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Selective lipid recruitment by an archaeal DPANN symbiont from its host

Author

Listed:
  • Su Ding

    (NIOZ Royal Institute for Sea Research)

  • Joshua N. Hamm

    (NIOZ Royal Institute for Sea Research)

  • Nicole J. Bale

    (NIOZ Royal Institute for Sea Research)

  • Jaap S. Sinninghe Damsté

    (NIOZ Royal Institute for Sea Research
    Faculty of Geosciences, Utrecht University)

  • Anja Spang

    (NIOZ Royal Institute for Sea Research
    Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam)

Abstract

The symbiont Ca. Nanohaloarchaeum antarcticus is obligately dependent on its host Halorubrum lacusprofundi for lipids and other metabolites due to its lack of certain biosynthetic genes. However, it remains unclear which specific lipids or metabolites are acquired from its host, and how the host responds to infection. Here, we explored the lipidome dynamics of the Ca. Nha. antarcticus – Hrr. lacusprofundi symbiotic relationship during co-cultivation. By using a comprehensive untargeted lipidomic methodology, our study reveals that Ca. Nha. antarcticus selectively recruits 110 lipid species from its host, i.e., nearly two-thirds of the total number of host lipids. Lipid profiles of co-cultures displayed shifts in abundances of bacterioruberins and menaquinones and changes in degree of bilayer-forming glycerolipid unsaturation. This likely results in increased membrane fluidity and improved resistance to membrane disruptions, consistent with compensation for higher metabolic load and mechanical stress on host membranes when in contact with Ca. Nha. antarcticus cells. Notably, our findings differ from previous observations of other DPANN symbiont-host systems, where no differences in lipidome composition were reported. Altogether, our work emphasizes the strength of employing untargeted lipidomics approaches to provide details into the dynamics underlying a DPANN symbiont-host system.

Suggested Citation

  • Su Ding & Joshua N. Hamm & Nicole J. Bale & Jaap S. Sinninghe Damsté & Anja Spang, 2024. "Selective lipid recruitment by an archaeal DPANN symbiont from its host," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47750-2
    DOI: 10.1038/s41467-024-47750-2
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    1. Louie Wurch & Richard J. Giannone & Bernard S. Belisle & Carolyn Swift & Sagar Utturkar & Robert L. Hettich & Anna-Louise Reysenbach & Mircea Podar, 2016. "Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
    2. Alexander J. Probst & Thomas Weinmaier & Kasie Raymann & Alexandra Perras & Joanne B. Emerson & Thomas Rattei & Gerhard Wanner & Andreas Klingl & Ivan A. Berg & Marcos Yoshinaga & Bernhard Viehweger &, 2014. "Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    3. Harald Huber & Michael J. Hohn & Reinhard Rachel & Tanja Fuchs & Verena C. Wimmer & Karl O. Stetter, 2002. "A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont," Nature, Nature, vol. 417(6884), pages 63-67, May.
    4. Olga V. Golyshina & Stepan V. Toshchakov & Kira S. Makarova & Sergey N. Gavrilov & Aleksei A. Korzhenkov & Violetta La Cono & Erika Arcadi & Taras Y. Nechitaylo & Manuel Ferrer & Ilya V. Kublanov & Yu, 2017. "‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. Susanne Krause & Sabrina Gfrerer & Andriko Kügelgen & Carsten Reuse & Nina Dombrowski & Laura Villanueva & Boyke Bunk & Cathrin Spröer & Thomas R. Neu & Ute Kuhlicke & Kerstin Schmidt-Hohagen & Karste, 2022. "The importance of biofilm formation for cultivation of a Micrarchaeon and its interactions with its Thermoplasmatales host," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Nina Dombrowski & Tom A. Williams & Jiarui Sun & Benjamin J. Woodcroft & Jun-Hoe Lee & Bui Quang Minh & Christian Rinke & Anja Spang, 2020. "Undinarchaeota illuminate DPANN phylogeny and the impact of gene transfer on archaeal evolution," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    7. Christian Rinke & Patrick Schwientek & Alexander Sczyrba & Natalia N. Ivanova & Iain J. Anderson & Jan-Fang Cheng & Aaron Darling & Stephanie Malfatti & Brandon K. Swan & Esther A. Gies & Jeremy A. Do, 2013. "Insights into the phylogeny and coding potential of microbial dark matter," Nature, Nature, vol. 499(7459), pages 431-437, July.
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