Skip to main content

The Study of Growth of Calogaya sp. PLM8 on Cyrus the Great’s Tomb, UNESCO World Heritage Site in Iran

International Journal of Environmental Research volume 11, pages 501–513 (2017)Cite this article

Abstract

The tomb of Cyrus the Great, the most important monument in Pasargadae, has been listed as a world heritage site by UNESCO. Like many other stone monuments, the tomb has been affected by the colonization of microbial communities, especially lichens that were subjected to physical elimination in 2006. In the present study, recolonization of Calogaya sp. PLM8, a crustose lichen and its role in biodeterioration of Cyrus the Great tomb have been evaluated. Calogaya sp. PLM8 commonly colonized on this monument with significant distribution in the different facades. The interface of Calogaya sp. PLM8 with the underlying substrate has been investigated using the periodic acid-Schiff staining, scanning electron microscopy and energy-dispersive spectroscopy techniques. The results showed that both colonization of the lichen on the surface and symbiont cells penetration into the stone had caused extensive physical and chemical biodeterioration of the substrate. Besides the presence of the symbionts in the endolithic niches, other lithobiont microorganisms have been detected inside the stones. The presence of these endolithic microorganisms seems to be conditioned by the presence of the epilithic lichen thallus and its effects on the formation of microenvironments in the colonized stone. The lithobiont communities interact both geophysically and geochemically with the lithic substrate, inducing biodeterioration alteration in the tomb of Cyrus the Great.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  • Aghamiri RR, Schwartzman DW (2002) Weathering rates of bedrock by lichens: a mini watershed study. Chem Geol 188:249–259. doi:10.1016/S0009-2541(02)00105-5

    CAS  Article  Google Scholar 

  • Alam MA (2014) Growth chamber experiments on lichens: temperature and humidity regimes rapidly shape growth rates and carbohydrate contents. Norwegian University of Life Sciences, Oslo

    Google Scholar 

  • Aptroot A, James PW (2002) Monitoring Lichens on Monuments. In: Nimis PL, Scheidegger C, Wolseley PA (eds) Monitoring with lichens—monitoring lichens. Springer, Dordrecht, pp 239–253. doi:10.1007/978-94-010-0423-7_16

  • Ariño X, Saiz-Jimenez C (1996) Colonization and deterioration processes in Roman mortars by cyanobacteria, algae and lichens. Aerobiologia 12:9–18. doi:10.1007/BF02248118

    Article  Google Scholar 

  • Armstrong RA (2005) Radial growth of Rhizocarpon section Rhizocarpon lichen thalli over six years at Snoqualmie Pass in the Cascade Range, Washington State. Arct Antarct Alp Res 37:411–415. doi:10.1657/1523-0430(2005)037[0411:RGORSR]2.0.CO;2

  • Armstrong RA (2014) Within-site variation in lichen growth rates and its implications for direct lichenometry. Geogr Ann Ser A Phys Geogr 96:217–226. doi:10.1111/geoa.12043

    Article  Google Scholar 

  • Armstrong RA (2015) The influence of environmental factors on the growth of lichens in the field. In: Upreti DK, Divakar PK, Shukla V, Bajpai R (eds) Recent advances in lichenology: modern methods and approaches in biomonitoring and bioprospection, vol 1. Springer, New Delhi, pp 1–18. doi:10.1007/978-81-322-2181-4_1

  • Ascaso C, Wierzchos J (1994) Structural aspects of the lichen-rock interface using back-scattered electron imaging. Bot Acta 107:251–256. doi:10.1111/j.1438-8677.1994.tb00793.x

    Article  Google Scholar 

  • Ascaso C, Wierzchos J, Souza-Egipsy V, delos Riosa A, Delgado Rodrigues J (2002) In situ evaluation of the biodeteriorating action of microorganisms and the effects of biocides on carbonate rock. Int Biodeterior Biodegr 49:1–12. doi:10.1016/S0964-8305(01)00097-X

