Int.J.Curr.Microbiol.App.

Sci (2017) 6(1): 143-154

International Journal of Current Microbiology and Applied Sciences

ISSN: 2319-7706 Volume 6 Number 1 (2017) pp. 143-154
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Original Research Article http://dx.doi.org/10.20546/ijcmas.2017.601.018

Production, Extraction and Characterization of Red Pigment Produced by

Serratia rubidaea JCM 1240T isolated from Soil
R.R. Rakh1*, S.M. Dalvi2, B.B. Musle3 and L.S. Raut4
1
Department of Microbiology, Shri Guru Buddhiswami Mahavidyalaya,
Purna (Jn.) Dist. Parbhani, India
2
Department of Botany, Shri Guru Buddhiswami Mahavidyalaya,
Purna (Jn.) Dist. Parbhani, India
3
Department of Chemistry, Shri Guru Buddhiswami Mahavidyalaya,
Purna (Jn.) Dist. Parbhani, India
4
Department of Microbiology, Sant Tukaram College, Parbhani, Dist. Parbhani, India
*Corresponding author

ABSTRACT

Keywords A red pigment producing bacteria was isolated from soil sample which was identified by
Serratia rubidaea 16S r RNA sequencing as Serratia rubidaea JCM 1204T. The red pigment produced was
JCM 1204T, tested for prodigiosin by presumptive color test, adsorption spectra, and its quantification
Prodigiosin, was carried out on King’s B medium. For presumptive color test, the extracted pigment
Presumptive color solution was divided into two portions. One part was acidified with a drop of concentrated
test, IR, NMR and HCl and the other part was alkalinized with a drop of concentrated ammonia solution. A
Mass
spectrophotometer.
red or pink color in the acidified solution and a yellow or tan color in the alkaline solution
indicated a positive, presumptive test for prodigiosin. For adsorption spectra, the ethanolic
Article Info acidified and alkalinized red pigment extract was tested by spectrophotometer in range
between 300 to 700 nm and found that the ethanolic acidified red pigment extract absorbed
Accepted: maximum light at 535 nm while ethanolic alkalinized red pigment extract absorbed
12 December 2016 maximum light at 470 nm which is characteristic of prodigiosin. The solid red pigment
Available Online: was also further characterized by IR, NMR, and Mass spectrophotometer, which confirms
10 January 2017 that the red pigment produced by Serratia rubidaea JCM 1204T as prodigiosin.

Introduction
Many artificial synthetic colorants, which been increasing in recent years thanks to the
have widely been used in foodstuff, dyestuff, knowledge about the harmful effects of
cosmetic and pharmaceutical manufacturing synthetic pigments and their industrial
processes, comprise various hazardous byproducts on humans and the environment
effects. To counter act the ill effect of (Unagul et al., 2005; Chidambaram and
synthetic colorants, there is worldwide Lakshmanaperumalsamy, 2009).
interest in process of development for the
production of pigments from natural sources. Natural pigments can be obtained from two
The utilization of natural pigments in major sources, plants (Mizukami, et al., 1978;
foodstuff, dyestuff, cosmetic and Papageorgiou et al., 1979) and micro-
pharmaceutical manufacturing processes has organisms (Cross and Edinberry, 1972; Ryu et

