review article colorful world of microbes: carotenoids...

Review ArticleColorful World of Microbes Carotenoidsand Their Applications

Kushwaha Kirti1 Saini Amita1 Saraswat Priti2

Agarwal Mukesh Kumar2 and Saxena Jyoti3

1 Department of Bioscience and Biotechnology Banasthali University Jaipur Rajasthan 304022 India2 Biotechnology Division Defence Research and Development Establishment Gwalior Madhya Pradesh 474012 India3 Biochemical Engineering Department BT Kumaon Institute of Technology Dwarahat Uttarakhand 263653 India

Correspondence should be addressed to Saxena Jyoti saxenajyoti30gmailcom

Received 26 January 2014 Revised 2 March 2014 Accepted 4 March 2014 Published 10 April 2014

Academic Editor Akikazu Sakudo

Copyright copy 2014 Kushwaha Kirti et alThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Microbial cells accumulate pigments under certain culture conditions which have very important industrial applicationsMicroorganisms can serve as sources of carotenoids the most widespread group of naturally occurring pigments More than 750structurally different yellow orange and red colored molecules are found in both eukaryotes and prokaryotes with an estimatedmarket of $ 919 million by 2015 Carotenoids protect cells against photooxidative damage and hence found important applicationsin environment food and nutrition disease control and as potent antimicrobial agents In addition tomany research advances thispaper reviews concerns with recent evaluations applications of microbial pigments and recommendations for future researcheswith an understanding of evolution and biosynthetic pathways along with other relevant aspects

1 Introduction

The human eye does not see in black and white Color is oneof the first characteristics perceived by the human senses Itis integral to the interface between people and nature Natureis rich in colors obtained from fruits vegetables roots min-erals plants microalgae and so forth and due to their originfrom biological material they are often called ldquobiocolorsrdquo [1]Humans have traditionally preferred natural sources to addcolors to food clothing cosmetics and medicines Amongthe molecules produced by microorganisms are carotenoidsmelanins flavins phenazines quinones and bacteriochloro-phylls andmore specificallymonascins violacein and indigo[2 3]

2 Pigments from Microbes

A variety of natural and synthetic pigments are availableNaturally derived pigments are represented by carotenoidsflavonoids (anthocyanins) and some tetrapyrroles (chloro-phylls and phycobiliproteins) Lately interest in synthetically

derived pigments has decreased due to their toxic car-cinogenic and teratogenic properties and attention towardsmicrobial sources has increased as a safe alternative [2 4ndash7] Several species of algae fungi and bacteria have beenexploited commercially for the production of pigments [2 57]

An inventory ofmicroorganisms producing different pig-ments is given in Table 1 An ideal pigment producingmicroorganism should be capable of using a wide range of CandN sourcesmust be tolerant to pH temperature andmin-erals and must give reasonable color yield The nontoxic andnonpathogenic nature coupled with easy separation fromcell biomass are also preferred qualities Microbial pigmentshave many advantages over artificial and inorganic colorsOne relates this to fermentation which is an inherentlyfaster and more productive process as compared to otherchemical processes The other enduring strength of microbesis their relatively large and easily manipulated strands ofgenes Besides pigment production from microorganisms isindependent of weather conditions which produce differentcolor shades and grow on cheap substrates [8] Moreover

Hindawi Publishing CorporationAdvances in BiologyVolume 2014 Article ID 837891 13 pageshttpdxdoiorg1011552014837891

2 Advances in Biology

Table 1 List of pigments produced by different microorganisms

Pigment MicroorganismIndigoidine (blue-green) Streptomyces aureofaciens CCM 323 Corynebacterium insidiumCarotenoid Gemmatimonas aurantiaca T-277

Melanin (black-brown) Kluyveromyces marxianus Streptomyces chibanensis Cryptococcus neoformansAspergillus spWangiella dermatitidis Sporothrix schenckii andBurkholderia cepacia

Prodigiosin (red) Serratia marcescens Rugamonas rubra Streptoverticillium rsubrireticuli Serratiarubidaea Vibrio psychroerythrus Alteromonas rubraand Vibrio gaogenes

Zeaxanthin Staphylococcus aureus Vibrio psychroerythrus Streptomyces sp and Hahellachejuensis

Canthaxanthin (orange) Monascus roseus Bradyrhizobium spXanthomonadin (yellow) Xanthomonas oryzaeAstaxanthin (red) Phaffia rhodozyma Haematococcus pulvialisViolacein (purple) Janithobacterium lividumAnthraquinone (red) Pacilmyces farinosusHalorhodopsin and rhodopsin Halobacterium halobiumRosy pink Lamprocystis roseopersicinaVioletpurple Thiocystis violacea Thiodictyon elegansRosy peach Thiocapsa roseopersicinaOrange brown Allochromatium vinosumPinkPurple violet Allochromatium warmingii

pigment production from microbial sources has gainedattention owing to public sensitivity regarding ldquosynthetic foodadditivesrdquo

Microbial pigment production can be increased in geo-metric proportions through genetic engineering comparedto the scaling up methods of chemists Microbes have alsoupper hand in versatility and productivity over higher formsof life in the industrial-scale production of natural pigmentsand dyes Fermentation process has been increased by geneticengineering and further research for nontoxic microbialpigment can make quantum leaps in the economics ofmicrobial pigments

21 Carotenoid Carotenoids are a group of pigments ofwidely distributed classes of structurally and functionallydiverse tints from red to yellow present in a wide variety ofbacteria algae fungi and plants They are natural pigmentswhich occur widely in nature and are synthesized by plantsand microorganisms in response to various environmentalstresses whereas animals have to obtain them from food[9] Carotenoids are lipid soluble classes of molecules asso-ciated with the lipidic fractions sensitive to oxygen heatand light [10] From a chemical point of view carotenoidsare polyisoprenoid compounds and can be divided intotwo main groups (i) carotenes or hydrocarbon carotenoidswhich are composed of carbon and hydrogen atoms and(ii) xanthophylls that are oxygenated hydrocarbon derivativesthat contain at least one oxygen function such as hydroxylketo epoxy methoxy or carboxylic acid groups

211 Nomenclature Carotenoids have been given trivialnames derived from the biological sources from which they

were isolated first which conveyed no information abouttheir structure and therefore semisynthetic scheme has beendevised to allow any carotenoid to be named unambiguouslyin a way that defines and describes its structure All specificnames are based on the stem name ldquocarotenerdquo preceded bythe Greek letter prefixes that designate the two end groupsout of seven (120595 120573 120576 120574 120581 Φ and 120594) [19] The carotenoidpigmentsmost commonly found in nature including the onesof microbial origin belong to the groups given in Table 2 andit is true formicrobial carotenoids alsoThe IUPAC-IUB rulesare given in full in an IUPAC publication and in volume 1Aof the series carotenoids [20]

Some carotenoids have structure consisting of fewer than40 carbon atoms and derived formally by loss of part ofthe C40 skeleton When carbon atoms have been lost fromends of the molecule these compounds are referred to asapocarotenoids or norcarotenoids when carbon atoms havebeen lost formally from within the chain

212 General Properties In terms of hydrophobicity caro-tenoids are a group of extremely hydrophobic moleculeswith little or no solubility in water which usually do notincrease with increase in temperature [21] In the inner coremembranes of the cell they are expected to be restricted tohydrophobic areas whereas when associated with proteinsthey access to an aqueous environment Polarity of caroten-oids is altered by polar functional groups and interaction ofcarotenoids with other molecules is also affected

Shape of the carotenoid molecule depends on isomericforms (trans and cis) and can thus change properties ofcarotenoid affecting solubility and absorbability Trans formof carotenoids are more rigid and have a greater tendency to

Advances in Biology 3

Table 2 List of naturally produced pigments and their examples

Group ExampleHydrocarbons Lycopersene Phytofluene Hexahydrolycopene Torulene and 120572-Zeacarotene

AlcoholsAlloxanthin Cynthiaxanthin Pectenoxanthin CryptomonaxanthinCrustaxanthin Gazaniaxanthin OH-Chlorobactene LoroxanthinLycoxanthin Rhodopin Rhodopinol aka Warmingol and Saproxanthin

