Phototrophic and fungal communities inhabiting the Roman cryptoporticus of the national museum Machado de Castro (UNESCO site, Coimbra, Portugal).
Cryptoporticus
Fungi
Limestone
Museum
Photoautotrophic communities
UNESCO
Journal
World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472
Informations de publication
Date de publication:
09 Jul 2022
09 Jul 2022
Historique:
received:
16
02
2022
accepted:
21
06
2022
entrez:
9
7
2022
pubmed:
10
7
2022
medline:
14
7
2022
Statut:
epublish
Résumé
Caves are oligotrophic environments, characterized by constant temperatures, high humidity and low natural light. However, microbial shifts can still happen in such environments, especially with the increase in tourist activity and implementation of artificial lights, making caves even more susceptible to environmental changes. As a result, proliferation of phototrophic organisms can increase dramatically, leading to their settlement on stone surfaces, which in turn facilitates the development of heterotrophic organisms, such as fungi and bacteria. The Roman Cryptoporticus of the National Museum Machado de Castro, erected by the Romans in the 1st or second century, is one of the most emblematic buildings in the city of Coimbra. However, the majority of the rooms that constitute this monument show signs of biodeterioration by microalgae and cyanobacteria as well as of fungi. The aim of this study was to characterize the phototrophic and fungal communities at this site, employing culture-dependent and-independent methodologies. Culture-dependent results showed that the phototrophic communities were mainly composed of green microalgae, whereas the culture-independent showed that cyanobacteria were the most dominant. As to the fungal communities, both approaches identified various entomopathogenic fungal species. In addition, the culture-independent analysis also allowed to verify the presence of animal reads, suggesting the hypothesis that animal vectored dispersion can play an important role in the development of fungi at this environment.
Identifiants
pubmed: 35809137
doi: 10.1007/s11274-022-03345-x
pii: 10.1007/s11274-022-03345-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
157Subventions
Organisme : Fundação para a Ciência e a Tecnologia
ID : SFRH/BD/139720/2018
Organisme : Fundação para a Ciência e a Tecnologia
ID : SFRH/BD/132523/2017
Organisme : Fundação para a Ciência e a Tecnologia
ID : POCI-01-0145-FEDERPTDC/EPH-PAT/3345/2014
Organisme : Fundação para a Ciência e a Tecnologia
ID : UIDB/04004/2020
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Abarenkov K, Henrik Nilsson R, Larsson K-H et al (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x
doi: 10.1111/j.1469-8137.2009.03160.x
pubmed: 20409185
Albertano P, Urzì C (1999) Structural interactions among epilithic cyanobacteria and heterotrophic microorganisms in Roman hypogea. Microbial Ecol 38:244–252. https://doi.org/10.1007/s002489900174
doi: 10.1007/s002489900174
Albertano P, Moscone D, Palleschi G et al (2003) Cyanobacteria attack rocks (CATS): control and preventive strategies to avoid damage caused by cyanobacteria and associated microorganisms in Roman hypogean monuments. In: Saiz-Jimenez C (ed) Molecular biology and cultural heritage. Swets & Zeitlinger BV, Lisse, pp 151–162
Albertano P (2012) Cyanobacterial biofilms in monuments and caves. In: Whitton BA (ed) Ecology of cyanobacteria. II: their diversity in space and time. Springer, Dordrecht, pp 317–343. https://doi.org/10.1007/978-94-007-3855-3
doi: 10.1007/978-94-007-3855-3
