and rapidly growing health problem,
R. SINGH et al.
especially among poor people, affecting around 40% of
the world population (Buyckx, 1993; Ramalingaswa-
mi, 1995). Welch (2002) pointed out that the Zn, Fe,
Cu, and iodine (I) deficiencies in plant and animal can
cause growth retardation, delayed skeletal and sexual
maturity, dermatitis, diarrhea, alopecia, and defects in
immune function with a resulting increase in suscep-
tibility to infection. Iron deficiency can cause nutri-
tional anaemia, problem pregnancies, stunted growth,
and lowered resistance to infections (Welch, 2002).
ACCESSIBILITY OF PLANTS TO MICRONUTRI-
ENTS
The physical and chemical properties of soils such
as soil texture, pH, CEC, anion exchange capacity
(AEC), and moisture contents are closely related to
the mobility of nutrients in soil, which increases the
availability of these nutrients to plants. Micronutri-
ent deficiencies occur not only because of insufficient
amounts present in soil, but also may occur due to
poor solubility, which may be affected by soil orga-
nic matter content, pH, adsorptive surface, texture,
and nutrient interactions (Ayele et al., 2013). Sustai-
nable productivity of an agroecosystem is determined
by soils and their physical, chemical, and biological
properties. The sustainability of soils depends on their
capacity to supply required nutrients to the develo-
ping plants; micronutrient deficiencies in soils decrease
plant strength, productivity, and (for perennials) fu-
ture sustainability (Bell and Dell, 2008). Increasing or
decreasing the range of soil pH affects the micronu-
trient availability to plants and is considered to be a
major factor for nutrient deficiency. Soils of high pH
ranges (> 6.5) may have limited nutrient availability to
plants, therefore requiring fertilizer amendment (Poh
et al., 2009). Solution theory holds that any ion in soil
solution is available to plants if their roots are capa-
ble of absorbing it (Alloway, 2004); ions must pass in-
to solution and move to plant roots by diffusion or
mass flow of water before being absorbed through sym-
plastic, apoplastic, and foliar ion pools (Foster, 1990;
Silva, 2000). Market research shows that over 90% of
farmers know that they have a problem with nutri-
ents in soil being unavailable to plants (Hodges, 1996;
Aref, 2012). Therefore, farmers generally add phospho-
rus and Zn fertilizers to agricultural soils to increase
crop productivity (López-Rayo et al., 2012; Rawashdeh
and Sala, 2013). On the other hand, these two elements
are often tied up with other compounds and become
less available to plants, which results in losses of far-
mers. Chelation/solubilization enhances the accessibi-
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY
lity of supplements in both manure and in soils (Alley
et al., 2010; Malik et al., 2012). In this way, the surfac-
tant is the most vital part of any chelating compounds.
The word surfactant means surface-active compound.
Surfactants unbind trace metals from the soil surface,
and chelating agents surround the trace metal ions and
keep them in solution. A method of sequestering mi-
cronutrients and providing them to a plant compri-
ses applying an effective amount of a plant fertilizer
comprising a surfactant composition to an area of the
plant or soil/substrate surrounding the plant (Bansi-
wal et al., 2006) and subsequent formation of coor-
dinate bonds with the micronutrients. The surfactant
then transports the micronutrients across plant mem-
branes and releases the micronutrients for use by the
plant (McLaughlin et al., 2012). Bansiwal et al. (2006)
reported surfactant-modified zeolite as a carrier for fer-
tilizer and for the slow release of phosphate. Zeolite
was modified by the addition of hexadecyltrimethylam-
monium bromide, a cationic surfactant, to modify its
surface to increase its capacity to retain anions (e.g.,
phosphate, PO3− 4 ).
GENERAL DESCRIPTION OF SURFACTANTS
Compounds that decrease the surface tension of a
fluid and the pressure at the interface between two flu-
ids or between a fluid and solid are known as surfac-
tants. These are usually amphiphilic organic compo-
unds containing hydrophobic tails and hydrophilic
heads (Fig. 1). The basic structure of a surfactant
contains hydrophilic (water-soluble) and hydrophobic
(water-insoluble) components, which is achieved using
mono-, di-, and polysaccharides and unsaturated and
saturated fatty acids, respectively. The ability of a
surfactant to develop micelles in solution through the
monomers gives detergent and solubilizing properties
to the surfactant in metal-deficient soil, which can be
formed in four different types according to the condi-
tion, i.e., normal, reverse, liposomic, and mixed mi-
celles (Fig. 1).
