marine pigmented bacteria: a prospective source of

© 2019 Journal of Natural Science, Biology and Medicine | Published by Wolters Kluwer - Medknow104

Abstract

Review Article

IntroductIon

Marine bacterial communities possess enormous potentiality to produce diverse bioactive molecules such as pigment molecules. On usual microbial culture media, several marine Gram-positive and Gram-negative bacteria appear to produce an array of pigments. Production of these pigments by microbes appears to mediated by the quorum-sensing mechanism.[1] Apparently, several marine bacterial pigments have demonstrated various biological activities such as antimicrobial, anticancer, and immunosuppressive activities.[2] Recently, studies on natural products and microbial autecology science have increased the demand for novel resources of eco-friendly natural products such as bacterial pigments for different biomedical and industrial applications.

Carotenes are polyunsaturated hydrocarbons that may contain 30, 40, or 50 carbon atoms in one molecule. Melanins are polyphenolic pigments that derived from phenolic compounds by the hydroxylation, oxidation, and polymerization reactions. Phenazines are tricyclic, redox-active, and small nitrogen-containing heterocyclic aromatic compounds. Prodiginines are aromatic chemical compounds with pyrrolyl

dipyrromethene core structure. Quinones are aromatic ring-structure containing compounds with yellow-to-red color hues. Tambjamines are alkaloid compounds that show yellow color. Violacein compounds are indole-pigmented compounds derived from tryptophan metabolism. Pigment molecules of these families of compounds originated from marine bacteria demonstrated potential biomedical applications such as cytotoxic activities, antioxidant, antimicrobial, antimalarial, anticancer, antitumor, and antifouling properties.[3]

Such natural pigment molecules of microbial origin have a great demand in the industry due to their functional attributes such as nontoxic nature, easier gene manipulation, large volume of biomass production, and environmental acceptability. Therefore, exploration, exploitation, and identification of novel or rare types of pigment compounds

Antimicrobial properties of several nonpigmented bacteria isolated from the marine environment have been well understood. However, marine bacteria with distinct asset of pigmentation have not been studied intensively and explored unlike nonpigmented bacteria. Recently, several studies have found multidrug-resistant microbes against various diseases. Therefore, search for alternative novel and natural bioactive compounds is in demand at current research. Furthermore, the application of synthetic colorants in the food industry has several harmful effects; thus, exploring pigments from natural environments is important to substitute synthetic colorants. This review emphasizes marine pigmented bacteria as a potential alternative source of natural compounds as well as natural colorants. The antibacterial potential of marine bacterial pigmented compounds reported from the year 2000 to hitherto is detailed cogitatively in this review, along with the best-known paradigms of pigments such as prodigiosin and violacein. In parenthesis, some other important applications of well-studied prodigiosin and violacein pigment molecules are highlighted briefly.

Keywords: Antibacterial activity, marine pigmented bacteria, pigment molecules, prodigiosin, violacein

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DOI: 10.4103/jnsbm.JNSBM_201_18

Address for correspondence: Dr. Chatragadda Ramesh, Andaman and Nicobar Centre for Ocean Science and Technology,

ESSO‑National Institute of Ocean Technology, Dollygunj, Port Blair ‑ 744 103, Andaman and Nicobar Islands.

E‑mail: [email protected]

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How to cite this article: Ramesh C, Vinithkumar NV, Kirubagaran R. Marine pigmented bacteria: A prospective source of antibacterial compounds. J Nat Sc Biol Med 2019;10:104-13.

Marine Pigmented Bacteria: A Prospective Source of Antibacterial Compounds

Chatragadda Ramesh, Nambali Valsalan Vinithkumar, Ramalingam Kirubagaran1

Andaman and Nicobar Centre for Ocean Science and Technology, ESSO‑NIOT, Dollygunj, Port Blair, Andaman and Nicobar Islands, 1Marine Biotechnology Group, ESSO‑National Institute of Ocean Technology (NIOT), Ministry of Earth Sciences (Govt. of India), Chennai, Tamil Nadu, India

Ramesh, et al.: Antibacterial potential of marine pigmented bacteria

Journal of Natural Science, Biology and Medicine ¦ Volume 10 ¦ Issue 2 ¦ July-December 2019 105

from marine-pigmented bacteria (MPB) are necessary for wide range of biomedical and industrial applications.[4] Currently, cognitive scientists and food industries are seeking for such natural pigments from marine bacteria due to their functional attributes. These pigment molecules have not been fully explored from marine microbes and are still untouched when compared to microbes of terrestrial origin. Several carotenoids with potent antioxidant activity have been frequently observed from marine bacteria.[4] However, there are scarcely few reports on marine antimicrobial pigments. Therefore, in this review, we have detailed the antibacterial potential of various pigment molecules originated from marine bacteria isolated from different milieus. This review will be a beginner’s guide and benefit the researchers greatly to work on MPB.

