Polysaccharide Utilization and Adhesion Enable the Genome-Streamlined Opacimonas immobilis to Adapt to the Diatom Phycosphere

Heterotrophic bacteria and microalgae are key regulators of marine biogeochemical cycles. The phycosphere, a nutrient-rich microenvironment surrounding microalgae, serves as a crucial interface for bacterial-algal interactions. Our previous work identified <i>Opacimonas immobilis</i> LMIT016^T, a phycosphere isolate from the diatom <i>Actinocyclus curvatulus</i> that possesses the smallest genome within the <i>Alteromonadaceae</i> family. However, its adaptation mechanisms to the phycosphere remain unclear, particularly given its extensive genome streamlining, a process involving the selective loss of non-essential and energetically costly genes to enhance fitness in nutrient-specific niches. Here, the co-cultivation experiments demonstrated significant mutual growth promotion between LMIT016^T and its host microalgae, with the bacterium forming dense attachments on diatom surfaces. Genomic analysis revealed that in addition to loss of motility-related genes, the strain exhibits a substantial reduction in c-di-GMP signaling components, including both synthases and receptors. Conversely, LMIT016^T harbors numerous genes essential for extracellular polysaccharide (EPS) biosynthesis and adhesion, supporting long-term attachment and biofilm formation. Other retained genes encode pathways for nutrient acquisition, stress response, and phosphate and nitrogen metabolism, reflecting its adaptations to the nutrient-rich phycosphere. Furthermore, the genome of LMIT016^T encodes two polysaccharide utilization loci (PULs) targeting laminarin and α-1,4-glucans, whose functions were experimentally validated by the transcriptional induction of the corresponding carbohydrate-active enzyme genes. These findings indicate that this strain counterbalances genome reduction by enhancing its attachment capabilities and metabolic specialization on algal polysaccharides, potentially facilitating stable association with diatom cells. Our results suggest that genome streamlining may represent an alternative ecological strategy in the phycosphere, highlighting a potential evolutionary trade-off between metabolic efficiency and niche specialization.