Surfactants can be categorized into synthetic sur-
factants and biosurfactants. Synthetic surfactants are
TABLE III
Ionic properties of some synthetic surfactants
Synthetic surfactant
Tween-80
Sodium dodecyl sulphate (SDS)
Cetyltrimethylammonium bromide (CTAB)
Triton X-100
Zwitterionic geminia)
a) Surfactants that are composed of two hydrophilic and two hydrophobic groups (Molinaro et al., 2002).
175
Fig. 1 Surfactant/biosurfactant monomers corresponding to
their ionic properties, nonionic (1), anionic (2), cationic (3), and
zwitterionic gemini (4) surfactants (a), and different types of
micelle formations by aggregation of biosurfactant monomers,
reverse (1), normal (2), mixed (3), and liposomic (4) micelles
(b).
manually chemically synthesized, and biosurfactants
are biologically synthesized.
Synthetic surfactants and their environmental hazards
Synthetic surfactants are classified into three ty-
pes: anionic (the polar group is usually either sulphate,
sulphonate, or carboxylate), cationic (the polar group
is a quaternary ammonium ion), and nonionic (the
polar group is polyoxyethylene, sucrose, or polypep-
tide). The hydrophobic chains of these three types
of synthetic surfactants include olefins, alkylphenols,
paraffins, and alcohols (Volkering et al., 1997). The
most common synthetic surfactants which are used
in trace metal/micronutrient solubilization in soils are
sodium dodecyl sulfate (SDS) (Romanell et al., 2004;
Shin, 2004; Sun et al., 2011), Triton X-100 (TX100)
(Shin, 2004; Chang et al., 2005), cetyltrimethylammo-
nium bromide (CTAB) (Sun et al., 2011), Tween-80
(TW80) (Sun et al., 2011; Dong et al., 2013), and
sodium N-lauroyl ethylenediamine triacetate (LED3A)
(Chang et al., 2005; Qiao et al., 2016). Table III shows
the different ionic properties of some synthetic surfac-
tants.
Unfortunately, synthetic surfactants may have a
negative impact on the environment during their life-
cycle. Typically, production, formulation, use phase,
and discharge phase are counted as parts of their life-
Ionic property Reference
Nonionic Dhote et al. (2013)
Anionic Xia et al. (2009)
Cationic Mohammad et al. (2003)
Nonionic Zhang et al. (2014)
Dipolar ionic Malik et al. (2011)
176
cycle. In the first two phases (production and formula-
tion), the amounts of chemicals released or emitted
into the environment (Mungray and Kumar, 2008,
2009) may bioaccumulate, and their production pro-
cesses and byproducts can be environmentally haza-
rdous (Banat et al., 2000).
Some synthetic surfactants, e.g., linear alkylben-
zene sulphonates (LAS) and alkylphenol ethoxylates
(APE), are known to exhibit estrogen-like properties,
possibly linked to a decreasing male sperm count and
carcinogenic effects (Scott and Jones, 2000; Edwards
et al., 2003). While there is little serious risk to the en-
vironment from the commonly used anionic synthetic
surfactants, cationic synthetic surfactants are known
to be more toxic, and at present there is a lack of da-
ta on the degradation of cationic synthetic surfactants
and their fate in the environment (Scott and Jones,
2000; McGuire and Compton, 2002; Mungray and Ku-
mar, 2009). Anionic synthetic surfactants (SDS) may
change the structure of DNA or polypeptide chains as
well as the surface charge of molecules in living or-
ganisms through binding to bioactive macromolecules
such as peptides, enzymes, and DNA (Cserháti et al.,
2002; Ivanković and Hrenović, 2010). These changes
can cause modifications in biological functions to oc-
cur (Cserháti et al., 2002). Cationic synthetic sur-
factants mainly target the cytoplasmic membrane on
any microorganism present in the soil quaternary am-
monium compound (QAC) which acts to disorganize
the inner membrane through their long alkyl chains
(McDonnell and Russell, 1999). Synthetic surfactants
in the nonionic category directly bind to different pro-
tein and phospholipid membranes and hence have an-
timicrobial activity. This binding increases the perme-
ability of membrane and vesicle, resulting in loss of
low-mass molecules (Contreras et al., 2006) and ulti-
mately in cell death through the loss of ions and amino
acids (Cserháti, 1995). Nonionic and cationic synthe-
tic surfactants adsorb to soil and sediment to a greater
extent than anionic synthetic surfactants. Most sur-
factants in soil can be degraded by some species of
microorganisms; however, anaerobic conditions might
make them more persistent (Scott and Jones, 2000;
