Subsurface environments are often conceptualized as static ecosystems governed by slow processes and persistent energy scarcity, reinforcing the notion that microbial life is largely inactive or maintained in a state of metabolic dormancy. Yet mounting evidence suggests that the subseafloor crustal biosphere is more dynamic, shaped by hydrothermal circulation, fluid–rock interactions, and steep, fluctuating redox gradients. These processes create transient phases of increased energy supply that can sustain ecologically significant microbial activity. To better understand the metabolic strategies enabling survival under these conditions, we investigated the genomic and physiological potential of a spore-forming bacterium, strain JdFR-1ᵀ, enriched from crustal fluids of the Juan de Fuca Ridge. Its genome encodes traits associated with survival and metabolic maintenance under extreme resource limitation, including pathways for sporulation and germination, fermentative and hydrolytic metabolism, and scavenging of organic substrates. These features suggest a capacity to alternate between dormancy and metabolic activity in response to environmental fluctuations. Strain JdFR-1ᵀ represents a new lineage within the Izemoplasmataceae family, for which we propose the name Izemobacterium crustae gen. nov., sp. nov., in accordance with the SeqCode rules. Together, these findings provide genomic evidence for potential adaptive strategies that enable persistence and energy-efficient metabolism in the deep oceanic crustal biosphere.