Glycosides Oscillaxanthin PhleixanthophyllEther Rhodovibrin Spheroidene

Epoxides Diadinoxanthin Luteoxanthin Mutatoxanthin Citroxanthin Zeaxanthinfuranoxide Neochrome Foliachrome Trollichrome and Vaucheriaxanthin

Aldehydes Rhodopinal Wamingone and TorularhodinaldehydeAcids and esters Torularhodin Torularhodin methyl ester

Ketones

Canthaxanthin aka Aphanicin Chlorellaxanthin CapsanthinCapsorubin Cryptocapsin 221015840Diketospirilloxanthin FlexixanthinPhoenicoxanthin Hydroxyspheriodenone Pectenolone Phoeniconone aka DehydroadonirubinPhoenicopterone Rubixanthone and Siphonaxanthin

Esters of alcohols Astacein Fucoxanthin Isofucoxanthin Physalien Zeaxanthindipalmitate and Siphonein

Apocarotenoids120573-Apo-21015840-carotenal Apo-2-lycopenal Apo-61015840-lycopenal AzafrinaldehydeBixin Citranaxanthin Crocetin Crocetinsemialdehyde Crocin DigentiobiosylHopkinsiaxanthin Paracentrone and Sintaxanthin

Nor or seco carotenoids Actinioerythrin 120573-Carotenone Peridinin Pyrrhoxanthininol Semi-120572-carotenoneSemi-120573-carotenone and Triphasiaxanthin

Retro carotenoids andretro apocarotenoids Eschscholtzxanthin Eschscholtzxanthone Rhodoxanthin and Tangeraxanthin

Higher carotenoid Nonaprenoxanthin Decaprenoxanthin and Bacterioruberin

crystallize or aggregate than cis forms Acyclic carotenoids(eg lycopene) are essentially long linear molecules withflexible end groups [19] The overall length of the moleculedepends on the effective bulk of the end groups Cyclizationshortens the overall length of the molecule and increases theeffective bulk of the end groups and space they occupy Thesteric factors and the presence of substituent groups decidethe preferred conformation of the effective bulk groupsOxidation reduction hydrogen abstraction and additionproperties of carotenoid molecule are given in detail bySimic [22] and Britton [19] However excited state propertiesof aryl carotenoids have been studied a few years backby femtosecond (10minus15 of a second) transient absorptionspectroscopy in important components of light harvestingantennae of green bacteria [23]

The carotenoid have many other independent biologi-cal functions including specific coloration in plants andanimals screening from excessive light and act as spec-tral filtering screenings in some invertebrates they pro-vide defensive action to egg protein against protease thedirect carotenoid derivative-retinal acts as visual pigmentin all animals and as chromophore in bacteriorhodopsinphotosynthesis retinoic acid in animals and abscisic acidin plants serve as hormones [24] Carotenoids are not onlyuseful for coloration but they have distinctive photochemicalproperties that form its basis as nutritional componentsvitamin A precursors in the prevention of human diseasessuch as cancer and as an industrial perspective The originof these photochemical properties lies in the disposition of

the low-lying excited energy (both singlet and triplet) of thecarotenoids Beta-carotene protects photosynthetic reactioncentre complexes against combination of light and oxygendamage [25] and provides effective treatment for humanpatients suffering from erythropoietic protoporphyria [26]Unique arrangement of electronic levels owing to polyenechain structuremakes carotenoid the only natural compoundthat protects the reaction centre from photo damage and iscapable of energy transfer from both carotenoid excited stateto chlorophyll in the light-harvesting complex and tripletchlorophyll or singlet oxygen to carotenoid in photosyntheticreaction centers [24] Last section of this review focuseson applications of pigments and carotenoids from microbialorigin while important physical chemical and biologicalproperties of carotenoids are compiled in Figure 1

213 Basic Structure

Conjugated Double and Single Bond Most striking featureof the carotenoid structure is the long system of alternateddouble and single bonds that forms the central part ofthe molecule which constitutes a conjugated system [19] Aconjugated double bond system of a polyene longer thannine is responsible for the pigment properties of carotenoidsNamely the energy of strong electronic transition [fromground energy level (1Ag

minus) to the S2 state (1Bu+)] corre-

sponds to the absorption between 400ndash500 nm and thereforecarotenoids are intensely coloured as yellow orange or red[19] The extent of the conjugation and the presence or


Carotenoids

Hydrophobic

Polar functional group governs polarity

Coloured yellow orange and red

Polyene chainstructure

Properties and functions dependon size and shape of end group structure of cis or trans isomer

Antioxidative agents due topresence of C

Lipophilic no solubility in water

Biological functions

Absorption in 400ndash500nm

C

- Vitamin A precursor

- Protection against oxidativedamage

- Preventing cancer

- Treatment of erythropoieticprotoporphyria

- Imparting colouration in plants

- Light and spectral filterationscreening

- Protection of egg protein(invertebrate) againstprotease

- Retinal visual pigment

- Environmental bioindicators

- Antimicrobial agent

- Food and nutrition

Figure 1 Important physical chemical and biological properties of carotenoids

absence of the functions determine the depth of colors ofthese molecules

Carotenoids are isoprenoid containing 40 carbon atomsper molecule variable number of hydrogen atoms and noother elementsThese are biosynthesized by tail to tail linkageof twoC-20 geranylgeranyl diphosphatemolecules to give theparent C-40 carbon skeleton from which all the individualvariations are derived Termination by hydrocarbon ring onone or both ends of the molecule is seen Since carotenesare hydrocarbons and therefore contain no oxygen Lycopeneand 120573120573-carotene can illustrate the basic C

40carbon skeleton

structure The basic structure can be modified by (i) cycliza-tion at one end or both ends of the molecule which givesrise to seven different end groups (Ψ 120573 120576 120574 120581 Φ and 120594)(ii) the change in hydrogenation level and (iii) the additionof oxygen containing functional groups to yield a family ofmore than 750 compounds [19] Structure and characteristicsof some common bacterial pigments are given in Table 3Theconjugated double bond system constitutes a rigid rod-likeskeleton of carotenoid molecules and provides high reduc-ing potential of carotenoid molecules which makes thempotent antioxidantsThe action of carotenoids as antioxidantsis importantly evaluated by reactions of carotenoids withoxidizing agents peroxy radicals and so forth This featureseems to play a key role in the stabilization function ofcarotenoids [27]

All carotenoids possess many conjugated double bondsusually 9ndash13 with each one being able to formmany geomet-rical isomers For example 120573-carotene has 9 double bonds inits polyene chain that can freely form cistrans configurationsTheoretically it can form 272 isomers while its asymmetric

isomer 120572-carotene is capable of forming 512 isomers [28]Chromophore and light absorption properties are widelyused in the identification of carotenoids [29]

214 Ultrastructural Organization of Carotenoids The caro-tenoids must have ability to fit in the correct location andorientation into this complex system The major featuressuch as overall shape size and hydrophobicity determine theability of a carotenoid to fit into the subcellular structuresThe characterization of the individual carotenoid given bystructural details then defines the precise orientation thatcarotenoid can adopt and interact with molecules of itssurroundings Interaction of polar functional group withmore polar molecules is focused on in order to allow thecarotenoid to participate in events in an aqueous subcellularmedium or at an interface or membrane

Carotenoid molecules interact with themselves and havea significant effect on properties They are hydrophobicand hence show a very strong tendency to aggregate andcrystallize in aqueous media In the form of microcrystallineaggregates carotenoids accumulation is commonly found inchromoplast of higher animals [19]

In membrane carotenoids are commonly located at anintegral part of complex membrane structure [30] In avariety of microorganisms orientation and localization ofcarotenoids in phospholipid liposome bilayer and monolayerinfluence membrane fluidity by increasing its rigidity andmechanical strength [19 31] The positioning of carotenoidin the membrane greatly depends on its molecular structurethe hydrocarbon 120573120573-carotene and lycopene are located inthe inner hydrophobic region of the membrane and helps to