Ying, 2006). Mungray and Kumar (2008) reported that
synthetic surfactants enter the environment through
discharge of sewage effluents into surface waters and
through application of sewage sludge on land (Mungray
and Kumar, 2008, 2009). High concentrations of syn-
thetic surfactants and their byproducts are often very
toxic, and they can also alter the composition of soil
biota. Environmental risks posed by synthetic surfac-
tants and their degradation byproducts can be assessed
R. SINGH et al.
in terms of toxicity based on the comparison of the pre-
dicted environmental concentration and the predicted
no-effect concentration. Nevertheless, more toxicity da-
ta are needed for terrestrial risk assessment of synthe-
tic surfactants and their degradation products (Ying,
2006; Cirelli et al., 2008). Many synthetic surfactants
pose significant environmental risks due to their harm-
ful chemical compounds and their incomplete degrada-
tion in water and soil. Synthetic surfactants are repor-
ted to cause long-term adverse effects, while bio-based
products are more likely to degrade easily and there-
fore not pollute the environment (Ying, 2006).
Biosurfactants
The increasing demand for environmentally friend-
ly products and favourable regulatory outlook from
developed countries are some of the driving fac-
tors in the market of mannosylerythritol lipid. This
biodegradable natural surfactant obtained from mi-
crobes can be an attractive alternative to synthe-
tic surfactants in micronutrient-deficient soil (Pacwa-
Plocinicz et al., 2011; Ehrhardt et al., 2015; Mnif and
Ghribi, 2016). Therefore, there is a need to identify and
evaluate chelators/solubilizers with potentially good
micronutrient-solubilizing efficiency and environmen-
tal compatibility, i.e., biosurfactants. There are three
different types of biosurfactants (Fig. 2): i) glycolipids
(glucose + lipid), e.g., rhamnolipid and sophorolipid,
ii) lipopeptides (protein + lipid), e.g., surfactin and
mycosubtilin, and iii) phospholipids (phosphate + li-
pid), e.g., sphingomyelin and lecithin.
Biosurfactants are amphiphilic molecules that are
produced by some plants, but mostly by microorga-
nisms (bacteria, fungi, and yeasts). They are exuded
into the extracellular space and act as surface-active
agents that reduce surface and interfacial tension be-
tween individual molecules at the surface and inter-
face, respectively (Ivshina et al., 1998; Hwang et al.,
2009). Some are produced as fermentation byproducts
(Kitamoto et al., 2009). They accumulate at the in-
terface between two immiscible liquids (e.g., oil and
water), between a liquid and a solid (e.g., soil and oil)
or between two solids (e.g., soil and metal). Biosur-
factants then reduce the surface and interfacial repul-
sive forces between the two dissimilar phases and al-
low these two phases to become miscible. Interest in
biosurfactants emanates from their potential for wide
applicability and their advantages over synthetic sur-
factants (Desai and Banat, 1997; Banat et al., 2000;
Rodrigues et al., 2006; Singh et al., 2007). A large nu-
mber of different microorganisms can produce surface-
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY 177

Fig. 2 Chemical structures of some common biosurfactants, rhamnolipid and sophorolipid (glycolipid), surfactin and mycosubtilin
(lipopeptide), and sphingomyelin and lecithin (phospholipid) (Salihu et al., 2009).

active compounds that vary in their chemical proper-
ties as well as molecular size (Table IV).
Biosurfactants can be monomeric or polymeric and
particulate compounds. The most promising and ef-
fective biosurfactants at the present time are sur-
factin, a lipopeptide from Bacillus subtilis, rhamno-
lipid, a glycolipid from Pseudomonas aeruginosa, and
sophorolipid, a glycolipid from Torulopsis bombicola
(Mulligan et al., 2001). Several reviews on microbially
produced surfactants have focused on their types and
commercial potentials (Banat et al., 2000), their natu-
ral roles (Ron and Rosenberg, 2002), their applications
in sustainable development (Mulligan, 2005), their use
in the production of inexpensive compounds (Haba et
al., 2000; Dubey and Juwarkar, 2001; Nitschke et al.,
2007), and their use in medical applications (Singh and
Cameotra, 2004; Rodrigues et al., 2006). Although mi-
crobes can grow anywhere on a very wide variety of
substrates, the yield of biosurfactants depends on nu-
tritional and physical conditions provided (Haba et al.,
2000; Dubey and Juwarkar, 2001; Singh and Cameotra,
2004; Rodrigues et al., 2006; Nitschke et al., 2007).
