journal article·2025-11-06Open access

A Metagenomic and Colorimetric Analysis of the Biological Recolonization Occurring at the “Largo da Porta Férrea” Statues (Coimbra UNESCO World Heritage Site), After Cleaning Interventions

Fabiana Soares, Lídia Catarino, Conceição Egas, João Trovão

Applied Sciences· Volume 15· Issue 21

Abstract

Biological recolonization after cleaning remains a major challenge for the conservation of stone cultural heritage. As recolonization can start within months to a few years following intervention, developing rapid, field-deployable diagnostic approaches is crucial to better monitor microbial reappearance and to assess treatment performance in real time. Traditional evaluation methods lack the capacity to take into consideration non-cultivable microorganisms or assess functional traits relevant to recolonization. To bypass this gap, we applied on-site direct Whole-Genome Sequencing (Oxford Nanopore® MinION™ sequencer) coupled with colorimetric analysis to understand the microbiome, resistome, and metabolic traits of subaerial biofilms present in untreated and treated (recolonized) areas of stone statues at the “Largo da Porta Férrea” (Coimbra’s UNESCO World Heritage site). Colorimetric analysis (ΔE of 32–40 in recolonized vs. 19–43 in untreated areas) and genomic data pointed out that the applied treatment provided only a short-term effect (roughly 4–5 years), with a marked decline in fungi (1–2% vs. 7–18%), coupled with an increased recolonization mainly by Cyanobacteriota (circa 35–45%) and several stress-resistant Bacteria (globally ~95% of reads vs. 73–79% in controls). Antimicrobial resistance profiles significantly differed between sites, with treated areas showing distinct and unique resistance genes, and plasmids containing the blaTEM-116 gene, which can indicate potential adaptive shifts in the resistomes profiles after intervention. Metabolic pathways analysis revealed that untreated areas retained more complete nitrogen and sulfur cycling gene sets, whereas treated areas showed reduced biogeochemical gene contents, consistent with earlier-stage recolonization steps. Given the current recolonization detection and the ongoing biofilm formation, routine monitoring efforts (e.g., every 6 months) are recommended. Overall, this study demonstrates the first on-site genomic characterization of recolonization events on heritage stone, providing a practical prompt-warning tool for conservation monitoring and future biofilm management strategies.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Building materials and conservation · Microbial Applications in Construction Materials · Forensic Entomology and Diptera Studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Centre for Functional Ecology (CFE)—Science for People & the Planet, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal

Geosciences Center, Department of Earth Sciences, University of Coimbra, Rua Sílvio Lima—Pólo II, 3030-790 Coimbra, Portugal

CNC-UC—Center for Neuroscience and Cell Biology, University of Coimbra, Rua Larga Edificio FMUC, Piso 1, 3004-504 Coimbra, Portugal

CIBB—Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Rua Larga Edificio FMUC, Piso 1, 3004-504 Coimbra, Portugal

Genoinseq—Next Generation Sequencing Unit, Biocant, Biocant Park, Núcleo 04, Lote 8, 3060-197 Cantanhede, Portugal

Funding

Santander/University of Coimbra in the framework of the SeedProjects@UC 2024 (Strategic Area Heritage, Culture and Inclusive Society) project

References (67)