Table 3 Structure and characteristics of some common bacterial pigments

Structure Characteristic Oxygen function

120573-Carotene

Bicyclic orange

LycopeneAcyclic red

NH

NH

N

O

Prodigiosin

Tripyrrole red 2 methoxy2 bipyrrole rings

HN

NH

NH

O

O

HO

Violacein

Purple-blue1 hydroxy group2 keto groups and3 bipyrrole ring

OH

HO

H3CH3C

H3C CH3CH3CH3

CH3CH3CH3

CH3

Zeaxanthin

Bicyclic yellow-orange 2 hydroxy groups

OH

HOO

O

Astaxanthin

Bicyclic red 2 hydroxy groups2 keto groups

OH

HO

H

Lutein

Bicyclic yellow 2 hydroxy groups


Table 3 Continued


OH

HOO

O

Violaxanthin

Bicyclic yellow 2 hydroxy groups2 epoxy-groups

HOOH

OHNeoxanthin

O Bicyclic yellow 3 hydroxy groups1 epoxy group

retain mobility On the other hand the diol zeaxanthin mayact as a revertThe entire membrane is spanned with its polarend groups which penetrates the surface of the membranestructure and increases its rigidity and mechanical strengthhence some carotenoids are more effective than others asmembrane based protective antioxidants [32]

Role of carotenoids in membrane stabilization has beencarried out by C-50 carotenoids with polar end groups as theyhave correct length for membrane stabilization C-50 bacte-rioruberin showed a higher rate of incorporation than thecyclic C-40 carotenoids particularly when the phospholipidmixture consisted of archaebacterial phytanyl lipids C-50carotenoids with polar end groups such as bacterioruberinhave a molecular length corresponding to the thickness ofvesicle lipid bilayers [33] In Acholeplasma laidlawii mobilityrestriction was studied by incubating the membrane withphosphatidylcholine vesicles The carotenoid depleted mem-brane showed an increase in the mobility of the hydrocarbonchain of the spin labeled fatty acids Artificial membraneincorporated with carotenoids restricted the mobility of thehydrocarbon chain hence it can be inferred that in Alaidlawii carotenoids act as a rigid insert which reinforced themembrane bilayer [34] Psychrotrophic strains ofMicrococcusroseus are also shown to produce bacterioruberin whichshows binding affinity with membrane vesicle and interactwithM roseus [35]

An experiment at ultrastructural and cytochemical levelby Petrunyaka [36] revealed localization of carotenoids incalcium sequestering organelles and their participation in themechanismofmembranous binding and transport of calciumin membrane structure of molluscan neurons

215 Carotenoid Protein Interaction Pigmentation is a com-mon feature of bacteria of different phylogenetic and environ-mental origins In general there are several groups of bacterialpigments which are non-covalently bound to proteins such aspigment-protein complexes These complexes are organizedas photosynthetic units consisting of either photosyntheticreaction centers or light harvesting complexe [37] Recently ina novel approachWackerbarth et al [38] bounded carotenoid

0

50

100

150

200

250

300

2007 2015

($ m

illio

n)

AstaxanthinCanthaxanthin

AnnatoOthers

120573-Carotene

Figure 2 Global carotenoid product market in 2007 and 2015 ($million) Analyst-Ulrich Marz

with bovine serum albumin (BSA) and then used carotenoid-protein complex to prepare food emulsions while Vernonand Augusto [39] studied action of 120572-chymotrypsin onchromatophores of Rhodospirillum rubrum which producedthree defined pigment protein complexes one with brownband and the other two were found in association withbacteriochlorophyll (blue B chl and green B chl)

216 Production and Biosynthesis of Carotenoids Accordingto a study the global market for carotenoid was $766 millionin 2007 and is expected to increase to $919 million by 2015with a compound annual growth rate (CAGR) of 23 120573-Carotene alone shared the market value at $247 million in2007 this segment is expected to be worth $285 millionby 2015 with CAGR of 18 as shown in Figure 2 [40]Carotenoids are composed of more than 700 structurallydifferent compounds typically consist of C-40 hydrocarbonbackbone and often produce cyclic and acyclic xanthophyllsby modification with various oxygen containing functional


groups [41] Carotenoid biosynthesis is catalyzed by a num-ber of enzymes which fall into few classes based on thetype of transformation they catalyze such as geranylger-anyl pyrophosphate synthase phytoene synthase carotenedesaturase and lycopene cyclase Modification of carotenesis further catalyzed by 120573-carotene ketolase and 120573-carotenehydrolase to generate various C-40 carotenoids The initialseries of steps in the formation of carotenoids belongs to themevalonate pathway the general biosynthesis scheme of allisoprenoid compounds This general isoprenoid biosyntheticpathway which synthesizes carotenoids and other importantnatural substances in oxygenic photosynthetic (cyanobacte-ria algae and higher plants) and nonphotosynthetic bacteriais been described step by step in detail by many researchers[37 42ndash48]

No animal is known to make antioxidants thereforescientists thought the only way animals could obtain thesethrough orange-red compounds was from their diet How-ever in recent findings researchers of Arizona Universityreported that aphids can make their own essential nutrientscalled carotenoids by lateral gene transfer [49]

In environment where colorful patterns in lakes and soilsare found a variety of bacterial pigments have been found toplay important roles Carotenoids were found in abundancein northern ice shelf microbial mats and exceeded the rangeof carotenoid concentration reported from Antarctica [50]and in the Arctic including those previously measured inMarkham ice shelf [51] However the ratio of chlorophyll ldquoardquowas higher than carotenoids but not as high as in Antarctica[52] and in nearby Arctic mats [53] Arctic ice shelf microbialmats contain a broadband pigment assemblage that absorbbetween the near UV-B to red photosynthetically activeradiation (PAR) which is probably beyond the absorption ofpigment present in photosynthetic bacteria These pigmentscan be classed as screening compounds (OS-MAArsquoS) lightharvesting and accessory pigments (chlorophylls phyco-biliproteins certain carotenoids and perhaps MAArsquoS) Redcolor of saltern crystallizer ponds and hypersaline lakes isdue to red halophilic archea of the family HalobacteriaceaeMost of the color of the saltern pond may still be attributedto bacterioruberin pigments and the effect is due to thelow in vivo optical cross section of the 120573-carotene whichis densely packed in granules in the inter thylakoid spacewithin chloroplast polar lipid analysis of biomass (Santa PolaSalterns) shower Further studies revealed that Salinibacterand other bacteria had minor contribution but halophilicbacteria significantly contributed in the color of ponds [54]

3 Applications of MicrobialPigments and Carotenoids

Carotenoids are an important group of natural pigmentswith specific applications as colorants food supplements andnutraceuticals they are also used for medical cosmetic andbiotechnological purposes [55]

31 Pigments as Bioindicators Violet pigmented bacteriaalong with species of Flexibacter and Sporocytophaga wereindicators of polluted drinking water samples [56] Blue

pigmented bacteria Vogesella indigofera can be used as abioindicator of chromium contaminated sites Under nor-mal environmental growth conditions bacterial colonies arepigmented blue but under metal contaminated growth con-ditions Cr6+ induces rugosity and inhibits gene expressionencoded for blue pigment production as it has been regardedas defensive mechanism performed by bacteria against heavymetal tolerance or environmental stress [57 58] Nianhonget al [59] used pigments derived from the anoxygenicphototrophic brown bacteria Chlorobium phaeovibroides andC phaeobacteroides to document the changes in hypoxicevent on the Louisiana shelf over the past 100 years

32 Pigments in Food and Nutrition Early in 1900 a fatsoluble principle was explored that was essential for life andwas termed as Vitamin A After a few decades a link betweenVitamin A and carotenoids was discovered and later on it wasconcluded thatmany of the carotenoids could bemetabolizedby the body to form Vitamin A 120573-Carotene finds applicationas solution or suspensions in vegetable oils in colouringmargarine baked products and some prepared foods inthe form of emulsions or microencapsulated beadlets Italso has applications in beverages such as orange drinksconfectionary and other prepared foods [60] In a novelapproach carotenoids were first bound to bovine serumalbumin (BSA) and later on this carotenoid-protein complexwas used to prepare fortified food emulsions [38] Table 4illustrates the microorganisms producing different pigmentsand their applications in various food industries

