Journal of Geochemical Exploration 174 (2017) 5965

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Journal of Geochemical Exploration

journal homepage: www.elsevier.com/locate/gexplo

Halophilic bacteria mediated phytoremediation of salt-affected soils

cultivated with rice
Gulmeena Shah a, Mehmood Jan a, Mehvish Afreen b, Muhammad Anees b, Shaq Rehman c, M.K. Daud a,
Ijaz Malook a, Muhammad Jamil a,
a
Department of Biotechnology and Genetic Engineering, Kohat University of Science and Technology, Kohat 26000, Pakistan
b
Department of Microbiology, Kohat University of Science and Technology, Kohat 26000, Pakistan
c
Department of Botany, Kohat University of Science and Technology, Kohat 26000, Pakistan

a r t i c l e i n f o a b s t r a c t

Article history: Salinity is a most important ecological constraint for cereal crop including rice nowadays. Phytoremediation has
Received 3 December 2015 been used to remediate salt affected soil but the use of halophilic bacteria is limited. In this study, the salt resistant
Revised 29 February 2016 Thalassobacillus denorans (NCCP-58) and Oceanobacillus kapialis (NCCP (National Culture Collection of Pakistan) -
Accepted 15 March 2016
76), halophilic bacteria isolated from salt mines near Karak, Pakistan were used to evaluate its effect on rice va-
Available online 16 March 2016
riety (Basmati-385)in soil contaminated with different concentrations (control, 50, 100 and 150 mM) of NaCl. It
Keywords:
has been observed that signicant increase in germination percentage and germination rate occurred in seeds
Phytoremediation primed with bacterial strains as compared to non-primed seeds. Root and shoot lengths were more in plants
Halophilic bacteria raised from primed seeds than non-treated seeds. Plants raised from inoculated seeds showed a signicant in-
Oryza sativa L. crease in fresh and dry weight of seedling after 15 days. Signicant increase in photosynthetic pigment; chloro-
Plant growth phyll a (Chl a), chlorophyll b (Chl b) and carotenoid contents occurred in 28 days old plants inoculated with
Salinity bacterial strains under different saline conditions. Similarly signicant increase occurred in total nitrogen and
protein contents in inoculated plants. Ca+2 and K+ ion concentration signicantly increased while Na+ ion con-
centration decreased in plants inoculated with bacterial strains as compared to non-inoculated plants under dif-
ferent saline conditions. Bacterial strains O. Kapialis (NCCP-76) was more responsive in term of physiological and
biochemical parameters than T. denorans sp. (NCCP-58). The corresponding strains have a positive effect in alle-
viating the salt stress in plants growing in saline condition.
2016 Elsevier B.V. All rights reserved.