AntIbActerIAl PotentIAl of MArIne‑PIgMented bActerIA

In the last decade, several marine bacterial species have been found to produce potential antimicrobial compounds against several pathogenic and nonpathogenic bacteria [Figure 1 and Tables 1, 2]. The yellow color of Cytophaga/Flexibaterium cluster strain AM13 is due to tryptanthrin; a rare bacterial compound possesses antibiotic activity. In most other cases, yellow cultures owe their color to the carotenoid zeaxanthin (Hel21) or one of the many Vitamin K derivatives (e.g., menaquinone MK6 in Hel21).[35] The antibacterial activity of violet pigment, a mixture of violacein and deoxyviolacein, produced by the psychrotrophic bacterium Janthinobacterium lividum RT102 have resulted in complete inhibition of several pathogenic and putrefactive bacteria at minimum inhibitory concentration value of >15 mg/L.[18] It was revealed that marine heterotrophic-pigmented bacteria

count for 1.4% of the total microbial community.[36] Evidently, marine heterotrophic-pigmented bacteria isolated from South China and the East China Sea and Pacific Ocean waters have displayed area-specific distribution and diversity with genus or species-specific color variation.[36]

A red-pigmented marine bacterium Pseudovibrio denitrificans Z143-1 isolated from an unidentified tunicate exhibited anti-Staphylococcus aureus activity.[12] Fabrics such as wool and nylon samples dyed with the bright red pigment prodiginines extracted from a marine sediment isolate of Vibrio sp. killed 50% of the S. aureus and Escherichia coli.[8] A study also reported the strong growth inhibition activity by xanthophyll, a yellow pigment-producing Pseudoalteromonas piscicida, against S. aureus DSM 6672.[37] Collimonas fungivorans CTE227 a blue-black indole-derived pigment (violacein)-producing bacteria that isolated from the sea surface microlayer off the coast of Trøndelag, Norway, displayed the antibacterial activity against Micrococcus luteus.[17] Similarly, a deep blue pigment “glaukothalin” extracted from Rheinheimera strains (isolated from diatom aggregates and organic particles) showed >5 or <5 mm inhibition zone against two marine bacterial groups (Bacillus/Clostridium group and Cytophaga–Flavobacter–Bacteroides group).[1]

Significantly, purple-, red-, or yellow-pigmented Pseudoalteromonas were predominantly isolated from swabs of live or inert surfaces of different marine organisms in warmer waters.[23] The inhibitory activities caused by brown-pigmented Phaeobacter and Ruegeria bacterial species are due to the production of tropodithietic acid which is a species-specific metabolite likely essential for species survival.[23] The production of a diffusible brownish orange pigment by a marine luminous bacterium Vibrio campbellii has been related to either due to proteorhodopsin[38] or pyomelanin.[39] Prodigiosin, a

Figure 1: Chemical structures of antibacterial pigment compounds of marine‑pigmented bacteria


Journal of Natural Science, Biology and Medicine ¦ Volume 10 ¦ Issue 2 ¦ July-December 2019106

Tabl

e 1:

Ant

imic

robi

al p

igm

ent

com

poun

ds f

rom

mar

ine‑

pigm

ente

d ba

cter

ia

Con

td...

Pigm

ent c

ompo

und

Mol

ecul

ar

form

ula

Mol

ecul

ar

wei

ght

Colo

rAb

sorp

tion

wav

elen

gth

(nm

)

Sour

ce o

f pr

oduc

er

genu

s/sp

ecie

s

Isol

atio

n so

urce

Med

ia u

sed

Incu

batio

n te

mpe

ratu

re

(°C)

Refe

renc

es

Prod

igio

sin

C20

H25

N3O

323.

