Anal Bioanal Chem (2006) 385: 46–56DOI 10.1007/s00216-006-0396-3

ORIGINAL PAPER

Howell G. M. Edwards . Mahmood A. Mohsin .Fadhil N. Sadooni . Nik F. Nik Hassan . Tasnim Munshi

Life in the sabkha: Raman spectroscopy of halotrophicextremophiles of relevance to planetary exploration

Received: 20 December 2005 / Revised: 21 February 2006 / Accepted: 22 February 2006 / Published online: 11 April 2006# Springer-Verlag 2006

Abstract The Raman spectroscopic biosignatures ofhalotrophic cyanobacterial extremophiles from sabkhaevaporitic saltpans are reported for the first time andideas about the possible survival strategies in operationhave been forthcoming. The biochemicals produced by thecyanobacteria which colonise the interfaces between largeplates of clear selenitic gypsum, halite, and dolomitizedcalcium carbonates in the centre of the salt pans areidentifiably different from those which are produced bybenthic cyanobacterial mats colonising the surface of thesalt pan edges in the intertidal zone. The prediction thatsimilar geological formations would have been present onearly Mars and which could now be underlying the highlyperoxidised regolith on the surface of the planet has beenconfirmed by recent satellite observations from Mars orbitand by localised traverses by robotic surface rovers. Thesuccessful adoption of miniaturised Raman spectroscopicinstrumentation as part of a scientific package for detectionof extant life or biomolecular traces of extinct life onproposed future Mars missions will depend critically oninterpretation of data from terrestrial Mars analogues suchas sabkhas, of which the current study is an example.

Keywords Raman spectroscopy . Sabkha . Evaporites .Halotrophs . Extremophiles . Cyanobacteria

Introduction

The importance of extremophiles in evolutionary biologyand to understanding the survival strategies adopted byorganisms in extreme terrestrial environments, which areoften considered to represent “limits of life” situations, iswell recognised in the literature [1–6]. A key factor in theadaptation of biological colonisation to hostile geologicalenvironments is the production of suites of protectivebiochemicals and accessories through which control of thesituation is effected. In this context, creation of combina-tions of specific biochemicals with targeted responses toextremes of temperature, pressure, desiccation, acidity, andalkalinity, and to excessive insolation by damaging low-wavelength radiation is a necessity for survival of theorganisms; this must also be achieved with energeticallyfavourable strategies for which adaptation of surroundinggeological matrices is essential. Hence, recognition of thestrategic methods through which extremophiles can controltheir environments depends not only on identification ofthe operational chemistry and production of protectivebiochemicals but also on the biogeological modificationsthat have been undertaken by the colonies in the adaptationof their environment [6–10].

In recent years the physical limits which terrestrial lifeforms can tolerate and survive have been extended by thediscovery of psychrophiles, thermophiles, xerophiles,barophiles, halophiles, acidophiles, and alkaliophiles; allare examples of extremophiles which have adapted to someof the most highly environmentally stressed terrestrialconditions, including temperatures from −50 to 113 °C,pressures up to 150 bar, zero humidity, and pH between 0.7and 12.

Robotic scientific missions to Mars have identified theplanet’s surface as highly peroxidising [11], subjected tointense insolation by UV radiation, with a low atmosphericpressure comprising mainly nitrogen and carbon dioxide,and suffering a temperature range of approximately −120to +10 °C (Table 1); it is, therefore, no surprise that theMartian surface seems to be devoid of organic chemicalswhich could be indicators of previous relict life. This has

H. G. M. Edwards (*) . N. F. Nik Hassan . T. MunshiChemical and Forensic Sciences, School of Life Sciences,University of Bradford,Bradford, BD7 1DP, UKe-mail: h.g.m.edwards@bradford.ac.uk

M. A. MohsinDepartment of Chemistry, Faculty of Science,United Arab Emirates University,P.O. Box 17551, Al-Ain, United Arab Emirates

F. N. SadooniDepartment of Geology, College of Science,United Arab Emirates University,P.O. Box 17551, Al-Ain, United Arab Emirates

not always been true, however—it is believed that earlyMars could have had liquid water [12–14] and an oxygenatmosphere. It is postulated that as the environment becameworse during Epochs III and IV (Fig. 1a,b) organismswould have retreated into rocks and minerals which couldbe adapted for their survival, that is, they would havebecome endolithic extremophiles [15, 16]. Even if laterconditions on Mars would have been too hostile for themost robust endolithic colonies to survive, traces of theirprotective biochemicals could still remain in the Martiansubsurface [17]. Recent evidence of the presence ofsulfates, carbonates, and subsurface water on Mars, fromthe Mars rovers “Spirit” and “Opportunity” and orbitingsatellites such as the Mars Global Surveyor and MarsExpress, increases the possibility that traces of extremo-philic life will be detected in future missions, if theappropriate niches can be identified.