Show source-provided references
2. Chapter 5 Microbial Deterioration of Stone Monuments—An Updated Overview10.1016/S0065-2164(08)00805-8 ↗
3. Microbially induced deterioration of architectural heritages: Routes and mechanisms involved10.1186/2190-4715-24-36 ↗
4. Villa, F., and Cappitelli, F. (2019). The Ecology of Subaerial Biofilms in Dry and Inhospitable Terrestrial Environments. Microorganisms, 7.10.3390/microorganisms7100380 ↗
5. Microbial deterioration and sustainable conservation of stone monuments and buildings10.1038/s41893-020-00602-5 ↗
6. Pinna, D. (2017). Coping with Biological Growth on Stone Heritage Objects: Methods, Products, Applications, and Perspectives, Apple Academic Press.10.1201/9781315365510 ↗
7. Cappitelli, F., Cattò, C., and Villa, F. (2020). The Control of Cultural Heritage Microbial Deterioration. Microorganisms, 8.10.3390/microorganisms8101542 ↗
8. Zezza, G.A. (2002). Resistance to Biodeterioration of Some Products Used for Rising Damp Barrier. Protection and Conservation of the Cultural Heritage of the Mediterranean Cities, Swets & Zeitlinger.
9. Caneva, G., Nugari, M.P., and Salvadori, O. (2008). Plant Biology for Cultural Heritage: Biodeterioration and Conservation, The Getty Conservation Institute. 5N81-606-CB10.
10. Caneva, G., Nugari, M.P., and Salvadori, O. (2008). Prevention of Biodeterioration. Outdoor Environments. Plant Biology for Cultural Heritage: Biodeterioration and Conservation, The Getty Conservation Institute.
11. Deteriorating effects of lichen and microbial colonization of carbonate building rocks in the Romanesque churches of Segovia, Spain10.1016/j.scitotenv.2008.09.042 ↗
12. Doehne, E., and Price, C.A. (2010). Stone Conservation: An Overview of Current Research, The Getty Conservation Institute. [2nd ed.].
13. Pinna, D. (2022). Can we do without biocides to cope with biofilms and lichens on stone heritage?. Int. Biodeter. Biodegrad., 172.10.1016/j.ibiod.2022.105437 ↗
14. Natural biocides for the conservation of stone cultural heritage: A review10.1016/j.culher.2019.01.005 ↗
15. Greener solutions for biodeterioration of organic-media cultural heritage: Where are we?10.1186/s40494-024-01442-8 ↗
16. Microbial recolonization of artificial and natural stone artworks after cleaning and coating treatments10.1016/j.culher.2023.04.006 ↗
17. Current knowledge regarding biological recolonization of stone cultural heritage after cleaning treatments10.1016/j.jobe.2024.109091 ↗
18. The use of -omics tools for assessing biodeterioration of cultural heritage: A review10.1016/j.culher.2020.03.006 ↗
19. Joseph, E. (2021). Molecular-Based Techniques for the Study of Microbial Communities in Artworks. Microorganisms in the Deterioration and Preservation of Cultural Heritage, Springer International Publishing.
20. Natural sciences at the service of art and cultural heritage: An interdisciplinary area in development and important challenges10.1111/1751-7915.13766 ↗
21. Pavlović, J., Cavalieri, D., Mastromei, G., Pangallo, D., Perito, B., and Marvasi, M. (2021). MinION technology for microbiome sequencing applications for the conservation of cultural heritage. Microbiol. Res., 247.10.1016/j.micres.2021.126727 ↗
22. Jroundi, F., Elert, K., Ruiz-Agudo, E., Gonzalez-Muñoz, M.T., and Rodriguez-Navarro, C. (2020). Bacterial Diversity Evolution in Maya Plaster and Stone Following a Bio-Conservation Treatment. Front. Microbiol., 11.10.3389/fmicb.2020.599144 ↗
23. Degradation of ancient Maya carved tuff stone at Copan and its bacterial bioconservation10.1038/s41529-021-00191-4 ↗
24. Innovative approaches to accurately assess the effectiveness of biocide-based treatments to fight biodeterioration of Cultural Heritage monuments10.1016/j.scitotenv.2023.165318 ↗