Aley T (2004) Tourist caves: algae and lampenflora. In: Gunn J (ed) Encyclopedia of Caves and Karst Science v2. Routledge, London. https://doi.org/10.4324/9780203483855
doi: 10.4324/9780203483855
Aleya L, Dauta A, Reynolds CS (2011) Endogenous regulation of the growth-rate responses of a spring-dwelling strain of the freshwater alga, Chlorella minutissima, to light and temperature. Eur J Protistol 47:239–244. https://doi.org/10.1016/j.ejop.2011.05.003
doi: 10.1016/j.ejop.2011.05.003
pubmed: 21696928
Alonso L, Pommier T, Kaufmann B et al (2019) Anthropization level of Lascaux Cave microbiome shown by regional-scale comparisons of pristine and anthropized caves. Mol Ecol. https://doi.org/10.1111/mec.15144
doi: 10.1111/mec.15144
pubmed: 31177607
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389
doi: 10.1093/nar/25.17.3389
pubmed: 9254694
pmcid: 146917
Alvarenga DO, Andreote APD, Branco LHZ et al (2021) Amazonocrinis nigriterrae gen. nov., sp. Nov., Atlanticothrix silvestris gen. nov., sp. nov. and Dendronalium phyllosphericum gen. nov., sp. nov., nostocacean cyanobacteria from Brazilian environments. Int J Syst Evol Microbiol 71:004811. https://doi.org/10.1099/ijsem.0.004811
doi: 10.1099/ijsem.0.004811
Baquedano Estévez C, Moreno Merino L, de la Losa RA et al (2019) The lampenflora in show caves and its treatment: an emerging ecological problem. Int J Speleol 48:249–277. https://doi.org/10.5038/1827-806X.48.3.2263
doi: 10.5038/1827-806X.48.3.2263
Bruno L, Albertano P (1996) First data on epilithic heterocystous cyanobacteria from Roman hypogea. Giorn Bot Ital 130:1013–1015. https://doi.org/10.1080/11263509609438384
doi: 10.1080/11263509609438384
Bruno L, Rugnini L, Spizzichino V et al (2019) Biodeterioration of Roman hypogea: the case study of the Catacombs of SS. Marcellino and Pietro (Rome, Italy). Ann Microbiol 69:1023–1032. https://doi.org/10.1007/s13213-019-01460-z
doi: 10.1007/s13213-019-01460-z
Cailhol D, Ciadamidaro L, Dupuy D et al (2020) Fungal and bacterial outbreak in the wine vinification area in the Saint-Marcel show cave. Sci Total Environ 733:138756. https://doi.org/10.1016/j.scitotenv.2020.138756
doi: 10.1016/j.scitotenv.2020.138756
pubmed: 32442874
Cappitelli F, Cattò C, Villa F (2020) The control of cultural heritage microbial deterioration. Microorganisms 8:1542. https://doi.org/10.3390/microorganisms8101542
doi: 10.3390/microorganisms8101542
pmcid: 7600914
Catarino L, Figueiredo R, Figueiredo FP et al (2019) The use of dolostone in historical buildings of Coimbra (Central Portugal). Sustainability 11:4158. https://doi.org/10.3390/su11154158
doi: 10.3390/su11154158
Chelius MK, Beresford G, Horton H et al (2009) Impacts of alterations of organic inputs on the bacterial community within the sediments of Wind Cave, South Dakota, USA. Int J Speleol 38:1–10. https://doi.org/10.5038/1827-806X.38.1.1
doi: 10.5038/1827-806X.38.1.1
Cigna A, Forti P (2013) Caves: the most important geotouristic feature in the world. Tourism Karst Areas 6:9–26
Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9. https://doi.org/10.1007/s00248-003-1052-5
doi: 10.1007/s00248-003-1052-5
pubmed: 15883863
Crous PW, Wingfield MJ, Burgess TI et al (2016) Fungal Planet description sheets: 469–557. Persoonia 37:218–403. https://doi.org/10.3767/003158516X694499
doi: 10.3767/003158516X694499
pubmed: 28232766
pmcid: 5315290
Crous PW, Schoch CL, Hyde KD et al (2009) Phylogenetic lineages in the Capnodiales. Stud Mycol 64:17-47-S7. https://doi.org/10.3114/sim.2009.64.02
doi: 10.3114/sim.2009.64.02
pubmed: 20169022
pmcid: 2816965