1. Introduction
Rice production is badly affected by abiotic stresses which result in
physio-chemical changes in the qualitative and quantitative environ-
ments of rice (Ferrero et al., 2001; Caliskon, 2009). In Pakistan, more
than 64% of its area is salt affected (Afzal et al., 2005). Day by day, salin-
ity is going a wide spread problem all over the world in the agricultural
eld which causes reduction in growth and yield (Ashraf, 2009). Salinity
affects all stages of growth and development of rice plant and the crop
responses to salt stress vary with growth stages, concentration and
duration of exposure to salt (Michael et al., 2004).
In the last few years, a number of plant growth promoting
rhizobacteria (PGPRs) have been identied and seen an increased in de-
mand because of its role in plant growth. PGPRs were reported to facil-
itate the growth of various plant species, particularly under biotic and
abiotic stress conditions such as phytopathogens, ooding, heavy
Corresponding author at: Department of Biotechnology and Genetic Engineering,
Kohat University of Science & Technology, Kohat 26000, Pakistan.
E-mail address: dr.jamil@kust.edu.pk (M. Jamil).
metals, drought and salinity (Kloepper et al., 1989; Joseph et al., 2007;
Mayak et al., 2004). They mainly contributed in increased uptake of ni-
trogen, phytohormone synthesis, mineral solubilization such as phos-
phorus, and production of siderophores that chelate iron and make it
accessible to the plant root (Glick et al., 1995). They are also able to sol-
ubilize inorganic and organic phosphates in soil (Liu et al., 1992).
These PGPRs can produce bacterial exopolysaccharides (EPS) which
bind in the root zone, decreased the Na uptake and thus help in alleviat-
ing salt stress (Han and Lee, 2005). Inoculation of crop plants with cer-
tain strains of PGPRs improves the percentage of seed germination
(Kaymak et al., 2008; Mishra et al., 2010), plant vigor, chlorophyll
content, yield, and nutrient uptake by variety of mechanisms under
salt stress condition (Saharan and Nehra, 2011).
The increased level of salt in soil has serious effects on plants such as
rice, which serves as staple food for the majority of the world's popula-
tion. Conventional methods to remove salt from soil are expensive and
also destroy the soil structure. Phytoremediation is a technique that is
used to mitigate organic or inorganic contaminants in soils. The use of
rhizobacteria in phytoremediation of soil contaminated with organic
or inorganic metals has recently received more attention but the use

http://dx.doi.org/10.1016/j.gexplo.2016.03.011
0375-6742/ 2016 Elsevier B.V. All rights reserved.
60 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965

2.4. Pot experiment

After one week of germination in distilled water, seedlings were

shifted to sand culture in plastic pots and irrigated with Hoagland solu-
tion for 3 weeks. After 3 weeks, NaCl at different concentrations i.e. con-
trol, 50, 100 and 150 mM were given along with PGPRs (10 ml) per pot
to the fully growing plants for one week (Chanwav and Nelson, 1990).
After one week of stress, the plants were harvested for different physi-
ological and biochemical tests.

2.5. Cell membrane stability

The cell membrane stability was calculated by using the formula rec-
ommended by Jamil et al. (2009).

2.6. Determination of chlorophyll and carotenoids

The chlorophyll and carotenoid contents were calculated by using

the formula suggested by Lichtenthaler and Wellburn (1985).

Fig. 1. Germination (a) and germination rate (b) of seeds inoculated with halophilic
bacterial strains NCCP-76 and NCCP-58 under various saline conditions.

of halophilic bacteria in phytoremediation is limited. Therefore the

present experiment was designed to assess the effects of halophilic
bacteria namely Thalassobacillus devorans (NCCP-58) and Oceanobacillus
kapialis (NCCP-76) in remediation of salt-affected soils cultivated with
rice using different physiological and biochemical characteristics.

2. Materials and methods

Seeds of Basmati-385 were obtained from the National Agriculture

Research Center (NARC) Islamabad, Pakistan. Seeds were surface steril-
ized in 3.5% NaOCl solution for 3 min.

2.1. Colony formulating unit (CFU)

Thalasso bacillus sp. (NCCP-58) and Oceano bacillus sp. (NCCP-76)

were isolated from salt mines near Karak, Pakistan (Roohi et al., 2012)
and grown in L.B. media, incubated at 37 C for 24 h.

2.2. Bio-priming

Two strains of Bacillus (T. devorans sp. NCCP-58) and (O. Kapialis sp.
NCCP-76) were cultured in L.B. broth for 24 h at 37 C. Seeds were
bio-primed in broth at 37 C for 30 min in the presence of 2% sucrose
for adhesion of bacteria with seeds.