In this context, we report here the first Raman spectro-scopic analysis of organisms which have colonised aterrestrial sabkha comprising extensive salt-pans withhalite crustal surface polygons and gypsum outcrops in ahot desert environment with the potential for highlylocalised colonisation of geological niches at the interfacesbetween the halite, gypsum, and subsurface carbonatedeposits [18]. The sabkha is subjected to periodic floodingfrom subsurface ground water and merges into an intertidalregion where black cyanobacterial mats cover much of the

surface. Clearly, in their survival strategies, the extremo-philes need to have adapted to or acquired a tolerancetoward high salt concentrations, high temperatures, andhigh insolation by low-wavelength radiation, factors whichwould have been significant in the adaptation of organismsto analogous situations on the Martian surface, especiallyin areas which are rich in sulfate and carbonate minerals,for example jarosite, gypsum, dolomite, and magnesite.This study will therefore be useful both for understandingthe biochemical protective strategies operating in halo-trophic extremophiles terrestrially and also for evaluationof the detection possible by Raman spectroscopic analysisof a planetary surface or subsurface where such organismsmay have once existed or, indeed, may still exist [19–24].

In a recent paper from our laboratory [25] we describedthe use of Raman spectroscopic techniques to identifyhalotrophic extremophilic cyanobacterial colonies whichhad established viable communities within selenitic gyp-sum crystals in breccia field deposits at the rim of theHaughton meteorite crater (∼26 Mya) in the CanadianArctic [26]. Selenite is a transparent form of crystallinegypsum. A particular advantage of the Raman spectro-scopic method in this context was analysis of the biologicaland geological components without separation, henceproviding useful information about biogeological interac-tions at the molecular level. Several bioprotective chemi-cals, including scytonemin, parietin, and carotenoids [8],

Table 1 Potential sequence of life on Mars (the McKay model) and current Antarctic analogs [12–14, 16]

Epoch Period(billion years ago)

Thermodynamicconditions

State of liquid water on Mars Earth (Antarctic) analogue

I 4.2–3.8 P≥2 bar Abundant. Origin of lifeT>0 °C(but global −53 °C)

Rivers and lakes, but partydependent on geothermal heat flux.

Primordial ‘‘soup’’

CO2, 50 mb N2 Clay as templates?Volcanoes Flowing surface waterMeteorites High UV toleranceHigh UVB

II 3.8–3.1 P∼1 bar Iced-covered lakes. Microbial (cyanobacteria) mats in dryvalley lakes

T<0 °C (−20 °C) Permafrost. Photosynthesis at low light.Peak T>0 °C Saline ground water at −21 °C UV–toleranceCarbonate.Dissolved gases

III 3.1–1.5 P∼100 mb Liquid water in porous rocks. Life inside rocks:Mainly CO2 Permafrost. Endolithic microbes, e.g. Beacon sandstonePeak T<0 °C Ground water.

IV 1.5–present P∼7 mb No liquid water on surface. No life on Martian surfaceLow CO2 Permafrost and ground ice. Trace endolithics?T (Equator) 55 °C Geothermal ground waterRange −110 to +7 °C Life or fossil biomolecules in

permafrost ground ice or rocks?T (Pole) −119 °C Life in geothermal habitats within

the Martian crust?

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were identified in the cyanobacterial colonies in this high-salt environment. For the first time, with the Raman datafrom the current study, we shall be able to compare directlythe protective chemical strategies being adopted byhalotrophic extremophiles in hot desert and cold desertenvironments.

The information acquired as a result of this study willalso be used to expand the database of sulfate-tolerantextremophiles for which the Raman spectroscopic signa-tures will be indicators of the protective biochemicals that

have been synthesised in their adaptative survival strate-gies. Future missions to Mars, which will involve remoterobotic geological exploration of the planetary surface andsubsurface, will rely on such data for interpretation of keyspectroscopic biomarkers and geomarkers that couldindicate a survival niche.