25. Dominance by cyanobacteria in the newly formed biofilms on stone monuments under a protective shade at the Beishiku Temple in China10.1016/j.envres.2024.118576 ↗
26. Kratter, M., Beccaccioli, M., Vassallo, Y., Benedetti, F., La Penna, G., Proietti, A., Zanellato, G., Faino, L., Cirigliano, A., and Neisje De Kruif, F. (2024). Long-term monitoring of the hypogeal Etruscan Tomba degli Scudi, Tarquinia, Italy. Early detection of black spots, investigation of fungal community and evaluation of their biodeterioration potential. J. Appl. Microbiol., 135.10.1093/jambio/lxae258 ↗
27. Méndez, A., Maisto, F., Pavlović, J., Rusková, M., Pangallo, D., and Sanmartín, P. (2024). Microbiome shifts elicited by ornamental lighting of granite facades identified by MinION sequencing. J. Photochem. Photobiol. B Biol., 261.10.1016/j.jphotobiol.2024.113065 ↗
28. Tichy, J., Sipek, B., Ortbauer, M., Fürnwein, L., Waldherr, M., Graf, A., Sterflinger, K., and Piñar, G. (2025). Microbial community shifts during salt mitigation treatments of historic buildings using mineral poultices: A long-term monitoring of salt and associated biofilms. Front. Microbiol., 16.10.3389/fmicb.2025.1603289 ↗
29. Microbiome and Response to Cleaning and Biocidal Treatments on Granite Historical Buildings Using MinION Sequencing10.1016/j.conbuildmat.2025.142589 ↗
30. Trovão, J., and Soares, F. (2024). Future Perspectives on the Application of the Oxford Nanopore® MinIONTM Sequencer in Cultural Heritage Biodeterioration Studies. Preprints, 2024061478.10.20944/preprints202406.1478.v2 ↗
31. Soares, F., Catarino, L., Egas, C., and Trovão, J. (2025). On-site Oxford Nanopore® MinION™ whole genome sequencing analysis to understand the microbiome, resistome and metabolic features of subaerial biofilms on stone monuments. Total Environ. Microbiol., 1.10.1016/j.temicr.2025.100011 ↗
32. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2020 update10.1093/nar/gkaa434 ↗
33. NanoPack: Visualizing and processing long-read sequencing data10.1093/bioinformatics/bty149 ↗
34. Fan, J., Huang, S., and Chorlton, S.D. (2021). BugSeq: A highly accurate cloud platform for long-read metagenomic analyses. BMC Bioinform., 22.10.1186/s12859-021-04089-5 ↗
35. Chandrakumar, I., Gauthier, N.P.G., Nelson, C., Bonsall, M.B., Locher, K., Charles, M., MacDonald, C., Krajden, M., Manges, A.R., and Chorlton, S.D. (2022). BugSplit enables genome-resolved metagenomics through highly accurate taxonomic binning of metagenomic assemblies. Commun. Biol., 5.10.1038/s42003-022-03114-4 ↗
36. Pavian: Interactive analysis of metagenomics data for microbiome studies and pathogen identification10.1093/bioinformatics/btz715 ↗
37. Dabdoub, S. (2025, November 03). kraken-Biom. GitHub Repository 2016, GitHub. Available online: https://github.com/smdabdoub/kraken-biom.
38. Easy16S: A user-friendly Shiny web-service for exploration and visualization of microbiome data10.21105/joss.06704 ↗
39. Rifa, É., and Theil, S. (2022, January 8–10). ExploreMetabar: A user-friendly Shiny application to explore the drivers of microbial communities. Proceedings of the Club des bactéries lactiques (CBL 2022), Nantes, France.
40. QUAST: Quality assessment tool for genome assemblies10.1093/bioinformatics/btt086 ↗
41. Prokka: Rapid prokaryotic genome annotation10.1093/bioinformatics/btu153 ↗
42. eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale10.1093/molbev/msab293 ↗
43. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences10.1016/j.jmb.2015.11.006 ↗
44. MEGARes and AMR++, v3.0: An updated comprehensive database of antimicrobial resistance determinants and an improved software pipeline for classification using high-throughput sequencing10.1093/nar/gkac1047 ↗
