Ecological and Biotechnological Aspects of Pigmented Microbes: A Way Forward in Development of Food and Pharmaceutical Grade Pigments

Abstract

Microbial pigments play multiple roles in the ecosystem construction, survival, and fitness of all kinds of organisms. Considerably, microbial (bacteria, fungi, yeast, and microalgae) pigments offer a wide array of food, drug, colorants, dyes, and imaging applications. In contrast to the natural pigments from microbes, synthetic colorants are widely used due to high production, high intensity, and low cost. Nevertheless, natural pigments are gaining more demand over synthetic pigments as synthetic pigments have demonstrated side effects on human health. Therefore, research on microbial pigments needs to be extended, explored, and exploited to find potential industrial applications. In this review, the evolutionary aspects, the spatial significance of important pigments, biomedical applications, research gaps, and future perspectives are detailed briefly. The pathogenic nature of some pigmented bacteria is also detailed for awareness and safe handling. In addition, pigments from macro-organisms are also discussed in some sections for comparison with microbes.
Keywords: pigments evolution; biological properties; horizontal gene transfer; fluorescent pigments

Full text

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Microorganisms2021,9,637.https://doi.org/10.3390/microorganisms9030637www.mdpi.com/journal/microorganisms
Review
EcologicalandBiotechnologicalAspectsofPigmented
Microbes:AWayForwardinDevelopmentofFood
andPharmaceuticalGradePigments
RameshChatragadda
1,
*andLaurentDufossé
2,
*
1
BiologicalOceanographyDivision(BOD),CouncilofScientificandIndustrialResearch‐NationalInstitute
ofOceanography(CSIR‐NIO),DonaPaula403004,Goa,India
2
ChemistryandBiotechnologyofNaturalProducts(CHEMBIOPROLab),EcoleSupérieured’Ingénieurs
RéunionOcéanIndien(ESIROI),Départementagroalimentaire,UniversitédeLaRéunion,
F‐97744Saint‐Denis,France
*Correspondence:chramesh@nio.org(R.C.);laurent.dufosse@univ‐reunion.fr(L.D.)
Abstract:Microbialpigmentsplaymultiplerolesintheecosystemconstruction,survival,andfitness
ofallkindsoforganisms.Considerably,microbial(bacteria,fungi,yeast,andmicroalgae)pigments
offerawidearrayoffood,drug,colorants,dyes,andimagingapplications.Incontrasttothenatural
pigmentsfrommicrobes,syntheticcolorantsarewidelyusedduetohighproduction,highintensity,
andlowcost.Nevertheless,naturalpigmentsaregainingmoredemandoversyntheticpigmentsas
syntheticpigmentshavedemonstratedsideeffectsonhumanhealth.Therefore,researchonmicro‐
bialpigmentsneedstobeextended,explored,andexploitedtofindpotentialindustrialapplications.
Inthisreview,theevolutionaryaspects,thespatialsignificanceofimportantpigments,biomedical
applications,researchgaps,andfutureperspectivesaredetailedbriefly.Thepathogenicnatureof
somepigmentedbacteriaisalsodetailedforawarenessandsafehandling.Inaddition,pigments
frommacro‐organismsarealsodiscussedinsomesectionsforcomparisonwithmicrobes.
Keywords:pigmentsevolution;biologicalproperties;horizontalgenetransfer;fluorescent
pigments
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1.Introduction
Thesurvivaloflifeformsonearthisdependentonvariouspigments,includinglight‐
harvestingpigmentslikechlorophylls,phycoerythrin,andphycobiliproteins[1,2];harm‐
fullight‐filteringpigmentslikeproteorhodopsins[3,4],melanin’s,pyomelanin,pyocya‐
nin,fluorescentproteins;predatordefendingpigmentslikeaplysioviolin[5],cephalopods
ink[6,7],Dendrobatidaefrogtoxins[8],microbialpigmentsandsoon[9].Thequantity,
quality,andattractivenessofpigmentsfromvarioussourcessuchasmicrobes,algae,in‐
vertebrates,andmacro‐organismsmaycompriseeitherbeneficialortoxicchemicalcon‐
stituents.Notallcolorsappealingtooureyesarebeneficialtohumans.Therefore,inves‐
tigationsonthechemistryofpigmentmoleculesaregainingmoreinterestinthecurrent
research.In1666,SirIsaacNewtonhadinitiatedthebeginningofresearchoncolorsby
developingthefirstcirculardiagramofcolors,andlatervariousresearcherslikeHarris
(1776)andGoethe(1810).SirHumphryDavydemonstratedthecausesofvariouscolors
oforganicmolecules[10].Laterin1820,FriedrichAccumrevealedthemanysideeffects
ofsyntheticcolorantsinvariousfoods[11].SirWilliamHenryPerkinwasthefirstmanto
developthefirstsynthetictextilecolorcompound“mauvine”in1856.Withthisbriefhis‐
toricalbackground,thevisiblespectralpigmentsandinvisiblenonspectralpigmentsgain
moreattentionduetonumerousapplicationsinecology,evolution,biomedical,andin‐
dustrialperspectives.Theinternationalcolorsymbolismchartindicatesthateachcolor
Citation:Ramesh,C.;Dufossé,L.
EcologicalandBiotechnological
AspectsofPigmentedMicrobes:
AWayForwardinDevelopment
ofFoodandPharmaceuticalGrade
Pigments.Microorganisms2021,9,
637.https://doi.org/10.3390/
microorganisms9030637
AcademicEditor:StefanJunne
Received:1February2021
Accepted:15March2021
Published:18March2021
Publisher’sNote:MDPIstaysneu‐
tralwithregardtojurisdictional
claimsinpublishedmapsandinsti‐
tutionalaffiliations.

Copyright:©2021bytheauthors.
LicenseeMDPI,Basel,Switzerland.
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ativecommons.org/licenses/by/4.0/).

