Int.J.Curr.Microbiol.App.Sci (2016) 5(8): 30-41

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 5 Number 8 (2016) pp. 30-41 Journal homepage: http://www.ijcmas.com

Original Research Article http://dx.doi.org/10.20546/ijcmas.2016.508.004

Mycosporine-like Amino Acids from Biological Integuments of Historical Monuments

Arun S. Sonker, Richa, Jainendra Pathak, Rajneesh, Vinod K. Kannaujiya and Rajeshwar P. Sinha*

Laboratory of Photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, , -221005, *Corresponding author

ABSTRACT

Biological crusts collected from seven historical monuments in and around K e yw or ds Varanasi, India, were screened for the presence of photoprotective mycosporine- like amino acids (MAAs). Nine strains of cyanobacterial genera such as Lyngbya Biological films,

Carotenoids, sp., Nostoc sp., Anabaena sp., Scytonema sp., Phormidium sp., Westiellopsis sp.,

Chlorophyll a, Aphanocapsa sp., Hapalosiphon sp. and Aphanothece sp. were found to be present in the samples collected from various monuments apart from other group of Cyanobacteria, Historical organisms. Cyanobacteria, the dominant population growing on all the monuments monuments, had a maximum diversity of 5 species in Brahaspati temple, 4 species in Ramnagar Mycosporine -like fort and LalKhan`s tomb, 3 species in Manikarnika and Sanskrit University amino acids. and only 1 species in and temple. Pigment profile of the crusts

Article Info from the seven monuments showed peaks at 665, 470, 310 and 386 nm that correspond to the presence of chlorophyll a, carotenoids, MAAs and scytonemin Accepted: respectively. High content of cholorophyll a was recorded in the crusts from 06 July 2016 Sarnath and the Brahaspati temple, whereas carotenoids content was higher in the Available Online: crust sample of LalKhan`s tomb. In all the collected samples from various 10 August 2016 monuments, photoprotective MAAs were found to be predominant than the photosynthetic pigments (chlorophyll a and carotenoids).

Introduction early Earth, when there was no ozone layer Cyanobacteria are Gram-negative (Schopf, 2000; Hedges et al., 2001; Häder et prokaryotes having a cosmopolitan al., 2015). The ancient monument all over distribution ranging from hot-springs to the the world are deteriorating due to the Arctic and Antarctic regions (Stanier and deposition of cyanobacteria, resulting in the Cohen-Bazire, 1977). They were the first loss of basic structure and creates pits, photosynthetic oxygen-evolving prokaryotes cracks and fissures (Ortega-Calvo et al., which appeared during the Precambrian era 1991; Dhami et al., 2014). (Brocks et al., 1999). Fossil records, organic biomarkers and genomic sequence analyses On ancient monuments, cyanobacteria indicate the presence of cyanobacteria on the played an important role as pioneer for 30

