Disturbance frequency directs microbial community succession in marine biofilms exposed to shear

Abstract

ABSTRACT Marine biofilm growth poses significant challenges across marine industries (“biofouling”). Understanding the microbial communities involved in biofouling processes is crucial for developing effective mitigation strategies. These communities experience strong disturbances under antifouling pressure, the implications of which must be considered when developing new technologies due to their potential to alter succession, invertebrate settlement, and invasive species establishment risk. We leveraged the development of a shear-based antifouling technique to examine marine biofilm community assembly and stability under disturbance. The influence of repeated underwater shear on microbial community succession and biofilm matrix stability was assessed over 37 days on uncoated and “foul release” paint-coated surfaces. Foul-release coating decreased matrix biomass, and uncoated and coated surfaces hosted different biofilm communities with converging bacterial compositions and diverging eukaryotic compositions over time. On both surfaces, highly frequent shear strongly shifted the community composition and enriched several shear-tolerant bacteria, diatoms, green algae, and ciliates. Infrequent shear decreased matrix biomass, resulted in weaker compositional shifts and fewer enriched taxa, and additionally prevented macrofouling growth when combined with foul-release coating. A cross-domain co-occurrence network revealed mostly positive correlations persisting through the disturbance continuum and identified the diatom Melosira as a highly connected genus. Infrequent shear on anti-biofouling paint-coated surfaces was the most effective biofilm removal strategy, demonstrating that longer recovery periods enabled continued biomass removal and fewer shear-tolerant taxa. The results support the idea that variability in the frequency of a stress disturbance can significantly alter microbial community succession and biomass stability in marine biofilms, resulting in a varied potential for species invasiveness. IMPORTANCE Disturbances are major drivers of community succession in many microbial systems; however, relatively little is known about marine biofilm community succession, especially under antifouling disturbance. Antifouling technologies exert strong local disturbances on marine biofilms, and resulting biomass losses can be accompanied by shifts in biofilm community composition and succession. We address this gap in knowledge by bridging microbial ecology with antifouling technology development. We show that disturbance by shear can strongly alter marine biofilm community succession, acting as a selective filter influenced by frequency of exposure. Examining marine biofilm succession patterns with and without shear revealed stable associations between key prokaryotic and eukaryotic taxa, highlighting the importance of cross-domain assessment in future marine biofilm research. Describing how compounded top-down and bottom-up disturbances shape the succession of marine biofilms is valuable for understanding the assembly and stability of these complex microbial communities and predicting species invasiveness.