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hasaspecificmeaningindifferentcountriesandcultures.Despitenumerousknownap‐
plications,evidenceshowsthatvisualpigments(colorandlight)candirectlyinfluencethe
brain[12],psychology[13],tasteandflavorofhumans[14–16],andsciencecommunica‐
tion[17].Thelackofdietarypigmentslikecarotenoidsinourdailyfoodintakemaylead
tovariousdiseasesandinrarecasedeath[18].Visualandfoodcolorantsareplayinga
significantroleindecisionmakinginourlifetochoosedifferentfoodsandmanyother
things[19],throughvision,flavor,olfaction,gustation,andoralsomatosensationways
[16].
Humanscannotseenonspectralcolorsduetoalackoftrichromaticortetrachromatic
colorvision‐relatedconetypesintheireyes.Arecentstudydemonstratedhummingbirdsʹ
abilitytoperceivenonspectralcolorsviathetetrachromacyphenomenon[20];anotherex‐
ampleofcategoricalcolorperceptionwasobservedinEstrildidfinches[21].Numerous
studieshavebeenexploringthespectralpigmentsfrommicrobesandhigherorganisms
forvariousapplications.Nevertheless,nonspectralpigmentsandtheirecologicalim‐
portanceinnatureandbiotechnologicalapplicationsarenotwellstudied.Thus,studies
onnonspectralpigmentsremainaresearchgapinthecurrentglobalsciencedevelopment
scenario.Indeed,theplanetearthisstructuredwithvisibleandinvisiblemicroandmac‐
romoleculesproducedbyprokaryotesandeukaryotes,regulatingvariousphysical,chem‐
ical,biological,andgeologicalprocesses.Aftergoingthroughavastliteratureonmicro‐
bialpigments,itisnowunderstoodthatmicrobesandmacro‐organismsproducevaried
pigmentmoleculeswithaspecificpurposeintherespectivemilieus.
Theresourceofpigments,productionrate,transport,price,sustainability,palatabil‐
ity,durability,effectiveness,legislativeandregulatoryapproval,anddemandbyconsum‐
ersaretheprimaryrequisitesforvariousbiotechnologicalapplicationsincommercialin‐
dustries.Inthiscontext,microbialpigmentsareattractinggreatdemandtodevelopfood
grade,textilegrade,anddruggradenaturalpigments.Thereasonsforhighdemandfor
microbialpigmentsaretheirpromisingunlimitedresources,highproductionofrequired
quantityofpigments,leastcost‐effective,easycultivationandcanbeharvestedthrough‐
outtheyear,adaptabilitytovariousenvironments,optimization,stability,geneticengi‐
neering,nosideeffects,eco‐friendly,biodegradable,andindispensableapplicationsin
multidisciplinaryaspectssuchasecological,evolutionary,biomedical,agriculture,and
industrialstudies[9,22–24].Manymicrobesareknowntoproduceawidevarietyofpig‐
mentmoleculeswithinnumerablebiologicalpropertiesandotherindustrialapplications
[9,25,26].Especially,naturalpigmentsofmicrobialoriginhavemanyadvantagesover
syntheticpigments.Althoughartificialcolorsaremoreattractiveandhavebeenwidely
usedaroundtheworldmarket(42%)[19,27–30],theyarefoundtohavemanysideeffects
(e.g.,teratogenic,cancer,etc.)[29–31],andsomearenotbiodegradable(e.g.,textiledyes),
causinghealthdisorderstoaquaticorganismsandhumans[32–34].Hence,researchers
aretryingtofindalternativephysical,chemical,andbiologicalmethodstodegradesyn‐
theticcolors[35–37]toavoidthesideeffectsposedtothepublicandenvironmentalhealth.
Therefore,insteadofdevelopingsyntheticcolorsandfindingnewmethodsfortheirdeg‐
radation,exploringnaturalpigmentsfrommicrobeswouldbringaboutinnumerablead‐
vantagesforthepublicandtheenvironment.
Lackofknowledgeonpigmentedmicrobialisolationsourcesandtheirbioprospect‐
ingmethodswouldmakeresearchersfacetrialsinmicrobialpigmentresearch.Thanks
mustbeextendedtoallthepastresearcherswhoexploredthepigmentedmicrobesfrom
variousenvironmentsanddemonstratednumerousapplicationsthroughvariousmeth‐
ods.Basedonthepublishedreviewoftheliterature[9,23,25,38–45],currentresearchers
arelookingfornovelstrains,newextractiontechniques,andnewapplicationsofpig‐
ments.Inthiscontext,thisreviewisintendedtoprovidethecurrentknowledgeonvari‐
ousaspectsofmicrobialpigmentssuchasclassification,evolution,horizontalgenetrans‐
fer,marketdemand,spatialdistribution,pigmenttherapy,andfutureperspectives.
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2.ClassificationofPigments
Microbesdisplayallkindsofcolorhuessuchasblack,blue,bronze,brown,cream,
grey,green,orange,purple,indigo,pink,red,yellow,metallicgreen,red,yellow,and
rainbow.Thesepigmentscanbeclassifiedintovariouscategoriesbasedontheirvisual,
chemical,andspectralpropertiesandsourceoforigin(basedonmobilegenes)[9].Based
onvisualappearance,prokaryotesandeukaryotesdisplaymonochromatictopolychro‐
maticpigmentcombinationswithintheMunsellcolorsystem.Somehigherorganismslike
dragonfish[46,47]andhummingbirds[20]exceptionallydisplayorseecolorsbeyondour
visiblespectrumandnear‐infraredspectrum.Theseincidentssuggestthathumanslack
nonspectralconestoperceivecolorsexistingbeyondthevisiblespectrum.Visually,pig‐
mentsrepresentthefollowingphenomenaonearth:(1)Naturalpigments,(2)Biolumines‐
cence,(3)Fluorescence,and(4)Iridescence(structuralcolors),and(5)Non‐spectralcolors.
Humanscanperceiveallthecolorphenomenaexceptnon‐spectralcolors.
Functionally,fivedifferenttypesofpigmentsarefoundinnature:(1)Biologicalpig‐
ments,(2)Fossilandsedimentarypigments,(3)Mineralpigments,(4)Synthetic&identi‐
calnaturalpigments,and(5)Caramelpigments(Figure1).Biologicalpigmentsarede‐
rivedfromlivemicrobes,plants,andanimals.Incontrast,fossilpigmentsareindeedbio‐
logicallyoriginatedbutpreservedinfossilsformillionsofyears,actingasevolutionary
evidence[48–53].Inrarecases,fossilpigmentscanbeofsyntheticorigin[54].Mineral
pigmentsareinorganicinsolublepigmentsusedinartistic,cosmetic,archeological,and
evolutionarystudies[55–60].Incontrast,syntheticcolorantsaresynthesizedinthelabor‐
atoryforfoodcolorantsanddyeingapplications[61].Dozensofsyntheticcolorantsare
beingusedinfoodandbeverages[61,62].Caramelpigmentsarenaturalsugar‐basedcol‐
orantsusedinavarietyoffoodandbeverageproducts.Thesecaramelcolorsareclassified
intoCaramelI,II,III,andIVclassestofulfilltherequirementoffoodsystems[63].Solva‐
tochromicityofthesepigmentsvariesaccordingtotheextractionsolvent.
.
Figure1.Awidearrayofpigmentedmicrobesseeninnature.Theabundanceofthetypeofpigmentedbacteriaisdepicted
inbarsbasedontheavailableliterature.Rainbowbacteriaareiridescent.Classificationofpigmentsbasedonvarious
aspectsofbiochromes.Chlorophyllpigmentsarenotincludedinthedataastheyareubiquitous.HGT:Horizontalgene
transfer.