Int.J.Curr.Microbiol.App.Sci (2016) 5(8): 30-41 establishing life on bare inorganic rocks and artistic work and are important part of produced considerable biomass. Most of glorious traditions and rich cultural heritage these cyanobacterial crusts growing on the of Varanasi. ancient monuments were colonial or filamentous and occurred in association with Photoprotective MAAs are <400 Da, other algae, fungi, bacteria, lichen and moss colorless, water-soluble compounds Protonema (Lüttge et al., 1995). Several composed of a cyclohexenone or studies on the cyanobacterial crust residing cyclohexenimine chromophore conjugated on the ancient monuments have been done with the nitrogen substituent of an amino in South-West USA and Mexico acid or its imino alcohol (Carreto et al., (Friedmann, 1972), monuments of Northern 2005; Richa and Sinha, 2015) and have Transvall, South Africa, marbles of absorption maxima in the range of 310-362 Parthenon (Acropolis-Athens) of Greece nm. Generally, the ring system contains a (Anagnostidis et al., 1983), Roman frescoes glycine subunit linked to the third carbon (Grilli-Caiola et al., 1987; Albertano and atom. Some MAAs also contains sulfate Grilli-Caiola, 1989), Inferniglio cave of Italy esters or glycosidic linkages through the (Abdelahad, 1989), Lund cathedral of imine substituents. Differences between the Sweden (Ortega-Calvoet al., 1991), Roman absorption spectra of MAAs are due to the Necropolis (Albertano et al., 1994) and attached side groups and nitrogen Goldengate highlands National Park, South substituent. The biosynthesis of MAAs has Africa (Wessels and Büdel,1989) etc. been predicted to occur via the first part of the shikimate pathway but concluding In Varanasi (India) region, so far no prior evidences are lacking. It has been found that studies have been done on the presence of 3-dehydroquinate, which is formed in the photoprotective MAAs in the crust forming centre of the shikimate pathway, acts as a cyanobacteria of the monuments. Some of precursor for the synthesis of fungal these monuments are situated in the warm mycosporines and MAAs via gadusols temperate region having a very suitable (Shick et al., 2002). condition for the growth and development of cyanobacteria which is responsible for the MAAs provide protection from UV defragmentation of the monuments. Though radiation not only in their producers but also such problems are important in humid and to primary and secondary consumers tropical climates, there is little information through the food chain. MAAs has been about the cyanobacteria growing on the reported in diverse organisms, such as, monuments of India (Tripathy et al., 1999; bacteria, cyanobacteria, macroalgae, Pattanaik and Adhikary, 2002). Some phytoplankton and various animals such as historical monuments of Varanasi such as, arthropods, rotifers, molluscs, fishes, Sarnath temple is about three hundred years cnidarians, tunicates, poriferans, nematodes, old and a holy place for Buddhists, LalKha echinodermates, platythelminthes, ka Rauza build by Mughal emperor is polychaetes, bryozoans and protozoans situated at the bank of sacred river , (Sinha et al., 2007; Kannaujiya et al., 2014; Sanskrit University is about 150 years old, Pathak et al., 2015), but not in animals as was manufactured by the they lack the shikimate pathway, but these King of Varanasi about five hundred years compounds may be accumulated either via ago and Manikarnika ghat temple is about the food chain or synthesized by their 600 hundred years old, have wonderful symbiotic algal partner (Shick and Dunlap,

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2002). Presently, about 22 MAAs have been 48 h. To examine the presence of reported from terrestrial, freshwater and cyanobacteria, a pinch of the rehydrated marine organisms. MAAs have high molar crusts were observed under compound extinction coefficient which favours them as microscope (Getneroptik KFS4 (I) 5582) strong photoprotectant. In addition, to their and photographed using Dewinter image photoprotective role in various organisms, microscope fitted with digital camera. MAAs are also of immense importance for Various cyanobacteria, such as, Anabaena humans as these compounds have been sp., Nostoc sp., Lyngbya sp. and Scytonema found to effectively block thymine dimer sp. etc. were found to be present in the formation by UVR in vitro, have antioxidant collected crusts. as well as growth stimulation activity in human cells and were recently found to Mycosporine-like amino acids (MAAs) reduce UV-induced aging (Oyamada et al., extraction and spectroscopic analysis 2008; Singh et al., 2010). In the present study, for the first time, we have reported For extraction of MAAs, equal amount of the diversity of cyanobacteria and the crust (0.5 mg) collected from various presence of photoprotective MAAs from the monuments were dissolved in 2 mL of exposed surfaces of different monuments of 100% methanol (HPLC-grade) and Varanasi, India. incubated at 4 °C for overnight. The methanol extracts were centrifuged at Materials and Methods 10,000 rpm for 10 min, and the supernatant was subjected to spectroscopic analysis Collection sites between 250-700 nm wavelengths, using a double beam spectrophotometer (UV-VIS The cyanobacterial samples were collected 2900, Hitachi, Japan). The raw spectra from various monuments such as, LalKhan`s (peaks) were analyzed using UV Probe tomb, Manikarnika ghat, Brahaspati temple, version software (Hitachi, Japan). Sarnath, Ramnagar fort, Sanskrit University and Bharat Mata temple. These monuments Purification and estimation of MAAs are situated between 25° 20' 0" North, 83° 0' 0"East in of , After initial characterization of MAAs by India. These historical places are very spectroscopic analysis, methanolic extracts popular and some are protected by the were evaporated to dryness at 450C, and the Archaeological survey of India. Since the dried product was dissolved in 1ml Milli Q cyanobacterial colonization occurs in the water in a microcentrifuge tube. After upper surface of the crust, we have collected adding a few drops of chloroform, the the crust growing over these monuments by suspension was subjected to centrifugation, a non-destructive double layered adhesive and the water phase was carefully tape method and then transferred to pre- transferred into a fresh microcentrifuge tube sterilized screw-cap bottles and transported to remove contaminating lipophillic to the laboratory for further analyses. compounds.