    Article  Google Scholar 

  • Bungartz F, Garvie LA, Nash TI (2004) Anatomy of the endolithic Sonoran Desert lichen Verrucaria rubrocincta Breuss: implications for biodeterioration and biomineralization. The Lichenologist 36:55–73. doi:10.1017/S0024282904013854

    Article  Google Scholar 

  • Cámara B, De los Ríos A, Urizal M, Álvarez de Buergo M, Varas M, Fort R, Ascaso C (2011) Characterizing the microbial colonization of a dolostone quarry: implications for stone biodeterioration and response to biocide treatments. Microb Ecol 62:299–313. doi:10.1007/s00248-011-9815-x

    Article  Google Scholar 

  • Cappitelli F, Villa F, Polo A (2014) Culture-Independent Methods to Study Subaerial Biofilm Growing on Biodeteriorated Surfaces of Stone Cultural Heritage and Frescoes. In: Donelli G (ed) Microbial biofilms: methods and protocols. Springer, New York, pp 341–366. doi:10.1007/978-1-4939-0467-9_24

  • Casanova Municchia A, Percario Z, Caneva G (2014) Detection of endolithic spatial distribution in marble stone. J Microsc 256:37–45. doi:10.1111/jmi.12155

    CAS  Article  Google Scholar 

  • Chen J, Blume H-P, Beyer L (2000) Weathering of rocks induced by lichen colonization—a review. CATENA 39:121–146. doi:10.1016/S0341-8162(99)00085-5

    CAS  Article  Google Scholar 

  • Clair LS, Seaward MR (2004) Biodeterioration of stone surfaces: lichens and biofilms as weathering agents of rocks and cultural heritage. Springer, New York. doi:10.1007/978-1-4020-2845-8

    Book  Google Scholar 

  • Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9. doi:10.1007/s00248-003-1052-5

    CAS  Article  Google Scholar 

  • Danin A, Caneva G (1990) Deterioration of limestone walls in Jerusalem and marble monuments in Rome caused by cyanobacteria and cyanophilous lichens. Int Biodeterior 26:397–417. doi:10.1016/0265-3036(90)90004-Q

    Article  Google Scholar 

  • de la Rosa JPMI, Casares Porcel M, Warke PA (2013a) Mapping stone surface temperature fluctuations: implications for lichen distribution and biomodification on historic stone surfaces. J Cult Herit 14:346–353. doi:10.1016/j.culher.2012.09.006

    Article  Google Scholar 

  • de la Rosa JPMI, Warke PA, Smith BJ (2013b) Lichen-induced biomodification of calcareous surfaces: bioprotection versus biodeterioration. Progress Phys Geography 37:325–351. doi:10.1177/0309133312467660

    Article  Google Scholar 

  • de Los Ríos A, Wierzchos J, Ascaso C (2002) Microhabitats and chemical microenvironments under saxicolous lichens growing on granite. Microb Ecol 43:181–188. doi:10.1007/s00248-001-1028-2

    Article  Google Scholar 

  • Dereeper A et al (2008) Phylogeny. Fr: robust phylogenetic analysis for the non-specialist. Nucl Acids Res 36:W465–W469. doi:10.1093/nar/gkn180

    CAS  Article  Google Scholar 

  • Di Carlo E, Barresi G, Palla F (2017) Biodeterioration. In: Palla F, Barresi G (eds) Biotechnology and conservation of cultural heritage. Springer, Cham, pp 1–30. doi:10.1007/978-3-319-46168-7_1

  • Farrar JF (1974) A method for investigating lichen growth rates and succession. The Lichenologist 6:151–155. doi:10.1017/S0024282974000247