Experimental

Site

The sabkha is a site of special environmental importance.The study area is the coast flanking Abu Dhabi, UnitedArab Emirates. It extends over several hundred km2 andcontains extensive areas of salt pan evaporites bounded bycyanobacterial benthic surface mats (Fig. 2) which blendinto intertidal and ground water zones. The prevailingtemperatures can exceed 60 °C, with insolation by lowwavelength ultraviolet radiation. Although sparse vegeta-tion, in the form of mangroves, is present at the edge of thesabkha, the evaporite pans themselves are devoid of

Fig. 2 Cyanobacterial mat in the intertidal zone at the edge of thesabkha, Salt evaporite basin, Al-Qanatir Island, Abu Dhabi, UnitedArab Emirates

Fig. 1 a Epoch III (3.1–1.5 Gya) b Epoch IV (1.5 Gya–presenttime) on Martian surface and subsurface [16]

Fig. 4 Large gypsum crystal in halite matrix with cream-colouredsedimentary subsurface deposits containing a layer of a greencyanobacterial colony

Fig. 3 Halite crust specimen, with brown particles on the underside,from polygons at the sabkha surface

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surface colonisation until the cyanobacterial mats arereached. High salinity prevents grazing gastropods fromdevouring the algal mats in this intertidal zone. The hotdesert location of the sabkha, with its large areas of halitepolygons and gypsum crystallites, coupled with cyclicperiods of flooding from subsurface ground water makesthe site potentially interesting for study of extremophilicactivity and survival strategy in this arid or semi-aridenvironment.

The mineralogy of the sabkha site [18] consists ofmarine evaporites, for example gypsum, anhydrite, halite,sylvite, and carnallite, which contain calcium, magnesium,sodium, and potassium with sulfate and chloride. Othernon-marine evaporite minerals, for example epsomite,natron, mirabilite, and gaylussite are also found, dependingon ground water composition. The sedimentation in thesabkha is a complex process that depends on the prevailinghydrology and diagenesis of the deposited minerals. Acharacteristic feature is a shallowing-upwards sequence inwhich can be identified halite at the surface overlayinggypsum and anhydrite, followed by fenestral, pelletal, andbioclastic limestones which can extend vertically for

several tens of metres thickness. The so-called “sabkhacycle” typically stacks sub-tidal carbonates of pelletal andbioclastic limestone, intertidal algal mats, and supratidalevaporates in one depositional sequence. After deposition,diagenesis leads to alteration of the original mineralogy andsedimentary fabric in which evaporitic minerals areremoved by dissolution and in which the uplifting ofanhydrite results in rehydration to gypsum, so forming verylarge crystals, porphyrotropes, and veins of fibrous crys-tals, satin spar. Re-burial of gypsum causes a change toanhydrite in the lower stacks sequence. An importantdiagenetic process which will be seen to have specialimportance in the current study is dolomitization, wherebycalcium carbonate is replaced by calcium magnesiumcarbonate, because this results in a 13% increase in thegeological porosity of the sediment that can materiallyassist in its colonisation by endolithic or subsurfaceextremophiles. The dolomitization process is believed tobe driven by precipitation of gypsum, leading to highmagnesium-to-calcium ratios in the ground water, and bymixing of seawater and fresh water in an aquifer zone nearadjacent platform carbonates. Dolomite has previously

Fig. 5 Raman spectrum,in the 100–1800 cm−1 range,of halite crust surface showingthe presence of dolomite, cal-cite, and anhydrite

Fig. 6 Raman spectrum, in the100–1800 cm−1 range, of theunderside of the halite crustspecimen, showing broadfeatures between 1200 and1500 cm−1 characteristicof chlorophyll and cyanolichenbiochemicals

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been related to microbial activity in which calcium iscomplexed with sulfate, leaving the water enriched withmagnesium, as in the role of sulfate-reducing bacteria andcyanobacteria in dolomite formation in distal ephemerallakes at Coorong, South Australia [27].

Several specimens taken from the sabkha during a fieldtrip in early 2005 by the authors were:

(1) a halite crust with several dark brown patches on theundersurface which could be residues of bacterialcolonies (Fig. 3);

(2) large gypsum crystals with inclusions;(3) a very large gypsum crystal surrounded by halite

deposits and sedimentary deposits attached to theunderside (Fig. 4); this specimen was particularlysignificant because it showed evidence of green layersof chlorophyll (?) situated at the junction between thelower surface of the gypsum and the sediments;

(4) sections of cyanobacterial mats from the surface of theintertidal zone (Fig. 2) at the edge of the sabkha.