Identification of organisms Finally, the resulting suspension was filtered through a 0.2 μm pore size syringe filters The collected crusts from the monuments (Axiva Sichem Biotech., New Delhi) and were soaked in sterile distilled water for 12- further subjected to high performance liquid chromatography (HPLC; Waters, 32

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Elstree,UK) analysis using a reverse phase Nostoc sp., Anabaena sp., Scytonema sp., semi preparative column (symmetry prep Phormidium sp., Hapalosiphon sp., C18, 7 μm particle size, 7.8mm × 300 mm Westiellopsis sp., Aphanocapsa sp. and long) connected to an asymmetry guard Aphanothece sp. were found to be present in column, outfitted with a Waters Photodiode the crust samples of various monuments. array detector. 0.2 % acetic acid was used as The 16S rRNA gene sequences analyses mobile phase and detection of MAAs was indicate the presence of similar done at 330 nm. Identification and cyanobacteria in sub-aerial habitats of characterization of MAAs was done on the monuments, sculptures and archeological basis of the retention time and their sites (Bruno et al., 2009). corresponding absorption spectra. Figure 1 shows the microphotographs of the Estimation of Chlorophyll a and cyanobacterial filaments collected from carotenoids various monuments. Among the algal group, cyanobacteria were the dominant population Crust (1g) collected from different growing over all the monuments with monuments of Varanasi was homogenized maximum diversity of 5 species in in 95% methanol with the help of motor and Brahaspati temple, 4 species in Ramnagar pestle. The homogenate was centrifuged at fort and LalKhan`s tomb, 3 species in 10,000 rpm for 10 min using Spinwin 650 Manikarnika ghat and Sanskrit university and the collected supernatants were and only 1 species in Sarnath and Bharat subjected to spectroscopic analysis between Mata temple. 400-700 nm wavelengths using a double beam spectrophotometer (UV-VIS 2900, Pigment analysis Hitachi, Japan). Chlorophyll a showed the maximum absorbance at 665 nm and total Pigment profile of the crusts collected from carotenoids at 470 nm. The amount of these the monuments are shown in Fig. 2. The pigments was calculated according to the absorption spectra of 100 % (v/v) formula of Lichtenthaler and Wellburn methanolic extract showed peaks at 665, (1985). 470, 310 and 386 nm that correspond to the presence of chlorophyll a, carotenoids, Results and Discussion MAAs and scytonemin respectively. In all the crust samples MAAs was found to be Nature of the crust and algal colonization quite predominant than the scytonemin, chlorophyll a and carotenoids (Pathak et al., The crust collected from all the monuments 2015). were blackish to brownish in color, predominately growing at the ledges of the Chlorophyll a content was recorded to be temples, roof of the fort and on the domes of highest in the samples collected from the monuments, which were exposed to Sarnath and Brahaspati temple. The level of wide spectrum of solar and UV radiation chlorophyll a in the crust samples of five (Polo et al., 2012; Pathak et al., 2015). other monuments of Varanasi (LalKhan`s There were almost no variations in the tomb, Ramnagar fort, Bharat Mata temple, climatic conditions of all the monuments Manikarnika ghat, Sanskrit University) were and their environment. Nine species of found to be very close to each other. cyanobacteria (Table 1) viz., Lyngbya sp., However, crust samples of Ramnagar Fort