    Article  Google Scholar 

  • Favero-Longo SE, Castelli D, Salvadori O, Belluso E, Piervittori R (2005) Pedogenetic action of the lichens Lecidea atrobrunnea, Rhizocarpon geographicum Gr and Sporastatia testudinea on serpentinized ultramafic rocks in an alpine environment. Int Biodeterior Biodegr 56:17–27. doi:10.1016/j.ibiod.2004.11.006

    CAS  Article  Google Scholar 

  • Frank-Kamenetskaya OV, Vlasov DY, Shilova OA (2012) Biogenic crystal genesis on a carbonate rock monument surface: the main factors and mechanisms, the development of nanotechnological ways of inhibition. In: Krivovichev SV (ed) Minerals as advanced materials II, vol 2. Springer, New York, pp 401–413. doi:10.1007/978-3-642-20018-2_37

  • Gazzano C, Favero-Longo SE, Matteucci E, Piervittori R (2009a) Image analysis for measuring lichen colonization on and within stonework. The Lichenologist 41:299–313. doi:10.1017/S0024282909008366

    Article  Google Scholar 

  • Gazzano C, Favero-Longo SE, Matteucci E, Roccardi A, Piervittori R (2009b) Index of lichen potential biodeteriogenic activity (Lpba): a tentative tool to evaluate the lichen impact on stonework. Int Biodeterior Biodegrad 63:836–843. doi:10.1016/j.ibiod.2009.05.006

    Article  Google Scholar 

  • Gerdes G, Dunajtschik-Piewak K, Riege H, Taher A, Krumbein W, Reineck H (1994) Structural diversity of biogenic carbonate particles in microbial mats. Sedimentology 41:1273–1294. doi:10.1111/j.1365-3091.1994.tb01453.x

    Article  Google Scholar 

  • Gholipour-Shahraki M, Sohrabi M, Mohammadi P (2013) Diversity of lichens on the tomb of Cyrus the great, Pasargadae, Iran. In: Paper presented at the BioSyst.EU 2013 Global systematics, Austria

  • Herrera LK, Videla HA (2009) Surface analysis and materials characterization for the study of biodeterioration and weathering effects on cultural property. Int Biodeterior Biodegrad 63:813–822. doi:10.1016/j.ibiod.2009.05.002

    CAS  Article  Google Scholar 

  • Hill DJ (2002) Measurement of lichen growth. In: Kranner IC, Beckett RP, Varma AK (eds) Protocols in lichenology: culturing, biochemistry, ecophysiology and use in biomonitoring, Springer, Berlin, pp 255–278. doi:10.1007/978-3-642-56359-1_16

  • Hoppert M, Flies C, Pohl W, Günzl B, Schneider J (2004) Colonization strategies of lithobiontic microorganisms on carbonate rocks. Environ Geol 46:421–428. doi:10.1007/s00254-004-1043-y

    CAS  Article  Google Scholar 

  • Jomelli V, Grancher D, Naveau P, Cooley D, Brunstein D (2007) Assessment study of lichenometric methods for dating surfaces. Geomorphology 86:131–143. doi:10.1016/j.geomorph.2006.08.010

    Article  Google Scholar 

  • Kondratyuk S et al (2014) A revised taxonomy for the subfamily caloplacoideae (Teloschistaceae, Ascomycota) based on molecular phylogeny. Acta Bot Hung 56:141–178. doi:10.1556/ABot.56.2014.1-2.12

    Article  Google Scholar 

  • Lan W, Li H, Wang W-D, Katayama Y, Gu J-D (2010) Microbial community analysis of fresh and old microbial biofilms on bayon temple sandstone of Angkor Thom, Cambodia. Microb Ecol 60:105–115. doi:10.1007/s00248-010-9707-5

    Article  Google Scholar 

  • Lisci M, Monte M, Pacini E (2003) Lichens and higher plants on stone: a review. Int Biodeterior Biodegrad 51:1–17. doi:10.1016/S0964-8305(02)00071-9

    Article  Google Scholar 

  • Mallowan M (1972) Cyrus the Great (558–529 Bc). Iran 10:1–17. doi:10.2307/4300460