Raman spectroscopy

Raman spectra were acquired using a Bruker Fourier-transform IFS 66 instrument with FRA 106 Raman moduleattachment operating with Nd 3+/YAG laser excitation at1064 nm with a spectral resolution of 4 cm −1. Up to 2000spectral scans were usually accumulated to improve signal-to-noise ratios, the process taking about 1 h per specimenregion scanned. The spectral footprint was 100 micronsdiameter in macroscopic mode and replicate spectra wereobtained to verify that the spectral data were representativeof the region under study.

Raman spectra were also obtained using a RenishawInVia confocal Raman microscope which operated at 514.5and 785 nm excitation from an argon ion gas laser and adiode laser, respectively. Raman spectra with a spectralresolution of 2 cm−1 could be obtained from spectralfootprints of approximately 2 microns diameter using 50×and 100× lens objectives. Spectral accumulations of up totwenty scans were needed to achieve good signal-to-noiseratios, which required approximately 30 min acquisitiontime per spectral region under study.

Fig. 7 Raman spectrum, in the100–3200 cm −1 range, of clearselenitic gypsum crystal

Fig. 8 Raman spectrum, inthe 100–1800 cm−1 range, ofanhydrite inclusion in theselenitic gypsum crystal

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Spectral data were compared with band wavenumberpositions from relevant materials in our laboratorydatabase, which has been compiled from analysis of arange of extremophiles found in a variety of terrestrialenvironments [2, 3, 7, 10].

Results and discussion

Although the fluorescence of many of the protectivebiochemicals produced by extremophiles in response toenvironmental stresses, which has been noted in theliterature [1], usually necessitates the use of long-wave-length excitation in the near infrared to acquire Ramanspectra, it has also been recognised that some keychemicals can be detected by resonance Raman spectros-copy even in the presence of high fluorescence emission.Of particular relevance in this respect are the carotenoids,which absorb in the green region of the visble spectrum,which gives rise to their characteristically deep yellow toorange–red colours. It has been found, therefore, that thekey molecular Raman signatures of the carotenes can beidentified by using 514.5 nm excitation. Hence, in thisstudy, we used both long and short-wavelength excitationto record the spectra and also examined the specimensusing confocal microscopy to eliminate the effects of thesurrounding geological matrices.

Raman spectra of the halite and gypsum crystallinedeposits collected, specimens 1–3, showed evidence of themineralogical composition of the sabkha. In Fig. 5, aspectrum taken from the halite crust of specimen 1, thepresence of weak features at 1097, 1086, and 1017 cm−1

are indicative of dolomite, calcium carbonate, andanhydrite, respectively. The presence of a band in thelow-wavenumber region at 283 cm−1 indicates that thecalcium carbonate is in the calcite polymorphic form. Otherfeatures at 854, 822, 685, and 384 cm−1 remain unassigned.A notable absence from the spectrum of the halite crust arethe signatures of gypsum, CaSO4.2H2O, with a sulfate

stretching band at 1007 cm −1 yet the dehydrated form ofcalcium sulfate, anhydrite, has been identified here.

A spectrum of the underside of the halite specimen(Fig. 6) reveals a broad sequence of features between 1200and 1500 cm−1 which we have assigned, in other work[25], to biochemicals and chlorophyll from organismscolonising the region immediately below the halite crust. Aweak dolomite signature is also recognised at 1098 cm −1.In all these spectra the halite is not seen, because thematerial has no activity in the Raman spectrum.

Figure 7 shows the Raman spectrum obtained from theclear gypsum specimens, which occur in the selenitic form,and here the sulfate stretch at 1007 cm−1 is indicative of adihydrate. In Fig. 8, however, there is evidence in theselenitic gypsum crystals of the dehydrated form ofcalcium sulfate, anhydrite, in several white inclusions. Inother inclusions in the selenitic gypsum crystals thepresence of dolomite, with a carbonate stretch at 1098cm−1, is clearly indicated, as shown in Fig. 9.

It should be noted that there is no evidence here foreither calcite or aragonite, with a feature expected at 1086cm −1.