 178

TABLE IV
Microorganisms that can produce biosurfactants and some properties of the biosurfactants produced

Microorganisms Type(s) of Biosurfactant property Reference(s)

biosurfactant
Charge CMCa) Surface Interfacial
tension tension
mg L−1 mN m−1
Torulopsis bombicola Glycolipid (sophorolipid) Nonionic/anionic 60–82 25–35 1–9 Siñeriz et al. (2001)
Pseudomonas aeruginosa Glycolipid (rhamnose lipid) Anionic 10–200 25–31 4–1 Abdel-Mawgoud et al. (2010)
Bacillus subtilis ATCC 21332 Lipoprotein Nonionic 5 27 1 Christofi and Ivshina (2002)
Bacillus licheniformis Surfactin Nonionic 0.02 25–27 <1 Kong et al. (2010)
Pseudomonas sp. DMS 2847 Glycolipid (rhamnose lipid) Anionic 19 29 11 Kosaric (2001)
Arthrobacter paraffineus Sucrose and fructose glycolipids Nonionic 3 32 16 Celiešiūtė et al. (2009)
Arthrobacteria Glycolipid Anionic 4 27 <1 Kügler et al. (2015)
Pseudomonas fluorescents Rhamnose lipid Anionic 2 23 1 Veremeichenko and Zdorovenko (2004)
Pseudomonas sp. MUB Rhamnose lipid Anionic 5 26 >2 Walia and Cameotra (2015)
Torulopsis petrophilum Glycolipid Anionic 23 30 12 Cooper and Paddock (1983), Bhardwaj et al. (2013)
Candida tropicalis Polysaccharide Anionic 12 – – Aguedo et al. (2003)
Corynebacterium lepus Corynomycolic acid Nonionic 5 – – Cooper et al. (1979), Mulligan et al. (2001)
Acinetobacter sp. HO1-N Mono- and diglycerides Nonionic 4 36 17 Singer et al. (1985), Celiešiūtė et al. (2009)
Acinetobacter calcoaceticus Rag1 Lipoheteropolysaccharide (emulsan) Anionic 18 – – Desai and Banat (1997), Rahman and Gakpe (2008)
A. calcoaceticus 2CAC Lipopeptide Nonionic 0.02–10 27 <1 Neufeld and Zajic (1984)
Candida lipolytica Liposan (mostly carbohydrate) Anionic – – – Cirigliano and Carman (1985), Rufino et al. (2014)
Candida petrophilum Peptidolipid Anionic – – – Dadrasnia and Ismail (2015)
Nocardia erythropolis Neutral lipid Anionic – – – Pirog et al. (2014)
Rhodococcus erythropolis Trehalose dimycolate Nonionic – – – Rapp et al. (1979), Niescher et al. (2006)
Corynebacterium hydrocarboclastus Polysaccharide Nonionic – – – Zajic et al. (1977)
a) CMC = critical micelle concentration at which there is a sudden increase in metal solubility in the system (Mulligan, 2005).
R. SINGH et al.
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY
BIOSURFACTANT PROPERTIES
Chemical properties of synthetic surfactants can be
similar to those of biosurfactants with regard to foa-
ming ability, emulsification, lubricity, surface tension
reduction, solubilization, etc. However, biosurfactants,
produced by microorganisms, are biodegradable and
less toxic compared to many synthetic surfactants (De-
sai and Banat, 1997; Mnif and Ghribi, 2016). They also
have better foaming properties and higher selectivity
(Edwards et al., 2003; Mulligan, 2005).
Biosurfactants are considered as very promising
biotechnological products. The use of biosurfactants
instead of synthetic surfactants in many applications
allows for high levels of specificity as well as efficien-
cy. Biosurfactants are good wetting agents and emul-
sifiers, having several advantages over synthetic sur-
factants including effectiveness over a wide range of
temperature, pH, and salinity (Kosaric, 1992; Das et
al., 2008; Pacwa-Plociniczak et al., 2011) and synthesis
under user-friendly conditions (e.g., low temperature
and pressure). Biosurfactants are described by prope-
rties including critical micelle concentration (CM-
C), hydrophilic-lipophilic equalization (HLE), chemi-
cal structure, and charge and also properties from their
biological source (Van Hamme et al., 2006). Some use-
ful properties of biosurfactants are described as follows.
Critical micelle concentration
Critical micelle concentration is the concentration
at which all of the molecules in a surfactant will exist
as micelles (even in very small quantities). Formation
of micelles needs a very low concentration in water,
and for the potential application, these micelles are
needed in a very low amount, i.e., the CMC (Barros
et al., 2007; Kumar and Lal, 2014; Ehrhardt et al.,
2015). Capacity to form micelles from monomers (esti-
mated colloidal clusters) in any liquid solution because
of the presence of hydrophilic and hydrophobic groups
in a monomer molecule in a concentrated form is also
a basic characteristic of biosurfactants (Rangel-Yagui
et al., 2005; Ying, 2006). Subsequently, the CMC is
the most critical parameter for any biosurfactant in
terms of its capability for solubilization of hydropho-
bic pollutants in contaminated soil. The wide use of
biosurfactants in different industrial fields (cosmetic,
medicinal, environmental agriculture, laundry, etc.) is
due to their tendency in various media to form micelles.