Cutler NA, Oliver AE, Viles HA et al (2010) The characterisation of eukaryotic microbial communities on sandstone buildings in Belfast, UK, using TRFLP and 454 pyrosequencing. Int Biodet Biodegradation 82:124–133. https://doi.org/10.1016/j.ibiod.2013.03.010
doi: 10.1016/j.ibiod.2013.03.010
Czerwik-Marcinkowska J, Wojciechowska A, Massalski A (2015) Biodiversity of limestone caves: aggregations of aerophytic algae and cyanobacteria in relation to site factors. Pol J Ecol 63:481–499. https://doi.org/10.3161/15052249PJE2015.63.4.002
doi: 10.3161/15052249PJE2015.63.4.002
Djemiel C, Plassard D, Terrat S et al (2020) µgreen-db: a reference database for the 23S rRNA gene of eukaryotic plastids and cyanobacteria. Sci Rep 10:5915. https://doi.org/10.1038/s41598-020-62555-1
doi: 10.1038/s41598-020-62555-1
pubmed: 32246067
pmcid: 7125122
Dyda M, Pyzik A, Wilkojc E et al (2019) Bacterial and fungal diversity inside the medieval building constructed with sandstone plates and lime mortar as an example of the microbial colonization of a nutrient-limited extreme environment (Wawel Royal Castle, Krakow, Poland). Microorganisms. https://doi.org/10.3390/microorganisms7100416
doi: 10.3390/microorganisms7100416
pubmed: 31623322
pmcid: 6843168
Fernandes P (2006) Applied microbiology and biotechnology in the conservation of stone cultural heritage materials. Appl Microbiol Biotechnol 73:291–296. https://doi.org/10.1007/s00253-006-0599-8
doi: 10.1007/s00253-006-0599-8
pubmed: 17043826
Fidanza MR, Caneva G (2019) Natural biocides for the conservation of stone cultural heritage: a review. J Cult Herit 38:271–286. https://doi.org/10.1016/j.culher.2019.01.005
doi: 10.1016/j.culher.2019.01.005
Gadd GM, Bahri-Esfahani J, Li Q et al (2014) Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev 28:36–55. https://doi.org/10.1016/j.fbr.2014.05.001
doi: 10.1016/j.fbr.2014.05.001
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
doi: 10.1111/j.1365-294X.1993.tb00005.x
pubmed: 8180733
Gaylarde PM, Gaylarde CC (2000) Algae and cyanobacteria on painted buildings in Latin America. Int Biodeterior Biodegradation 46:93–97. https://doi.org/10.1016/S0964-8305(00)00074-3
doi: 10.1016/S0964-8305(00)00074-3
Golubic S, Perkins RD, Lukas KJ (1975) Boring microorganisms and microborings in carbonate substrates. In: Frey RW (ed) The study of trace fossils. SpringerVerlag New York Inc, New York, pp 229–259
doi: 10.1007/978-3-642-65923-2_12
Grant C (1982) Fouling of terrestrial substrates by algae and implications for control—a review. Int Biodeterior Bull 18:57–65
Griffin PS, Indictor N, Kloestler RJ (1991) The biodeterioration of stone: a review of deterioration mechanisms, conservation case histories, and treatment. Int Biodeterior 28:187–207. https://doi.org/10.1016/0265-3036(91)90042-P
doi: 10.1016/0265-3036(91)90042-P
Griffin DW, Gray MA, Lyles MB et al (2014) The transport of nonindigenous microorganisms into caves by human visitation: a case study at Carlsbad Caverns National Park. Geomicrobiol J 31:175–185. https://doi.org/10.1080/01490451.2013.815294
doi: 10.1080/01490451.2013.815294
Gutarowska B (2020) The use of -omics tools for assessing biodeterioration of cultural heritage: a review. J Cult Herit 45:351–361. https://doi.org/10.1016/j.culher.2020.03.006
doi: 10.1016/j.culher.2020.03.006
Hallmann C, Stannek L, Fritzlar D et al (2013) Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiol Ecol 84:355–372. https://doi.org/10.1111/1574-6941.12065
doi: 10.1111/1574-6941.12065
pubmed: 23278436
Hallmann C (2015) Biodiversity of Terrestrial Algal Communities from Soil and Air-Exposed Substrates Using a Molecular Approach. PhD thesis, Universität Göttingen.