4R

ed53

5Se

rrat

ia sp

.Se

awat

erM

arin

e ag

ar28

[5]

Red

535

S. m

arce

scen

sM

arin

e sp

onge

X. te

stud

inar

iaM

arin

e ag

ar25

[6]

324.

2R

ed53

5H

. che

juen

sis

Coa

stal

mar

ine

sedi

men

tM

arin

e ag

ar25

[7]

323.

19R

ed53

0Vi

brio

sp.

Mar

ine

sedi

men

tSe

awat

er-b

ase

rich

med

ia

agar

25[8

]

324

Red

Z. ru

bidu

sTi

dal fl

at se

dim

ent

Mar

ine

agar

25[9

]Pr

odig

iosi

n R

1C

27H

37N

3O42

0.30

Red

533

S. g

rise

ovir

idis

27[1

0]C

yclo

prod

igio

sin

C20

H23

N3O

Red

P. d

enitr

ifica

ns,

P. ru

bra

Seaw

ater

[11]

322

Red

Z. ru

bidu

sTi

dal fl

at se

dim

ent

Mar

ine

agar

25[9

]H

epty

l pro

digi

osin

C22

H29

N3O

351

Red

P. d

enitr

ifica

nsM

arin

e tu

nica

teM

arin

e ag

ar27

[12]

Nor

prod

igio

sin

C19

H23

N3O

309.

41O

rang

e47

0Se

rrat

ia sp

.Se

awat

erM

arin

e ag

ar28

[5]

310

Red

535

H. c

heju

ensi

sC

oast

al m

arin

e se

dim

ent

Mar

ine

agar

25[7

]

Dip

yrro

lyld

ipyr

rom

ethe

ne

prod

igio

sin

C19

H18

N4O

233

5R

ed53

5 nm

H. c

heju

ensi

sC

oast

al m

arin

e se

dim

ent

Mar

ine

agar

25[7

]

Und

ecyl

prod

igin

ine

C25

H35

N3O

394

Red

535

H. c

heju

ensi

sM

arin

e se

dim

ent

Mar

ine

agar

25[7

]B

rom

oalte

roch

rom

ides

Yello

wP.

mar

ical

oris

Spon

ges

[11]

Stre

ptop

hena

zine

BC

24H

28N

2O5

424.

49Ye

llow

Stre

ptom

yces

sp.

Mar

ine

sedi

men

tB

acto

-aga

r28

[13]

N-a

cety

l-N-

dem

ethy

lmay

amyc

inC

27H

25N

O8

514.

14D

ark

brow

n32

8 an

d 44

3St

rept

omyc

es sp

.M

arin

e se

dim

ent

Bac

to-a

gar

28[1

4]

May

amyc

in

C26

H25

NO

746

4.17

Bro

wn

236

Stre

ptom

yces

sp.

Mar

ine

spon

ge

H. p

anic

eaG

YM

med

ium

28[1

5]

Gla

ukot

halin

C34

H56

N4O

458

4.85

Dar

k bl

ue63

6Rh

einh

eim

era

stra

ins

Dia

tom

agg

rega

tes

and

orga

nic

parti

cles

Mar

ine

brot

h ag

ar15

[1]

Indi

goid

ine

C10

H8N

4O4

248.

2D

ark

blue

299

Leis

inge

ra sp

.E.

scol

opes

squi

d eg

gsSW

T m

ediu

m28

[16]

Viol

acei

nC

20H

13N

3O3

Purp

le b

lue

C. m

arin

um34

2.08

82B

lack

blu

e57

2C

. fun

givo

rans

Seaw

ater

Kus

ters

st

rept

omyc

ete

isol

atio

n ag

ar

20[1

7]

344.

1213

Viol

et57

9J.

livi

dum

Org

anic

resi

due

of

a w

ater

tank

Kee

ping

rain

bow

tro

ut

Glu

cose

, ca

sein

, and

ye

ast e

xtra

ct

med

ium

20[1

8]

343.

34Vi

olet

575

P. lu

teov

iola

cea

Sea

spon

ge

surf

ace

Nut

rient

aga

r28

[19]



Tabl

e 1:

Con

td...