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al., 1989; Parisot et al., 1990; Yongsmith et regulators (Haddix et al., 2008) and can be
al., 1994; Kim et al., 1998a, and Cho et al., used as a natural dye (Alihosseini, et al.,
2002). Biopigments from the micro- 2008).
organisms have been preferred over those
from plants because of their stability The present investigation focuses on i)
(Raisainen et al., 2002) and the availability of Identification of red pigment producing
their cultivation technology (Kim et al., 1999; bacteria by 16 S rRNA Sequencing ii) Test
Parekh et al., 2000) throughout the year. On the red pigment produced by the red bacteria
the other hand, biopigments from plants have for prodigiosin by presumptive color test and
numerous drawbacks like instability against adsorption spectra, and iii) confirmation red
light, heat or adverse pH, low water solubility pigment as prodigiosin by IR, NMR and Mass
and often non-availability throughout the year spectrophotometer.
(Chandni et al., 2012).
Materials and Methods
One of the studied biopigments of microbial
origin is the prodigiosin. Prodigiosin (PDG) is Isolation of Red Pigment Producing
a natural red pigment characterized by a bacteria from Soil
common pyrrolylpyrromethane skeleton,
having low molecular weight (323.4 Dalton), Soil samples, for isolation of red pigment
appearing only in the late stages of bacterial producing bacteria, were collected from
growth as secondary metabolite (Harris et al., different field and brought in poly-ethylene
2004) and produced by many bacterial bags to the laboratory, Department of
species, including many strains of Serratia Microbiology, Shri Guru Buddhiswami
marcescens, Hahella chejuensis, Mahavidyalaya, Purna.
Streptomyces variegatus, Colwellia (Vibrio)
psychrerythraea, “Pseudomonas The collected soil samples were serially
magnesiorubera, and other eubacteria diluted and plated on King’s B agar plates.
(Yamamoto et al., 1999). The prodiginine Red-pigmented colonies were isolated on the
group, of which prodigiosin is a member, is a plates after incubation and preserved at 4°C.
group of structural isomers that contain a The isolated red pigmented bacteria were
tripyrrole core with different alkyl chains, identified by 16S r RNA gene sequence
have no defined role in the physiology of analysis carried out commercially from
producing strains but have been reported to Agharkar Research Institute, Pune.
have antifungal, antibacterial, algicidal,
antiprotozoal, antimalarial, immuno- Presumptive color tests for prodigiosin
suppressive, anticancer and antiproliferative
activities (Castro, 1967; Boger and Patel, Red pigment produced in suitable medium
1988;Williams and Quadri, 1980; Demain, was presumptive tested (Gerber and
1995; Han et al., 1998;Cerdeno et al., 2001; Lechevalier, 1976) for prodigiosin. For
Furstner, 2003; Montaner and Pe´rez-Toma´s presumptive test, pigmented broth was
2003and Samrot et al., 2011). suspended overnight in 95% ethanol at 22 to
24°C. Debris was removed from the
According to a recent report, prodigiosin or suspension by centrifugation at 5,000 rpm for
its analogues have been considered effective 15 min. The clear solution was then divided
biological control agents against harmful into two portions. One part was acidified with
algae (Jeong et al., 2005; Nakashima et al., a drop of concentrated HCl and the other part
2006) have been considered cell growth was alkalinized with a drop of concentrated
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ammonia solution. A red or pink color in the Production of Prodigiosin in suitable

acidified solution and a yellow or tan color in Medium and Quantification of prodigiosin
the alkaline solution indicative of a positive
presumptive test for prodigiosin. In order to determine the suitable media
supporting the maximal production of
Determination of adsorption spectra prodigiosin, red pigment producing bacteria
was grown in Nutrient Broth, and King’s B
For determination of absorption spectra, Broth, at 25 °C.The levels of prodigiosin in
Gerber and Lechevalier, (1976) method was these conditions were estimated after 24hr,
used. Pigmented bacteria were treated with 48hr, 72hr and 96 hr.
ethanol, and the cell debris in the suspensions
was removed by centrifugation at 5,000 rpm For quantification of prodigiosin produced,
for 15 min. bacterial cell absorbance in the King’s broth
and Nutrient broth was measured at 620 nm,
Samples (1 ml) of the ethanol extracts were following which the broth suspensions were
acidified or alkalinized with 0.1 ml of 1 N subjected to centrifugation at 5000 rpm for 15
HCI or 1 N NaOH, respectively. The min to collect the cell pellet. 10 ml of 95%
absorbance spectrum of sample was measured methanol was added to the cell pellet and
with a Single Beam UV – Visible centrifuged under the same condition. 95%
Spectrophotometer (Bioera Life Science Pvt. methanol was used as a blank. Methanolic
Ltd.) in the range of 300 to 700 nm. Acidified extract of prodigiosin showed characteristic
or alkalinized 95% ethanol was used as a maxima at 499 nm. Extracted prodigiosin
blank. was estimated using the following equation
(Mekhael and Yousif, 2009).

