Skip to main content

Endolithic Phototrophs in Built and Natural Stone

Current Microbiology volume 65, pages 183–188 (2012)Cite this article

Abstract

Lichens, algae and cyanobacteria have been detected growing endolithically in natural rock and in stone buildings in various countries of Australasia, Europe and Latin America. Previously these organisms had mainly been described in natural carbonaceous rocks in aquatic environments, with some reports in siliceous rocks, principally from extremophilic regions. Using various culture and microscopy methods, we have detected endoliths in siliceous stone, both natural and cut, in humid temperate and subtropical climates. Such endolithic growth leads to degradation of the stone structure, not only by mechanical means, but also by metabolites liberated by the cells. Using in vitro culture, transmission, optical and fluorescence microscopy, and confocal laser scanning microscopy, both coccoid and filamentous cyanobacteria and algae, including Cyanidiales, have been identified growing endolithically in the facades of historic buildings built from limestone, sandstone, granite, basalt and soapstone, as well as in some natural rocks. Numerically, the most abundant are small, single-celled, colonial cyanobacteria. These small phototrophs are difficult to detect by standard microscope techniques and some of these species have not been previously reported within stone.

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

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

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

Fig. 1
Fig. 2

References

  1. Aghamiri R, Schwartzman DW (2002) Weathering rates of bedrock by lichens: a mini watershed study. Chem Geol 188:249–259

    Article  CAS  Google Scholar 

  2. Albertano P, Ciniglia C, Pinto G, Pollio A (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433:137–143

    Article  Google Scholar 

  3. Asada R, Tazaki K (2001) Silica biomineralization of unicellular microbes under strongly acidic conditions. Can Mineral 39:1–24

    Article  CAS  Google Scholar 

  4. Banerjee M, Whitton BA, Wynn-Williams DD (2000) Surface phosphomonoesterase activity of a natural immobilized system: Chroococcidiopsis in an Antarctic desert rock. J App Phycol 12:549–552

    Article  CAS  Google Scholar 

  5. Bell RA (1993) Cryptoendolithic algae of hot semiarid lands and deserts. J Phycol 29:133–139

    Article  Google Scholar 

  6. Blackhurst RL, Genge MJ, Kearsley AT, Grady MM (2005) Cryptoendolithic alteration of Antarctic sandstones: pioneers or opportunists? J Geophys Res 110:E12S24. doi:10.1029/2005JE002463

    Article  Google Scholar 

  7. Boone DR, Castenholz RW, Garrity GM (2001) Bergey’s manual of systematic bacteriology, vol 1. Springer, New York

    Book  Google Scholar 

  8. Burford EP, Kierans M, Gadd GM (2003) Geomycology: fungi in mineral substrata. Mycologist 17:98–107

    Article  Google Scholar 

  9. Crispim CA, Gaylarde CC, Gaylarde PM (2004) Biofilms on church walls in Porto Alegre, RS, Brazil, with special attention to cyanobacteria. Int Biodeterior Biodegrad 54:121–124

    Article  Google Scholar 

  10. De los Ríos A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8:181–188

    PubMed  Google Scholar 

  11. De los Ríos A, Galván V, Ascaso C (2004) In situ microscopy diagnosis of biodeterioration processes occurring in the convent of Santa Cruz la Real (Segovia, Spain). Int Biodeterior Biodegrad 54:113–120

    Article  Google Scholar 

  12. De los Ríos A, Grube M, Sancho LS, Ascaso C (2007) Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59:386–395. doi:10.1111/j.1574-6941.2006.00256.x

    PubMed  Article  Google Scholar 

  13. De los Rios A, Wierzchos J, Sancho LG, Green TGA, Ascaso C (2005) Ecology of endolithic lichens colonizing granite in continental Antarctica. The Lichenologist 37:383–395

    Article  Google Scholar 

  14. Diels L (1914) Die Algen-Vegetation der Südtiroler Dolomitriffe. Ber Dtsch Bot Ges 32:502–526

    Google Scholar 

  15. Ferris FG, Lowson EA (1997) Ultrastructure and geochemistry of endolithic microorganisms in limestone of the Niagara Escarpment. Can J Microbiol 43:211–219

    Article  CAS  Google Scholar 

  16. Friedmann EI, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacterial communities of the Ross desert, Antarctica. Polarforschung 58:251–259

    PubMed  CAS  Google Scholar 

  17. Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169

    PubMed  CAS  Google Scholar 

  18. Garcia-Pichel F, Belnap J, Neuer S, Schanz F (2003) Estimates of global cyanobacterial biomass and its distribution. Arch Hydrobiol Suppl Algol Stud 109:213–228

    Google Scholar 

  19. Garcia-Pichel F, Lopez-Cortes A, Nübel U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67:1902–1910

    PubMed  Article  CAS  Google Scholar 

  20. Gaylarde CC, Gaylarde PM (2005) A comparative study of the major microbial biomass of biofilms on exteriors of buildings in Europe and Latin America. Int Biodeterior Biodegrad 55:131–139

