Bacterium–Phage Interactions Enhance Biofilm Resilience during Membrane Filtration Biofouling under Oxidative and Hydraulic Stresses

Microbial interactions on membrane
surfaces can facilitate biofilm
formation and biofouling, which poses a significant challenge for
pressure-driven membrane filtration systems. This multiomics study
investigates the adaptive responses of bacterium–phage interactions
under varying oxidative and hydraulic stress during membrane backwashing
and their biological contributions to biofouling. Oxidative and hydraulic
stress distinctly shaped bacteria and phage diversity and community
composition. Under moderate oxidative backwashing (300 ppm of NaClO),
diversity was maintained, with increased antioxidant enzyme activities,
extracellular polymeric substance (EPS) production, and quorum sensing
(QS) signaling, promoting bacterial resilience and biofilm formation.
In contrast, excessive oxidative stress (600 ppm of NaClO) reduced
bacteria and phage diversity, disrupted antioxidant responses, and
increased microbial sensitivity. Hydraulic stress predominantly influenced
viral diversity and co-occurrence network topology, favoring the expansion
of broad host-range phages and lysogenic lifestyles under combined
stresses. Phage–bacterium interaction analyses highlighted
phages’ adaptive preferences for hosts with high network centrality
and broad ecological niches, which enhanced microbial interactions
and resilience. Transcriptomic profiling demonstrated the early enrichment
of genes associated with energy metabolism, ROS detoxification, and
biofilm formation, followed by stabilization as biofilms matured.
Phage-encoded auxiliary metabolic genes were involved in DNA repair,
QS, and EPS biosynthesis, contributing to microbial adaptation through
oxidative stress resistance and biofilm stabilization. Overall, these
findings provide mechanistic insights into biofouling dynamics and
highlight the need to optimize chlorine dosing to prevent suboptimal
levels of microbial adaptation and biofouling.