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

TL;DR

This study explores how a bacteria with a small genome adapts to the nutrient-rich environment around diatoms by using specialized genes for attachment and polysaccharide metabolism.

Contribution

The study reveals how genome streamlining in Opacimonas immobilis supports adaptation to the phycosphere through enhanced adhesion and metabolic specialization.

Findings

LMIT016T forms dense attachments on diatom surfaces and promotes mutual growth with its host microalgae.

The genome of LMIT016T contains genes for EPS biosynthesis, adhesion, and polysaccharide utilization, which support long-term attachment and biofilm formation.

Genome streamlining in LMIT016T involves loss of motility and c-di-GMP signaling genes but retention of nutrient acquisition and stress response pathways.

Abstract

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 Opacimonas immobilis LMIT016T, a phycosphere isolate from the diatom Actinocyclus curvatulus that possesses the smallest genome within the Alteromonadaceae 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 LMIT016T 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, LMIT016T 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 LMIT016T 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.

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