Sample 3 provided a wealth of information in that itconsisted of large crystals of gypsum located in a halitematrix, underneath which a layer of green-colouredmaterial was observed situated between the surface gyp-sum/halite crust and a cream coloured sedimentary materialbelow. Figure 10 shows a montage of spectra taken fromthe region between the gypsum surface crystal and thelower sediments. In Fig. 10a we see the Raman spectrum ofpredominantly gypsum. In Fig. 10b, a spectrum taken fromthe underside of the gypsum crystal, weaker featuresappear at 1157 and 1517 cm −1; these are assignable tobeta-carotene, characteristic of biological colonisation ofthis region. There is also a sharp band at 1122 cm −1, whichwe can ascribe [28] to hydromagnesite, a hydratedmagnesium carbonate.

The green areas of the interface and its substrate gavespectra such as that shown in Fig. 10c, which shows the

Fig. 9 Raman spectrum, in the400–1800 cm−1 range, of adolomite inclusion in theselenitic gypsum crystal

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clear signatures of dolomite, with a band at 1098 cm −1, andseveral weaker features at 1757, 1629, 1525, 1442, 1155,and 1000 cm −1, which can all be assigned to organic

protective chemicals produced by organisms—the bands at1525, 1155, and 1000 cm −1 are all signatures of anextended-chain carotenoid, for example lutein, whereas

Fig. 10 Raman spectra of thesubsurface regions of the gyp-sum/halite specimen: a, subsur-face gypsum; b, underside ofsubsurface gypsum crystal at theinterface with sedimentary de-posits, showing the presence ofbeta-carotene and hydromagne-site; c, green colony in thesubsurface, showing the pres-ence of dolomite, lutein, andcyanolichen protective bio-chemicals; d, gypsum, dolomite,and magnesite in the subsurfacesediments

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those at 1442, 1629, and 1757 cm−1 possibly belong to anaromatic polyphenolic compound such as lecanoric acid oratranorin, found in cyanolichens [7]. Finally, in Fig. 10d wesee the Raman spectrum of the substrate on which the greenmaterial is located, showing strong bands from gypsum,dolomite, and magnesite, with weaker features from theorganic components. With laser excitation of spectra fromthe crystal interface with the green area at lower wave-length, 514.5 nm, as shown in Fig. 11, the presence ofgypsum is seen on a broad band fluorescence emissionarising from the organic component.

Sample 4 was taken from the cyanobacterial matsgrowing at the intertidal zone; the Raman spectrum of thesurface shown in Fig. 12 is characteristic of the UV-radiation-protectant molecule scytonemin, a supremelyefficient absorber of ultraviolet radiation. Characteristicbands [3, 29] are at, 1631, 1591, 1552, 1477, 1390, 1355,and 1165 cm −1; also in this spectrum can be seensignatures of dolomite, aragonite, and magnesite, withbands at 1098, 1086, and 1065 cm −1 and supportingfeatures at 705 and 203 cm −1 for aragonite, the marine formof calcium carbonate. Chlorophyll appears at 1320 cm −1.On the reverse side of the cyanobacterial mat (Fig. 13)

several regions indicate the presence of dolomite andaragonite. An interesting result was obtained from thisspecimen by excitation at 514.5 nm—the key signatures ofboth scytonemin and beta-carotene were shown to bepresent, superimposed on a fluorescence emission back-ground (Fig. 14). The beta carotene signatures did notoccur in the spectrum obtained by excitation at 1064 nm,which was dominated by the spectrum of scytonemin. Wecan explain this result in terms of resonance Ramanscattering enhancement from the carotenoid component asa result of the use of green laser radiation.

Conclusions

The following conclusions can be made from the results ofthis study:

– The presence of cyanobacterial colonisation of theevaporite salt-pan environment in the sabkha wasconfirmed by the Raman spectroscopic signatures ofkey biochemicals.

Fig. 10 (continued)

Fig. 11 Raman spectrum(514.5 nm excitation, 100–1800cm−1 range) of the gypsumcrystal interface with subsurfacecolony, showing fluorescenceemission interference

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– Three types of halotrophic extremophiles were identi-fied in this study, two of which are subsurface and thethird is a surface benthic mat.

