Biosurfactant production under cold-saline stress is a strain specific trait independent from phylogeny and biosynthetic gene content

Abstract

Abstract Microbial genomes code for far more biosynthetic potential than a single cell typically expresses, but the environmental and cellular controls that determine whether the latent capacity is realised remain poorly understood. Biosurfactants, surface-active metabolites proposed to aid survival in cold and saline habitats, exemplify this gap: capacity is often inferred from genomes or detected chemically, but is rarely linked to the specific conditions that stimulate its production in the same organisms. Here we combine whole-genome sequencing, untargeted LC-MS/MS metabolomics, and quantitative surface-tension assays across 25 bacterial isolates isolated from the cold, hypersaline Qaidam Basin (a terrestrial analogue for ancient Mars) and contrasting marine environments. We show that biosurfactant production is not a fixed lineage trait but a regulated, strain-specific response that emerges under combined cold and salt stress. This response is structured into three tiers: genomic capacity defines the accessible chemical space; the genomic complement of pathway-regulator genes tracks responsiveness; strain-level physiological state determines realised output. Regulatory-gene content, rather than biosynthetic-cluster count, predicted surfactant production across strains. Production was amplified by low temperature and high salinity and showed little phylogenetic signal, with near-clonal strains differing in their stress-response. These findings reshape biochemical adaptation in extreme environments as a problem of conditional activation, not only of genomic potential, but of cellular systems that permit its expression, which requires looking beyond biosynthetic-gene content to the cellular factors that determine whether that potential is expressed.