Hernández-Mariné M, Asencio-Martínez A, Canals A et al (1999) Discovery of populations of the lime incrusting genus Loriella (Stigonematales) in Spanish caves. Arch Hydrobiol Algol Stud 94:121–138. https://doi.org/10.1127/algol_stud/94/1999/121
doi: 10.1127/algol_stud/94/1999/121
Hodač L, Hallmann C, Rosenkranz H et al (2012) Molecular evidence for the wide distribution of two lineages of terrestrial green algae (Chlorophyta) over tropics to temperate zone. ISRN Ecol 795924:1–9. https://doi.org/10.5402/2012/795924
doi: 10.5402/2012/795924
Hodač L, Brinkmann N, Mohr KI et al (2015) Diversity of microscopic green algae (Chlorophyta) in calcifying biofilms of two karstic streams in Germany. Geomicrobiol J 32:275–290. https://doi.org/10.1080/01490451.2013.878418
doi: 10.1080/01490451.2013.878418
Horath T, Bachofen R (2009) Molecular characterization of an endolithic microbial community in dolomite rock in the central Alps (Switzerland). Microb Ecol 58:290–306. https://doi.org/10.1007/s00248-008-9483-7
doi: 10.1007/s00248-008-9483-7
pubmed: 19172216
Hyde KD, Tennakoon DS, Jeewon R et al (2019) Fungal diversity notes 1036–1150: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity 96:1–242. https://doi.org/10.1007/s13225-019-00429-2
doi: 10.1007/s13225-019-00429-2
Isola D, Zucconi L, Cecchini A et al (2021) Dark-pigmented biodeteriogenic fungi in etruscan hypogeal tombs: New data on their culture-dependent diversity, favouring conditions, and resistance to biocidal treatments. Fungal Biol 125:609–620. https://doi.org/10.1016/j.funbio.2021.03.003
doi: 10.1016/j.funbio.2021.03.003
pubmed: 34281654
Joshi SR, Chettri U (2019) Fungi in hypogean environment: bioprospection perspective. In: Satyanarayana T, Deshmukh SK, Deshpande MV (eds) Advancing frontiers in mycology & mycotechnology. Springer, Singapore, pp 539–561. https://doi.org/10.1007/978-981-13-9349-5_22
doi: 10.1007/978-981-13-9349-5_22
Jurado V, Sanchez-Moral S, Saiz-Jimenez C (2008) Entomogenous fungi and the conservation of the cultural heritage: a review. Int Biodeterior Biodegradation 62:325–330. https://doi.org/10.1016/j.ibiod.2008.05.002
doi: 10.1016/j.ibiod.2008.05.002
Jurado V, del Rosal Y, Gonzalez-Pimentel JL et al (2020) Biological control of phototrophic biofilms in a show Cave: the Case of Nerja Cave. Appl Sci 10:3448. https://doi.org/10.3390/app10103448
doi: 10.3390/app10103448
Jurado V, Gonzalez-Pimentel JL, Fernandez-Cortes A et al (2022) Early detection of phototrophic biofilms in the polychrome panel, El Castillo Cave, Spain. Appl Biosci 1:40–63. https://doi.org/10.3390/applbiosci1010003
doi: 10.3390/applbiosci1010003
Lamprinou V, Danielidis DB, Economou-Amilli A et al (2012) Distribution survey of cyanobacteria in three Greek caves of Peloponnese. Int J Speleol 41:267–272. https://doi.org/10.5038/1827-806X.41.2.12
doi: 10.5038/1827-806X.41.2.12
Lefèvre M (1974) La “maladie verte” de Lascaux. Stud Conserv 19:126–156. https://doi.org/10.2307/1505660
doi: 10.2307/1505660
Lombard L, van der Merwe NA, Groenewald JZ et al (2015) Generic concepts in Nectriaceae. Stud Mycol 80:189–245. https://doi.org/10.1016/j.simyco.2014.12.002
doi: 10.1016/j.simyco.2014.12.002
pubmed: 26955195
pmcid: 4779799
Macedo MF, Miller AZ, Dionísio A et al (2009) Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: an overview. Microbiol 155:3476–3490. https://doi.org/10.1099/mic.0.032508-0
doi: 10.1099/mic.0.032508-0
Marco A, Santos S, Caetano J et al (2020) Basil essential oil as an alternative to commercial biocides against fungi associated with black stains in mural painting. Build Environ 167:106459. https://doi.org/10.1016/j.buildenv.2019.106459