– Although the chemical strategies adopted for theirsurvival by these cyanobacterial colonies are different,there is a common factor in that each extremophilerequires the presence of dolomite or a magnesiated

Fig. 13 Raman spectrum, range100–1800 cm −1, of the under-side of the intertidal cyanobac-terial mat, showing the presenceof dolomite, aragonite, and abroad chlorophyll signature

Fig. 14 Raman spectrum ob-tained from the cyanobacterialmat surface after excitation at514.5 nm, showing the presenceof scytonemin and beta-caroteneon a fluorescence emissionbackground

Fig. 12 Raman spectrum, range100–1800 cm −1, of the surfaceof the intertidal cyanobacterialmat, showing the presence ofscytonemin, the UV-protectivecyanobacterial pigment

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carbonate as a substrate. A particular feature of thegeological evolution of the sabkha is the dolomitiza-tion of calcium carbonate sediments.

– In addition to the organic biochemicals identified, thepresence of aragonite and magnesite from possiblebiological geomodification have been detected in thezones of biological colonisation.

– Specimen 3, which showed the presence of carotenoidsand chlorophyll in a biological zone at the interfacebetween halite, gypsum, and carbonate sediments,provides a key result, because scytonemin was notfound at this location, in contrast with the surface matin specimen 4. The implication is that production of theUV-radiation protectant scytonemin is not necessary inthe subsurface site because protection is afforded bythe gypsum and halite deposits. This is in contrast withprevious conclusions made about colonies of cyano-bacteria underlying gypsum crusts; production ofscytonemin was still necessary to protect theseorganisms against low-wavelength radiation. We con-clude that the thickness of the superficial gypsum andthe presence of the halite both materially assist inprotection of the underlying organisms in the sabkha.

– All three types of halotrophic extremophile identifiedin this study are closely associated with sedimentarydeposits containing magnesium and carbonate ions; theavailability of the former for chlorophyll synthesiscould be a factor in this, as would be the porosity of thecarbonates for access of water and nutrients.

This study has revealed some novel features ofextremophile behaviour which can be compared withanalogous situations elsewhere. Previous studies of cya-nobacteria underlying gypsum crusts [7], in the AntarcticDry Valleys [3] and at Mars Oasis [10] in Antarctica, and in

gypsum deposits formed in a meteorite impact crater [25]have indicated the diversity of biological adaptation whichcan occur a molecular level, both in the synthesis of suitesof biochemicals for protection of the colonies againstradiation and desiccative stresses and also for the modifi-cation of their geological substrates to control access towater and nutrients.

Table 2 gives a listing of the key biosignature bands inthe Raman spectra of the protectant biomolecules producedby a range of extremophiles, several of which have beenidentified in the sabkha environment here.

The sabkha study provides another example of theRaman spectroscopic characterisation of extremophilebiogeology which adds to our knowledge of these diversesystems and which could be applied to interpretation of theanalytical molecular spectroscopic data which will emergefrom the robotic sensing and life-detection experimentscurrently being proposed by NASA and ESA for futureMars landers and rovers.

Acknowledgements The authors are grateful to the ResearchCouncil, the United Arab Emirates University, Al Ain (ResearchGrant No. 01-05-2-12/03), for logistic and financial support providedfor the expedition to the sabkha to collect the specimens used in thisstudy. We also thank the Malaysian Government for a studentship forNF Nik Hassan during the tenure of which this work was carried out.

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Table 2 Raman spectral bands for functional microbial pigments in extreme habitats

Function Pigment Pigment type Raman vibrational bands (wavenumber cm-1)

Ultraviolet-screening pigments Usnic acid Cortical acid 2930 1607 1322 1289Pulvinic dilactone Pulvinic derivative 1672 1405Parietin Anthraquinone 1675 1099 551Calycin Pulvinic derivative 1611 1379Atranorin para-Depside 2942 1666 1303 1294 1266Gyrophonic acid Tri-depside 1661 1290Fumarprotocetraric acid Depsidone 1642 1630 1290 1280Emodin Quinone 1659MAA(Nostoc) 7437 Mycosporine Am. Acid 2920 1400 820Scytonemin Eight-ring dimer 1590 1549 1323 1172

Anti-oxidants β-Carotene Carotenoid 1524 1155Rhizocarpic acid Isoprenoid 1665 1620 1596

Photosynthesis Porphyrin Tetrapyrrole ring 1453Chlorophylla (Cyano) Tetrapyrrole ring na 1360 1320BChla (Rhodopseudomonas) Tetrapyrrole ring naChlorobium Ch1 Tetrapyrrole ring

AccessoryLight harvesting Phycocyanin Phycobilin 1638 1369

Phycoerythrin Phycobilin na

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