The amphiphilic nature of biosurfactant molecules
allows them to partition at surface interfaces and re-
duces surface and interfacial tension. The surface ten-
sion of water was found to be reduced even through
179
exposure to low concentrations of biosurfactants (Law
and Kunze, 1966). Biosurfactants can reduce the sur-
face tension of water from 72 to 30 mN m−1 or less
of liquid-liquid interfaces such as oil-water interfaces.
Researchers also found that biosurfactants have the a-
bility to reduce the interfacial tension to as low as 1 mN
m−1 (Mulligan, 2005). There is no further reduction in
surface or interfacial tension above the CMC. At the
CMC, the biosurfactant molecules themselves assem-
ble to form structures such as vesicles, bilayers, and
micelles. Formation of CMC is dependent on pH, ionic
strength, and temperature. Biosurfactants exhibit low
CMC with the values ranging from 0.15 to 30 mg L−1
(Desai and Banat, 1997; Pichot et al., 2013). Biosur-
factants with lower CMC values are better and more
efficient than their synthetic counterparts (Figs. 1 and
3).
Surface and interfacial tension of biosurfactants
A good surfactant can lower the surface tension
of water from 72 to 25 mN m−1 and the interfacial
tension of water/hexadecane from 40 to 1 mN m−1
(Mulligan, 2005; Muthusamy et al., 2008; Vijayakumar
and Saravanan, 2015). Biosurfactants have a struc-
ture with two different characteristics, i.e., hydrophilic
and hydrophobic, making them surface active and in-
creasing the absorbance properties, causing an inter-
face between polar and nonpolar media so that the
head aggregate is soluble in the polar and the tail in
the nonpolar medium. Surface tension is quite simi-
lar to interfacial tension in that cohesive forces are al-
so included; however, the interfacial tension involves
the adhesive forces between the liquid-liquid, liquid-
solid, and liquid-gas phases of two different substances
(Bustamante et al., 2012). Biosurfactants also may en-
hance the release of trace metals from soil through
ion exchange and electrostatic and other attractions
(Shin et al., 2005). Since rhamnolipids are negative-
ly charged, they may form metal-surfactant comple-
xes with cations (micronutrients) (Wang and Mulligan,
2004).
The movement of micronutrients in soil is main-
ly controlled by solid-liquid interfacial reactions be-
tween the surface of soil particles and the metal in soil
water. Therefore, when we deal with micronutrient-
deficient soils, it is essential to understand how trace
metals/nutrients behave at the solid-liquid interface
(Fig. 3).
Solubility and mobility of biosurfactants
Biosurfactants, through their accumulation at the
180
Fig. 3 Interrelationship between biosurfactant concentration and physical properties. Concentration of monomers in a biosurfactant
solution represents the micelle formation and its role in surface and interfacial tension reduction. CMC = critical micelle concentration
at which there is a sudden increase in metal solubility in the system (Mulligan, 2005).
immiscible fluid interfaces can reduce surface tension,
increasing the surface area of such compounds with di-
fferent degrees of polarity and allowing increased mo-
bility, bioavailability, and biodegradation (Banat et al.,
2000). Biosurfactants can be effectively used to solu-
bilize, mobilize, and increase the availability of mi-
cronutrients and trace metals in deficient soil (Maier
et al., 2001; Sheng et al., 2008). Cationic, anionic, and
nonionic surfactants contain both hydrophobic and hy-
drophilic portions, making them ideal for solubiliza-
tion of hydrophobic compounds (Georgiou et al., 1992;
Makkar and Cameotra, 2002). Different types of bio-
surfactants, low- and high-molecular-mass biosurfac-
tants, have different physical characteristics. For exam-
ple, low-molecular-mass biosurfactants lower the sur-
face and interfacial tension and are effective in solu-
bilizing metals in water and soil, as well as reducing
repulsive forces between two non-similar phases. On
the other hand, high-molecular-mass biosurfactants are
able to reduce repulsive forces between two immisci-
ble compounds through higher emulsification activity,
making it easier for them to mix (Calvo et al., 2009;
Soberón-Chávez and Maier, 2011).