    Article  Google Scholar 

  21. Gaylarde CC, Gaylarde PM, Copp J, Neilan BA (2004) Polyphasic detection of cyanobacteria in terrestrial biofilms. Biofouling 20:71–79

    PubMed  Article  CAS  Google Scholar 

  22. Gaylarde PM, Crispim CA, Neilan BA, Gaylarde CC (2005) Cyanobacteria from Brazilian building walls are distant relatives of aquatic genera. OMICS 9:30–42

    PubMed  Article  CAS  Google Scholar 

  23. Gaylarde PM, Gaylarde CC (2004) Deterioration of siliceous stone monuments in Latin America: microorganisms and mechanisms. Corr Rev 22:395–415

    Article  CAS  Google Scholar 

  24. Gaylarde PM, Jungblut A-D, Gaylarde CC, Neilan BA (2006) Endolithic phototrophs from an active geothermal region in New Zealand. Geomicrobiol J 23:579–587

    Article  CAS  Google Scholar 

  25. Gaylarde CC, Rodríguez CH, Navarro-Noya YE, Ortega-Morales BO (2012) Microbial biofilms on the sandstone monuments of the Angkor Wat complex, Cambodia. Curr Microbiol 64:85–92

    PubMed  Article  CAS  Google Scholar 

  26. Gerrath JF, Gerrath JA, Larson DW (1995) A preliminary account of the endolithic algae of limestone cliffs of the Niagara Escarpment. Can J Bot 73:788–793

    Article  Google Scholar 

  27. Gerrath JF, Gerrath JA, Matthes U, Larson DW (2000) Endolithic algae and cyanobacteria from cliffs of the Niagara Escarpment, Ontario, Canada. Can J Bot 78:807–815

    Google Scholar 

  28. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sed Petrol 51:475–478

    Google Scholar 

  29. Gross W, Heilmann I, Lenze D, Schnarrenberger C (2001) Biogeography of the Cyanidiaceae (Rhodophyta) based on 18S ribosomal RNA sequence data. Eur J Phycol 36:275–280

    Article  Google Scholar 

  30. Gross W, Kuver J, Tischendorf G, Bouchaala N, Busch W (1998) Cryptoendolithic growth of the red alga Galdieria suphuraria in volcanic areas. Eur J Phycol 33:25–31

    Article  Google Scholar 

  31. Hernández-Chavarría F, Sittenfeld A (2006) Preliminary report on the extreme endolithic microbial consortium of ‘Pailas Frías’, ‘Rincón de la Vieja’ volcano, Costa Rica. Phycol Res 54:104–107

    Article  Google Scholar 

  32. Hirsch P, Eckhardt FEW, Jr Palmer RJ (1995) Fungi active in the weathering of rock and stone monuments. Can J Bot 73:S1384–S1390

    Article  Google Scholar 

  33. Horath T, Bachofen R (2009) Molecular characterization of an endolithic microbial community in dolomite rock in the central Alps (Switzerland). Microb Ecol. doi: 10.1007/s00248-008-9483-7

  34. Horath T, Neu R, Bachofen R (2006) An endolithic microbial community in dolomite rock in central Switzerland: characterization by reflection spectroscopy, pigment analyses, scanning electron microscopy, and laser scanning microscopy. Microb Ecol 51:353–364

    PubMed  Article  CAS  Google Scholar 

  35. Kelly LC, Cockell CS, Herrera-Belaroussi A, Piceno Y, Andersen G, DeSantis T, Brodie E, Thorsteinsson T, Marteinsson V, Poly F, Leroux X (2011) Bacterial diversity of terrestrial crystalline volcanic rocks, Iceland. Microb Ecol 62:69–79. doi:10.1007/s00248-011-9864-1

    PubMed  Article  CAS  Google Scholar 

  36. Lange OL, Meyer A, Büdel B (1994) Net photosynthesis activation of a desiccated cyanobacterium without liquid water in high air humidity alone. Experiments with Microcoleus sociatus isolated from a desert soil crust. Func Ecol 8:52–57

    Article  Google Scholar 

  37. Macintyre IG, Prufert-Bebout L, Reid RP (2000) The role of endolithic cyanobacteria in the formation of lithified laminae in Bahamian stromatolites. Sedimentology 47:915–921

    Article  Google Scholar 

  38. McLoughlin N, Brasier MD, Wacey D, Green OR, Perry RS (2007) On biogenicity criteria for endolithic microborings on early Earth and beyond. Astrobiology 7:10–27

    PubMed  Article  CAS  Google Scholar 

  39. Neilan BA, Jacobs D, Del Dot T, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int J Syst Bacteriol 47:693–697

    PubMed  Article  CAS  Google Scholar 

  40. Neilan BA, Burns BP, Relman D, Lowe DR (2002) Molecular identification of cyanobacteria associated with stromatolites from distinct geographical locations. Astrobiol 7:10–26

    Google Scholar 

  41. Nienow JA, McKay CP, Friedmann EI (1988) The cryptoendolithic microbial environment in the Ross Desert of Antarctica: light in the photosynthetically active region. Microb Ecol 16:271–289

