Isolation of the first cultured representative from a deep-branching phylum in serpentinite-hosted ecosystems

Abstract

Serpentinization drives abiotic synthesis of organics (e.g., hydrocarbon) potentially conducive to the emergence of life, making serpentinite-hosted systems and associated microbial community key windows into nature of lifes origin. Although cultivation-independent studies uncovered the Candisdatus Bipolaricaulota widely distributed in serpentinizing environments, cultivation of this phylum has been unsuccessful. Here we cultured the first pure strain, J31, of Ca. Bipolaricaulota from the Lost City hydrothermal field, a well-characterized marine serpentinite system, using hydrocarbons as the primary nutrient source. As an early-branching bacterial lineage, strain J31 exhibits an unusual morphology composed of a central rod and elongated Toga-like extensions at both ends, and divides by binary fission. Strain J31 absorbs hexadecane through Toga ends via coordinated processes resembling inhalation and swallowing, after which hexadecane is efficiently transported to the central rod in the vesicle-like structures and subsequently converted into membrane lipids to support Toga synthesis and cellular growth. Hydrocarbon-degrading capability is widespread among the globally distributed members of Ca. Bipolaricaulota. Strain J31 colonizes serpentine minerals, facilitating the utilization of hydrocarbons derived from serpentines and promoting the release of soluble iron and silicon, thereby linking microbial activity to geochemical cycling. Thus, our study presents a novel strategy for cultivating deep-branching bacteria and offers insights into the metabolic foundations of early life on Earth--and potentially on other rocky planets undergoing serpentinization.