Variations in environmental conditions in the context of climate change are expected to affect biofilm-associated organisms on granite heritage buildings. The number and duration of drought periods should be considered, as these factors will affect the availability of water for the microorganisms. In this study, mature biofilms were exposed to various drying-rewetting cycles, and the effects of water stress on the SAB and their resilience were evaluated in terms of the variation in microbial composition, extracellular polymeric substance production, and photosynthetic efficiency. The structure of the biofilm changed after exposure to drought, becoming more heterogeneous and with an increase in the carbohydrate to protein ratio, especially after the second day of total drought. YMAX and YEF parameters proved to be the most informative, showing that the photosynthetic efficiency and recovery capacity were inversely related to the duration of the drought period. Furthermore, cyanobacteria resisted drought better than algae, giving rise to a decrease in the algae to cyanobacteria ratio.
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Leissner J, Kilian R, Kotova L, Jacob D, Mikolajewicz U, Broström T, Ashley-Smith J, Schellen HL, Martens M, van Schijndel J, Antretter F, Winkler M, Bertolin C, Camuffo D, Simeunovic G, Vyhlídal T (2015) Climate for culture: assessing the impact of climate change on the future indoor climate in historic buildings using simulations. Herit Sci 3:1–15. https://doi.org/10.1186/s40494-015-0067-9
UNESCO (2007) Case studies of climate change and world heritage
Joh G, Lee J (2012) Cyanobacterial biofilms on sedimentation basins in a water treatment plant in South Korea. J. Appl. Phycol. 24:285–293. https://doi.org/10.1007/s10811-011-9678-z
Witt V, Wild C, Uthicke S (2012) Interactive climate change and runoff effects alter O2 fluxes and bacterial community composition of coastal biofilms from the Great Barrier Reef. Aquat. Microb. Ecol. 66:117–131. https://doi.org/10.3354/ame01562
Gorbushina AA (2007) Life on the rocks. Environ. Microbiol. 9:1613–1631. https://doi.org/10.1111/j.1462-2920.2007.01301.x
Viles HA, Cutler NA (2012) Global environmental change and the biology of heritage structures. Glob. Chang. Biol. 18:2406–2418. https://doi.org/10.1111/j.1365-2486.2012.02713.x
Sabbioni C, Cassar M, Brimblecombe P, Lefevre RA (2009) Vulnerability of cultural heritage to climate change. Pollut Atmos 157–169
Gómez-Bolea A, Llop E, Ariño X, Saiz-Jimenez C, Bonazza A, Messina P, Sabbioni C (2012) Mapping the impact of climate change on biomass accumulation on stone. J. Cult. Herit. 13:254–258. https://doi.org/10.1016/j.culher.2011.10.003
Gladis F, Schumann R (2011) Influence of material properties and photocatalysis on phototrophic growth in multi-year roof weathering. Int. Biodeterior. Biodegrad. 65:36–44. https://doi.org/10.1016/j.ibiod.2010.05.014
Gladis-Schmacka F, Glatzel S, Karsten U, Böttcher H, Schumann R (2014) Influence of local climate and climate change on aeroterrestrial phototrophic biofilms. Biofouling 30:401–414. https://doi.org/10.1080/08927014.2013.878334
Quagliarini E, Gianangeli A, D’Orazio M et al (2019) Effect of temperature and relative humidity on algae biofouling on different fired brick surfaces. Constr. Build. Mater. 199:396–405. https://doi.org/10.1016/j.conbuildmat.2018.12.023
Barthès A, Ten-Hage L, Lamy A et al (2015) Resilience of aggregated microbial communities subjected to drought—small-scale studies. Microb. Ecol. 70:9–20. https://doi.org/10.1007/s00248-014-0532-0
Prieto B, Vázquez-Nion D, Fuentes E, Durán-Román AG (2020) Response of subaerial biofilms growing on stone-built cultural heritage to changing water regime and CO2 conditions. Int. Biodeterior. Biodegrad. 148:104882. https://doi.org/10.1016/j.ibiod.2019.104882
Ortega-Calvo JJ, Hernandez-Marine M, Saiz-Jimenez C (1992) Experimental strategies for investigating algal deterioration of stone. In: Proceedings of the 7th International Congress on Deterioration and Conservation of Stone: held in Lisbon, Portugal, 15-18 June 1992
Ortega-Morales BO, Narváez-Zapata JA, Schmalenberger A, Sosa-López A, Tebbe CC (2004) Biofilms fouling ancient limestone Mayan monuments in Uxmal, Mexico: a cultivation-independent analysis. Biofilms 1:79–90. https://doi.org/10.1017/s1479050504001188
Ramirez M, Hernandez-Marine M, Novelo E, Roldan M (2010) Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling. https://doi.org/10.1080/08927011003660404, 26, 399, 409
Cutler NA, Viles HA, Ahmad S, McCabe S, Smith BJ (2013) Algal “greening” and the conservation of stone heritage structures. Sci. Total Environ. 442:152–164. https://doi.org/10.1016/j.scitotenv.2012.10.050
Häubner N, Schumann R, Karsten U (2006) Aeroterrestrial microalgae growing in biofilms on facades-response to temperature and water stress. Microb. Ecol. 51:285–293. https://doi.org/10.1007/s00248-006-9016-1