Pigm

ent c

ompo

und

Mol

ecul

ar

form

ula

Mol

ecul

ar

wei

ght

Colo

rAb

sorp

tion

wav

elen

gth

(nm

)

Sour

ce o

f pr

oduc

er

genu

s/sp

ecie

s

Isol

atio

n so

urce

Med

ia u

sed

Incu

batio

n te

mpe

ratu

re

(°C)

Refe

renc

es

342.

5Pu

rple

575

Pseu

doal

tero

mon

as

sp.

Dee

p se

awat

erPP

ES-I

I pla

te

med

ium

20[2

0]

Viol

etP.

lute

ovio

lace

aSu

rfac

e se

awat

er

or a

lgae

Mar

ine

min

imal

m

ediu

m

25[2

1]

Viol

acei

n-lik

eD

ark

red

brow

n to

bl

ack

520

J. sv

alba

rden

sis

Gla

cier

ice

LB, B

HI

and

min

imal

m

ediu

m (E

)

20[2

2]

Deo

xyvi

olac

ein

C20

H13

N3O

232

9.11

20Vi

olet

579

J. li

vidu

mO

rgan

ic re

sidu

e of

a

wat

er ta

nkK

eepi

ng ra

inbo

w

trout

Glu

cose

, ca

sein

, and

ye

ast e

xtra

ct

med

ium

20[1

8]

326.

0938

Viol

et57

2C

. fun

givo

rans

Seaw

ater

Kus

ters

st

rept

omyc

ete

isol

atio

n ag

ar

20[1

7]

Trop

odith

ietic

aci

dC

8H4O

3S2

212.

246

Bro

wn

Rose

obac

ter,

Rueg

eria

and

Ph

aeob

acte

r

Seaw

ater

and

sw

ab sa

mpl

es o

f m

arin

e or

gani

sms

Mar

ine

agar

20[2

3]

Act

inom

ycin

DC

62H

86N

12O

1612

55.4

0O

rang

e24

2S.

par

vulu

sM

arin

e se

dim

ent

Star

ch c

asei

n ag

ar27

[24]

Pyoc

yani

nC

13H

10N

2O21

0.24

Blu

e gr

een

P. a

erug

inos

aM

angr

ove

sedi

men

tsM

arin

e ag

ar35

[25]

Pyor

ubin

C14

H12

N3O

225

4.26

Bro

wn

P. a

erug

inos

aM

angr

ove

sedi

men

tsM

arin

e ag

ar35

[25]

Mel

anin

Bro

wn-

B

lack

480

Stre

ptom

yces

sp.

Mar

ine

sedi

men

tSt

arch

cas

ein

agar

28

[26]

3,3’

,5,5

’-te

tra-b

rom

o-

2,2-

biph

enyl

diol

C12

H6B

r 4O2

501.

7B

row

n53

0P.

phe

nolic

aSe

awat

erZo

Bel

l 221

6E

agar

25[2

7]

Tam

bjam

ines

C22

H33

N3O

356.

27Ye

llow

425

P. tu

nica

taM

arin

e al

ga,

tuni

cate

s[1

1,28

]

Him

alom

ycin

AC

43H

52O

1682

4.87

4O

rang

e-

yello

wSt

rept

omyc

esC

oast

al se

dim

ent

Ols

on m

ediu

m28

[29]

Him

alom

ycin

BC

43H

56O

1682

8.90

6Ye

llow

Stre

ptom

yces

Coa

stal

sedi

men

tO

lson

med

ium

28[2

9]Fr

idam

ycin

DC

31H

32O

1259

6.58

7Ye

llow

Stre

ptom

yces

Coa

stal

sedi

men

tO

lson

med

ium

28[2

9]S.

mar

cesc

ens:

Ser

ratia

mar

cesc

ens,

X. te

stud

inar

ia: X

esto

spon

gia

test

udin

aria

, H. c

heju

ensi

s: H

ahel

la c

heju

ensi

s, S.