    Article  Google Scholar 

  • McNamara CJ, Mitchell R (2005) Microbial deterioration of historic stone. Front Ecol Environ 3:445–451. doi:10.1890/1540-9295(2005)003[0445:MDOHS]2.0.CO;2

    Article  Google Scholar 

  • Mihajlovski A, Seyer D, Benamara H, Bousta F, Di Martino P (2015) An overview of techniques for the characterization and quantification of microbial colonization on stone monuments. Ann Microbiol 65:1243–1255. doi:10.1007/s13213-014-0956-2

    Article  Google Scholar 

  • Miller AZ, Sanmartín P, Pereira-Pardo L, Dionísio A, Saiz-Jimenez C, Macedo MF, Prieto B (2012) Bioreceptivity of building stones: a review. Sci Total Environ 426:1–12. doi:10.1016/j.scitotenv.2012.03.026

    CAS  Article  Google Scholar 

  • Mohammadi P, Krumbein WE (2008) Biodeterioration of ancient stone materials from the persepolis monuments (Iran). Aerobiologia 24:27–33. doi:10.1007/s10453-007-9079-6

    Article  Google Scholar 

  • Mohammadi P, Maghboli-Balasjin N (2014) Isolation and molecular identification of deteriorating fungi from Cyrus the Great tomb stones. Iran J Microbiol 6(5):361–370

    Google Scholar 

  • Mozaffari A (2014) World heritage in Iran: perspectives on pasargadae. Heritage, culture and identity. Ashgate Publishing Ltd, Famham

    Google Scholar 

  • Nascimbene J, Salvadori O (2008) Lichen recolonization on restored calcareous statues of three Venetian villas. Int Biodeterior Biodegrad 62:313–318. doi:10.1016/j.ibiod.2007.11.005

    CAS  Article  Google Scholar 

  • Nascimbene J, Salvadori O, Nimis PL (2009) Monitoring lichen recolonization on a restored calcareous statue. Sci Total Environ 407:2420–2426. doi:10.1016/j.scitotenv.2008.12.037

    CAS  Article  Google Scholar 

  • Nimis PL (2001) Artistic and historical monuments: threatened ecosystems. In: Frontiers of life, part 2: man and the environment, vol 2. Academic Press, San Diego, pp 557–569

  • Nimis PL, Salvadori O, Accornero E (1997) La Crescita Dei Licheni Sui Monumenti Di Un Parco. Uno Studio Pilota a Villa Manin. Il restauro delle sculture lapidee nel parco di Villa Manin a Passariano Il viale delle Erme 4:109–141

    Google Scholar 

  • Nuhoglu Y, Oguz E, Uslu H, Ozbek A, Ipekoglu B, Ocak I, Hasenekoglu İ (2006) The accelerating effects of the microorganisms on biodeterioration of stone monuments under air pollution and continental-cold climatic conditions in Erzurum, Turkey. Sci Tot Environ 364:272–283. doi:10.1016/j.scitotenv.2005.06.034

    CAS  Article  Google Scholar 

  • Prieto Lamas B, Rivas Brea MT, Silva Hermo BM (1995) Colonization by lichens of granite churches in Galicia (Northwest Spain). Sci Total Environ 167:343–351. doi:10.1016/0048-9697(95)04594-Q

    Article  Google Scholar 

  • Rafiee Fanood M, Saradj FM (2013) Learning from the past and planning for the future: conditions and proposals for stone conservation of the Mausoleum of Cyrus the Great in the world heritage site of pasargadae. Int J Archit Herit 7:434–460. doi:10.1080/15583058.2011.643527

    Article  Google Scholar 

  • Rodrigues JD, Anjos MV, Charola AE (2011) Recolonization of marble sculptures in a garden environment. Smithson Contrib Mus Conserv. doi:10.5479/si.19492359.2.1