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and Sanskrit University showed a slightly a corresponding absorption maxima (λmax) higher content of Chl a in comparison to between 307-330 nm ( Fig. 5), whereas, in other three monuments (Fig. 3). Carotenoids case of crust from Sarnath temple the level was highest in crust sample of presence of five MAAs having RT 2.0 -14.4 LalKhan`s tomb followed by Sarnath and min (λmax: 310-330 nm) ( Fig. 6) were Brahaspati temple (Fig. 4). The levels of recorded. carotenoids in crust samples of remaining monuments were negligible. The aqueous solution of crust from Sanskrit university (Fig. 6), Brahaspati temple and Analysis of photoprotective compound Bharatmata temple showed the presence of six (RT-2.0-4.4 min; λmax: 307-330 nm), The absorption spectra of methanolic extract three (RT- 2.3-4.1 min; λmax: 310-330 nm) showed the presence of a photoprotective and eight (RT- 2.2-7.3 min; λmax: 313-330 compound, mycosporine-like amino acids nm) MAAs respectively (Fig. 7). The crust peaking around 307-330 nm (Fig. 2). HPLC from Ramnagar fort and LalKhan`s tomb chromatogram of the aqueous solution of showed the presence of five (RT- 2.0- Manikarnika ghat sample showed the 20.0min; λmax: 307-330 nm) and nine (RT- presence of eight MAAs having retention 2.13-7.2 λmax: 307-330 nm) (Fig. 7) MAAs times (RT) ranging from 2.19-13.2 min and respectively.

Table.1 Cyanobacterial strains inhabiting different historical monuments of Varanasi, India

Historical monuments Cyanobacteria Ramnagar Bharat Mata Brihaspati LalKhan’s Sanskrit Sarnath Manikarnika Fort Temple Temple Tomb University Ghat Lyngbya sp. + - - + + + + Nostoc sp. + - + - + - + Anabaena sp. + - + - - - - Scytonema sp. - + + + + - + Phormidium sp. + ------Hapalosiphon - - + - - - - sp. Westiellopsis - - + - - - - sp. Aphanocapsa - - - + - - - sp. Aphanothece - - - + - - - sp. + = Present; - = Absent

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Fig.1 Cyanobacteria isolated from different monuments. (A) Lyngbya sp., (B) Westiellopsis sp. (C) Hapalosiphon sp., (D) Nostoc sp., (E) Aphanothece sp. (F) Scytonema sp., (G) Phormidium sp. (H) Anabaena sp. and (I) Aphanocapsa sp.

A B C

D E F

G H I

Fig.2 Absorption spectra showing the presence of Chl a, carotenoids and the predominant MAAs in biological crusts of different monuments.

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Fig.3 Chlorophyll a content in biological crusts collected from different monuments of Varanasi, India

Fig.4 Carotenoids content in biological crusts collected from different monuments of Varanasi, India

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Fig.5 Photographs showing different collection sites of Manikarnika Ghat (A-C). The HPLC chromatograms (D-F) and the corresponding absorption maxima (G-I) of MAAs present in the biological crusts. Red arrows show the point of crust collection.