gri

seov

irid

is: S

trept

omyc

es g

rise

ovir

idis

, P. d

enitr

ifica

ns: P

seud

oalte

rom

onas

de

nitr

ifica

ns, P

. rub

ra: P

seud

oalte

rom

onas

rubr

a, P

. den

itrifi

cans

: Pse

udov

ibri

o de

nitr

ifica

ns, P

. mar

ical

oris

: Pse

udoa

ltero

mon

as m

aric

alor

is, H

. pan

acea

: Hal

icho

ndri

a pa

nace

a, E

. sco

lope

s: E

upry

mna

sc

olop

es, C

. mar

inum

: Chr

omob

acte

rium

mar

inum

, C. f

ungi

vora

ns: C

ollim

onas

fung

ivor

ans,

P. a

erug

inos

a: P

seud

omon

as a

erug

inos

a, P

. phe

nolic

a: P

seud

oalte

rom

onas

phe

nolic

a, P

. tun

icat

e:

Pseu

doal

tero

mon

as tu

nica

te, S

WT:

Sea

wat

er-tr

ypto

ne, S

. par

vulu

s: S

trept

omyc

es p

arvu

lus,

LB: L

uria

–Ber

tani

, BH

I: B

rain

hea

rt in

fusi

on, P

. lut

eovi

olac

ea: P

seud

oalte

rom

onas

lute

ovio

lace

a,

J. li

vidu

m: J

anth

inob

acte

rium

livi

dum

, J. s

valb

arde

nsis

: Jan

thin

obac

teri

um sv

alba

rden

sis,

Z. ru

bidu

s: Z

oosh

ikel

la ru

bidu

s, G

YM

: Glu

cose

, yea

st e

xtra

ct a

nd m

alt e

xtra

ct



Table 2: Antibacterial activities of marine pigmented bacteria against different pathogenic and nonpathogenic bacteria

Contd...

Pigment compound Producer Antibacterial activity against Inhibition zone (mm)

Effective dose/MIC value

References

Prodigiosin Serratia sp. B. subtilis ATCC 11774 + 25-400 µl/ml [5]Methicillin‑resistant S. aureus +S. aureus ATCC 11632 +V. parahaemolyticus ATCC 17802 +

S. marcescens A. anitratus ≤9 20 µl [6]A. tumefaciens 10-14B. licheniformis 10-14B. cereus 10-14B. subtilis ≤9B. thuringiensis ≤9Erwinia sp. ≤9E. coli ≤9Micrococcus sp. ≤9Methicillin-resistant S. aureus ≥15S. epidermidis ≤9S. saprophyticus ≤9S. aureus ≤9

S. marcescens Alteromonas sp. 16.3±2.08 12.5-100 mg/L [30]Bacillus sp. 8.3±1.5Gallionella sp. 9.3±1.15Pseudomonas sp. 6.3±1.5

Vibrio sp. E. coli K-12 52% [8]S. aureus ATCC 12600 46%

Cycloprodigiosin Z. rubidus B. subtilis <9 50 µg [9]C. albicans <8.5E. coli 91.37%-96.98%Salmonella serovar Typhimurium <9S. aureus 96.62%-99.98%

Heptyl prodigiosin P. denitrificans S. aureus + [12]Norprodigiosin Serratia sp. B. subtilis ATCC 11774 + 50-400 µl/ml [5]

P. aeruginosa ATCC 27853 +S. aureus ATCC 11632 +Methicillin-resistant S. aureus +V. parahaemolyticus ATCC 17802 +

Glaukothalin Rheinheimera spp. Cytophaga Flavobacter Bacteroides group + 50 µL [1]Bacillus/clostridium group +

Indigoidine Leisingera sp. Muricauda sp. 5.9 500 mg/mL [16]P. leiognathi 2.9Ruegeria sp. 6.3V. anguillarum 3.3V. fischeri 4.2 250 mg/mL

Violacein C. fungivorans E. coli K12 + [17]M. luteus ATCC 9341 +Mycobacterium +N. meningitidis +Streptococcus spp. +

P. luteoviolacea S. aureus + >128 µg/mL [21]V. anguillarum +

J. lividum B. licheniformis IFO 12107 + 15 mg/L [18]B. megaterium IAM 1111 + 15 mg/LB. subtilis IAM 1026 + 10 mg/LE. coli HB 101 + >50 mg/L



Table 2: Contd...

Contd...