33 Pigments in Disease Control and Human Health Inhuman beings carotenoids as provitamin A can serve asseveral important functions [61] Recently it has been con-cluded that ingestion of carotene rich yellow and greenleafy vegetables improved the total body Vitamin A poolsize and hemoglobin concentration subsequently decreasedanaemia rates in Fillipino school children with no effect oniron deficiency [62] Role of carotenoids on photoprotectionagainst genetic diseases erythropoietic protoporphyria (EPP)and erythema (skin reddening) has been observed due tophotosensitivity associated with quinidine ingestion whichabsorb dangerous short wavelength part of light spectrum[63 64]

Premature deaths in the developing nations particularlyamongst children have been attributed to deficiency ofVitamin A Vitamin A which performs many vital functionsin human can be produced within the body from certaincarotenoids particularly 120573-carotene [65 66] Lycopene ahydrocarbon with antioxidant effect mitigated the damagingeffect of oxidation which majorly contributes to the riskof chronic diseases [67] and was found to be effective atquenching the destructive potential of singlet oxygen [68]Lutein zeaxanthin and xanthophyll occur in corn kale andspinach and are believed to play a critical role in protectionof the age-relatedmacular degeneration (ARMD) the leadingcause of blindness in human retina by action as an antioxidant[69] Astaxanthin has also health benefits in cardiovasculardisease prevention immune system boosting bioactivity


Table 4 Microbial pigments in food industry

Microorganism Pigment Application in food

Xanthophyllomyces dendrorhous Astaxanthin Feed supplement for salmons crabs shrimps chickens and eggproduction

Ashbya gossypii Riboflavin

Pseudomonas aeruginosa Colorant in beverages cakes confectionaries pudding decorationof food items [11]

Monascus sp Ankaflavin Color supplementPenicillium oxalicum AnthraquinoneFusarium sporotrichioides LycopeneHaematococcus pluvialis Astaxanthin As animal feed fish mealSaccharomyces neoformans Melanin

Monascus sp MonascorubraminRubropunctatin

Neospongiococcum excentricum Zeaxanthin Colorant for poultry and fishCordyceps unilateralis NaphtoquinoneRhodotorula sp Torularhodin

Flavobacterium ZeaxanthinAs an additive in poultry feed to increase yellow color of animalrsquosskin and eggyolk [12]Colorant in cosmetic and food industry

Bradyrhizobium sp Canthaxanthin Impart color in farmed salmonsHalobacterium sp Canthaxanthin [13]Cantharellus cinnabarinus Canthaxanthin Poultry feeds and fish feedsBrevibacterium KY-4313Rhodococcus maris(Mycobacterium brevicale)

Canthaxanthin

Corynebacterium michiganense [2]Agrobacterium auranticum Astaxanthin Food colourant [14]Paracoccus carotinifaciens Astaxanthin Food colourant [15]Mycobacterium lacticola Astaxanthin Fish feedsBrevibacterium 10Phafja rhodozymaPeniophora sp [2]Streptomyces echinoruber Rubrolone Food colorantParacoccus zeaxanthinifaciens Zeaxanthin Food colorant [16]Flavobacterium sp Zeaxanthin Poultry feed and fish feed [2]Streptomyces coelicolor Actinorhodin Edible natural pigment and food colorant [17]Blakeslea trispora and Dunaliellasalina 120573-Carotene Food colourant [2]

Blakeslea trispora Lycopene Food colourantStreptomyces chrestomyceticus [2]Spongiococcum excentricum Lutein Poultry feedsChlorella pyrenoidosa [2]Protomonas extorquens Rhodoxanthin [2]

against Helicobacter pylori and cataract prevention due to itshigh antioxidant activityThehealth benefits of astaxanthin inin vitro studies and also in the preclinical trials with humanshave mostly been performed inmany researches [2 5 70 71]

Other antioxidant carotenoids were used to treat car-diovascular disease (CVD) using membrane enriched withpolyunsaturated fatty acids [72] enhancement of immune

system function [73] sun burn protection [74] and inhibitionof the development of certain types of cancer [75] Oxidationof low density lipoprotein (LDL) cholesterol and reduction inthe risk of development of arteriosclerosis and coronary heartdiseases were observed due to lycopene [76] Carotenoidpigments present in the eye and photoreceptors seemespecially suited to protect against the deleterious effects


Table 5 Microbial pigments as potential virulence agents [18] (ROS reactive oxygen species)

Pigment Chemistry Color Human pathogens Virulence functionsStaphyloxanthin Carotenoid Golden Staphylococcus aureus Antioxidant detoxify ROS

Pyocyanin Phenazine derivedZwitterion

Bluegreen Pseudomonas sp Cytotoxicity neutrophil apoptosis

ciliary dysmotility proinflammatory

Melanin Polyacetylene orpolypyrrole polymers

Dark-brownblack

Cryptococcus neoformansWangiella dermatitidisSporothrix schenckiiSporothrix schenckii

Aspergillus sp

AntioxidantsAntiphagocytic

Block antimicrobials

Porphyrin Heteromacrocycle Black Porphyromonas gingivalis Antioxidant detoxify ROS

Granadaene Ornithinerhamno-polyene

Orangered Streptococcus agalactiae Antioxidant detoxify ROS

Violacein Rearrangedpyrrolidone scaffold Purple Chromobacterium

violaceum Antioxidant detoxify ROS

Prodigiosin Linear tripyrrole Red Serratia marcescens Immunosuppressant

Hemozoin 120573-hematin aggregates Brown-black Plasmodium sp Detoxification macrophage suppressionproinflammatory

of light because of their capability to absorb the dangerousshort wavelength of the light spectrum Carotenoids are wellknown for ldquoquenchingrdquo in plant tissues and photoexcitationof sensitizing pigments and oxygen in animal tissues [64]Prodigiosin from Serratia marcescens is the pigment ofhigh medical importance as its anticancerous activity onHeLa cell lines was reported by Campas et al [77] Earliermany other medically important activities of prodigiosinhave also been reported such as in lymphocytic leukemiaapoptosis in gastric (HGT-1) cancer cell lines apoptosis inhaematopoietic cancer cell line [78] cytotoxic sensitivity ofthe human small cell lung doxorubicin resistant carcinoma(GLC4ADR) cell lines [79] synergistic inhibitory activityagainst spore germination of Botrytis cinerea [80] andselective activity against cancer cell lines [81] Prodigiosinfrom Serratia marcescens [82] Vibrio psychroerythrous [83]and Pseudomonas magneslorubra also have been reported asantifungal immunosuppressive and antiproliferative agentsin early days of 1970s

Data has been collected regarding the efficacy of variouscarotenoids in prevention of diseases in combination withother therapies [84ndash90] A leading hypothesis in mechanismof action of carotenoids is that they serve as singlet oxygenquenchers and antioxidants a group of large number ofdietary and endogenous components functions as antioxi-dants in preventing free radical damage to critical cellularcomponents as carotenoids do not act alone [91]

34 Pigments and the Immune System Role of carotenoidsin modulating immunological reactions has been noticed byseveral workers The pigments enhanced both specific andnonspecific immune functions and showed the capability toenhance tumor immunity Postulates have been given for roleof carotenoids in enhancing immune activity by (i) quenchingexcessive reactive species formed by various immunoac-tive cells (ii) quenching immunosuppressive peroxides andmaintaining membrane fluidity (iii) helping to maintain

membrane receptors essential for immune functions and (iv)acting in the release of immunomodulatory lipid moleculessuch as prostaglandins and leukotrienes [92] Color ofcolonies is a hallmark feature of several pathogenic microbesBy interfering with host immune clearance mechanismsor by exhibiting proinflammatory or cytotoxic propertiesthe microbial pigment sometimes contributes to diseasepathogenesis Contribution of pigmentation in virulence byallowing a givenmicrobe to evade host immunity by killing orprovoking inflammatory damage to cells and tissues is givenin Table 5 [18]

35 Pigments as Antimicrobial Agents Nature is rich in colors(minerals plants microalgae etc) and pigment producingmicroorganisms (fungi yeast and bacteria) As stated inintroduction among the molecules produced by microorgan-isms (carotenoidsmelanins flavins and quinones andmorespecifically monascins violacein and indigo) pyocyaninand pyorubin pigments of Pseudomonas aeruginosa showeddistinct antibacterial effect against Citrobacter sp a mem-ber of the family Enterobacteriace which causes urinarytract infections wound infections and sometimes pneumo-nia in humans especially in immunocompromised persons[11] Seven carotenoids namely (all-E)-luteoxanthin (all-E)-neoxanthin (91015840Z)-neoxanthin (all-E)-antheraxanthin (all-E)-violaxanthin (91015840Z)-violaxanthin and (all-E)-lutein wereisolated from golden delicious apple and showed potentanti-Helicobacter pylori activity (CMIC

