Phototrophic biofilm communities and adaptation to growth on ancient archaeological surfaces

Abstract

Hypogea can be considered under-examined environments as regards microbial biodiversity. New understanding has been gained about the predominant phototrophic microorganisms forming biofilms colonising archaeological surfaces in hypogea. In fact, the description of new taxa has remained elusive until recently, as many biofilm-forming phototrophs possess a cryptic morphology with a lack of specialised cells. A multiphasic study, including cytomorphological and ecological descriptions, genetic and biochemical analysis was carried out on the biofilms colonising hypogean environments around the Maltese islands. Molecular studies were imperative because biodiversity was found to be more complex than that indicated by classical taxonomy. The dominant microbial life-form on archaeological surfaces is a compact subaerial biofilm. This study has led to new strains of the eukaryotic microalgal genus Jenufa, and the prokaryotic cyanobacteria Oculatella, Albertania and Nodosilinea being identified as the principal phototrophic biofilm-formers colonising the ancient decorated surfaces of Maltese hypogea. Complex morphologies and elaborate life cycles were eliminated as biodiversity was dictated only by the local contemporary microenvironment. The production of thick multilayered sheaths aided adherence to the substrate, concentrating microbial cells in biofilm formation. Albertania skiophila trichomes were able to glide inside the extracellular matrix. Oculatella subterranea exhibited phototaxis associated with a photosensitive apical cell containing a rhodopsin-like pigment. The biofilm provided a protective barrier and an improved chance of survival for cells growing in a low-nutrient, low-light environment. Effective strategies to prevent and control the growth of biofilms on the archaeological surface should take into consideration the adaptation of microorganisms to this particular mode of life.