2.3. Seed germination

Bio-primed seeds were grown on nutrient agar media in Petri plates,

having a different NaCl solution (Control, 50, 100, and 150 mM), sealed
with paralm to prevent contamination. Seed germination was evaluat-
ed after every 12 h up to 5 days. After 15 days of germination, root and
shoot lengths were measured. Root and shoot were dried at 80 C in an Fig. 2. Seedlings growth of rice plant treated with distilled water (A), NCCP-76 (B) and
incubator for 2 days to take dry weights. NCCP-58 (C) under different NaCl concentrations.
 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965 61

Fig. 3. Shoot (a) and root (b) lengths of plants raised from seeds inoculated with halophilic
bacterial strains NCCP-76 and NCCP-58 under various saline condition.
2.7. Determination of total organic nitrogen and protein content
The protein and nitrogen contents were calculated by using the
equations suggested by Pellett and Young (1980).
Fig. 4. Fresh shoot (a) and root (b) weights of plants raised from seeds inoculated with
halophilic bacterial strains NCCP-76 and NCCP-58 under various saline conditions.
(NCCP-76) had more length as compared to control and other NaCl
treatments (Fig. 3). There was a remarkable decreased in non-bio-
primed seedling of fresh and dry weights of root and shoot when com-
pared with bio-primed seedlings of both the strains (Figs. 4 and 5). The
plant raised from seed inoculated with NCCP-76 had more fresh and dry
weights than control.

2.8. Ion analysis

Plant materials (25 mg dried) were digested with the help of H2SO4
and H2O2 (2:1). Then the digested material was diluted with 20 ml of
distilled water. The Na, K and Ca ion concentrations were estimated
with the help of a ame photometer (jenway pf7f).

2.9. Data analysis

Analysis of variance was performed using the Statistix 9 software.

Mean values for different rice characteristics were compared via LSD
test (Li, 1964).

3. Results

3.1. Physiological parameters

A decrease occurred in seed germination and germination rate with

increasing NaCl concentration from 50 to 150 mM, while bio-primed
seeds with both bacterial strains (NCCP-76 and NCCP-58) had higher
seed germination and germination rates as compared to untreated
seeds. However, seeds treated with NCCP-76 had more seed germina-
tion than NCCP-58 (Fig. 1). A gradual decrease occurred in rice seedling
as the NaCl concentration increases from 50 to 150 mM while seedling
raised from seeds treated with bacterial strains had more seedling
length (Fig. 2).
A considerable decrease was observed in root and shoot lengths as
the salinity level increased but seedling raised from seeds inoculated
with bacterial strain had more root and shoot lengths. In roots, at Fig. 5. Dry shoot (a) and root (b) weights of plants raised from seeds inoculated with
100 mM the plants raised from bio-primed seeds with bacterial strain halophilic bacterial strains NCCP-76 and NCCP-58 under various saline conditions.
62 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965

Fig. 6. Growth of the rice plant inoculated with halophilic bacterial strains NCCP-76 and NCCP-58. (A) Control, NCCP-76 and NCCP-58 (B) 50 mM NaCl, NCCP-76 + 50 mM NaCl and NCCP-
58 + 50 mM NaCl (C) 100 mM NaCl, NCCP-76 + 100 mM NaCl and NCCP-58 + 100 mM NaCl (D) 150 mM NaCl, NCCP-76 + 150 mM NaCl and NCCP-58 + 50 mM NaCl.