45. Deciphering environmental resistome and mobilome risks on the stone monument: A reservoir of antimicrobial resistance genes10.1016/j.scitotenv.2022.156443 ↗
46. Ondov, B.D., Bergman, N.H., and Phillippy, A.M. (2011). Interactive metagenomic visualization in a Web browser. BMC Bioinform., 12.10.1186/1471-2105-12-385 ↗
47. Tang, D., Chen, M., Huang, X., Zhang, G., Zeng, L., Zhang, G., Wu, S., and Wang, Y. (2023). SRplot: A free online platform for data visualization and graphing. PLoS ONE, 18.10.1371/journal.pone.0294236 ↗
48. Biofilm quantification on stone surfaces: Comparison of various methods10.1016/j.scitotenv.2004.05.003 ↗
49. Prieto, B., Vázquez-Nion, D., Fuentes, E., and Durán-Román, A.G. (2020). Response of subaerial biofilms growing on stone-built cultural heritage to changing water regime and CO2 conditions. Int. Biodeter. Biodegrad., 148.10.1016/j.ibiod.2019.104882 ↗
50. Spectrophotometric color measurement for early detection and monitoring of greening on granite buildings10.1080/08927014.2012.673220 ↗
51. Sanmartín, P., Rodríguez, A., and Aguiar, U. (2020). Medium-term field evaluation of several widely used cleaning-restoration techniques applied to algal biofilm formed on a granite-built historical monument. Int. Biodeter. Biodegrad., 147.10.1016/j.ibiod.2019.104870 ↗
52. Relationship between color and pigment production in two stone biofilm-forming cyanobacteria (Nostoc sp. PCC 9104 and Nostoc sp. PCC 9025)10.1080/08927011003774221 ↗
53. Recolonization of mortars by endolithic organisms on the walls of San Roque church in Campeche (Mexico): A case of tertiary bioreceptivity10.1016/j.conbuildmat.2013.11.114 ↗
54. Lichen colonization and associated deterioration processes in Pasargadae, UNESCO world heritage site, Iran10.1016/j.ibiod.2016.12.012 ↗
55. Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: An overview10.1099/mic.0.032508-0 ↗
56. Microbiologically induced aesthetic and structural changes to dimension stone10.1038/s41529-021-00180-7 ↗
57. Biodeterioration of stone: A review10.1016/S0964-8305(00)00109-8 ↗
58. Chemoorganotrophic bacteria isolated from biodeteriorated surfaces in cave and catacombs10.5038/1827-806X.41.2.1 ↗
59. Li, Q., Zhang, B., He, Z., and Yang, X. (2016). Distribution and Diversity of Bacteria and Fungi Colonization in Stone Monuments Analyzed by High-Throughput Sequencing. PLoS ONE, 11.10.1371/journal.pone.0163287 ↗
60. Bacterial diversity on rock surface of the ruined part of a French historic monument: The Chaalis abbey10.1016/j.ibiod.2017.02.019 ↗
61. Biocontamination and diversity of epilithic bacteria and fungi colonising outdoor stone and mortar sculptures10.1007/s00253-022-11957-4 ↗
62. Li, Q., Wu, C., He, J., and Zhang, B. (2023). Unraveling the microbiotas and key genetic contexts identified on stone heritage using illumina and nanopore sequencing platforms. Int. Biodeter. Biodegrad., 185.10.1016/j.ibiod.2023.105688 ↗
63. Metagenomic insight into the pathogenic-related characteristics and resistome profiles within microbiome residing on the Angkor sandstone monuments in Cambodia10.1016/j.scitotenv.2024.170402 ↗
64. Metagenomic and metaproteomic insights into the microbiome and the key geobiochemical potentials on the sandstone of rock-hewn Beishiku Temple in Northwest China10.1016/j.scitotenv.2023.164616 ↗
65. Bindschedler, S., Cailleau, G., and Verrecchia, E. (2016). Role of Fungi in the Biomineralization of Calcite. Minerals, 6.10.3390/min6020041 ↗
66. Microbiome Characteristics and the Key Biochemical Reactions Identified on Stone World Cultural Heritage under Different Climate Conditions10.1016/j.jenvman.2021.114041 ↗
67. Cyanobacteria and Biodeterioration of Cultural Heritage: A Review10.1007/s00248-003-1052-5 ↗