    PubMed  Article  CAS  Google Scholar 

  42. Norris TB, Castenholz RW (2006) Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone National Park. FEMS Microbiol Ecol 57:470–483

    PubMed  Article  CAS  Google Scholar 

  43. Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. PNAS 24:19964–19969

    Google Scholar 

  44. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  45. Schwabe GH (1936) Übereinige Blaualgen aus dem mitleren und südlichen Chile. Verh Deutsch Wiss Ver Santiago de Chile N.F (Valparaiso) 3:113–146

    Google Scholar 

  46. Seeler J-S, Golubic S (1991) Iyengariella endolithica sp. nova, a carbonate boring stigonematalean cyanobacterium from a warm spring-fed lake: nature to culture. Algol Stud 64:399–410

    Google Scholar 

  47. Siebert J, Hirsch P, Hoffmann B, Gliesche CG, Peissl K, Jendrach M (1996) Cryptoendolithic microorganisms from Antarctic sandstone of Linnaeus Terrace (Asgard Range): diversity, properties and interactions. Biodivers Conserv 5:1337–1363

    Article  Google Scholar 

  48. Sigler WV, Bachofen R, Zeyer J (2003) Molecular characterization of endolithic cyanobacteria inhabiting exposed dolomite in central Switzerland. Environ Microbiol 5:618–627

    PubMed  Article  CAS  Google Scholar 

  49. Tretiach M, Pecchiari M (1995) Gas exchange rates and chlorophyll content of epi- and endolithic lichens from the Trieste Karst (NE Italy). New Phytol 130:585–592

    Article  Google Scholar 

  50. Vincent WF (2000) Cyanobacterial dominance in the Polar regions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, The Netherlands, pp 321–340

    Google Scholar 

  51. Wade BD, Garcia-Pichel F (2003) Evaluation of DNA extraction methods for molecular analyses of microbial communities in modern calcarious microbialites. Geomicrobiol J 20:549–561

    Article  CAS  Google Scholar 

  52. Walker JJ, Pace NR (2007) Phylogenetic composition of Rocky Mountain endolithic microbial ecosystems. Appl Environ Microbiol 73:3497–3504

    PubMed  Article  CAS  Google Scholar 

  53. Walker JJ, Pace NR (2007) Endolithic microbial ecosystems. Ann Rev Microbiol 61:331–347

    Article  CAS  Google Scholar 

  54. Ward DM, Sategoeds CM, Nold SC, Ramsing NB, Ferris MJ, Bateson MM (1997) Biodiversity within hot spring microbial mat communities: molecular monitoring of enrichment cultures. Antonie Van Leeuwenhoek 71:143–150

    PubMed  Article  CAS  Google Scholar 

  55. Weber B, Wessels DCJ, Budel B (1996) Biology and ecology of cryptoendolithic cyanobacteria of a sandstone outcrop in the Northern Province, South Africa. Algol Stud 83:565–579

    Google Scholar 

  56. Wessels DCJ, Budel B (1995) Epilithic and cryptoendolithic cyanobacteria of Clarens sandstone cliffs in the Golden Gate Highlands National Park. S Afr Bot Acta 108:220–226

    Google Scholar 

  57. Whitton BA, Potts M (2000) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  58. Wierzchos J, Ascaso C (1996) Morphological and chemical features of bioweathered granitic biotite induced by lichen activity. Clays Clay Miner 44:652–657

    Article  CAS  Google Scholar 

  59. Wong FKY, Lau MCY, Lacap DC, Aitchison JC, Cowan DA, Pointing SB (2010) Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb Ecol: 689–699. doi: 10.1007/s00248-009-9607-8

  60. Yoon HS, Ciniglia C, Wu M, Cameron JM, Pinto G, Pollio A, Bhattacharya D (2006) Establishment of endolithic populations of extremophilic Cyanidiales (Rhodophyta) BMC Evolut Biol 6:78. doi:10.1186/1471-2148-6-78 On-line at http://www.biomedcentral.com/1471-2148/6/78

Download references

Acknowledgments

We are indebted to Helen Dalton at UNSW for assistance with CLSM. BAN thanks the Australian Research Council for financial support.

Author information

Affiliations

  1. Microbiology Research Laboratory, School of Pharmacy and Biomedical Sciences, University of Portsmouth, St. Michael’s Building, White Swan Rd, Portsmouth, PO1 2DT, UK

    Christine C. Gaylarde

  2. London, UK

    Peter M. Gaylarde

  3. University of New South Wales, Sydney, NSW, Australia

    Brett A. Neilan

Authors
  1. Christine C. Gaylarde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Gaylarde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brett A. Neilan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine C. Gaylarde.

Additional information

Peter M. Gaylarde—Deceased.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gaylarde, C.C., Gaylarde, P.M. & Neilan, B.A. Endolithic Phototrophs in Built and Natural Stone. Curr Microbiol 65, 183–188 (2012). https://doi.org/10.1007/s00284-012-0123-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-012-0123-6

Keywords

  • Sandstone
  • Stromatolite
  • Yucatan Peninsula
  • Cyanobacterial Biomass
  • Volcanic Tuff