References

P. aeruginosa IAM 1054 + 15 mg/LS. aureus IAM 1011 + 15 mg/LT. cutaneum IFO 1198 + >50 mg/L

Deoxyviolacein J. lividum B. licheniformis IFO 12107 + 15 mg/L [18]B. megaterium IAM 1111 + 15 mg/LB. subtilis IAM 1026 + 10 mg/LE. coli HB 101 + >50 mg/LP. aeruginosa IAM 1054 + 15 mg/LS. aureus IAM 1011 + 15 mg/LT. cutaneum IFO 1198 + >50 mg/L

Tropodithietic acid Phaeobacter Halomonas sp./C. marina 3.0±0.0 70 μl [31]Micrococcus sp. 3.0±0.2Pseudomonas sp. 3.0±0.0Pseudoalteromonas sp. 3.0±0.0Marinomonas sp. 3.0±0.0Rhodococcus sp. 1.0±0.0O. marilimosa 2.9±0.3K. algicida 3.0±0.2V. anguillarum 3.0±0.3

Ruegeria Halomonas sp./C. marina 1.6±0.5Micrococcus sp. 2.9±0.3Pseudomonas sp. 0.9±0.8Pseudoalteromonas sp. 2.0±0.9Marinomonas sp. 2.3±1.0O. marilimosa 2.1±0.9K. algicida 2.0±0.5V. anguillarum 2.7±0.7

Roseobacter B. subtilis >6 10 µl of 1 mM concentration

[32]

Roseobacter V. anguillarum and V. splendidus

20-28 60 µl [33]

Roseobacter S. aureus 9 A colony spot of each strain

[23]R. mobilis/pelagia S. aureus 12-16

V. anguillarum 10-17Actinomycin D S. parvulus B. cereus 27 100 µg/mL [24]

B. megaterium 16B. sphaericus 24B. stearothermophilus 25B. subtilis 29E. coli 40K. pneumoniae 28M. luteus 27P. mirabilis 22P. aeruginosa 25P. putida 30S. paratyphi 25S. typhi 23

Pyocyanin P. aeruginosa Citrobacter sp. 17 25 mg/mL [25]P. aeruginosa M. smegmatis 24±1 [34]

Pyorubin P. aeruginosa Citrobacter sp. 13 25 mg/mL [25]Streptophenazine B Streptomyces sp. S. aureus ATCC 43300 + 4.2 µg/mL [13]N-acetyl-N-demethylmayamycin Streptomyces sp. S. aureus ATCC 43300 + 20.0 µM [14]



red pigment compound has been extracted from a marine sponge Xestospongia testudinaria associated bacteria Serratia marcescens. Intracellular extract of this S. marcescens showed

a wide range of antibacterial activity against Gram-positive and Gram-negative bacteria, and the highest zone of inhibition was found against methicillin-resistant S. aureus.[6]

Table 2: Contd...



References

Mayamycin Streptomyces sp. B. subtilis DSM 347 + IC50=8.0 µM [15]B. epidermidis DSM 20660 + IC50=7.45 µMD. hominis DSM 7083 + IC50=8.4 µMK. pneumoniae ATCC 700603 + IC50=2.5 µMP. acnes DSM 1897 + IC50=31.2 µMP. aeruginosa DSM 50071 + IC50=2.5 µMS. aureus ATCC 12600 + IC50=2.5 µMS. aureus‑MRSA ATCC 33593 + IC50=1.25 µMS. epidermidis DSM 20044 + IC50=0.31 µMS. lentus DSM 6672 + IC50=8.0 µMX. campestris DSM 2405 + IC50=30.0 µM

Melanin Streptomyces sp. E. coli 20 100 µl [26]K. oxytoca 17L. vulgaris 20P. mirabilis 19S. paratyphi 17S. typhae 17S. aureus 19V. cholerae 19

3,3’,5,5’-tetra-bromo-2, 2-biphenyldiol

P. phenolica E. faecalis + [27]E. faecium +E. serolicida +S. aureus MRSA + 1-2 µg/mlStreptococcus spp. +

Himalomycin A Streptomyces E. coli 25 ~50 µg/disk [29]S. aureus 32S. viridochromogenes 26 B. subtilis 23

Himalomycin B Streptomyces E. coli 24 ~50 µg/disk [29]S. aureus 33S. viridochromogenes 28B. subtilis 25

Fridamycin D Streptomyces E. coli 24 ~50 µg/disk [29]S. aureus 32S. viridochromogenes 25B. subtilis 26

