Biofilm lifestyle as a common trait of ammonia-oxidizing archaea

Although widespread in nature, growth in biofilms has been relatively little explored in the globally distributed ammonia oxidizing archaea (AOA). Here we investigated six representatives of three different terrestrial and marine clades of AOA in a longitudinal and quantitative study for their ability to form biofilm and studied gene expression patterns of three representatives. While all strains grew on a solid surface, soil strains exhibited the highest capacity for biofilm formation. Based on microscopic and gene expression data, two different colonization strategies could be distinguished. S-layer containing AOA (from both soil and marine habitats) initialized attachment as single cells and subsequently formed denser layers and three-dimensional structures, while the S-layer free species of the Nitrosocosmicus clade attached as suspended aggregates to the surface and henceforth showed fastest establishment of biofilm. Transcription profiles were significantly different between planktonic and biofilm growth in all strains and revealed individual reactions, often fulfilling shared functions. In particular the strong expression of different types of multicopper oxidases was observed in all strains indicating modifications of their cell coats. S-layer carrying AOA each additionally expressed a set of adhesion proteins supporting attachment. Detoxification of nitrous compounds, copper acquisition as well as the expression of transcription factor B were also shared reactions among biofilm producing strains. However, the majority of differentially expressed protein families was distinct among the three strains illustrating that individual solutions have evolved for the shared growth mode of biofilm formation in AOA, probably driven by the different ecological niches.