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Basedonchemicalgroups,microbialpigmentsarebroadlydifferentiatedintoanthra‐
quinones,carotenoids,indoles,phycobiliproteins,prodigiosin,rhodopsins,melanins,and
violacein[9,64].Forunderstandingtheevolutionaryaspects,rhodopsins,melanins,and
iridescent(structural)pigmentsarebrieflydiscussedherein.Microbialrhodopsinsare
light‐harvestingphotoproteinsthatbindtoretinalandrespondtolight,whichhasevolu‐
tionaryimportance.TheserhodopsinarefoundinArchaea,bacteria,fungi,viruses[65],
andsomeeukaryotes[66].Basedontheknownfunctions,rhodopsinsareclassifiedas
lightsensors(rhodopsins,opsins),energy‐conservingtransmembraneprotonpumps
(bacteriorhodopsins,proteorhodopsins,andxanthorhodopsins),andtransmembrane
chloridepumps(halorhodopsins)[4].InHaloarchaea,asinglecellcanpossessmultiple
rhodopsinswithvariedfunctions[4].Melaninsarebiosynthetically,functionally,and
structurallydiversepigments,includingfiveknowngroupsofallomelanin,eumelanin,
andneuromelaninpheomelanin,andpyomelanin[67].Itisofteneasytoisolatemono‐
chromaticpigment‐producingmicroorganismsfromdifferentenvironments,butisolation
ofpolychromaticpigmentsproducingbacteriasuchasPseudomonasaeruginosa(blueand
greenpigments),Streptomycessp.(yellow,orangeandbrown)[25]andiridescentorshim‐
meringbacteria(VIBGYOR)[68](https://www.hoekmine.com;accessedon10January
2021;HoekmineBV,2020)arerarelyisolated.Structuralcolorsarealsorecordedinfossil
feathers,suggestingtheimportanceofevolutionaryaspects[69].
Ingeneral,microbespossessinnatepigmenttraits,butsomenon‐pigmentedmi‐
crobesacquirepigmenttraitsfrompigmentedmicrobes(seethesectionbelow:Horizontal
genetransfer).Forthisreason,microbialpigmentsareclassifiedasinnatepigmentsand
acquiredpigments.Often,pigmentedmicrobesreleasediffusibleandnon‐diffusiblepig‐
mentsinculturemedia.However,rarely,somepigmentsarewater‐insoluble,forinstance,
bluepigmentindigoidine[70],redpigment[71],andviolacein[72].Somepigmentseven
donotdissolveinsolvents;insuchincidents,resinextractioncanbeemployedtoextract
pigments.
3.FunctionsofMicrobialPigments
Microbialpigmentsareknowntoplayavarietyofecologicalfunctionsintheirmi‐
lieus.(Figure2).Antioxidantpropertiesofdifferentmicrobialpigmentsaredetailedinthe
supplementaryfileprovidedinthepreviousreviewpublishedin2019(seesupplementary
file)[9].ProdigiosinpigmentproducedbysomestrainsofVibriosp.functionasphotopro‐
tectantsagainstUVlight[73].ViolaceinpigmentofJanthinobacteriumlividumandChromo‐
bacteriumviolaceumdemonstratedantipredatoractivityagainstbacterivorousnanoflagel‐
lates,indicatingitsdefensivefunction[74].J.lividumassociatedwiththeskinsofsome
frogsandsalamanders,secretesviolaceinpigmenttoprotectthemfrompathogenicfungi,
Batrachochytriumdendrobatidis[75–77].Phenazinecompoundsproducedbybacteriaplay
multiplefunctions,includingchemicalsignaling,biofilmformation,survival,andviru‐
lence[78].Pyoverdine,afluorescentyellow‐greenpigment,regulatesirontransportand
virulencefunctionsinPseudomonasfluorescens[79].Tambjamine,ayellowpigmentpro‐
ducedbyPseudoalteromonastunicata[80],issuggestedtohelpitshostpreventotherpred‐
atoryfoulingorganisms[81].Likewise,indigoidine,abluepigmentproducedbyPhaeo‐
bacterstrains,issuggestedtoinhibitcompetingbacteriaintheenvironment[82].Bacterial
melaninpigmentsactasphotoprotectants[83–87].Forinstance,Vibriocholeraemelanins
serveassurvivalfitnessfactorswhenphysico‐chemicalfactorsbecomeunfavorable[88].
Someendophyticfungireleasesanthraquinones,toprotectthehostplantfromdamage
duetoinsectsandmicrobes[89];while,fungalmelaninsdemonstratemultiplefunctions
[90].
Bacteriochlorophyllsarephotosensitizers(lightharvesters)inphotosyntheticbacte‐
riabutabsentinnon‐photosyntheticbacteria[91].Non‐photosyntheticbacteriamayuti‐
lizeaself‐photosensitizationmechanism[92].Inphotosyntheticandnon‐photosynthetic
bacteria,carotenoids,theaccessoryphotosyntheticpigmentsactasphotoprotectantsand
antioxidants,thusprotectingcellsfromdamageduetoUVandsunlightillumination