Stability of biosurfactants under different environmen-
tal conditions
Most of the biosurfactants and their surface activi-
ty are resistant towards changing environmental con-
ditions such as temperature and pH (Vijayakumar and
Saravanan, 2015). McInerney et al. (1990) found that
lichenysin produced by Bacillus licheniformis is effec-
tive at a temperature of up to 50 ◦ C, over the pH range
of 4.5–9.0, and at up to 50 g L−1 NaCl or 25 g L−1
CaCl2 . In addition, a biosurfactant from Arthrobac-
R. SINGH et al.
ter protophormiae was found to be stable at 30–100
◦
C and at pH 2–12 (Singh and Cameotra, 2004; Vi-
jayakumar and Saravanan, 2015). Similarly, Sudha et
al. (2010) observed that sophorolipid production and
stability from Candida tropicalis was optimum at 30
◦
C. Moreover, the optimum temperature for bioemul-
sifier production and stability was found to be from 37
to 100 ◦ C (Jagtap et al., 2010). Below pH 7 and at
a temperature of 20 ◦ C, lipopeptide from B. subtilis
LB5a was stable after autoclaving (121 ◦ C, 20 min)
and after 6 months at 18 ◦ C; in addition, the surface
activity did not change between pH 5 and 11 and be-
tween 0% and 20% NaCl (Nitschke and Pastore, 2006;
Nitschke and Costa, 2007).
Degradability of biosurfactants
Along with increasing environmental concern a-
mong consumers, governmental legislation forces in-
dustry to search for easily biodegradable microbially
produced surfactants (Cameotra and Makkar, 1998;
Nitschke and Costa, 2007). Chemically synthesized
surfactants are generally non-biodegradable, while bi-
osurfactants such as sophorolipids, surfactins, and
arthrofactins are rapidly degradable in the environ-
ment (Hirata et al., 2009). Mohan et al. (2006) indi-
cate that microbially produced biosurfactants are ea-
sily degraded and are particularly suited for environ-
mental applications such as nutrient solubilization and
bioremediation. Conversely, Pei et al. (2009) studied
the degradation of rhamnolipids by incubation in black
loamy soil and red sandy soil for 7–8 d and concluded
that the degradation rate was slow (Pei et al., 2009;
Lima et al., 2011).
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY
Environmental friendly nature of biosurfactants
Many studies have reported ecofriendly nature of
biosurfactants through assessment of their toxicity to
various test organisms, and they are generally very low
or non-toxic products and are appropriate for phar-
maceutical, cosmetic, and food uses (Kuyukina et al.,
2007; Hwang et al., 2009; Sahnoun et al., 2014). The
properties of any biosurfactant control its suitability
for application in any environment in that it should
be low in toxicity, ecofriendly, eco-biodegradable, and
stable in nature (Bezerra de Souza Sobrinho et al.,
2013). Ivshina et al. (1998) reported that the toxici-
ty of a biosurfactant produced by Rhodococcus ruber
at the concentration that inhibits 50% of test species
(bacterium Vibrio fischeri) (inhibitory concentration,
IC50 ) is 10–100 times lower (and therefore 10–100 times
more efficient) than several commercial synthetic sur-
factants (Ivshina et al., 1998). A study suggested that
an anionic synthetic surfactant (Corexit) has a con-
centration that is lethal to 50% of test species (lethal
concentration, LC50 ) against Photobacterium phospho-
reum ten times lower than rhamnolipid, indicating
the greater toxicity of synthetic surfactant. In com-
parison to cationic synthetic surfactants (e.g., CTAB,
tetradecyltrimethylammonium bromide (TTAB), and
cetyltrimethylammonium chloride (CTAC)) and ani-
onic synthetic surfactants (e.g., SDS), biosurfactants
show much lower hemolytic activity to human erythro-
cytes (Shin et al., 2005; Mȩdrzycka et al., 2009). Beze-
rra de Souza Sobrinho et al. (2013) indicated that
the biosurfactant from Candida sphaerica UCP 0995
demonstrated no toxicity against the seeds of Brassi-
ca oleracea, Chicoria intybus, and Solanum gilo em-
ployed as bioindicators. Toxicity screening of the bio-
surfactant from Lactobacillus helveticus MRTL91 had
much lower cytotoxicity and phytotoxicity in compa-
rison to SDS (Sharma et al., 2014). Therefore, given
their much lower level of toxicity, biosurfactants are
TABLE V
Application of biosurfactants to solubilize metals and enhance their availability
Biosurfactant Microbe producing the biosurfactant
Di-rhamnolipid Pseudomonas aeruginosa BS2
Lipopeptide Bacillus sp. J119
Rhamnolipid Pseudomonas aeruginosa
NSa)
NS
NS
Saponin NS
a) NS = not specified.
181
more sustainable for use and are considerably safer to
living organisms than synthetic surfactants (Rebello et
al., 2014). However, biosurfactants are also known to
increase the mobility and bioavailability of toxic metals
such as Pb and Cd in soil (Juwarkar et al., 2007) and
uptake of Cd in grass (Gunawardana et al., 2010). Site-
specific considerations for application of biosurfactants
should therefore also include a preliminary assessment
of site history, soil heavy metal content, and underly-
ing geology in order to safeguard the environment and
human health.