50= 36 120583gmL) [93]

An actinomycete strain Streptomyces hygroscopicus subspossamyceticus D

10 produced a yellow color sugar containing

pigment with antimicrobial activity against drug resistantpathogens such asmethicillin resistant and vancomycin resis-tant strains of Staphylococcus aureus 120573-lactamase producingculture of E coli Pseudomonas aeruginosa and Klebsiella sp[94] Similarly a yellowish pigment 4-hydroxynitrobenzenefrom Streptomyces species was isolated which later showedantibiotic activity against Bacillus subtilis and Shigella shiga


[95] Hydrophobic amino acid derivatives (L-Tyr and L-Phe)from monascins exhibited antimicrobial activity against Ecoli [96] Inhibition of human pathogenic bacteria Staphy-lococcus aureus Klebsiella pneumoniae and Vibrio cholerawas observed by endophytic fungal pigment of Monodictyscastaneae [97]

4 Questions to Be Answeredand Future Outlook

Steps are being taken towards understanding the unfamiliarworld of microbes but there are still many questions tobe explored and currently exist as unanswered The spectraof compounds that are potentially diverse in function aregenerated by pigment biosynthetic pathways The functionsand the regulation of synthesis of specific product subsetsunder different environmental conditions are another areawaiting to be investigated A large number of catalyticsteps and metabolic expenditure are involved in biosyntheticpathways and hence pigments are very important The otherquestions which often arise are as follows How do microbialcells put together complex pigment biosynthetic pathwaysand what are evolutionary processes shape assembly of thefinal pathway How can pigment properties and biosyntheticpathways be exploited for drug discovery and other impor-tant applications for engineering of novel agents

The understanding of structure-function relationshipswill enable researchers to tailor new bacterial pigmentsfor biotechnological applications Due to the high cost ofthe currently used technology for the microbial pigmentproduction on an industrial scale there is a need fordeveloping low cost process for the production of the pig-ments that could replace the synthetic ones Developmentsin research is expected from interchange of experiencesbetween biochemists geneticists biochemical engineers andso forth Colorful bacteria represent an extremely versatilegroup of microorganisms capable of a variety of importantapplications thereby presenting a fascinating field for futureresearch

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] P Pattnaik U Roy and P Jain ldquoBiocolours new generationadditives for foodrdquo Indian Food Industry vol 16 no 5 pp 21ndash321997

[2] H J Nelis and A P de Leenheer ldquoMicrobial sources ofcarotenoid pigments used in foods and feedsrdquo Journal of AppliedBacteriology vol 70 no 3 pp 181ndash191 1991

[3] L Dufosse ldquoPigmentsrdquo Encyclopedia of Microbiology vol 4 pp457ndash471 2009

[4] S Babu and I S Shenolikar ldquoHealth and nutritional implica-tions of food coloursrdquo Indian Journal of Medical Research vol102 pp 245ndash249 1995

[5] E A Johnson and W A Schroeder ldquoMicrobial carotenoidsrdquoAdvances in biochemical engineeringbiotechnology vol 53 pp119ndash178 1996

[6] V R O Canizares L E Rios R R Olvera N T Ponceand R F Marquez ldquoMicrobial sources of pigmentsrdquo RevistaLatinoamericana de Microbiologıa vol 40 no 1-2 pp 87ndash1071998

[7] S Babitha Biotechnology for Agro-Industrial Residues Utiliza-tion II Microbial Pigments 2009

[8] V K Joshi D Attri A Bala and S Bhushan ldquoMicrobialpigmentsrdquo Indian Journal of Biotechnology vol 2 no 3 pp 362ndash369 2003

[9] H Klaui ldquoIndustrial and commercial uses of carotenoidsrdquo inIUPAC Carotenoid Chemistry and BioChemistry G Britton andTW Goodwin Eds pp 309ndash317 Pergamon Press Oxford UK1982

[10] I H Ciapara L F Valenzuela F M Goycoolea and WA Monal ldquoMicroencapsulation of astaxanthin in a chitosanmatrixrdquo Carbohydrate Polymers vol 56 no 1 pp 41ndash45 2004

[11] S Saha R Thavasi and S Jayalakshmi ldquoPhenazine pigmentsfrom Pseudomonas aeruginosa and their application as antibac-terial agent and food colourantsrdquo Research Journal of Microbiol-ogy vol 3 no 3 pp 122ndash128 2008

[12] S Alcantara and S Sanchez ldquoInfluence of carbon and nitrogensources on Flavobacterium growth and zeaxanthin biosynthe-sisrdquo Journal of Industrial Microbiology and Biotechnology vol23 no 1 pp 697ndash700 1999

[13] J Lorquin F Molouba and B L Dreyfus ldquoIdentification ofthe carotenoid pigment canthaxanthin from photosyntheticBradyrhizobium strainsrdquo Applied and Environmental Microbi-ology vol 63 no 3 pp 1151ndash1154 1997

[14] A Yokoyama H Izumida and W Miki ldquoProduction ofastaxanthin and 4-ketozeaxanthin by the marine bacteriumAgrobacteriumaurantiacumrdquoBioscience Biotechnology andBio-chemistry vol 58 no 10 pp 1842ndash1844 1994

[15] A Tsubokura H Yoneda and H Mizuta ldquoParacoccus caro-tinifaciens sp nov a new aerobic Gram-negative astaxanthin-producing bacteriumrdquo International Journal of Systematic Bac-teriology vol 49 no 1 pp 277ndash282 1999

[16] M Humbelin A Thomas J Lin J Li J Jore and A BerryldquoGenetics of isoprenoid biosynthesis in Paracoccus zeaxanthini-faciensrdquo Gene vol 297 no 1-2 pp 129ndash139 2002

[17] H C Zhang J X Zhan K M Su and Y X Zhang ldquoA kindof potential food additive produced by Streptomyces coelicolorcharacteristics of blue pigment and identification of a novelcompound 120582-actinorhodinrdquo Food Chemistry vol 95 no 2 pp186ndash192 2006

[18] G Y Liu and V Nizet ldquoColor me bad microbial pigments asvirulence factorsrdquoTrends inMicrobiology vol 17 no 9 pp 406ndash413 2009

[19] G Britton ldquoStructure and properties of carotenoids in relationto functionrdquo The FASEB Journal vol 9 no 15 pp 1551ndash15581995

[20] ldquoIUPAC commission on the nomenclature of organic chemistryand IUPAC-IUB commission on biochemical nomenclaturenomenclature of carotenoids (Rules approved 1974)rdquo Pure andApplied Chemistry vol 41 pp 407ndash431 1975

[21] A Wisniewska and W K Subczynski ldquoEffects of polarcarotenoids on the shape of the hydrophobic barrier of phos-pholipid bilayersrdquo Biochimica et Biophysica Acta vol 1368 no2 pp 235ndash246 1998


[22] MG Simic ldquoCarotenoid free radicalsrdquoMethods in Enzymologyvol 213 pp 444ndash453 1992

[23] M Fuciman P Chabera A Zupcanova et al ldquoExcited stateproperties of aryl Carotenoidsrdquo Physical Chemistry ChemicalPhysics vol 12 no 3 pp 3112ndash3120 2010

[24] A Vershinin ldquoBiological functions of Carotenoidsmdashdiversityand evolutionrdquo BioFactors vol 10 no 2-3 pp 99ndash104 1999

[25] H A Frank and R J Cogdell ldquoThe photochemistry andfunctions of carotenoids in photosynthesisrdquo in Carotenoids inPhotosynthesis A Young and G Britton Eds pp 252ndash326Springer London UK 1993

[26] M M Mathews-Roth ldquoMedical application and uses ofCarotenoidsrdquo in Carotenoid-Chemistry and BoichemistryIUPAC G Britton and T W Goodwin Eds pp 297ndash307Pergamon Press Oxford UK 1982

