4.8 Article

Characterization of the first cultured free-living representative of Candidatus Izemoplasma uncovers its unique biology

Journal

ISME JOURNAL
Volume 15, Issue 9, Pages 2676-2691

Publisher

SPRINGERNATURE
DOI: 10.1038/s41396-021-00961-7

Keywords

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Funding

  1. Major Research Plan of the National Natural Science Foundation [92051107]
  2. China Ocean Mineral Resources R&D Association Grant [DY135-B2-14]
  3. Key Deployment Projects of Center of Ocean Mega-Science of the Chinese Academy of Sciences [COMS2020Q04]
  4. Strategic Priority Research Program of the Chinese Academy of Sciences [XDA22050301]
  5. National Key R and D Program of China [2018YFC0310800]
  6. Taishan Young Scholar Program of Shandong Province [tsqn20161051]
  7. Qingdao Innovation Leadership Program [18-1-2-7-zhc]
  8. Open Research Project of National Major Science & Technology Infrastructure (RV KEXUE) [NMSTI-KEXUE2017K01]

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This study successfully isolated a representative strain of Izemoplasma from a deep-sea methane seep, providing detailed insights into its physiological, genomic, and metabolic characteristics. The novel strain demonstrated strong DNA-degradation potentials and the ability to utilize extracellular DNA for growth. The proposed new species and genus Xianfuyuplasma coldseepsis based on the description of strain zrk13 contributes to a better understanding of the metabolic potential and ecological role of Izemoplasma bacteria in deep ocean biogeochemical cycling.
Candidatus Izemoplasma, an intermediate in the reductive evolution from Firmicutes to Mollicutes, was proposed to represent a novel class of free-living wall-less bacteria within the phylum Tenericutes. Unfortunately, the paucity of pure cultures has limited further insights into their physiological and metabolic features as well as ecological roles. Here, we report the first successful isolation of an Izemoplasma representative from the deep-sea methane seep, strain zrk13, using a DNA degradation-driven method given Izemoplasma's prominent DNA-degradation potentials. We further present a detailed description of the physiological, genomic and metabolic traits of the novel strain, which allows for the first time the reconstruction of the metabolic potential and lifestyle of a member of the tentatively defined Candidatus Izemoplasma. On the basis of the description of strain zrk13, the novel species and genus Xianfuyuplasma coldseepsis is proposed. Using a combined biochemical and transcriptomic method, we further show the supplement of organic matter, thiosulfate or bacterial genomic DNA could evidently promote the growth of strain zrk13. In particular, strain zrk13 could degrade and utilize the extracellular DNA for growth in both laboraterial and deep-sea conditions. Moreover, the predicted genes determining DNA-degradation broadly distribute in the genomes of other Izemoplasma members. Given that extracellular DNA is a particularly crucial phosphorus as well as nitrogen and carbon source for microorganisms in the seafloor, Izemoplasma bacteria are thought to be important contributors to the biogeochemical cycling in the deep ocean.

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