BIOSURFACTANT APPLICATION FOR PLANT
NUTRIENT AVAILABILITY IN MICRONUTRIENT-
DEFICIENT SOIL
Advanced food production technology is required
to meet the food demand of the growing world popu-
lation. Worldwide, millions of hectares of arable land
are deficient in plant-available trace elements such as
Cu, Fe, Mn, and Zn (Li et al., 2013). Among the most
important risk factors for disease in low-income coun-
tries, the deficiencies of Zn and Fe are ranked the fifth
and sixth, respectively, by WHO (2002). Trace element
deficiencies affect both global food production and hu-
man nutrition and health. There are several factors
such as soil pH, CEC, salinity, organic matter, cal-
cium carbonate, and texture and climate (Schnug et
al., 1998; Stacey et al., 2007; Najafi-Ghiri et al., 2013)
that can substantially reduce the efficacy of trace ele-
ment fertilizers and thus decrease the solubility and
availability of these metals/nutrients in soil and plant.
Biosurfactants play an important role in providing mi-
cronutrients in nutrient-deficient soil; they chelate and
form complexes with trace metals, followed by adsorp-
tion, desorption, and removal of the metals from the
soil surface interfaces (Table V), resulting in increased
micronutrient concentrations and bioavailability in soil
(Abdul et al., 1990; Roy et al., 1997).
Metal(s) Plant(s) Reference
Cd, Pb – Juwarkar et al. (2007)
Pb, Cd, Cu, Tomato, maize, Sheng et al. (2008)
Ni, Zn sudangrass, canola
Cu – Venkatesh and Vedaraman (2012)
Zn, Cd Sunflower Wen et al. (2016)
Cu, Cd, Pb Perennial ryegrass Gunawardana et al. (2010)
Cd, Zn Maize, sunflower Wen et al. (2010)
Pb, Cd, Zn Italian ryegrass Zhu et al. (2015)
182 R. SINGH et al.

Biosurfactants can enhance the mobility of metals
by reducing the interfacial tension between the metals
and soil and by forming micelles (Pacwa-Plociniczak
et al., 2011). Interfacial tension is normally measured
in mN m−1 , and it is the power/force that holds two
different phases together. Under conditions of reduced
interfacial tension, biosurfactants can bind to sorbed
micronutrients directly and transfer them to the root
zone interface (Singh and Cameotra, 2004).
The use of bacterial strains capable of producing
biosurfactants is a relatively new approach increasing
the availability of micronutrients to plants (Pacwa-
Plociniczak et al., 2011). Biosurfactants and inorganic
ligands are efficient for simultaneous solubilization of
micronutrients and trace metals in soil (Olaniran et al.,
2013). Hydrophilic and hydrophobic groups are the two
basic domains of biosurfactants; therefore, biosurfac-
tants have the ability to reduce surface and interfacial
tension of two immiscible liquids as well as to enhance
the solubility of inorganic and organic components in
insoluble compounds (Bustamante et al., 2012). Glyco-
lipids are the best studied microbial surfactants for me-
tal complexes. The best-known glycolipids are rhamno-
lipid, trehalolipid, sophorolipid, and mannosylerythri-
tol lipid (Edwards et al., 2003; Thavasi, 2011). The
addition of a biosurfactant, such as a rhamnolipid, in
soil can effectively decrease the interfacial tension be-
tween solid surfaces and trace metal cations, therefore
increasing the solubility and mobility. This may also be
applicable for explaining desorption of weakly bound
trace metals/micronutrients from solid surfaces of soil
(Wang and Mulligan, 2004). Biosurfactants are able to
increase the availability of metals such as Zn, Mn, Cu,
and Fe in soil to plants in various ways. According
to Le Chatelier’s principle, biosurfactants can chelate
and form a complex with ionic and nonionic metals and
then release them from soil (Miller, 1995). With ani-
onic characteristics, biosurfactants can form comple-
xes with positively charged metals. This offers the op-
portunity to use biosurfactants as metal-sequestering
agents permitting metal desorption from soil and con-
taminated water. Interestingly, as suggested by Pacwa-
Plociniczak et al. (2011), the electrostatic interactions
between the positively charged metal and the nega-
tively charged surfactant is so strong that flushing wa-
ter through soil removes the surfactant-metal complex
from the soil. This is because the polar head group of
micelles can bind metals, thereby mobilizing the me-
tals in water (Fig. 4) (Mnif and Ghribi, 2015).