A D 0.015 G

0.02 0.010 RT-3.1min

0.015 RT-4.0min AU 0.005 0.01 RT-4.8min

0.000 0.005 Absorbance[O.D.] 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 0 Minutes 250 300 350 400 Wavelength[nm]

H B E 0.08 RT- 2.1 min 0.020 0.07 0.06 RT-3.9 min 0.05 RT-4.1 min

AU 0.010 0.04 0.03 RT- 4.9 min 0.02 RT-5.6 min

0.000 Absorbance[O.D. ] 0.01 0 RT-7.0min 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 250 300 350 400 Minutes RT- 1.9 min Wavelength[nm]

I C F 0.01 RT-2.0min 0.002 0.008 RT-3.1min

0.001 0.006

AU RT-3.9min

0.004 0.000 RT-4.7min

Absorbance[O.D. Absorbance[O.D. ] 0.002 RT-13.2min

0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 0 Minutes 250 350 450 Wavelength[nm]

Fig.6 Photographs showing different collection sites of Sarnath (A and B) and Sanskrit University (C). The HPLC chromatograms (D-F) and the corresponding absorption maxima (G- I) of MAAs present in the biological crusts. Red arrows show the point of crust collection.

RT-2.2min

A D G ] 0.0005 0.08 RT-3.2min 0.06

0.0000 RT-3.8min AU -0.0005 0.04 RT-4.7min 0.02 RT-6.3min

-0.0010 Absorbance[O.D. 0 RT-7.6min 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 250 300 350 400 RT-14.0min Minutes Wavelength[nm] RT-14.4min

B E 0.002 H 0.08 RT-2.2min 0.06 RT-3.2min 0.001 RT-3.8min AU 0.04 RT-4.7min RT-6.3min 0.02 RT-7.6min 0.000 RT-14.0min

0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 Absorbance[O.D] 0 RT-14.4min Minutes 250 300 350 400 Wavelength[nm]

C F I 0.008 RT-2.0min 0.004 0.006 RT-3.7min AU 0.002 0.004 0.002 RT-4.4min 0.000 0 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 ] Absorbance[O.D. 250 350 Minutes Wavelength[nm]

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Fig.7 Photographs showing different collection sites of Brihaspati temple (A), Bharat Mata temple (B), Ramnagar Fort (C) and LalKhan’s Tomb (D). The HPLC chromatograms (E-H) and the corresponding absorption maxima (I-L) of MAAs present in the crusts. Red arrows show the point of crust collection

E I A 0.002 0.004

0.003 RT-2.3min

AU 0.001 RT-3.8min 0.002 RT-4.1min

0.000 0.001 Absorbance[O.D. ] Absorbance[O.D. 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 22.00 24.00 0 250 350 Minutes Wavelength[nm] F B J RT-2.2min 0.002 0.008 RT-2.29min 0.006 RT-3.8min

AU 0.001 0.004 0.002 RT-4.1min 0.000 0 RT-6.9min 200 400

0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 22.00 24.00 Absorbance[O.D.] Wavelength[nm] Minutes

G0.010 K C 0.05 RT-2.0min 0.04 RT-2.58min 0.005 0.03 RT-3.0min AU 0.02 RT-3.7min 0.01 RT-4.7min 0.000 0 RT-20.0min

0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 22.00 24.00 Absorbance[O.D.] 250 450 Minutes Wavelength[nm]

D H L 0.025 RT-2.1min 0.015 RT-2.5min 0.02 RT-2.9min 0.010 RT-3.6min AU 0.015 RT-3.7min 0.005 0.01 RT-4.3min RT-4.5min 0.000 0.005 RT-5.6min 0.00 2.00 4.00 6.00 8.00 10.00 12.00 14.00 16.00 18.00 20.00 RT-7.2min

Absorbance[O.D. ] Absorbance[O.D. 0 Minutes 250 350 Wavelength[nm]

Analysis of the result showed that species and Phormidium sp. whereas the decorated composition in the crusts of temples, , walls were dominated by mosque and old building varied with the unicellular/colonial forms of cyanobacterial nature of the substratum (solid rock, bare species such as Westiellopsis sp., rocks, bare bricks, cement, etc.). The Aphanocapsa sp. and Aphanothece sp., etc. exposed roof top part of the monument Cyanobacteria are the dominant species which is composed of bricks without any colonizing on the sub aerial surfaces in uneven sculptures is mostly covered by warm temperate to tropical regions (Videla black colored crust dominated by Lyngbya et al., 2000; Couradeau et al., 2016). During sp., Nostoc sp., Anabaena sp., Scytonema sp. summer season, the temperature of different

