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Final Report Summary - ESENCYA (Environmental sensory perception in cyanobacterial biofilms: understanding biodeterioration of outdoor stone materials in a changing environment)

Many of the world’s most precious artworks are made of stone. Their irreversible deterioration due to biological attack is a worldwide concern. Microorganisms colonize outdoor lithic surfaces and develop into biofilms at the solid/air interface (subaerial biofilms, SABs), sometimes causing aesthetic, chemical and physical decay. The fragile character of the stone heritage material is further exacerbated by the unpredictable nature of impacts from environmental changes, posing challenges for conservation management.
Although it has been estimated that at least 99% of the world's microbial biomass exists in biofilms, the role and behavior of microorganisms within the biofilm matrix and their complex interactions with the external environment is still unknown.
The ESENCYA project provides a pioneering and multidisciplinary research to investigate the behavior of microorganisms within the biofilm matrix for sorting out time-spatial relationships and to elucidate microorganism-EPS, inter-organism, biofilm-atmosphere and biofilm-stone interactions. In addition, this work offers a system-level understanding of community organization and function of SABs.
ESENCYA spans sophisticated molecular, chemical, physical and data modeling techniques and it is approached from two complementary angles: 1) Lab-scale studies to delineate specific transcriptional responses of mono- and multi-species biofilms as well as the biofilm-stone interactions under controlled environmental conditions; 2) Real heritage case studies to investigate the shifts in the microbial community structure and function under different environmental conditions. Through comparing phylogenetic and functional diversity under different environmental scenarios, we provide evidence that any information gathered through the lab-scale experiments is relevant to true environmental biofilms.

A first accomplishment of this work was the development of a methodology to obtain a laboratory model of a dual-species SAB that is relevant to cultural heritage studies. The results demonstrated the ability to grow consortial SAB on stone. The results obtained underscore the ability of the dual-species SAB model to capture functional traits characteristic of biofilms inhabiting lithic substrata such as cooperation between phototrophs and heterotrophs, cross feeding processes, the ability to change the chemical parameters that characterize the microhabitats, and biocide tolerance. In addition, the microscopic investigation and microsensor measurements indicated that the dual-species biofilm sequestered more calcium from the stone than the mono-species cyanobacterial biofilm, and it was able to re-precipitate the sequestered calcium as a calcium calcite crust.
To the best of our knowledge, this is the first time that a phototroph-heterotroph association at the stone/air interface has been successfully obtained at laboratory scale starting from two introduced, controlled species and not from an environmental microbial consortium.
The present lab-scale system of SABs has the potential to significantly advance our mechanistic understanding of the biofilm-stone-air interplay that has proven difficult to study in field experiments due to the inaccessibility of samples and the complexity of the ecosystem under investigation.
With its advantages in control, replication, range of different experimental scenarios and matches with the real ecosystem, the developed dual-species SAB model system is crucial to addressing ecological and biogeochemical questions, as well as developing tools to predict and model biodeterioration/bioprotection processes on lithic surfaces.

Global climate change is predicted to alter precipitation and drought patterns, resulting in more extreme conditions, especially for Mediterranean ecosystems. The intensification of extreme droughts from climate change raises concerns about how SABs respond to such events and their impact to the stone substrata. In the light of the previous consideration, the feedback responses of SABs to desiccation were investigated.
Sophisticated imaging techniques showed i) the fast recovery of desiccated SABs followed by exposure to atmospheric moisture in form of humid air and ii) different behavior of the lithic substrate in presence of the biofilm whenever the temperature changes.
The results obtained clarified the relationship among SABs, stone porosity, evaporation flux, water absorption by capillarity and diffusion phenomena.
Omics-based investigations have been carried out to delineate specific responses of SABs to drying and wetting events, and elucidate the ability of the biofilm to perceive an environmental signal and its adaptive capacity.

Real case studies located in the North East of USA (Jefferson Memorial, Washington DC and Federal Hall, NY city) and in Italy (Monza Cathedral, a masterpiece of the northern Italian architectural heritage dated at the beginning of the 14th century) were also included in the investigations. These sites were chosen because (i) they are situated in a stable environment with well-defined and well-characterized physical/chemical gradients and forces, (ii) the external physical and chemical environments are relatively simple and measurable (consisting essentially of characterizable inflows from rainfall and air together with a sunlight energy source), (iii) the biofilms are pristine and ecologically isolated due to starkness of the stone substratum and to their protected location within areas closed to the general public, (iv) the two US sites differ in exposure – Federal Hall is relatively protected in an artificial canyon formed by the Wall Street corridor whereas Jefferson Memorial is relatively exposed in the open DC tidal basin, v) the Monza Cathedral offered different litotypes (namely Candoglia marble, Musso marble, Crevola marble and Oira stone) under the same environmental conditions.
The functional diversity, composition, structure, metabolic potential/activity and dynamic of the biofilm community inhabiting stone surfaces exposed to the external environment has been monitored by using whole shot-gun metagenomic. Results demonstrated that functional differences, even in only few critical pathways, could reflect dramatically altered ecosystem service. In addition, the rate of microbial colonization of the different litotypes was linked to the chemical composition of the stone for the same environmental conditions. The predicted and real functional profiles of SABs was compared and correlated to the environmental scenarios and to the damage diagnoses at stone monuments.

Finally, modeling works were developed to incorporate data on microbial community ecology and function into computational biofilm models that predict biofilm-induced chemistry and its effect on stone substrata under different environmental conditions.
For instance, a rate-based model of a phototroph-heterotroph microbial consortium was developed. The model combines flux-based kinetics at the small scale to concentration-based physics (diffusive transport in particular) at the large scale, and it sees three pathways: photosynthesis, photorespiration and the heterotrophic anabolisms. In addition, the interesting data obtained so far have been used to develop a new mathematical model to portray the mechanisms that drive the mobilization and re-precipitation of calcium within the physical and chemical microenvironment of a dual-species biofilm growing at the stone/air interface.

The findings obtained so far will contribute to a better understanding of the complexity of all the interactions encountered within SAB communities, and how these interactions may influence the biofilm outcome and behavior and the biodeterioration/bioprotection of the stone materials under different environmental conditions.

Contacts:
Prof. Francesca Cappitelli, francesca.cappitelli@unimi.it
Dr Federica Villa, federica.villa@unimi.it
www.esencya.unimi.it

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Margherita Pasetti, (principal administrative officer of the Department)
Tel.: +39 02 503 19194
Fax: +39 02 503 19228
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Subjects

Life Sciences
Record Number: 192414 / Last updated on: 2016-12-08
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