Microbially produced surfactants confer a wide
range of properties including the ability to lower sur-
face and interfacial tension of liquids and the formation
of micelles and microemulsions between two different
phases (Banat et al., 2010). This also enhances the bio-

Fig. 4 Impact of micronutrient deficiency on plant growth and soil quality on a micronutrient-deficient soil (a) and mechanisms
of biosurfactant application enhancing micronutrient availability in micronutrient-deficient soil to the plant, soil quality, and related
water quality through increasing nutrient solubility at a fixed concentration of biosurfactant molecule (modified from Mao et al., 2015)
(b). CMC = critical micelle concentration at which there is a sudden increase in metal solubility in the system (Mulligan, 2005).
BIOSURFACTANTS AND SOIL MICRONUTRIENT AVAILABILITY
availability of the products which helps to increase the
availability of micronutrients and metals from soil to
plant (Fig. 4). Therefore, biosurfactant-enhanced solu-
bility of trace elements has potential applications in
agriculture (Bezza et al., 2015). Soil alkalinity is one
of the major causes of micronutrient deficiency in soil.
In this case, biosurfactants help to unbind the metals
from the soil complex and form new bioavailable metal-
biosurfactant complexes (Rufino et al., 2011).
The method of increasing the uptake of micronu-
trients by a plant through application of biosurfac-
tants to the soil surrounding the plants root may be a
useful tool in developing sustainable agriculture. Ionic
biosurfactants in trace metal/micronutrient-deficient
soil can create metal-biosurfactant complexes. These
bonds are stronger than the metal bonds with soil, and
metal-biosurfactant complexes are desorbed from the
soil matrix to the soil solution due to the lowering of
the interfacial tension by which trace metals become
readily available to plant roots (Gregory, 2006; Pacwa-
Plociniczak et al., 2011). One of the more common
ways of delivering the appropriate metal micronutri-
ent has been to form a chelated complex of the me-
tal ion with surfactant/biosurfactant or any synthetic
chelants as this maintains the metal ion in a soluble
form for ease of application and reduces metal adsorp-
tion and fixation in soil (McLaughlin et al., 2012). The
efficiency and availability of micronutrient in soil (to
plants) might be increased, either by the bioaugmenta-
tion of biosurfactant-producing bacteria or through a-
mendments of biosurfactants in micronutrient-deficient
soil. Several studies have reported the bioaugmenta-
tion of potential bacteria in soil for improving plant
growth and soil quality (Singh et al., 2011). For exam-
ple, Sheng et al. (2008) investigated a biosurfactant-
producing Bacillus sp. strain J119 for its ability to pro-
mote plant growth and trace metal uptake in canola,
maize, sudangrass, and tomato. In addition, Stacey
et al. (2007) investigated the formation and plant up-
take of lipophilic metal-rhamnolipid complexes. In this
case, monorhamnosyl and dirhamnosyl rhamnolipids
formed lipophilic complexes with Cu, Mn, and Zn, fa-
cilitating the uptake of these metals by Brassica napus
and Triticum durum roots.
CONCLUSIONS
Soil fertility is one of the most important factors
controlling the yields of crops. The characterization
of soil fertility status is important for sustainable and
productive agriculture. Use of biosurfactant, a multi-
functional microbial metabolite, is an approach that
183
can increase nutrient availability thereby facilitating
success in agriculture, provided that the mobility of
toxic elements such as Cd, Pb, and Ni are also consi-
dered. To enhance micronutrient availability from de-
ficient sites there are several advantages of using of bio-
surfactants over synthetic surfactants: biosurfactants
are biodegradable, cost effective, and of low toxicity
and can be produced from renewable resources at low
cost. Biosurfactants increase the availability of metals/
micronutrients from soil columns through solubiliza-
tion. Bonds formed between anionic biosurfactants and
cationic metals are strong, and the resultant complexes
are readily taken up by plant roots. In short, biosurfac-
tants are capable of enhancing the nutrient/trace metal
mobility in soil through reduction of surface and in-
terfacial tension and micelle formation. Currently, the
increased interest in the application of biosurfactants
is due to their potential use in industry and in the field
as a replacement for synthetic surfactants. Biosurfac-
tants exhibit greater emulsification, foaming, and sur-
face activity properties than synthetic surfactants. In
addition, biosurfactants are stable over a wider range
of environmental conditions compared to synthetic sur-
factants, including pH, temperature, moisture, and
salinity. Thus, the potential role and application of bio-
surfactants in agriculture is promising although addi-
tional research is required in nutrient-deficient soil for
sustainable agriculture.
ACKNOWLEDGEMENT
The first author Miss Ratan Singh is thankful to
the Ministry of Human Resource and Development
(MHRD), India, for granting a fellowship (No. RGNF-
2012-13DGEN-UTT-56466).
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