[27] W I Gruszecki and K Strzałka ldquoCarotenoids as modulators oflipid membrane physical propertiesrdquo Biochimica et BiophysicaActa vol 1740 no 2 pp 108ndash115 2005

[28] J A Olson and N I Krinsky ldquoIntroduction the colorfulfascinating world of the carotenoids important physiologicmodulatorsrdquo The FASEB Journal vol 9 no 15 pp 1547ndash15501995

[29] G Britton ldquoUVVisible spectroscopyrdquo in Spectroscopy 1BG Britton J S Liaanen and H Pfander Eds pp 13ndash62Birkhauser Basel Switzerland 1995

[30] W I Gruszecki and J Sielewiesiuk ldquoOrientation of xanthophyllsin phosphatidylcholine multibilayersrdquo Biochimica et BiophysicaActa vol 1023 no 3 pp 405ndash412 1990

[31] G A Armstrong ldquoGenetics of eubacterial carotenoid biosyn-thesis a colorful talerdquo Annual Review of Microbiology vol 51pp 629ndash659 1997

[32] N J C Fong M L Burgess K D Barrow and D R GlennldquoCarotenoid accumulation in the psychrotrophic bacteriumArthrobacter agilis in response to thermal and salt stressrdquoApplied Microbiology and Biotechnology vol 56 no 5-6 pp750ndash756 2001

[33] G Ourisson and Y Nakatani ldquoBacterial Carotenoids as mem-brane reinforcers a general role of polyterpenoids membranestabilizationrdquo in Carotenoids Chemistry and Biochemistry N IKrinsky M M Mathew-Roth and R F Taylor Eds pp 237ndash245 Plenum Press New York NY USA 1989

[34] S Rottem and O Markowitz ldquoCarotenoids act as reinforcers oftheAcholeplasma laidlawii lipid bilayerrdquo Journal of Bacteriologyvol 140 no 3 pp 944ndash948 1979

[35] M V Jagannadham K Narayanan C Mohan Rao and SShivaji ldquoIn vivo characteristics and localisation of carotenoidpigments in psychrotrophic and mesophilicMicrococcus roseususing photoacoustic spectroscopyrdquo Biochemical and BiophysicalResearch Communications vol 227 no 1 pp 221ndash226 1996

[36] V V Petrunyaka ldquoLocalization and role of carotenoids inmolluscan neuronsrdquo Cellular and Molecular Neurobiology vol2 no 1 pp 11ndash20 1982

[37] R J Cogdell P Fyfe N Fraser et al ldquoPhotosynthetic lightharvestingrdquo in Microbial Responses to Light and Time M XCaddick S Baumberg D AHodgson andMK Phillips JonesEds pp 143ndash158 SGM symposium Cambridge UniversityPress Cambridge UK 1998

[38] HWackerbarth T Stoll S Gebken C Pelters and U BindrichldquoCarotenoid-protein interaction as an approach for the formu-lation of functional food emulsionsrdquo Food Research Interna-tional vol 42 no 9 pp 1254ndash1258 2009

[39] L P Vernon and F G Augusto ldquoPigment protein complexesderived from Rhodospirillum rubrum chromatophores by enzy-matic digestionrdquo Biochimica et Biophysica Acta vol 143 no 1pp 144ndash153 2003

[40] report code FOD025C 2008 httpwwwbccresearchcomreportFOD025Chtml

[41] G A Armstrong ldquoEubacteria show their true colors geneticsof carotenoid pigment biosynthesis from microbes to plantsrdquoJournal of Bacteriology vol 176 no 16 pp 4795ndash4802 1994

[42] S Pandian S Saengchjan and T S Raman ldquoAn alternativepathway for the biosynthesis of isoprenoid compounds inbacteriardquo Biochemical Journal vol 196 no 3 pp 675ndash681 1981

[43] M S Anderson J G Yarger C L Burck andCD Poulter ldquoFar-nesyl diphosphate synthetaseMolecular cloning sequence andexpression of an essential gene from Saccharomyces cerevisiaerdquoJournal of Biological Chemistry vol 264 no 32 pp 19176ndash191841989

[44] Y Tani ldquoMicrobial production of vitamin B6 and derivativesrdquoin Biotechnology of Vitamins Pigments and Growth Factors E JVandamme Ed pp 221ndash230 Elsevier London UK 1989

[45] S Fujisaki H Hara Y Nishimura K Horiuchi and T NishinoldquoCloning and nucleotide sequence of the ispA gene responsiblefor farnesyl diphosphate synthase activity in Escherichia colirdquoJournal of Biochemistry vol 108 no 6 pp 995ndash1000 1990

[46] J SchwenderM SeemannH K Lichtenthaler andMRohmerldquoBiosynthesis of isoprenoids (carotenoids sterols prenyl side-chains of chlorophylls and plastoquinone) via a novel pyru-vateglyceraldehyde 3-phosphate non-mevalonate pathway inthe green alga Scenedesmus obliquusrdquo Biochemical Journal vol316 no 1 pp 73ndash80 1996

[47] D Umeno A V Tobias and F H Arnold ldquoDiversifyingcarotenoid biosynthetic pathways by directed evolutionrdquoMicro-biology and Molecular Biology Reviews vol 69 no 1 pp 51ndash782005

[48] C Liang F Zhao W Wei Z Wen and S Qin ldquoCarotenoidbiosynthesis in cyanobacteria structural and evolutionary sce-narios based on comparative genomicsrdquo International Journal ofBiological Sciences vol 2 no 4 pp 197ndash207 2006

[49] N A Moran and T Jarvik ldquoLateral transfer of genes from fungiunderlies carotenoid production in aphidsrdquo Science vol 328 no5978 pp 624ndash627 2010

[50] W F Vincent M T Downes RW Castenholz and C Howard-Williams ldquoCommunity structure and pigment organisationof cyanobacteria-dominated microbial mats in AntarcticardquoEuropean Journal of Phycology vol 28 no 4 pp 213ndash221 1993

[51] W F Vincent D R Mueller and S Bonilla ldquoEcosystems on icethe microbial ecology of Markham Ice Shelf in the high ArcticrdquoCryobiology vol 48 no 2 pp 108ndash112 2004

[52] K Sabbe D A Hodgson E Verleyen et al ldquoSalinity depth andthe structure and composition of microbial mats in continentalAntarctic lakesrdquo Freshwater Biology vol 49 no 3 pp 296ndash3192004

[53] D R Mueller W F Vincent S Bonilla and I LaurionldquoExtremotrophs extremophiles and broadband pigmentationstrategies in a high arctic ice shelf ecosystemrdquo FEMS Microbi-ology Ecology vol 53 no 1 pp 73ndash87 2005

[54] A Oren and F Rodriguez-Valera ldquoThe contribution ofhalophilic Bacteria to the red coloration of saltern crystallizerpondsrdquo FEMS Microbiology Ecology vol 36 no 2-3 pp 123ndash130 2001


[55] J F Martin E Gudina and J Barredo ldquoConversion of 120573-carotene into astaxanthin two separate enzymes or a bifunc-tional hydroxylase-ketolase proteinrdquo Microbial Cell Factoriesvol 7 no 3 pp 1475ndash2859 2008

[56] P R G Schindler and H Metz ldquoBacteria of the FlexibacterSporocytophaga group and violet-colored bacteria as indicatorsof hygienic hazardous drinking waterrdquo Zentralblatt fur Hygieneund Umweltmedizin vol 189 no 1 pp 29ndash36 1989

[57] J-D Gu and K H Cheung ldquoPhenotypic expression ofVogesellaindigoferaupon exposure to hexavalent chromiumCr6+rdquoWorldJournal ofMicrobiology and Biotechnology vol 17 no 5 pp 475ndash480 2001

[58] Z Vanessa and C Cardona Molecular analysis physiologicalstudy and biotechnological capabilities of blue pigmented bacteriafrom Puerto Rico [PhD dissertation] University of Puerto Rico2010

[59] C Nianhong T S Bianchi B A McKee and J M BlandldquoHistorical trends of hypoxia on the Louisiana shelf applicationof pigment as biomarkersrdquoOrganic Geochemistry vol 32 no 4pp 543ndash561 2001