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Int.J.Curr.Microbiol.App.Sci (2016) 5(8): 30-41 monuments and Ghats goes beyond 650C, the financial support in the form of a coupled with high light intensity, UV fellowship. This work was also partially radiation and extreme dryness and supported by Department of Science and cyanobacteria can survive in such extreme Technology sponsored project (No. environment in the surfaces of these SR/WOS-A/LS-140/2011) sanctioned to monuments as blackish-brownish crust. Richa. J. Pathak and V.K. Kannaujiya are Since the Ramnagar fort and Sarnath thankful to CSIR, New Delhi, India for the monument is fully exposed to UV radiation, financial support in the form of JRF and hence probably had maximum diversity of SRF respectively. Rajneesh is thankful to cyanobacteria. Cyanobacterial species DBT for the financial support in the form of exposed to strong UV radiation have also JRF. been found to contain one or more UV- absorbing mycosporine-like amino acid References compounds and/or extracellular sunscreen pigment scytonemin which have been Abdelahad, N. 1989. On four myxosarcina- suggested as a protective/defensive strategy like species (Cyanophyta) living in the against high UV radiation (Garcia-Pichel Inferniglio cave (Italy). Algological and Castenholz 1991; Keshari and Adhikary, Studies, 54: 3-13. 2013). Albertano, P., Grilli-Caiola, M. 1989. A hypogean algal association. Braun In conclusion, we studied the presence of Blanquetia, 3: 287-292. photoprotective compound mycosporine-like Albertano, P., Kovacik, L., and Grilli- amino acid, cyanobacterial diversity, Caiola, M. 1994. Preliminary chlorophyll a and carotenoids content in the investigations on epilithiccyanophytes crust samples collected from several from a Roman necropolis. Algological monuments of Varanasi. We observed that 9 Studies, 75: 71-74. species of cyanobacteria such as Lyngbya Anagnostidis, K., Economou-Amilli, A., and sp., Nostoc sp., Anabaena sp., Scytonema Roussomoustakaki, M. 1983. Epilithic sp., Phormidium sp., Westiellopsis sp., and chasmolithic microflora Aphanocapsa sp., Hapalosiphon sp. and (Cyanophyta, Bacillariophyta) from Aphanothece sp. were present in the crust marbles of the parthenon (Acropolis, samples. There was almost no variation in Athens, Greece). Nova Hedwigia, 38: the climatic conditions of all the monuments 227-277. and their environment. All the Brocks, J.J., Logan, G.A., Buick, R., cyanobacterial samples inhabiting the Summons, R.E. 1999. Archean monuments showed high content of MAAs, molecular fossils and the early rise of followed by Chl a and carotenoids. The Eukaryotes. Sci., 285: 1033-1036. higher MAAs concentration could probably Carreto, J.I., Carignan, M.O., Montoya, be responsible for providing protection to N.G. 2005. A high-resolution reverse- these organisms which are continuously phase liquid chromatography method exposed to intense UV radiation on the for the analysis of mycosporine-like monument surfaces. amino acids (MAAs) in marine organisms. Marine Biol., 146: 237- Acknowledgements 252. Couradeau, E., Karaoz, U., Lim, H.C., da Arun S. Sonker is thankful to University Rocha, U.N., Northen, T., Brodie, E., Grant Commission, New Delhi, India, for and Garcia-Pichel, F. 2016. Bacteria 39

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How to cite this article:

Arun S. Sonker, Richa, Jainendra Pathak, Rajneesh, Vinod K. Kannaujiya and Rajeshwar P. Sinha. 2016. Mycosporine-like Amino Acids from Biological Integuments of Historical Monuments. Int.J.Curr.Microbiol.App.Sci. 5(8): 30-41. doi: http://dx.doi.org/10.20546/ijcmas.2016.508.004

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