doi: 10.1016/j.buildenv.2019.106459
Mulec J, Kosi G, Vrhovsek D (2008) Characterization of cave aerophytic algal communities and effects of irradiance levels on production of pigments. J Cave Karst Stud 70:3–12
Němcová Y, Eliáš M, Škaloud P et al (2011) Jenufa, gen. nov.: a new genus of coccoid green algae (Chlorophyceae, incertae sedis) previously recorded by environmental sequencing. J Phycol 47:928–938. https://doi.org/10.1111/j.1529-8817.2011.01009.x
doi: 10.1111/j.1529-8817.2011.01009.x
pubmed: 27020027
Neustupa J, Škaloud P (2010) Diversity of subaerial algae and cyanobacteria growing on bark and wood in the lowland tropical forests of Singapore. Plant Ecol Evol 143:51–62. https://doi.org/10.5091/plecevo.2010.417
doi: 10.5091/plecevo.2010.417
Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332. https://doi.org/10.1128/aem.63.8.3327-3332.1997
doi: 10.1128/aem.63.8.3327-3332.1997
pubmed: 9251225
pmcid: 168636
Nugari MP, Pietrini AM, Caneva G et al (2009) Biodeterioration of mural paintings in a rocky habitat: the Crypt of the Original Sin (Matera, Italy). Int Biodeter Biodegradation 63:705–711. https://doi.org/10.1016/j.ibiod.2009.03.013
doi: 10.1016/j.ibiod.2009.03.013
Ortega-Calvo JJ, Sánchez Castillo PM, Hernández-Mariné M et al (1993) Isolation and characterization of epilithic chlorophytes and cyanobacteria from two Spanish cathedrals (Salamanca and Toledo). Nova Hedwigia 57:239–253. https://doi.org/10.13039/501100000780
doi: 10.13039/501100000780
Pangallo D, Kraková L, Chovanová K et al (2013) Disclosing a crypt: Microbial diversity and degradation activity of the microflora isolated from funeral clothes of Cardinal Peter Pázmány. Microbiol Res 168:289–299. https://doi.org/10.1016/j.micres.2012.12.001
doi: 10.1016/j.micres.2012.12.001
pubmed: 23305771
Pereira de Oliveira B, Miller A, Sequeira Braga MA et al (2008) Characterization of dark films in granites The case study of Igreja da Ordem de São Francisco in Oporto (Portugal). In: Urzi (ed) Proceedings of the 14th International Biodeterioration and Biodegradation Symposium. International Biodeterioration and Biodegradation Society, Messina
Pereira de Oliveira B (2008) Caracterização de filmes negros em pedras graníticas. O caso de estudo da Igreja da Ordem de São Francisco do Porto. MSc Thesis, Universidade Nova de Lisboa.
Pfendler S, Karimi B, Maron PA et al (2018) Biofilm biodiversity in French and Swiss show caves using the metabarcoding approach: first data. Sci Tot Environ 615:1207–1217. https://doi.org/10.1016/j.scitotenv.2017.10.054
doi: 10.1016/j.scitotenv.2017.10.054
Pfendler S, Karimi B, Alaoui-Sosse L et al (2019) Assessment of fungi proliferation and diversity in cultural heritage: reactions to UV-C treatment. Sci Total Environ 647:905–913. https://doi.org/10.1016/j.scitotenv.2018.08.089
doi: 10.1016/j.scitotenv.2018.08.089
pubmed: 30096678
Piano E, Bona F, Falasco E et al (2015) Environmental drivers of phototrophic biofilms in an Alpine show cave (SW-Italian Alps). Sci Total Environ 536:1007–1018. https://doi.org/10.1016/j.scitotenv.2015.05.089
doi: 10.1016/j.scitotenv.2015.05.089
pubmed: 26112916
Ponizovskaya VB, Rebrikova NL, Kachalkin AV et al (2019) Micromycetes as colonizers of mineral building materials in historic monuments and museums. Fungal Biol 123:290–306. https://doi.org/10.1016/j.funbio.2019.01.002
doi: 10.1016/j.funbio.2019.01.002
pubmed: 30928038
Procházková K, Němcová Y, Neustupa J (2015) A new species Jenufa aeroterrestrica (Chlorophyceae incertae sedis, Viridiplantae), described from Europe. Preslia 87:403–416. https://doi.org/10.1111/j.1529-8817.2011.01009.x