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[91,93,94].Bacterialcommunitiesintheair‐waterinterfacedidproducemorepigmenta‐
tiontotoleratesunlightandarerelativelydrug‐resistantcomparedtonon‐pigmentedbac‐
teria[95].Theextremophilicbacteriaisolatedfromsaltlakes[96]andcoldenvironments
likeAntarctica[97,98]adoptenvironmentalstresswithcarotenoidsandotherpigments.
TheyellowpigmentofThermuswasproposedasaphotoprotectant[99].Carotenoidsof
archaea[100],yeasts[101,102],cyanobacteria,andalgae[103]alsofunctionasphotopro‐
tectants.Marennine,abluepigmentproducedbydiatomHasleaisinvolvedingreening
onoysters[104],anddisplayedaprophylacticeffect[105,106].Foodcolorants,drug,dye,
andotherbiotechnologicalapplicationsofmicrobialpigmentsaredetailedinthesection
below.
.
Figure2.Ecologicalfunctionsandotherapplicationsofimportantmicrobialpigments.
4.PathogenicityofPigmentedMicrobes
Despitethenumerousknownpigments’applications,theliteraturesuggeststhat
somepigmentedbacteriaareemergingaspathogensinaquaculturefarmsandevenin
humans.Violacein‐producingbacteriumChromobacteriumviolaceumhasbeenreportedto
causeinfectionsinchildrenandadults[107].Janthinobacteriumlividum,anotherviolacein‐
producingbacterium,resultedinmassmortalityofrainbowtroutOncorhynchusmykissin
thehatcheryfromKorea[108].ProdigiosinproducingSerratiamarcescensalsoinfectsin‐
sects,otherinvertebrates,andvertebrates,includinghumans[109,110].StrainsofS.mar‐
cescensandC.violaceumarereportedtobeopportunisticpathogenstohumans[111,112].
Inallthesecases,thereisnoevidencesabouttheroleofviolaceinandprodigiosinpig‐
mentsinvirulencefunction.Arecentstudydemonstratedthatprodigiosinpigmentdid
notplayavirulencefunctioninentomopathogenicS.marcescens[113].
However,fewpigmentssuchasbacterialmelanins[114]andpyoverdines[115]reg‐
ulatevirulencefunction.TheredpigmentproducingfungisuchasFusariumandMonascus
producemycotoxins(e.g.,citrininand4,15‐diacetoxyscirpenol)linkedtopathogenicity
[116].Thus,researchersaresearchingforfungalspeciesthatdonotproduceanytoxins
[117].Wesuggestthatdetermininganisolatedpigmentedmicrobe’spathogenicity(he‐
molyticactivity)wouldhelptoavoidinfectionsandmortality.
5.HorizontalGeneTransfer(HGT)ofPigmentGenes
Inthelasttwodecades,studiesobservedrareincidencesofacquisitionortransferof
pigmentgenesbetweenrelatedandnon‐relatedmicrobialcommunities.Thetransferor
acquisitionofpigmentgenesbetweenvariousmicro‐organismsisasignofenvironmental
function.Theacquiredpigmenttraitactsasadefensivemechanismagainstothermicro‐
organisms,actingassunscreen(photoprotection)againstUVraysandharvestslightfor
enhancedphotosynthesis.Thisisanexcitingareaofresearchtostudytheecologicalim‐
portanceofpigmentgenetransferamongmicrobes.
Genescodingforlight‐harvestingpigmentproteinssuchasproteorhodopsinswere
reportedlytransferredbetweenplanktonicbacteriaandarchaealcommunitiesdispersed
onlyinthephoticzone[4].Theseproteorhodopsinsencodinggenesreportedlyacquired

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byeukaryotes,dinoflagellateprotistsfrombacteria[66],andprotists’viruses[65].Bacteria
likeCollimonasCTweresuggestedtoproducebluepigment(violacein)viapigmentgene
acquisition,probablyacquiredfromJ.lividumand/orDuganellasp.[118](Figure3).LuxA
genesresponsibleforlightemissionintheluminescentbacteriawerealsoreportedlyac‐
quiredbynon‐luminousvibriosthroughHGTandbecomeluminescent[119].Similarly,
pathogenicity‐relatedgeneswerealsosharedamongmanybacteriaviaHGT[120].Stud‐
yingtheHGTmechanismsinthesemicrobeswillhelpustounderstandtheroleofHGT
inevolution.
.
Figure3.AcquisitionofpigmentencodinggenesbyArchaea,bacteria,andviruses.
6.CosmopolitanDistributionofPigmentedMicrobes
Thedistributionpatternsofwell‐knownpigmentedmicrobeshavenotbeendetailed
intheliteraturetounderstandtheirevolutionaryspreadindifferentgeographicalenvi‐
ronments.Thecurrentliteraturepublishedsofarrevealsthatpigmentsareenvironment‐
specific,depth‐specific,host‐specific,andfunctionallydistinct[9,121].Chlorophyllpig‐
mentsareubiquitous,whereasotherpigmentmoleculesarenotwidespreadbutrestricted
tospecificgroupsofbacteria,indicatingtheevolutionaryimportanceofpigments.Tolink

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theevolutionaryconceptwithmicrobialpigmentdistribution,thewell‐knownprodigi‐
osin,violacein,andiridescentbacteriaaremappedinthisreview(Figure4).Themap
showsthecosmopolitandistributionofthesebacteriaintropical,subtropical,andtemper‐
ateenvironments.Thisspreadpatternwillhelpustounderstandthehydrothermalvent‐
basedoriginoflifetheorybytestingpresenceandabsence,abundance,andlowlevelsof
microbialpigmentsincoastalanddeep‐seaenvironmentsofdifferentgeographicalareas.
Thus,furtherin‐depthstudiesarerequiredtolinktheirdistributionpatternstoevolution‐
arystudies.
.
Figure4.Cosmopolitandistributionofwell‐knownpigmentedmicrobesindifferentgeographicalareas.
7.EvolutionofPigments
Fromtheevolutionaryperspective,theoriginofmicrobialpigmentsremainsvery
littleknown.Itiswellunderstoodthatallthechemicalmoleculeshaveoriginatedfrom
theoriginofelementsprocess[122].Pigmentsofprokaryotesandeukaryotesdisplayspe‐
cificecologicalandbioactivefunctions[9,123,124].Pigmentsarealsoidentifiedinnon‐
livingmatterslikefossils,sediments,andinorganicminerals[49,125].Fossilpigments
[49,126]andsedimentarypigments[125,127]aregaininginecologicalandevolutionary
importancetostudyenvironmentalandpopulationdynamicsandchemicalconstituents
ofthepast.Microbialpigmentsareubiquitousindifferentenvironmentsatvariousdepths
andevolvedforaspecificfunctioninrespectivemilieus[9].Incontrasttomicrobialpig‐
ments,mineralpigmentsareintenselycoloredinorganicmoleculeswithpotentialappli‐
cationsinartistic,cosmetic,forensic,archaeological,andevolutionaryperspectives[55].
Intheevolutionaryperspectiveandaccordingtotheclay‐mineraltheoryonthechemical
originoflife[128]andrecentevidences[129],wemaybeabletointerlinktheoriginof
molecules,includingpigmentsinprotocell,whichhelpedprotocellstosurviveinextreme
conditionsandsupportedtheformationofmulticellularorganisms.