[60] E J Vandamme ldquoBiotechnology of Vitamins Pigments ofgrowth factorsrdquo in Applied Sciences E J Vandamme Ed pp15ndash21 Elsevier Science Publishers London UK 1989

[61] A Zeb and S Mehmood ldquoCarotenoids content from varioussources and their potential health applicationsrdquo Pakistan Jour-nal of Nutrition vol 3 no 3 pp 199ndash204 2004

[62] C C Maramag J D Ribaya-Mercado P Rayco-Solon et alldquoInfluence of carotene-rich vegetable meals on the prevalenceof anaemia and iron deficiency in Filipino school childrenrdquoEuropean Journal of Clinical Nutrition vol 64 no 5 pp 468ndash474 2010

[63] A Kornhauser W Wamer and L Lambert in CarotenoidsChemistry and Biology N I KrinskyMMMathews-Roth andR F Taylor Eds pp 301ndash312 Plenum Press New York NYUSA 1990

[64] K Ibrahim T J Hassan and S N Jafarey ldquoPlasma vitamin Aand carotene inmaternal and cord bloodrdquoAsia-Oceania Journalof Obstetrics and Gynaecology vol 17 no 2 pp 159ndash164 1991

[65] S Patton L M Canfield G E Huston A M Ferris and R GJensen ldquoCarotenoids of human colostrumrdquo Lipids vol 25 no3 pp 159ndash165 1990

[66] A V Rao and L G Rao ldquoCarotenoids and human healthrdquoPharmacological Research vol 55 no 3 pp 207ndash216 2007

[67] P Di Mascio S Kaiser and H Sies ldquoLycopene as the most effi-cient biological carotenoid singlet oxygen quencherrdquoArchives ofBiochemistry and Biophysics vol 274 no 2 pp 532ndash538 1989

[68] D M Snodderly ldquoEvidence for protection against age-relatedmacular degeneration by carotenoids and antioxidant vita-minsrdquo American Journal of Clinical Nutrition vol 62 no 6 pp1448Sndash14615S 1995

[69] M G Sajilata R S Singhal and M Y Kamat ldquoThe carotenoidpigment zeaxanthinmdasha reviewrdquoComprehensive Reviews in FoodScience and Food Safety vol 7 no 1 pp 29ndash49 2008

[70] P Bhosale ldquoEnvironmental and cultural stimulants in the pro-duction of carotenoids frommicroorganismsrdquoAppliedMicrobi-ology and Biotechnology vol 63 no 4 pp 351ndash361 2004

[71] H McNulty R F Jacob and R P Mason ldquoBiological activityof Carotenoids related to distinct membrane physiochemicalinteractionsrdquo American Journal of Cardiology vol 101 no 10pp 20Dndash29D 2008

[72] A Bendich ldquoCarotenoids and the immune responserdquo Journal ofNutrition vol 119 no 1 pp 112ndash115 1989

[73] M M Mathews-Roth ldquoPlasma concentrations of carotenoidsafter large doses of 120573-carotenerdquo American Journal of ClinicalNutrition vol 52 no 3 pp 500ndash501 1990

[74] H Nishino ldquoCancer prevention by carotenoidsrdquo MutationResearch vol 402 no 1-2 pp 159ndash163 1998

[75] S Agarwal and A V Rao ldquoTomato lycopene and low densitylipoprotein oxidation a human dietary intervention studyrdquoLipids vol 33 no 10 pp 981ndash984 1998

[76] N V Raj D Dhanashekaran T Nooruddin and A Panneersel-vam ldquoProduction of prodigiosin from Serratia marescens andits cytotoxicity activityrdquo Journal of Pharmacy Research vol 2no 4 pp 590ndash593 2009

[77] C Campas M Dalmau B Montaner et al ldquoProdigiosininduces apoptosis of B and T cells from B-cell chronic lympho-cytic leukemiardquo Leukemia vol 17 no 4 pp 746ndash750 2003

[78] B Montaner S Navarro M Pique et al ldquoProdigiosin fromthe supernatant of Serratia marcescens induces apoptosis inhaematopoietic cancer cell linesrdquo British Journal of Pharmacol-ogy vol 131 no 3 pp 585ndash593 2000

[79] E Llagostera V Soto-Cerrato R Joshi B Montaner PGimenez-Bonafe and R Perez-Tomas ldquoHigh cytotoxic sensi-tivity of the human small cell lung doxorubicin-resistant carci-noma (GLC4ADR) cell line to prodigiosin through apoptosisactivationrdquo Anti-Cancer Drugs vol 16 no 4 pp 393ndash399 2005

[80] S Nobutaka N Masami H Kazayuki H Tadaaki and M Kat-sumi ldquoSynergistic antifungal activity of chitinolytic enzymesand prodigiosin produced by biocontrol bacterium serratiamarescens strain B2 against gray mold pathogen Botyritiscinereardquo Journal of General Plant Pathology vol 67 no 4 pp312ndash319 2001

[81] R A Manderville ldquoSynthesis proton-affinity and anti-cancerproperties of the prodigiosin-group natural productsrdquo CurrentMedicinal Chemistry-Anti-Cancer Agents vol 1 no 2 pp 195ndash218 2001

[82] A V Giri N Anandkumar G Muthukumaran and G Pen-nathur ldquoA novel medium for the enhanced cell growth andproduction of prodigiosin from Serratia marcescens isolatedfrom soilrdquo BMCMicrobiology vol 4 pp 1ndash10 2004

[83] D K Paruchuri and R M Harshey ldquoFlagellar variation inSerratia marcescens is associated with color variationrdquo Journalof Bacteriology vol 169 no 1 pp 61ndash65 1987

[84] Q-J Lu C-Y Huang S-X Yao R-S Wang and W U Xiao-Na ldquoEffects of fat soluble extracts from vegetable powder andbeta-carotene on proliferation and apoptosis of lung cancer cellYTMLC-90rdquo Biomedical and Environmental Sciences vol 16no 3 pp 237ndash245 2003

[85] D D Karp A S Tsao and E S Kim ldquoNonsmall-cell lungcancer chemoprevention studiesrdquo Seminars in Thoracic andCardiovascular Surgery vol 15 no 4 pp 405ndash420 2003

[86] N van Zandwijk and F R Hirsch ldquoChemoprevention of lungcancer Current status and future prospectsrdquo Lung Cancer vol42 no 2 pp S71ndashS79 2003

[87] R M Russell ldquoThe enigma of 120573-carotene in carcinogenesiswhat can be learned from animal studiesrdquo Journal of Nutritionvol 134 no 1 pp 262Sndash268S 2004

[88] A R Kristal ldquoVitaminA Retionoids andCarotenoids as chemopreventive agents for prostrate cancerrdquo Journal Of Urology vol171 no 2 pp 54ndash58 2004


[89] M A Murtaugh K-N Ma J Benson K Curtin B Caan andM L Slattery ldquoAntioxidants Carotenoids and risk of rectalcancerrdquo American Journal of Epidemiology vol 159 no 1 pp32ndash41 2004

[90] S Mannisto S A Smith-Warner D Spiegelman et al ldquoDietarycarotenoids and risk of lung cancer in a pooled analysis ofseven cohort studiesrdquo Cancer Epidemiology Biomarkers andPrevention vol 13 no 1 pp 40ndash48 2004

[91] N I Krinsky ldquoMechanism of action of biological antioxi-dantsrdquo Proceedings of the Society for Experimental Biology andMedicine vol 200 no 2 pp 248ndash254 1992

[92] A Bendich ldquoCarotenoids and the immune systemrdquo inCarotenoids Chemisrty and Biology N I Krinsky M MMathews-Roth and R F Taylor Eds pp 323ndash336 PlenumPress NewYork NY USA 1990

[93] P Molnar J Deli T Tanaka et al ldquoCarotenoids with anti-Helicobacter pylori activity from Golden delicious applerdquo Phy-totherapy Research vol 24 no 5 pp 644ndash648 2010

[94] L Selvameenal M Radhakrishnan and R BalagurunathanldquoAntibiotic pigment from desert soil actinomycetes Biologicalactivity purification and chemical screeningrdquo Indian Journal ofPharmaceutical Sciences vol 71 no 5 pp 499ndash504 2009