doi: 10.1111/j.1529-8817.2011.01009.x
Rehner SA, Minnis AM, Sung G-H et al (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302
doi: 10.3852/10-302
pubmed: 21482632
Reynolds CS (1997) Vegetation processes in the pelagic: a model for ecosystem theory. Excellence in ecology, 9. Ecology Institute, Oldendorf. https://doi.org/10.1017/S0025315400036432
doi: 10.1017/S0025315400036432
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile opensource tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
doi: 10.7717/peerj.2584
pubmed: 27781170
pmcid: 5075697
Roldán M, Hernández-Mariné M (2009) Exploring the secrets of the three—dimensional architecture of phototrophic biofilms in caves. Int J Speleol 38:41–53. https://doi.org/10.5038/1827-806X.38.1.5
doi: 10.5038/1827-806X.38.1.5
Roldán M, Clavero E, Canals TA et al (2004) Distribution of phototrophic biofilms in cavities (Garraf, Spain). Nova Hedwigia 78:329–351. https://doi.org/10.1127/0029-5035/2004/0078-0329
doi: 10.1127/0029-5035/2004/0078-0329
Del Rosal PY, Jurado Lobo V, Hernández-Mariné M et al (2016) Biofilms en cuevas turísticas: La Cueva de Nerja y la Cueva del Tesoro. In: Andreo B, Durán JJ (eds) El Karst y el Hombre: Las Cuevas como Patrimonio Mundial. Asociación de Cuevas Turísticas Españolas, Madrid, pp 103–114
Saiz-Jimenez C (2010) Painted material. In: Mitchell R, McNamara CJ (eds) Cultural heritage microbiology: fundamental studies in conservation science. ASM Press, Washington DC, pp 3–13
Sankar SS, Rani PR (2019) Pathogenicity and field efficacy of the entomopathogenic fungus, Lecanicillium saksenae Kushwaha, Kurihara and Sukarno in the management of rice bug, Leptocorisa acuta Thunberg. J Biol Control 32:230–238. https://doi.org/10.18311/jbc/2018/19808
doi: 10.18311/jbc/2018/19808
Santos MFA (2003) Optical microscopy of the microbial samples collected on the cloisters of church of Santa Cruz in Coimbra (Portugal). Universidade de Coimbra, Coimbra
Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—An updated overview. Adv Appl Microbiol 66:97–139. https://doi.org/10.1016/S0065-2164(08)00805-8
doi: 10.1016/S0065-2164(08)00805-8
pubmed: 19203650
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
doi: 10.1128/AEM.01541-09
pubmed: 19801464
pmcid: 2786419
Selbmann L, Zucconi L, Isola D et al (2015) Rock black fungi: excellence in the extremes, from the Antarctic to space. Curr Genet 61:335–345. https://doi.org/10.1007/s00294-014-0457-7
doi: 10.1007/s00294-014-0457-7
pubmed: 25381156
Sherwood AR, Presting GG (2007) Universal primers amplify a 23S rDNA plastid marker in eukaryotic algae and cyanobacteria. J Phycol 43:605–608. https://doi.org/10.1111/j.1529-8817.2007.00341.x
doi: 10.1111/j.1529-8817.2007.00341.x
Soares F, Portugal A, Trovão J et al (2019) Structural diversity of photoautotrophic populations within the UNESCO site ‘old Cathedral of Coimbra’ (Portugal), using a combined approach. Int Biodeterior Biodegradation 140:9–20. https://doi.org/10.1016/j.ibiod.2019.03.009
doi: 10.1016/j.ibiod.2019.03.009
Song H, Li S, Liu X et al (2017) Jenufa lobulosa sp. nov. (Chlorophyceae, Chlorophyta), a new epilithic, terrestrial species described from China. Phycologia 57:52–60. https://doi.org/10.2216/17-20.1
doi: 10.2216/17-20.1
Song H, Zhang Q, Liu G et al (2015) Polulichloris henanensis gen. et sp. nov (Trebouxiophyceae, Chlorophyta), a novel subaerial coccoid green alga. Phytotaxa. 218:137–146. https://doi.org/10.11646/phytotaxa.218.2.3
doi: 10.11646/phytotaxa.218.2.3