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Sinceprotocells’origin,naturalpigmentshavetransformedintovariousphenomena
suchaspigments,fluorescence,andbioluminescence,foundinprokaryotesandeukary‐
otes.Currently,researchersbelievethatlifehadoriginated4.5billionyearsagofromthe
extremeenvironmentlikehydrothermalventsintheocean[130]orwarmwaterpoolsin
thevolcaniclandorgeothermal(hotspring)areas[129,131,132],basedontheevidences
ofhypotheticprotocellstructures,i.e.,vesiclesformedbysimplefattyacids[130]andpro‐
teins[133],RNA[131]andDNAmolecules[129].Theabundantexternalredpigments
seenindeep‐seatubewormsathydrothermalventsareindeedhemoglobinsthatactas
bindingsitestooxygenandhydrogensulfideandtransportthesemoleculestointernal
bacterialsymbionts[134].Incontrast,theevidenceofopsinsandpigmentmoleculesin
thermalventsisnotasabundantasinthephoticzoneorterrestrialenvironments.Deep‐
seamicrobialpigmentsisunderexploredduetodifficultiesinthecultureandmainte‐
nanceofsamplesunderinsituconditions.Opsinsarephylogeneticallywell‐diversified
andstructurallydifferentlightsensorsobservedinprokaryotes[135,136],invertebrates,
andvertebrates[137,138].Opsinssenselightandrespondtophysiological,chemical,and
behavioralfunctions,anddevelopevolutionaryadaptations.Phycobiliproteinsarelight‐
harvestingchromophorespresentincyanobacteriaandsomealgae,whoseevolutionary
originisrelatedtoglobinproteinsandGCcontents[139].Effortstounderstandtheevo‐
lutionofphycobiliproteinsincyanobacteria[140,141]andalgae[139,142]usingspecific
genesandtargetedmoleculesisunderway.Light‐harvestingpigments,phycobiliproteins,
andchlorophyllsmighthavearisenindependentlyseveraltimesindifferentlineages
[143].Apieceofevidenceexistsontheoriginandbiosynthesisofbacteriochlorophyllaby
abacterialenzyme“3‐vinyl‐bacteriochlorophyllhydratase[144],suggestingtheoriginof
enzymesfirst,followedbynotionsofcoexistenceofRNAandDNA[145]orhomogenous
RNAworld[131,146,147]orDNAworld[148],orstilldebatingprebioticDNAworld
[149].Theoriginofothermicrobialpigments(e.g.,prodigiosin,violacein,etc.)alsoneeds
tobeevaluatedforin‐depthunderstandingandtointerlinktheevidence.
Thechemistryandmechanismsinvolvedinformingpigmentsinprotocellsandtheir
divergenceintodifferentlineagesareyettobeunveiled.Thelackofenoughevidenceof
protocellsintheenvironmentmakesitdifficultforresearcherstounderstandprotocells’
exactorigin.Theexactenvironmentalconditionsthatfavoredprotocellstodevelopvari‐
ouspigmentsareunknown.Thesepigmentsmighthaveevolvedtotoleratetheintense
illuminationduringtheearlyearthformationgeneratedfromthechromosphere,photo‐
sphere,andatmosphere.Thisresearchangleremainsuntouchedconcerningtheevolution
ofchromophores.Furtherdetailedinvestigationsonspatialandtemporalpatternsofvar‐
iouspigmentedmicrobesfromdifferentenvironmentsandtheircompletegenomics,pro‐
teomics,andchemicalomicsmayrevealsomecluesontheorigin,evolution,andinher‐
itanceofpigmentsfromprotocelltoeukaryotes.Arecentconceptualstudyprovidesa
newideatounderstandthesynthesisanddevelopmentofprebioticmoleculesinprimitive
cells[150].Roboticsbasedchemicalsynthesisstudieshavebeenarisinginrecenttimes
[150,151],whichmayhelpustounderstandthepossiblewaysoforiginofprimitivemol‐
ecules.However,thisconceptisstilltobevalidatedinrealtime,basedonfieldevidences
ratherthanempiricalevidences.Inthecomingtwotothreedecades,life’strueoriginis
expectedtobeincompletelightwithintegratedevidence.
8.PigmentGeneCassettes
Microbesproducinghighpigmentyieldaretheprimaryresearchtargetsforcommer‐
cialpurposes.Manynaturalmicrobeshavefailedtoproducetheexpectedyieldofpig‐
mentsforfood,drug,cosmetics,andtextileapplications.Therefore,exploringtheentire
pigmentgenecassetteofaninterestedmicrobialspeciesisfoundtobethebestapproach
toachievehighpigmentyieldthroughrecombinantDNAtechnology.Someresearchers
mightnotbeawareofthegenesresponsibleforpigments;thus,thissectionhasgarnered
informationondifferentmicrobes’geneclusters.Piggeneclusterforprodigiosinbiosyn‐