[95] Z S Sathi N SugimotoM I Khali andM A Gafur ldquoIsolationof yellowish antibiotic pigment 4-hydroxy Nitrobenzene from astrain of Streptomycesrdquo Pakistan Journal of Biological Sciencesvol 52 pp 201ndash203 2002

[96] C Kim H Jung J H Kim and C S Shin ldquoEffect of monascuspigment derivatives on the electrophoretic mobility of bacteriaand the cell adsorption and antibacterial activities of pigmentsrdquoColloids and Surfaces B vol 47 no 2 pp 153ndash159 2006

[97] S Visalakchi and J Muthumary ldquoAntimicrobial activity of thenew endophyticMonodictys castaneae SVJM139 pigment and itsoptimizationrdquo African Journal of Microbiology Research vol 4no 1 pp 38ndash44 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


Table 1 List of pigments produced by different microorganisms

Pigment MicroorganismIndigoidine (blue-green) Streptomyces aureofaciens CCM 323 Corynebacterium insidiumCarotenoid Gemmatimonas aurantiaca T-277

Melanin (black-brown) Kluyveromyces marxianus Streptomyces chibanensis Cryptococcus neoformansAspergillus spWangiella dermatitidis Sporothrix schenckii andBurkholderia cepacia

Prodigiosin (red) Serratia marcescens Rugamonas rubra Streptoverticillium rsubrireticuli Serratiarubidaea Vibrio psychroerythrus Alteromonas rubraand Vibrio gaogenes

Zeaxanthin Staphylococcus aureus Vibrio psychroerythrus Streptomyces sp and Hahellachejuensis

Canthaxanthin (orange) Monascus roseus Bradyrhizobium spXanthomonadin (yellow) Xanthomonas oryzaeAstaxanthin (red) Phaffia rhodozyma Haematococcus pulvialisViolacein (purple) Janithobacterium lividumAnthraquinone (red) Pacilmyces farinosusHalorhodopsin and rhodopsin Halobacterium halobiumRosy pink Lamprocystis roseopersicinaVioletpurple Thiocystis violacea Thiodictyon elegansRosy peach Thiocapsa roseopersicinaOrange brown Allochromatium vinosumPinkPurple violet Allochromatium warmingii

pigment production from microbial sources has gainedattention owing to public sensitivity regarding ldquosynthetic foodadditivesrdquo

Microbial pigment production can be increased in geo-metric proportions through genetic engineering comparedto the scaling up methods of chemists Microbes have alsoupper hand in versatility and productivity over higher formsof life in the industrial-scale production of natural pigmentsand dyes Fermentation process has been increased by geneticengineering and further research for nontoxic microbialpigment can make quantum leaps in the economics ofmicrobial pigments

21 Carotenoid Carotenoids are a group of pigments ofwidely distributed classes of structurally and functionallydiverse tints from red to yellow present in a wide variety ofbacteria algae fungi and plants They are natural pigmentswhich occur widely in nature and are synthesized by plantsand microorganisms in response to various environmentalstresses whereas animals have to obtain them from food[9] Carotenoids are lipid soluble classes of molecules asso-ciated with the lipidic fractions sensitive to oxygen heatand light [10] From a chemical point of view carotenoidsare polyisoprenoid compounds and can be divided intotwo main groups (i) carotenes or hydrocarbon carotenoidswhich are composed of carbon and hydrogen atoms and(ii) xanthophylls that are oxygenated hydrocarbon derivativesthat contain at least one oxygen function such as hydroxylketo epoxy methoxy or carboxylic acid groups

211 Nomenclature Carotenoids have been given trivialnames derived from the biological sources from which they

were isolated first which conveyed no information abouttheir structure and therefore semisynthetic scheme has beendevised to allow any carotenoid to be named unambiguouslyin a way that defines and describes its structure All specificnames are based on the stem name ldquocarotenerdquo preceded bythe Greek letter prefixes that designate the two end groupsout of seven (120595 120573 120576 120574 120581 Φ and 120594) [19] The carotenoidpigmentsmost commonly found in nature including the onesof microbial origin belong to the groups given in Table 2 andit is true formicrobial carotenoids alsoThe IUPAC-IUB rulesare given in full in an IUPAC publication and in volume 1Aof the series carotenoids [20]

Some carotenoids have structure consisting of fewer than40 carbon atoms and derived formally by loss of part ofthe C40 skeleton When carbon atoms have been lost fromends of the molecule these compounds are referred to asapocarotenoids or norcarotenoids when carbon atoms havebeen lost formally from within the chain

212 General Properties In terms of hydrophobicity caro-tenoids are a group of extremely hydrophobic moleculeswith little or no solubility in water which usually do notincrease with increase in temperature [21] In the inner coremembranes of the cell they are expected to be restricted tohydrophobic areas whereas when associated with proteinsthey access to an aqueous environment Polarity of caroten-oids is altered by polar functional groups and interaction ofcarotenoids with other molecules is also affected

Shape of the carotenoid molecule depends on isomericforms (trans and cis) and can thus change properties ofcarotenoid affecting solubility and absorbability Trans formof carotenoids are more rigid and have a greater tendency to








Ketones










213 Basic Structure





Carotenoids

Hydrophobic









C



- Preventing cancer












40carbon skeleton










120573-Carotene

Bicyclic orange

LycopeneAcyclic red

NH

NH

N

O

Prodigiosin


HN

NH

NH

O

O

HO

Violacein


OH

HO

H3CH3C

H3C CH3CH3CH3

CH3CH3CH3

CH3

Zeaxanthin


OH

HOO

O

Astaxanthin


OH

HO

H

Lutein



Table 3 Continued


OH

HOO

O

Violaxanthin


HOOH

OHNeoxanthin






0

50

100

150

200

250

300

2007 2015

($ m

illio

n)


AnnatoOthers

120573-Carotene


























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Ketones










213 Basic Structure





Carotenoids

Hydrophobic









C



- Preventing cancer












40carbon skeleton










120573-Carotene

Bicyclic orange

LycopeneAcyclic red

NH

NH

N

O

Prodigiosin


HN

NH

NH

O

O

HO

Violacein


OH

HO

H3CH3C

H3C CH3CH3CH3

CH3CH3CH3

CH3

Zeaxanthin


OH

HOO

O

Astaxanthin


OH

HO

H

Lutein



Table 3 Continued


OH

HOO

O

Violaxanthin


HOOH

OHNeoxanthin






0

50

100

150

200

250

300

2007 2015

($ m

illio

n)


AnnatoOthers

120573-Carotene


























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Carotenoids

Hydrophobic









C



- Preventing cancer












40carbon skeleton










120573-Carotene

Bicyclic orange

LycopeneAcyclic red

NH

NH

N

O

Prodigiosin


HN

NH

NH

O

O

HO

Violacein


OH

HO

H3CH3C

H3C CH3CH3CH3

CH3CH3CH3

CH3

Zeaxanthin


OH

HOO

O

Astaxanthin


OH

HO

H

Lutein



Table 3 Continued


OH

HOO

O

Violaxanthin


HOOH

OHNeoxanthin






0

50

100

150

200

250

300

2007 2015

($ m

illio

n)


AnnatoOthers

120573-Carotene


























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




120573-Carotene

Bicyclic orange

LycopeneAcyclic red

NH

NH

N

O

Prodigiosin


HN

NH

NH

O

O

HO

Violacein


OH

HO

H3CH3C

H3C CH3CH3CH3

CH3CH3CH3

CH3

Zeaxanthin


OH

HOO

O

Astaxanthin


OH

HO

H

Lutein



Table 3 Continued


OH

HOO

O

Violaxanthin


HOOH

OHNeoxanthin






0

50

100

150

200

250

300

2007 2015

($ m

illio

n)


AnnatoOthers

120573-Carotene


























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table 3 Continued


OH

HOO

O

Violaxanthin


HOOH

OHNeoxanthin






0

50

100

150

200

250

300

2007 2015

($ m

illio

n)


AnnatoOthers

120573-Carotene


























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology























Canthaxanthin













Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Dark-brownblack


Aspergillus sp















50= 36 120583gmL) [93]











References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








References












































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology























































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

review article colorful world of microbes: carotenoids...

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