Z. rubidus: Zooshikella rubidus, S. marcescens: Serratia marcescens, P. denitrificans: Pseudovibrio denitrificans, C. fungivorans: Collimonas fungivorans, S. parvulus: Streptomyces parvulus, P. aeruginosa: Pseudomonas aeruginosa, B. subtilis: Bacillus subtilis, S. aureus: Staphylococcus aureus, V. parahaemolyticus: Vibrio parahaemolyticus, A. anitratus: Acinetobacter anitratus, A. tumefaciens: Agrobacterium tumefaciens, B. licheniformis: Bacillus licheniformis, B. cereus: Bacillus cereus, B. thuringiensis: Bacillus thuringiensis, E. coli: Escherichia coli, S. epidermidis: Staphylococcus epidermidis, S. saprophyticus: Staphylococcus saprophyticus, C. albicans: Candida albicans, P. leiognathi: Photobacterium leiognathi, V. anguillarum: Vibrio anguillarum, V. fischeri: Vibrio fischeri, M. luteus: Micrococcus luteus, N. meningitidis: Neisseria meningitidis, B. megaterium: Bacillus megaterium, P. luteoviolacea: Pseudoalteromonas luteoviolacea, J. lividum: Janthinobacterium lividum, T. cutaneum: Trichosporon cutaneum, C. marina: Cobetia marina, B. sphaericus: Bacillus sphaericus, B. stearothermophilus: Bacillus stearothermophilus, K. pneumonia: Klebsiella pneumonia, P. mirabilis: Proteus mirabilis, P. putida: Pseudomonas putida, S. paratyphi: Salmonella paratyphi, R. mobilis: Ruegeria mobilis, M. smegmatis: Mycobacterium smegmatis, P. acnes: Propionibacterium acnes, S. lentus: Staphylococcus lentus, X. campestris: Xanthomonas campestris, K. oxytoca: Klebsiella oxytoca, L. vulgaris: Lactobacillus vulgaris, P. mirabilis: Proteus mirabilis, S. paratyphi: Salmonella paratyphi, V. cholera: Vibrio cholera, E. faecalis: Enterococcus faecalis, P. phenolica: Pseudoalteromonas phenolica, E. faecium: Enterococcus faecium, S. viridochromogenes: Streptomyces viridochromogenes, E. serolicida: Enterococcus serolicida, MRSA: Methicillin-resistant S. aureus, IC50: Half maximal inhibitory concentration, MIC: Minimum inhibitory concentration, O. marilimosa: Olleya marilimosa, K. algicida: Kordia algicida, S. typhi: Salmonella typhi, B. epidermidis: BreVibacterium epidermidis, S. typhae: Salmonella typhae, D. hominis: Dermabacter hominis, ATCC: American type culture collection, IFO: Institute for fermentation, IAM: Institute of applied microbiology, DSM: Deutsche sammhatg von mikroorganismen



Janthinobacterium sp. a violacein-producing bacterium isolated from Antarctic soil sample demonstrated potential inhibitory activity against different human Gram-negative bacterial pathogens, with varying concentrations of 0.5 and 16 µg/ml.[40] Pyocyanin a blue-green pigment produced by a hot spring isolate Pseudomonas aeruginosa possessed potential antimycobacterial activity against Mycobacterium smegmatis and other pathogenic bacteria.[34] Significantly, the production of indigoidine, a dark blue pigment by Leisingera sp., appeared to vary in pigment intensity in the presence of co-culture experiment, where higher pigment intensity was observed with the co-culture of Vibrio fischeri.[16] This Leisingera sp. is reported to display the antibacterial activity against different marine heterotrophic bacteria. Investigation by Leiva group found the association of a diverse community of Gram-positive yellow-, orange-, and amber-pigmented bacteria on Antarctic macroalgae (Adenocystis utricularis, Iridaea cordata, Monostroma hariotii, Plocamium cartilagineum, Phycodrys antarctica, and Pyropia endiviifolia) with potential antimicrobial activity against a set of macroalgae-associated bacteria.[41]

P. aeruginosa isolated from mangrove sediment samples of Vellar estuary produced blue-green pyocyanin and brownish pyorubin pigment compounds. These two compounds displayed maximum antibacterial activity at a concentration of 25 mg/mL with inhibition zones of 17 and 13 mm, respectively against Citrobacter sp.[25] Red pigment-producing vibrios (related to Vibrio rhizosphaerae and Vibrio ruber) isolated from different mangrove rhizospheres (Avicennia marina, Porteresia coarctata, and Rhizophora mucronata) have displayed antagonistic activity against both bacterial (Xanthomonas oryzae) and fungal (Fusarium oxysporum and Magnaporthe grisea) phytopathogens.[42]