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thesisinSerratiamarcescens[152,153],andredgeneclusterforundecylprodigiosinbiosyn‐
thesisinStr.coelicolorA3(2)wereidentified[154].ProdigiosinsynthesizinggenesinHa‐
hellachejuensisKCTC2396,andPseudoalteromonasspecieswereidentifiedashapgeneclus‐
ter[155].IndigoidinebiosynthesizinggeneclusterinPhaeobactersp.strainY4Iencodedas
igioperon[82].Violaceinbiosyntheticgenecluster“vio”wasidentifiedinChromobacterium
violaceum[156]andPseudoalteromonasspecies[157].Tambjamine,ayellowpigmentof
Pseudoalteromonastunicataissynthesizedbytamgenecluster[158].Pyomelaninsynthesiz‐
inggeneswerenamedashatABCDEoperon[159].Bikaverin,areddishpigmentproduced
byFusariumfujikuroi,carriesbikaverinsynthesizingbikgenecluster[160].Monascusred
pigmentsbiosynthesizinggenesinMonascusruberandM.pilosus,aredesignatedasMrPig,
andmokgeneclusters,correspondingly[161,162].OtherstrainsofM.pilosuspossess
MpPKS5andmppgenes[163],whereasM.purpureabearsMpPKS9andmokgenecluster
[164].ThecrtgenesareinvolvedinthebiosynthesisofcarotenoidsinBrevundimonassp.
[165],Hematococcuspluvialis[166],Deinococcuswulumuqiensis[167],Xanthophyllomycesden‐
drorhous(Phaffiarhodozyma)[168],Antarcticbacteria[169],andotherbacteria[170].Dunal‐
iellasp.carotenoidsaremainlytriggeredbytwoessentialgenesCGPandLCYB[171].In
Rhodotorulamucilaginosa,CARgeneclustersynthesizescarotenoids[172].
9.Substrates,MutagenAgents,andAdsorbents
Theuseofnaturalagro‐industrialwasteshasbeenarecenttrendandstrategyinthe
biotechnologicalprocesstoincreasepigmentyield.Thenaturalandgeneticallyengi‐
neeredmicrobesaresubjectedtofermentationstudiestoidentifytheoptimalculturecon‐
ditionsformaximumpigmentyieldwithvarioussubstrates(Table1).Avarietyofcost‐
effectivesubstratessuchascopraseed,peanutseed,sesameseed,coconutoil,peanutoil,
sesameoil[173],sunfloweroil[174],peanutpowder[175],cornsteepliquor,cassava
waste[176],squidpenpowder[175],brownsugar[177],tanneryfleshing[178],ramhorn
peptone[179],kitchenwaste[180],wheatbran[181],casein,sweetpotatopowder[182],
bagasse[183],sawdust,palmoilfiberandricehusk[184]hadbeenutilizedtoenhance
andimprovetheprodigiosinpigmentproductionfromS.marcescens.Violaceinproduc‐
tionratewasincreasedusingbrownsugar,molasses,sugarcanebagasse,andpineapple
waste[185,186].TheenhancedproductionofpyocyaninfromPseudomonasaeruginosawas
successfulwithcottonseedmeal[187].
Monascuspigmentproductionwasenhancedbyutilizingtapiocastarch[188],cas‐
savapowder,coconutoilcake,groundnutoilcake,jackfruitseedpowder,ricebran,palm
kernelcake,sesameoilcake,spentbrewinggrain,tamarindseedpowder,wheatbran
[189,190],cheesewhey,grapewaste,ricehulls,soybeanbran[191],coconutresidue,corn‐
meal,peanutmeal,soybeanmeal[192],corncob[193],jackfruitseed[194],avarietyof
rice[195–197],durianseed[198],sugarcanebagasse[199],sweetpotato[200],andbrew‐
ery’sspentgrain[201].
Carotenoidsproductioninyeastswasimprovedbysupplementingpeatextracts
[202],grapejuice[203],beetmolasses,glucosesyrup,grapemust,maizeflourextract,soy‐
beanflourextract[204],canemolasses[205–207],sugarcanejuice[208],cornsyrup
[207,209],coconutmilk[210],brewermaltwaste[211],cornmeal[212],mustardwaste
[213],rawmaltextract[207],tomatowaste[214],chickenfeatherpeptone[215],wheyfil‐
trate,coconutwater[216],datepalmwaste,maizewaste,mangopeels,onionwaste,pea‐
nutleafandfruitwastes,potatopeels,ricestraw,sugarcanewaste,wheatstraw[217],and
powdersofonionpeel,mungbean,peapodsandpotatoskin[218].


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Table1.Substratespromotinghighpigmentyieldfromvariousmicrobesarealonedetailedhereinforfurtherbiotechno‐
logicalapplications.
OrganismSubstratePigmentMaximumPigment
YieldReference
Bacteria
S.marcescensPeanutseedbrothProdigiosin38.75mg/mL[173]
S.marcescensCassavawasteProdigiosin49.50mg/mL[176]
S.marcescensTanneryfleshingProdigiosin33mg/mL[178]
S.marcescensRamhornpeptone Prodigiosin27.77mg/mL[179]
S.marcescensKitchenwaste Prodigiosin22.3mg/mL[180]
S.marcescensBagasseProdigiosin40.86gkg−1[183]
S.marcescensSunfloweroil Undecylprodigiosin7.90mg/mL[174]
Chromobacteriumvio‐
laceumLiquidpineapplewasteViolacein57.90mg/mL[185,186]
PseudomonasaeruginosaCottonseedmealPyocyanin9.2μg/mL[187]
Fungi
M.purpureus
J
ackfruitseedMonascus10.2OD/g[189]
M.purpureusGrapewasteMonascus20–22.5g/L[191]
M.purpureusCornmealMonascus129.63U/g[192]
M.purpureusCorncob Monascus25.42OD/g[193]
M.purpureusBrewery’sspentgrainMonascus16.75UA500[201]
Yeast
RhodotorularubraPeatextractβ‐Carotene1,256μgg−1[202]
RhodotorulaglutinisGrapemustCarotenoid915.4μgg−1[204]
Rh.glutinisMolassesCarotenoid185mgL−1[206]
Rh.glutinisChickenfeatherpep‐
toneCarotenoid92mgL−1[215]
Xanthophyllomycesden‐
drorhousGrapejuiceAstaxanthin9.8μgmL−1[203]
X.dendrorhousMustardwasteAstaxanthin25.8mgL−1[213]
X.dendrorhousMolassesCarotenoid40mgL−1[205]
X.dendrorhousCoconutmilk Astaxanthin850μgg−1[210]
UA:Absorbanceunits;OD:Opticaldensity.
Mutagenicagentssuchasvariouschemicalreagents,UVillumination,andgamma
radiationhavebeenusedtoenhancepigmentproductionfromnaturalandrecombinant
microbialstrains[219,220].CarotenoidcontentofRhodopseudomonaspalustriswasstimu‐
latedwithblue,yellow,white,green,incandescentlamp,red,halogen,andfluorescence
lamp[221].Theenhancedprodigiosinproductionwassuccessfulwithgammaradiation
[219].Stimulatedpigmentproductioninfilamentousfungiwasevidentwithblue(forca‐
rotenoids)[222],green,red,andUV‐light(redpigmentbikaverin)[223].Mutationsinthe
genescausedFusariumfujikuroitoproducedifferenthuesofpigments[160].Foryeasts,
lowenergyionbeamimplantation[224],gammaradiation[225],light‐emittingdiodes
[226,227],andUVlight[228]wereusedasaneffectiveapproachforcarotenoidsenhance‐
ment.Highproductionofphycobiliproteinswasachievedfromcyanobacteria,Pseudana‐
baenamucicolaculturesgrownunderwhitelight[229].Theincreaseofphycocyaninpro‐
ductionfromSpirulinaplatensis[230]andPseudanabaenasp.[231]wasevidentunderred
light.MaximumproductionofphycoerythrinandcarotenoidsfromPseudanabaenasp.was
observedingreenlight[231].Inunicellularmicroalgae,carotenoidsproductionisen‐
hancedthroughUVradiation[232–235],blueandredlight[236,237],light‐emittingdiodes
[238,239],andvarioustoxicchemicals[233,240].

