Diversity and activities of pioneer bacteria, algae, and fungi colonizing ceramic roof tiles during the first year of outdoor exposure

Abstract

Abstract Like other building materials, ceramic roof tiles are biodeteriorated over time. Natural conditions affect deterioration processes, but the development of a biofilm composed of many types of microorganisms also plays a critical role in biodeterioration. However, the pioneering stages of biofilm formation remain poorly studied, whereas they determine the development of the well-characterized mature biofilms. To further characterize this pioneering microbial diversity, the bacterial, algal, and fungal colonization of new tiles exposed to outdoor conditions over one full year was monitored, combining fluorimetry, biofilm imaging (SEM, confocal macroscopy), culture-based, and high-throughput sequencing approaches. For all the samples, pioneering biofilms were found to be extremely diverse but dominated by Actinobacteria (Pantoea sp. - up to 90% of the bacterial diversity -, and Pseudomonas sp. -up to 75%-), Chlorophyta (Trebouxiophyceae -100% of the algal diversity-), and Pleosporales (Alternaria sp. -up to 75% of the fungal diversity-). Interestingly, if biofilm development was highly heterogeneous between tiles and exposition sites, microbial colonization patterns succession remained comparable regardless of tile type and exposure site. Additionally, we investigated whether microbial isolates collected in this study harbor some physiological traits related to their pioneer character. This work revealed that pioneer organisms colonizing tiles harbored interesting features like the ability to produce biofilm matrix and anti-quorum sensing and antimicrobial compounds, highlighting the intense competition between the microbial players during the priming of the tile colonization. Altogether, our results emphasize the necessity to taxonomically and functionally characterize the key pioneering microorganisms involved in biofilm formation to design innovative antifouling solutions for ceramic roof tiles.