3.2. Biochemical analysis Na+ by increasing the salt concentration, an increase occurred from
control to 150 mM, however priming with bacterial strains had low
All the plant inoculated with bacteria strains had more vigorous Na+ ion concentration thus it helps in alleviating salt stress (Fig. 10A).
growth as compared to non-treated plants (Fig. 6). By increasing NaCl Rice plants treated with NCCP-76 had more K+ ion than plants treated
concentration, cellular injury was increased, however higher cellular with NCCP-58 (Fig. 10C).
injury was observed at 150 mM as compared to 50 and 100 mM NaCl.
Plants inoculated with bacterial strains alleviated the stress and had
less cellular injury as compared to non-inoculated plants particularly
in the case of NCCP-76 (Fig. 7). NaCl concentration decreased chloro-
phyll and carotenoid contents with increasing salinity levels (Fig. 8).
By comparing with non-inoculated plants both bacterial strains had
promoting effect on the Chl a, Chl b and total carotenoid content in inoc-
ulated plants. However, Chl a content was affected more as compared to
Chl b. In the case of Chl a and carotene both strains had a similar effect
on the plants but NCCP-58 was more effective than NCCP-76 in the
case of Chl b (Fig. 8). NaCl concentration had a great effect on total nitro-
gen and protein contents. By increasing NaCl concentration a decreased
occur in total nitrogen and protein contents (Fig. 9). In contrast, the rice
plants inoculated with bacterial strains had more nitrogen and protein
contents than non-inoculated plants (Fig. 9). Both bacterial strains had
a similar effect on total nitrogen and protein contents under saline
condition.
Increase in NaCl concentration caused a signicant decrease in Ca+2
and K+ ion, in control as well as in 50, 100 and 150 mM. While plants
inoculated with bacterial strains promoted the ion concentration in Fig. 7. Cellular injury of plants inoculated with halophilic bacterial strains NCCP-76 and
control as well as in NaCl concentrations (Fig. 10). But in the case of NCCP-58 under various saline conditions.
 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965 63

Fig. 8. Chl a (a) Chl b (b) and carotenoid (C) contents of plants inoculated with halophilic bacterial strains NCCP-76 and NCCP-58 under various saline conditions.