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Theuseofvariousadsorbentsinmicrobialfermentationappearstobethemostef‐
fectivestrategytoenhancepigmentproductionandmaximumpigmentrecovery.Studies
haveutilizeddifferentinternaladsorbentsformaximumpigmentrecovery.Treatingcul‐
tureflaskswithSigmacotetoreduceattachmentofpigmentcellstoaglasssurface[241];
useofresinslikeX‐5,HZ806,andHZ802inculturesforpigmentadsorption[242];adding
ricehusks[243]oralginatebeadstoculturesforadsorbingmorepigmentcells[244];ad‐
ditionofDiaionHP‐20resin[245–247]andpolyurethanefoamcubes[248]tocellculture
aretheadditionalstrategiesinprodigiosinpigmentrecovery.Monascinpigmentsarere‐
coveredbyaddingrice,called“redmoldrice”[161].Highmonascuspigmentyieldwas
achievedwithstirreddrumbioreactor[249].Variousextractiontechniquessuchasionic
liquid–assistedextraction,microwave‐assistedextraction,ultrasound‐assistedextraction,
pressurizedliquidextraction,pulsedelectricfieldassistedextraction,andsupercritical
CO2extractionareemployedtorecoverpigmentsfromfungi[220].Findingthenewad‐
sorbentsandextractiontechniquestorecoverpigmentsareimportantrequisitesinmicro‐
bialpigmentresearch.
10.BiomedicalandIndustrialApplications
Thissectionprovidesvariousapplicationsofmicrobialpigmentsthatwerenotcov‐
eredinthepreviousreview[9].Dozensofsyntheticandnaturalpigmentshavebeenused
inbeverages,foods,dyeing,andtextiles(Figures5and6).Ared‐pigmented(relatedto
carotenoid)Arthrobactersp.offertheantitumoractivityagainstesophagealcancercells
[71].ProdigiosinproducedbyPseudomonasrubradisplayedantimicrobialactivityagainst
pathogenicbacteriaandyeast[250].ProdigiosinextractedfromS.marcescensdisplayed
potentialinsecticidalactivityagainstDrosophilamelanogasterlarvae[175],ants,cock‐
roaches,andtermites[251].Prodigiosinandglycolipidbiosurfactant’ssynergisticeffect
demonstratedantimicrobialactivityagainstpathogenicbacteria[252].Prodigiosinex‐
tractedfromZooshikellasp.andStreptomycessp.andotherpigmentsfrommarinebacteria
displayedpotentialapplicationinstainingandfoodcolorants[253].Currently,inourlab,
calciumoxalateanduricacidstonesdissolvingpigmentsfrommarinebacteriaarebeing
isolated.ProdigiosinfromS.marcescens[254]andviolaceinfromC.violaceum[255]prom‐
isetotreatthechagasdisease.Violaceinpigmentisemployedincottonfabricsdyeing
[256],andleaddetectingwhole‐cellleadbiosensor[257].ViolaceinproducedbyMi‐
crobulbifersp.demonstratedantinematodeactivityagainstCaenorhabditiselegans[258];a
strainofviolaceinproducingChromobacteriumisolatedfromtheHimalayaregion,pro‐
ducedbybioplasticpolyhydroxyalkanoates[259].
IndigopigmentisolatedfromPseudomonassp.displayedantioxidantproperty[260].
Glaukothalin,abluepigmentproducedbyRheinheimerasp.,showedantibacterialactivity
againstfewmarinebacteria[261].PyocyaninfromPseudomonasaeruginosademonstrated
textiledyeingproperties,antifungalactivityagainstblastfungus,Magnaporthegrisea,and
antibacterialpropertiesagainstblightofrice,Xanthomonasoryzae[262].Micrococcussp.’s
yellowpigmentshowedexcellentwoundhealingandanti‐inflammatorypropertyinal‐
binorats[263].Bacterioruberincarotenoidsofhalophilicbacteriahavesignificantantiox‐
idantandantibacterialactivities[264].Microbialpigments(Actinorhodin,carotenoids,
flexirubin,melanin,phycocyanin,phycoerythrin,bluepigment)arealsousedtosynthe‐
sizevariousnanoparticleswithbiologicalpropertieslikeantioxidant,antimicrobial,anti‐
canceractivities[265].
Fungalpigmentswerereviewedtohaveawiderangeofapplicationsinfoodcolor‐
ants[266,267],bioactiveproperties,andtextiledyeing[40,268–270].Incontrast,bacterial
pigmentslikeprodigiosinandviolaceinareusedtocolorpapers,candles,soaps,ink,
clothes[271],andtextiledyeing[272].Monascuspigmentoranthocyaninpigmentareem‐
ployedasnoninvasivedyeindicatorsinsafecellviabilityassayforParamecium[273],Eu‐
glena[274],andbreastcancercells[275].Microbesisolatedfromcryosphereenvironments
alsoproducedvariouspigmentswithmultifacetedapplications[269,276,277],including
anticanceractivities[278].

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Carotenoidsofarchaea[100]andThraustochytrids[279,280]havepotentialnutraceu‐
ticalapplications.However,pigmentsfrommarinearchaeaandprotistsremaintheleast
studiedgroups.RedalgaeextractsareusedtomakeL’OrealParisPureClayMaskforskin
glowandsmoothening.Similarly,othercommercialcosmeticproductshavebeendevel‐
opedfromcyanobacteriaandmicroalgae[281].Phycobiliproteinsfromcyanobacteriaand
algaedemonstratedcosmetic,dye,nutraceutical,andbioactiveapplications[282–284].
Marennine,abluepigmentproducedbydiatoms,Hasleaspecies,promisesantimicrobial,
antiviral,anticancer,andantioxidantactivities[285].
.
Figure5.Chemicalsstructuresofsyntheticpigments.

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Figure6.Chemicalstructuresofimportantmicrobialpigments.