[OD499 – (1.381 x OD620)] x 1000

Prodigiosin unit/cell =
OD620
Where,

OD499 – pigment absorbance;

OD620 – bacterial cell absorbance
1.381 – constant

Extraction and Characterization of Red to obtain crude pigment. The crude

pigment concentrated pigment was recrystallized with
methanol (Min – Jung – Song et al., 2005;
Serratia rubidaeagrown in King’s B broth Chandrashekhar et al., 2012).
was centrifuged at 10000 rpm for 20 minutes
and the cell pellet was collected. The pigment The chemical structure of the purified
from the cell pellet was extracted with pigment was characterized by FTIR
acidified methanol (1N HCl 1ml: Methanol BRUKER model RXI Spectrometer, mass
24 ml) and the extract was centrifuged at spectrometry and NMR (Bruker, Germany).
5000 rpm for 15 minutes. The supernatant IR Spectra of prodigiosin was scanned on
was concentrated in Rota evaporator at 60 °C FTIR BRUKER model RXI Spectrometer.

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1
HNMR spectra were recorded in DMSO on alkaline solution. This test indicative for
Gemini 200 MHz instrument using TMS as an presumptive test for prodigiosin.
internal standard (chemical shift given in δ
ppm). The mass spectrum was recorded on Determination of adsorption spectra
Cintra – 15 – GCMS – Spectrophotometer.
For determination of absorption spectra,
Result and Discussion pigmented ethanol extracts were acidified or
alkalinized with 0.1 ml of 1 N HCI or 1 N
Isolation of Red Pigment producing
NaOH, respectively. The absorbance
bacteria from Soil
spectrum of sample was measured with a
Serially diluted soil samples plated on king’s Single Beam UV – Visible Spectrophotometer
B agar plates produced wide range of red (Bioera Life Science Pvt. Ltd.) in the range of
pigmented colony. Out of these colonies, a 300 to 700 nm. Acidified or alkalinized 95%
red pigment colony was selected whose ethanol was used as a blank.
pigment was to be tested for prodigiosin,
isolated on the plates after incubation and Pigment extracted with ethanol from Serratia
preserved at 4°C. Later on the isolated red rubidaea JCM 1240T showed characteristic
pigmented bacterium was identified by 16S r maxima of 535 (Figure 3.3) and 470 nm in
RNA gene sequence analysis as Serratia acid and alkaline solutions, respectively,
rubidaea JCM 1240T (photo plate 3.1) whose which is indicative that the pigment extracted
phylogenetic relation (Figure 3.2) and partial with ethanol was prodigiosin. Similarly,
16S r RNA gene sequence is as follows Prodigiosin extracted with ethanol from S.
(Figure 3.1). marcescens Nima showed characteristic
maxima of 535 and 470 nm in acid and
Presumptive color tests for prodigiosin alkaline solutions, respectively (Williams and
Qadri, 1980; Ming-Jer Ding and Robert
For this presumptive test pigmented broth was Williams, 1983).
suspended overnight in 95% ethanol at 22 to
24°C. Debris was removed from the Prodigiosin was reported to display a
suspension by centrifugation at 5,000 rpm for characteristic absorption spectrum in ethanol,
15 min. The clear solution was then divided with a maximum at 534 nm (Slater et al.,
into two portions. One part was acidified with 2003) and single peak absorbance at 535 Nm
a drop of concentrated HCl and the other part (Giri et al., 2004; Song et al., 2006; Montaner
was alkalinized with a drop of concentrated et al., 2000) extracted prodigiosin by shaking
ammonia solution. A red or pink color in the the S. marcescens 2170 cells with a mixture
acidified solution was observed while a of methanol/lN HCl in the ratio 24:l.
yellow or tan color in the alkaline solution
indicated a positive presumptive test for Absorption spectrum of the pigment produced
prodigiosin as shown (photo plate 2). by Serratia rubidaea JCM was dependent on
pH value similar to that reported earlier (Song
Similar types of results were also shown in et al., 2006). Thus at pH 2.0, the pigment was
studies carried out by Ming-Jer Ding and red and showed a maximum absorption at 535
Robert P. Williams (1983) where strain of nm, which is identical to that of prodigiosin
Serratia marcescens isolated from clinic hydrochloride. Under neutral condition (pH
shows a red or pink color in the acidified 7.3), its absorption intensity decreased and the
solution while a yellow or tan color in the colour of the pigment changed to pink.