4. Discussion

Phytoremediation technique has been widely used to remediate

metals, petroleum waste, pesticides, and saline soils (Bose et al., 2008;
Huang et al., 2005; Huang et al., 2004; Qadir et al., 2007).
Phytoremediation can be an economical and environment friendly tech-
nique for remediation of salt-affected soils, if it can be appropriately uti-
lized. Sometimes phytoremediation process can prolong since it needs
numerous growing seasons to decrease the amount of salt in soil. The ef-
ciency of this process can be improved by the use of halophilic bacteria.
Therefore, in the present study, halophilic Bacillus strains (T. devorans
(NCCP-58) and O. kapialis (NCCP-76) were used for remediation of
salt affected soil.
We had observed that by increasing NaCl concentration, germina-
tion percentage and rate decrease but inoculation with bacterial strain
considerably improved the germination percentage and germination
rate (Fig. 1). It may be due to the fact that the bacterial strains use
Na+ as a factor for its metabolism and due to this, the Na+ amount
reduced and as a result seeds were able to grow normally. Inoculation
of PGPRs strains signicantly improves the seed germination under
salt stress conditions (Mishra et al., 2010). A similar kind of results has
been reported by Kaymak et al. (2008). They had observed that treat-
ment with PGPRs under stress conditions might be helpful to obtain a
higher seed germination percentage.
PGPRs are naturally present in the soil that insistently colonize plant Fig. 9. Total organic nitrogen (a) and total protein (b) contents of plants inoculated with
root zone and promote plant growth. The NaCl concentration caused a halophilic bacterial strains NCCP-76 and NCCP-58 under various saline conditions.
64 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965
considerable decrease in lengths and fresh and dry weights of shoot and
root while bio-priming alleviated the adverse effect (Figs 3 and 4). Bac-
terial strains can make bacterial exopolysaccharides (EPSs) bind to cat-
ions as well as increase the population density of EPS-producing
bacteria in the root zone which would reduce the content of Na+ and
accessibility for plant uptake (Han and Lee, 2005). The improved
growth of rice seedlings by application of halophilic bacteria may also
be due to production of IAA. According to Mishra et al. (2010), inocula-
tion of bacterial strains caused a considerable increase in root and shoot
lengths and dry matter production of shoot and root of Cicer arietinum
seedlings. Similar results were reported by Ashrafuzzaman et al.
(2009) wherein plant length, root length and dry matter production of
shoot and root of rice seedlings increased in PGPRs treated plants over
non-inoculated control.
It has been conrmed through many reports that the measurement
of the membrane stability is an important technique in identifying salin-
ity tolerance in plants. Salt had a negative effect on the cell membrane
stability and as the salt concentration was increased so does the mem-
brane injury (Fig. 6).It may be due to the reason that plants absorbed in-
sufcient amount of water under stress condition, due to which Na+
accumulates in plant cells causing excessive cellular damage. Halophilic
Fig. 10. Sodium (a) calcium (b) and potassium (c) contents of plants inoculated with halophilic bacterial strains NCCP-76 and NCCP-58 under various saline conditions.
bacteria alleviated the salt stress due to less uptake of Na+ (Fig. 6). Jamil
et al. (2010a, 2010b) also showed that by increasing NaCl concentration
cell injury rate increases which is also in accord with our result. The
plasma membrane and activities of antioxidant enzymes are synchro-
nized by Na deposition to avoid damage of chloroplasts under salinity
stress, which contain photosynthetic pigment (Demiral and Trkan,
2005).
Leaf chlorophyll content is the most important physiological traits
directly related to photosynthesis ability in rice (Teng et al., 2007).
Chlorophyll and carotene contents of plant leaves were signicantly re-
duced with the increase in salt stress but plant inoculated with bacteria
had more leaf chlorophyll contents (Fig. 7). PGPRs can directly affect
plant growth through the production of phytohormones i.e. indole-3-
acetic acid and cytokines (Yildirim et al., 2011). Yildirim et al. (2011)
also reported that PGPRs strains increase the chlorophyll and carotenoid
content in NaCl conditions. PGPRs are also contributing to increasing
crop nutrient uptake of nitrogen from nitrogen xing bacteria linked
with roots. A decrease occurs in nitrogen and protein contents with in-
creasing NaCl concentrations, in contrast to inoculated plants (Fig. 8).
Saharan and Nehra (2011) also reported that nitrogen xing bacteria
provide only a modest increase in crop nitrogen uptake. PGPRs are
 G. Shah et al. / Journal of Geochemical Exploration 174 (2017) 5965
mainly involved in increased uptake of nitrogen, synthesis of phytohor-
mones and solubilization of minerals (Glick et al., 1998).
The possible role of PGPRs in solubilization of mineral nutrients and
thus alleviating soil salinity stress during plant growth has not yet been
established. NaCl treatment induced decrease in Ca+2 and K+ and
increase in Na+ contents in the rice plant, however the inoculation
with both the bacterial strains improved the rate of Ca+2 and K+ ion
uptake but reduced uptake of Na+ ion content (Fig. 9). Salinity not
only reduces macromineral contents of plant leaves, especially Ca+ 2
and K+ availability, but also reduces Ca+2 and K+ transport and mobil-
ity to growing regions of the plants (Yildirim et al., 2011). PGPRs are
reported to affect the plant growth, yield, and nutrient uptake by a
variety of mechanisms (Saharan and Nehra, 2011). Direct mechanisms
may act on the plant itself and affect growth by means of plant growth
regulators, solubilization of mineral materials and xation of
atmospheric nitrogen (Glick et al., 1998; Yildirim et al., 2011). PGPRs
can produce bacterial exopolysaccharides to bind cations as well as
increase the population density of EPS-producing bacteria in the root
zone which would reduce the content of Na+ available for plant uptake,
thus help in alleviating salt stress in plants growing in saline environ-
ments (Han and Lee, 2005).
In conclusion, both bacterial strains T. denoran (NCCP-58) and
O. kapialis (NCCP-76) were effective in improving plant growth but
NCCP-76 was more responsive in terms of physiological and biochemi-
cal parameters in alleviating salt stress. The NCCP-76 strain has a poten-
tial to be used for phytoremediation under saline condition.
Acknowledgments
Financial support for this work was partially provided by Higher Ed-
ucation of Pakistan through grant no. 1348.
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