Karsten U, Holzinger A (2012) Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high Alpine soil crust. Microb. Ecol. 63:51–63. https://doi.org/10.1007/s00248-011-9924-6
Vázquez-Nion D, Rodríguez-Castro J, López-Rodríguez MC, Fernández-Silva I, Prieto B (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
Serrano-Notivoli R, de Luis M, Beguería S (2017) An R package for daily precipitation climate series reconstruction. Environ. Model. Softw. 89:190–195. https://doi.org/10.1016/j.envsoft.2016.11.005
Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica. 40:13–29. https://doi.org/10.1023/A:1020125719386
CIE (1978) Commission Internationale d’Eclairage. Recommendations on Uniform Colour Spaces, Colour Difference Equations, Psychometrice Colour Terms. J. Oral Rehabil
Timoner X, Acuña V, Von Schiller D, Sabater S (2012) Functional responses of stream biofilms to flow cessation, desiccation and rewetting. Freshw. Biol. 57:1565–1578. https://doi.org/10.1111/j.1365-2427.2012.02818.x
Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct. Plant Biol. 33:9–30. https://doi.org/10.1071/FP05095
Muñoz I, Abril M, Casas-Ruiz JP, Casellas M, Gómez-Gener L, Marcé R, Menéndez M, Obrador B, Sabater S, von Schiller D, Acuña V (2018) Does the severity of non-flow periods influence ecosystem structure and function of temporary streams? A mesocosm study. Freshw. Biol. 63:613–625. https://doi.org/10.1111/fwb.13098
Unger S, Máguas C, Pereira JS, David TS, Werner C (2010) The influence of precipitation pulses on soil respiration-assessing the “Birch effect” by stable carbon isotopes. Soil Biol. Biochem. 42:1800–1810. https://doi.org/10.1016/j.soilbio.2010.06.019
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. https://doi.org/10.1890/06-0219
Kim DG, Vargas R, Bond-Lamberty B, Turetsky MR (2012) Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research. Biogeosciences. 9:2459–2483. https://doi.org/10.5194/bg-9-2459-2012
Meisner A, Rousk J, Bååth E (2015) Prolonged drought changes the bacterial growth response to rewetting. Soil Biol. Biochem. 88:314–322. https://doi.org/10.1016/j.soilbio.2015.06.002
Romero F, Sabater S, Timoner X, Acuña V (2018) Multistressor effects on river biofilms under global change conditions. Sci. Total Environ. 627:1–10. https://doi.org/10.1016/j.scitotenv.2018.01.161
Suggett DJ, Borowitzka MA (2010) Chlorophyll a fluorescence in aquatic sciences: methods and applications, Developments in Applied Phycology. https://doi.org/10.1007/978-90-481-9268-7_333
Zlatev Z (2009) Drought-induced changes in chlorophyll fluorescence of young wheat plants. Biotechnol. Biotechnol. Equip. 23:438–441. https://doi.org/10.1080/13102818.2009.10818458
Singh H, Anurag K, Apte SK (2013) High radiation and desiccation tolerance of nitrogen-fixing cultures of the cyanobacterium Anabaena sp. strain PCC 7120 emanates from genome/proteome repair capabilities. Photosynth Res. https://doi.org/10.1007/s11120-013-9936-9
Rajeev L, Da Rocha UN, Klitgord N et al (2013) Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J 7:2178–2191. https://doi.org/10.1038/ismej.2013.83
Chang WS, Van De Mortel M, Nielsen L, et al (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. In: Journal of Bacteriology. https://doi.org/10.1128/JB.00727-07
Wingender J, Neu TR, Flemming H-C (1999) Microbial extracellular polymeric substances: characterization, structure, and function. https://doi.org/10.1007/978-3-642-60147-7_1
Flemming HC, Wingender J (2010) The biofilm matrix. Nat. Rev. Microbiol. 8:623–633. https://doi.org/10.1038/nrmicro2415
Prieto B, Rivas T, Silva B (2002) Rapid quantification of phototrophic microorganisms and their physiological state through their colour. Biofouling. 18:229–236. https://doi.org/10.1080/08927010290014908
Prieto B, Sanmartín P, Aira N, Silva B (2010) Color of cyanobacteria: some methodological aspects. Appl. Opt. 49:2022–2029. https://doi.org/10.1364/AO.49.002022
This study was financed through the Project CGL2016-79778-R from the Agencia Estatal de Investigación/Fondo Europeo de Desarrollo Regional, European Union (AEI/FEDER, UE). E. Fuentes is financially supported by a PhD Fellowship-Contract from Ministerio de Ciencia e Innovación (MICINN-FPI) (BES-2017-079927).
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• The deteriorating activity of the colonizing organisms of Cultural Heritage will be affected by environmental changes related to climate change.
• The effect of water restriction on biofilm performance depends on the duration of drought.
• In the tested laboratory conditions, biofilms did not show recovery capacity after 2 days of total drought.
• Biofilms developed on granite seems to have low resilience to reduction in water availability.
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Fuentes, E., Prieto, B. Recovery Capacity of Subaerial Biofilms Grown on Granite Buildings Subjected to Simulated Drought in a Climate Change Context. Microb Ecol 82, 761–769 (2021). https://doi.org/10.1007/s00248-021-01692-0
- Climate change
- Granite-built heritage
- Water availability
- Photosynthetic performance