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However, in alkaline condition (pH 10.0) the rubidaea JCM 1240T was grown in Nutrient
colour was orange and its absorption Broth, King’s B Broth, at 25 °C.
spectrum shifted to 470 nm. Pigment
produced by Serratia rubidaea JCM 1240T For quantification of prodigiosin produced,
recorded maximum absorption at and 470 nm bacterial cell absorbance in the medium was
in acid and alkaline solutions, respectively measured at 620 nm, while absorbance of
suggesting that this pigment is prodigiosin. methanolic extract of prodigiosin was
measured at 499 nm (Table 3.1). The
Production of Prodigiosin in suitable concentrations of prodigiosin in these
Medium and Quantification of prodigiosin conditions were estimated after 0hr, 24hr,
48hr 72hr and 96 hr. By using these
To determine suitable medium for production absorbance, prodigiosin concentration was
and quantification of prodigiosin,Serratia determined as represented in (Table 3.2).

Table.3.1 Pigment Absorbance at 499nm

Hour Nutrient Broth (O.D.) King’s B Broth (O.D.)

24 hr 00 00
48 hr 1.603 1.673
72 hr 1.654 1.686
96 hr 1.566 1.580

Table.3.2 Total prodigiosin estimated in nutrient broth and King’s B broth

Hour Prodigiosin in Prodigiosin in

Nutrient Broth mg/lit King’s B Broth mg/ lit
24 hr 00 00
48 hr 1070.33 1188.94
72 hr 1055.96 1246.10
96 hr 885.38 957.10

Fig 3.1

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Fig 3.2

Fig 3.3

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Fig 3.4

Fig 3.5

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Photo 3.1

Photo 3.2

Prodigiosin unit per cell after 48hr was Hiwarale (2012) where they compared
found to be 1070.33 and 1188.94 in prodigiosin production in Nutrient Broth and
nutrient broth and King’s B broth Peptone Glycerol Broth. In this study, they
respectively. Maximum production was found highest prodigiosin production after 72
reported in 72hr thereafter production ceased hr in peptone glycerol broth than nutrient
towards 96hr. The lowest prodigiosin unit per broth.
cell was found after 96hr i.e. in nutrient broth
it was 885 and in peptone glycerol broth i.e. Extraction and Characterization of Red
957.1. pigment

Similar results were obtained by Kamble and The chemical structure of the purified
prodigiosin was characterized by FTIR

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BRUKER model RXI Spectrometer, mass spectroscopic analyses of the red pigment
spectrometry and NMR (Bruker, Germany). with IR, 1HNMR and Mass spectra very
IR Spectra of prodigiosin was scanned on clearly testify that the pigment produced by
FTIR BRUKER model RXI Spectrometer. Serratia rubidaea JCM 1240T is prodigiosin-
1
HNMR spectra were recorded in DMSO on like pigment. Sumathi et al., 2014 used same
Gemini 200 MHz instrument using TMS as an technique to characterize the pigment
internal standard (chemical shift given in δ produced bySerratia marcescens NPLR1
ppm). The mass spectrum was recorded on where they found the pigment produced was
Cintra – 15 – GCMS – Spectrophotometer. also prodigiosin.

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How to cite this article:

Rakh, R.R., S.M. Dalvi, B.B. Musle and Raut, L.S. 2017. Production, Extraction and
Characterization of Red Pigment Produced by Serratia rubidaea JCM 1240T isolated from
Soil. Int.J.Curr.Microbiol.App.Sci. 6(1): 143-154.
doi: http://dx.doi.org/10.20546/ijcmas.2017.601.018

154