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11.Photo‐PigmentTherapy
Thecombinationsoflightandpigmentswerefoundtobeaneffectivestrategyin
antimicrobialassays.Astudyfoundthatthebactericidaleffectofbluelightirradiated
intracellularblackpigment(protoporphyrinIX)onPorphyromonasgingivalis[286].Like‐
wise,flavinmononucleotideactivatedbybluelightresultedininhibitionofStaphylococcus
aureusbiofilm[287].Suchstrategiesmaybeadoptedandemployedtoincreasethebioac‐
tiveeffectivityofmicrobialpigmentsagainstvariouspathogens.
12.MarketDemandforMicrobialPigments
Inrecenttimes,peoplearoundtheworldhavecometoknowtheharmfuleffectsof
syntheticcolorantsinfoods(Figure7).Thus,demandonnaturalpigmentsisincreasing
overartificialcolorants.In1971,theUnitedStatesspentaround1billionUSdollarsto
increasethesupplyofnaturalcolorantsfromvariousnaturalresources[288].Thereare
inadequateorscarcedataontheglobalmarketvalueoffood‐grademicrobialpigments.
Veryfewpigmentssuchasβ‐carotene,astaxanthin,andmonascusareavailableinthe
market.Lackofsurveysandliteratureonmicrobialpigments’costanddemandarebe‐
cominghurdlestoestimatetheactualglobalmarketdemandonmicrobialpigments.

Figure7.Anillustrationexplainingtherequirementofnaturalcolorantsoversyntheticcolorants.
MonascuspigmentsaretraditionalfoodcolorantswidelyusedinsoutheastAsian
countries,whichhadanestimatedmarketvalueof$12.0milliondollarsduring1992[289].
MonascuspigmentsareprohibitedintheUnitedStatesandEuropeduetothepresence
ofmycotoxins[290].Theglobalcommercialmarketvalueforcarotenoidsreached$1.2
billionin2010,$1.5billionin2014,andisexpectedtoreach$2.0billionby2022
[228,291,292],withanannualgrowthrateof5.7%fortheperiod2017–2022[293].Prodigi‐
osinandviolacein(chemicalstandards)arefetchingabout$5000×10
5
perkginthemarket
[271].Naturalcarotenoids(24%)aregainingahighmarketvalueof$350to7500kg
−1
than
syntheticcarotenoids(76%)withavalueof$250–2000kg
−1
[294].Astaxanthinandβ‐car‐
otenearethehighlydemandedpigmentsgloballywithanexpectedmarketvalueof$225
and$309milliondollarsby2018,respectively[295].Luteinisaxanthophyllpigmentex‐
pectedtogaina$308millionmarketvalueby2018[296].Theglobalmarketvalueofca‐

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rotenoidsisprojectedtoreachupto2.0billionby2026[297].Accordingtotheglobalphy‐
cobiliproteinsmarketresearchreport,marketdemandforphycobiliproteinsisexpected
toriseby2026.Currently,thephycobiliproteins(10mg)priceinMerckrangesfrom$200
to$270.Arecentreporthasestimatedtheexpectedglobaldyesandpigmentsmarket
valueof$33.2to49.1billiondollarsby2027[298].Indeed,80to90%ofthecarotenoids
supplyinthemarketisfulfilledviachemicalsynthesis[299].However,duetosynthetic
colorants’sideeffectsandtheexpensivepigmentsourceofplants,microbialpigments
havebeengaininghighdemandinrecenttimes.Therefore,findingpotentialpromising
microbesbecamearesearchinterestinfoodanddrugindustries.Forinstance,yeastca‐
rotenoids’marketvaluehasdeclinedduetolowdryweightproduction(0.40%)compared
toalgae,Haematococcussp.(3.0%)[295].Inthecurrentglobalpopulationrisescenario,de‐
mandforediblemicrobialpigmentsasfoodcolorantsisexpectedtorisetofulfillthefood
industryrequirements[300].
Microbialspecieswithhighbiomassandpigmentyield,includingthegenetically
modifiedmicrobes,arehighlyinterestedinthecurrentresearch.Ontheotherhand,in
viewofthesideeffectsposedwithsyntheticcolorants[31,36,301],thescientificcommu‐
nityhastoreachthepublicthroughvarioussocialprogramstomakeawarenessaboutthe
importanceofnaturalpigmentsandnegativeimpactsofsyntheticcolorantsonhealth.
Theseawarenessprogramswouldsavemanylivesfromvarioushealthdisorders,includ‐
inglife‐threateningcancer.
13.FuturePerspective
Microbialpigmentsdemonstratedawidevarietyofapplicationsinfood,drug,and
textiles.Thesenaturalpigmentscanreplacesyntheticcolorantsandfulfilltheemerging
needonfoodcolorantsintheglobalmarket.Microbialpigmentsplayanindirectrolein
theconservationofplantsandanimalresourcesbysubstitutingthemfrompigmentre‐
sources.Manyresearchersarerestrictedtopigmentslikeprodigiosin,violacein,monas‐
cin,astaxanthin,lutein,andphycobiliproteins.Therefore,exploringothermicrobialpig‐
mentsfromdifferentenvironmentswouldoffernovelandpotentialknownpigmentmol‐
eculesformultifacetedapplications.Researchonmicrobialpigmentswouldultimately
revealtheevolutionarylineagesoforiginoflifeandthedispersalofvariouschromophore‐
basedphenomenainalllineages.Isolationandchemicalcharacterizationofmicrobialpig‐
mentsareeasierthannon‐pigmentedmicrobes,whosecompounds’characterizationis
arduousandtime‐consuming.Thus,focusingonmicrobialpigmentswouldgarnermore
attentiontoresearchanddevelopmentandtheireconomicdemandinvariousindustries.
AuthorContributions:R.C.conceptualizedthereviewsections,wrotethemanuscript,anddrew
allfigures.L.D.wrotesectionsofthemanuscript,editedthewholetext.R.C.andL.D.bothvali‐
datedthefinalproof.Allauthorshavereadandagreedtothepublishedversionofthemanu‐
script.
Funding:LaurentDufossédeeplythankstheConseilRégionaldeLaRéunion,IndianOcean,for
continuousfinancialsupportofresearchprojectsdedicatedtomicrobialpigments.
DataAvailabilityStatement:Datasharingnotapplicable.
Acknowledgments:TheauthorChatragaddaRameshthankstheDirector,NIO,forhissupport
andencouragement.ThisisCSIR–NIO’scontributionreferencenumber:6706.LaurentDufossé
showsgratitudetoMireilleFouillaudandYanisCaroformanyyearscloserelationshipinmicro‐
bialpigmentsresearch.
ConflictsofInterest:Theauthorsdeclarenoconflictofinterest.


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