Sterflinger K, Piñar G (2013) Microbial deterioration of cultural heritage and works of art—tilting at windmills? Appl Microbiol Biotechnol 97:9637–9646. https://doi.org/10.1007/s00253-013-5283-1
doi: 10.1007/s00253-013-5283-1
pubmed: 24100684
pmcid: 3825568
Sugiyama J, Kiyuna T, Nishijima M et al (2017) Polyphasic insights into the microbiomes of the Takamatsuzuka Tumulus and Kitora Tumulus. J Gen Appl Microbiol 63:63–113. https://doi.org/10.2323/jgam.2017.01.007
doi: 10.2323/jgam.2017.01.007
pubmed: 28344193
Sun M, Zhang F, Huang X et al (2020) Analysis of microbial community in the Archaeological Ruins of Liangzhu City and study on protective materials. Front Microbiol 11:684. https://doi.org/10.3389/fmicb.2020.00684
doi: 10.3389/fmicb.2020.00684
pubmed: 32351492
pmcid: 7174599
Tanney JB, Seifert KA (2020) Mollisiaceae: an overlooked lineage of diverse endophytes. Stud Mycol 95:293–380. https://doi.org/10.1016/j.simyco.2020.02.005
doi: 10.1016/j.simyco.2020.02.005
pubmed: 32855742
pmcid: 7426276
Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688. https://doi.org/10.1126/science.1256688
doi: 10.1126/science.1256688
pubmed: 25430773
Tomaselli L, Lamenti G, Bosco M et al (2000) Biodiversity of photosynthetic microorganisms dwelling on stone monuments. Int Biodeterior Biodegradation 46:251–258. https://doi.org/10.1016/S0964-8305(00)00078-0
doi: 10.1016/S0964-8305(00)00078-0
Trovão J, Portugal A, Soares F et al (2019) Fungal diversity and distribution across distinct biodeterioration phenomena in limestone walls of the old cathedral of Coimbra, UNESCO World Heritage Site. Int Biodeterior Biodegradation 142:91–102. https://doi.org/10.1016/j.ibiod.2019.05.008
doi: 10.1016/j.ibiod.2019.05.008
Vázquez-Martínez J, Gutierrez-Villagomez JM, Fonceca-García C et al (2018) Nodosilinea chupicuarensis sp. nov. (Leptolyngbyaceae, Synechococcales) a subaerial cyanobacterium isolated from a stone monument in central Mexico. Phytotaxa. 334:167–182. https://doi.org/10.11646/phytotaxa.334.2.6
doi: 10.11646/phytotaxa.334.2.6
Vázquez-Nion D, Rodríguez-Castro J, López-Rodríguez MC et al (2016) Subaerial biofilms on granitic historic buildings: microbial diversity and development of phototrophic multi-species cultures. Biofouling 32:657–669. https://doi.org/10.1080/08927014.2016.1183121
doi: 10.1080/08927014.2016.1183121
pubmed: 27192622
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
doi: 10.1128/jb.172.8.4238-4246.1990
pubmed: 2376561
pmcid: 213247
Wagner L, Stielow B, Hoffmann K et al (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia 30:77–93. https://doi.org/10.3767/003158513X666268
doi: 10.3767/003158513X666268
pubmed: 24027348
pmcid: 3734968
Wei D-P, Wanasinghe DN, Hyde KD et al (2019) The genus simplicillium. Mycokeys 60:69–92. https://doi.org/10.3897/mycokeys.60.38040
doi: 10.3897/mycokeys.60.38040
pubmed: 31798310
pmcid: 6879665
White T, Bruns T, Lee S et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand D, Shinsky J, White T (eds) Innis M. A Guide to Methods and Aplications. Academic Press Cambridge, PCR Protocols, pp 315–322
Woudenberg JHC, Sandoval-Denis M, Houbraken J et al (2017) Cephalotrichum and related synnematous fungi with notes on species from the built environment. Stud Mycol 88:137–159. https://doi.org/10.1016/j.simyco.2017.09.001
doi: 10.1016/j.simyco.2017.09.001
pubmed: 29158610
pmcid: 5679026
Zammit G (2019) Phototrophic biofilm communities and adaptation to growth on ancient archaeological surfaces. Ann Microbiol 69:1047–1058. https://doi.org/10.1007/s13213-019-01471-w
doi: 10.1007/s13213-019-01471-w