    Google Scholar 

  • Sáiz-Jiménez C (1984) Weathering and colonization of limestones in an urban environment. In: Szegi J (ed) Soil biology and conservation of the biosphere, vol 2. Akademiai Kiado. Budapest, Hungary, pp 757–767

    Google Scholar 

  • Scheerer S, Ortega‐Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—an updated overview. In: Advances in applied microbiology, vol 66. Academic Press, Cambridge, pp 97–139. doi:10.1016/S0065-2164(08)00805-8

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    CAS  Article  Google Scholar 

  • Schoch CL et al (2012) Nuclear ribosomal internal transcribed spacer (Its) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci 109:6241–6246. doi:10.1073/pnas.1117018109

    CAS  Article  Google Scholar 

  • Seaward MR (2015) Lichens as agents of biodeterioration. In: Upreti DK, Shukla V, Divakar PK, Bajpai R (eds) Recent advances in lichenology, vol 1, Springer, pp 189–211. doi:10.1007/978-81-322-2181-4_9

  • Steiger M, Charola AE, Sterflinger K (2011) Weathering and deterioration. In: Stone in architecture. Springer, New York, pp 227–316. doi:10.1007/978-3-642-14475-2_4

  • Stronach D (1964) Excavations at Pasargadae: second preliminary report. Iran 2:21–39. doi:10.2307/4299550

    Article  Google Scholar 

  • Tiano P (2002) Biodegradation of cultural heritage: decay mechanisms and control methods. In: Proceedings ARIADNE Workshop 9—historic materials and their diagnostic. http://www.arcchip.cz/w09/w09_tiano.pdf. Accessed 23 Mar 2012

  • Vondrak J et al (2016) The extensive geographical range of several species of teloschistaceae: evidence from Russia. The Lichenologist 48:171–189. doi:10.1017/S0024282916000116

    Article  Google Scholar 

  • Wadsten T, Moberg R (1985) Calcium oxalate hydrates on the surface of lichens. The Lichenologist 17:239–245. doi:10.1017/S0024282985000305

    CAS  Article  Google Scholar 

  • Warscheid T (2015) Microbiology and archaeology. Microbial impacts at historical sites during excavation and conservation. ICOMOS–Hefte des Deutschen Nationalkomitees 42:35–48. doi:10.11588/ih.2005.0.20601

  • Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegrad 46:343–368. doi:10.1016/S0964-8305(00)00109-8

    CAS  Article  Google Scholar 

  • Whitlatch RB, Johnson RG (1974) Methods for staining organic matter in marine sediments. J Sediment Res. doi:10.1306/212F6CAD-2B24-11D7-8648000102C1865D

    Google Scholar 

  • Wierzchos J et al (2015) Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the atacama desert. Front Microbiol. doi:10.3389/fmicb.2015.00934

    Google Scholar 

Download references

Acknowledgements

This project was supported by Iran National Science Foundation (INSF), Code Number 88001692 and was carried out at the national laboratory of industrial microbiology of Alzahra University. The authors would like to thank Professor Ali Asghar Masoumi and his lichen herbarium staffs for their scientific help and the personnel of Pasargadae site for their supports and assistance during the field activity.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Biological Sciences, Alzahra University, Vanak St, Tehran, Islamic Republic of Iran

    Mahnaz Gholipour-Shahraki & Parisa Mohammadi

Authors
  1. Mahnaz Gholipour-Shahraki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Parisa Mohammadi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Parisa Mohammadi.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gholipour-Shahraki, M., Mohammadi, P. The Study of Growth of Calogaya sp. PLM8 on Cyrus the Great’s Tomb, UNESCO World Heritage Site in Iran. Int J Environ Res 11, 501–513 (2017). https://doi.org/10.1007/s41742-017-0044-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41742-017-0044-0

Keywords

  • Cyrus the Great tomb
  • Biodeterioration
  • Lichen
  • Endoliths
  • Calogaya sp. PLM8