A yellow-pigmented marine bacterium, M. luteus, isolated from seawater revealed the potential antibacterial activity against Staphylococcus sp., Klebsiella sp., and Pseudomonas sp.[43] Conversely, a strain of M. luteus BWCY16 isolated from seawater did not show inhibitory activity against Staphylococcus but showed the activity against Klebsiella and Pseudomonas.[44] These reports indicating that geographically different strains demonstrate species-specific antagonistic activity. S. marcescens CMST07, a red-pigmented estuarine bacterium exhibited antibacterial activity against different fouling bacteria Alteromonas, Bacillus, Gllionella, and Pseudomonas.[30] Streptomyces parvulus isolated from marine sediment sample produced a diffusible yellow pigment on YEME medium and also produced orange-red color antibiotic Actinomycin D that resulted potent antibacterial activity against different Gram-positive and Gram-negative bacterial pathogens and streptomycin-resistant strains such as Bacillus cereus and Pseudomonas putida.[24] Different textile fabrics treated with red pigment from a Vibrio species isolated from sweater sample has revealed distinctive inhibition activity against E. coli and S. aureus.[45] The yellow compounds fridamycin D and himalomycin A and B produced by Streptomyces sp. isolate B6921 have exhibited strong

inhibition activity against E. coli, S. aureus, Streptomyces viridochromogenes, and Bacillus subtilis [Tables 1 and 2]. Biological activities of several other novel pigment bacterial species being reported in the International Journal of Systematic and Evolutionary Microbiology are still remained to be investigated for biomedical applications.

HorIzontAl gene trAnsfer/gene AcquIsItIon

Pigment production in most of the known marine bacteria is due to the innate characteristic. However, the recent findings have suggested that bacteria-like Collimonas CT produce pigments due to gene acquisition (acquiring genes responsible for pigment production), probably acquired from J. lividum and/or Duganella sp.[17]

otHer APPlIcAtIons of PIgMents

Reputedly prodigiosins and violacein pigment molecules have been widely used in several other applications regardless of biomedical applications. Prodigiosins are reported to have high color staining capability and thus they are used to stain candles, soap, papers, as ink in ballpoint and highlighter pens, and have potential dye application as colorants to different fabrics such as acrylic fiber, cotton, polyester, and silk.[46,47] Application of virtual screening and prediction of bioactive nature of compounds in silico using various databases and docking programs would help to narrow down the range of such molecules to be tested in vitro and in vivo, which in turn can greatly reduce the economical investment in chemical synthesis and/or preliminary testing.[48]

conclusIon

Although synthetic medicines appear to fight against human pathogenic bacteria, a variety of side effects have reported due to these medicines. While synthetic food colorants also found to cause several side effects such as cancer. Therefore, search and demand for natural pigments from marine bacteria is required to replace synthetic compounds. Microbial pigments could certainly replace such synthetic compounds. Since marine microbes tolerate a wide range of environmental factors, they can be cultured in vitro and desired level of pigment production can be achieved for various applications such as dyes, textiles, food colorants, and medicines. Pigmented bacteria are indeed displayed multifunctional compounds over other nonpigmented bacteria. Although bioactive nature of several nonpigmented bacteria has been reported from the sea, the vast marine environment has not been explored for pigmented bacteria. Therefore, studies on isolation, maintenance, and pigment production by pigmented bacteria are required in vitro to explore and standardize and to develop novel pigments.

AcknowledgmentsRamesh is grateful to the Science and Engineering Research Board, New Delhi, for funding under the National



Postdoctoral Research Fellowship, grant number: SERB/N-PDF/2016/000354. We also thank the anonymous reviewers for their valuable comments and suggestions on this manuscript.

Financial support and sponsorshipThis work has been funded by Science and Research Engineering Board, New Delhi, under National Postdoctoral Research Fellowship awarded to Ramesh.

Conflicts of interestThere are no conflicts of interest.

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marine pigmented bacteria: a prospective source of

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