Thermal modulation of transcriptional states, biofilm architecture and survival strategies in Cobetia marina

Abstract

Inroduction Cobetia marina is a marine bacterium that sustains growth and biofilm formation across a broad thermal range, serving as an ideal model for exploring adaptability in thermally dynamic and warming oceans. In this study, we investigated how growth temperature reshapes transcriptional regulation and biofilm architecture in C. marina strain MM1IDA2H-1, as well as its trajectories under thermal stress. Methods We integrated transcriptomic profiling with confocal and electron microscopy at different growth temperatures. Additionally, we conducted adaptive laboratory evolution (ALE) under progressive heat stress coupled with whole-genome sequencing. Results Transcriptomes from cultures grown at 16 °C, 35 °C, 38 °C, and 41 °C were linked to physiology and biofilm structure, whereas ALE revealed strategies under warming stress. Low temperature promoted a biofilm-competent program driving motility and exopolysaccharide production. Conversely, growth at 41 °C induced a stress-survival state with repression of cooperative traits—quorum sensing—and the activation of DNA repair and oxidative stress responses. Exploratory network analyses predicted NarL, NtrC, CysB, and CsgD as putative components of a temperature-responsive control core, with a reduction in regulatory connectivity at 38 °C, representing a transitional stop-and-reprogram state. Finally, ALE selected for recurrent clone-specific mutations in csgD1, resolving a phenotypic trade-off by downregulating costly biofilm production to maintain growth capacity. Discussion Overall, our findings show how C. marina transitions across a wide temperature range and under thermal stress via state-dependent network rewiring, offering a comprehensive eco-physiological framework that links environmental sensing, multicellular organization, and evolutionary trade-offs in highly dynamic and warming oceans.