Impacts of UV-C Irradiation on Marine Biofilm Community Succession.

Abstract

Marine biofilms are diverse microbial communities and important ecological habitats forming on surfaces submerged in the ocean. Biofilm communities resist environmental disturbance, making them a nuisance to some human activities ("biofouling"). Antifouling solutions rarely address the underlying stability or compositional responses of these biofilms. Using bulk measurements and molecular analyses, we examined temporal and UV-C antifouling-based shifts in marine biofilms in the coastal western North Atlantic Ocean during early fall. Over a 24-day period, bacterial communities shifted from early dominance of Gammaproteobacteria to increased proportions of Alphaproteobacteria, Bacteroidia, and Acidimicrobiia. In a network analysis based on temporal covariance, Rhodobacteraceae (Alphaproteobacteria) nodes were abundant and densely connected with generally positive correlations. In the eukaryotic community, persistent algal, protistan, and invertebrate groups were observed, although consistent temporal succession was not detected. Biofilm UV-C treatment at 13 and 20 days resulted in losses of chlorophyll a and transparent exopolymer particles, indicating biomass disruption. Bacterial community shifts suggested that UV-C treatment decreased the biofilm maturation rate and was associated with proportional shifts among diverse bacterial taxa. UV-C treatment was also associated with increased proportions of protists potentially involved in detritivory and parasitism. Older biofilm communities had increased resistance to UV-C, suggesting that early biofilms are more susceptible to UV-C-based antifouling. The results suggest that UV-C irradiation is potentially an effective antifouling method in marine environments in terms of biomass removal and in slowing maturation. However, as they mature, biofilm communities may accumulate microbial members that are tolerant or resilient under UV treatment. IMPORTANCE Marine biofilms regulate processes ranging from organic matter and pollutant turnover to eukaryotic settlement and growth. Biofilm growth and eukaryotic settlement interfering with human activities via growth on ship hulls, aquaculture operations, or other marine infrastructure are called "biofouling." There is a need to develop sustainable antifouling techniques by minimizing impacts to surrounding biota. We use the biofouling-antifouling framework to test hypotheses about marine biofilm succession and stability in response to disturbance, using a novel UV-C light-emitting diode (LED) device. We demonstrate strong bacterial biofilm successional patterns and detect taxa potentially contributing to stability under UV-C stress. Despite UV-C-associated biomass losses and varying UV susceptibility of microbial taxa, the overall bacterial community composition remained relatively stable, suggesting decoupling of disruption in biomass and community composition following UV-C irradiation. We also report microbial covariance patterns over 24 days of biofilm growth, pointing to areas for study of microbial interactions and targeted antifouling.