IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47750-2.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47750-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47750-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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. 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.
    5. 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.
    6. 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.
    7. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Joshua N. Hamm & Yan Liao & Andriko Kügelgen & Nina Dombrowski & Evan Landers & Christopher Brownlee & Emma M. V. Johansson & Renee M. Whan & Matthew A. B. Baker & Buzz Baum & Tanmay A. M. Bharat & Ia, 2024. "The parasitic lifestyle of an archaeal symbiont," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Zhiguang Qiu & Li Yuan & Chun-Ang Lian & Bin Lin & Jie Chen & Rong Mu & Xuejiao Qiao & Liyu Zhang & Zheng Xu & Lu Fan & Yunzeng Zhang & Shanquan Wang & Junyi Li & Huiluo Cao & Bing Li & Baowei Chen & , 2024. "BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Matthew D. Johnson & Doulin C. Shepherd & Hiroyuki D. Sakai & Manasi Mudaliyar & Arun Prasad Pandurangan & Francesca L. Short & Paul D. Veith & Nichollas E. Scott & Norio Kurosawa & Debnath Ghosal, 2024. "Cell-to-cell interactions revealed by cryo-tomography of a DPANN co-culture system," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    6. Roopnarain, Ashira & Rama, Haripriya & Ndaba, Busiswa & Bello-Akinosho, Maryam & Bamuza-Pemu, Emomotimi & Adeleke, Rasheed, 2021. "Unravelling the anaerobic digestion ‘black box’: Biotechnological approaches for process optimization," Renewable and Sustainable Energy Reviews, Elsevier, vol. 152(C).
    7. Hao Leng & Yinzhao Wang & Weishu Zhao & Stefan M. Sievert & Xiang Xiao, 2023. "Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Yan-Ling Qi & Ya-Ting Chen & Yuan-Guo Xie & Yu-Xian Li & Yang-Zhi Rao & Meng-Meng Li & Qi-Jun Xie & Xing-Ru Cao & Lei Chen & Yan-Ni Qu & Zhen-Xuan Yuan & Zhi-Chao Xiao & Lu Lu & Jian-Yu Jiao & Wen-She, 2024. "Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Armando Azua-Bustos & Alberto G. Fairén & Carlos González-Silva & Olga Prieto-Ballesteros & Daniel Carrizo & Laura Sánchez-García & Victor Parro & Miguel Ángel Fernández-Martínez & Cristina Escudero &, 2023. "Dark microbiome and extremely low organics in Atacama fossil delta unveil Mars life detection limits," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Antonia Bruno & Giulia Agostinetto & Sara Fumagalli & Giulia Ghisleni & Anna Sandionigi, 2022. "It’s a Long Way to the Tap: Microbiome and DNA-Based Omics at the Core of Drinking Water Quality," IJERPH, MDPI, vol. 19(13), pages 1-16, June.
    11. Natasha K. Dudek & Jesus G. Galaz-Montoya & Handuo Shi & Megan Mayer & Cristina Danita & Arianna I. Celis & Tobias Viehboeck & Gong-Her Wu & Barry Behr & Silvia Bulgheresi & Kerwyn Casey Huang & Wah C, 2023. "Previously uncharacterized rectangular bacterial structures in the dolphin mouth," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Tamara Nazina & Tamara Babich & Nadezhda Kostryukova & Diyana Sokolova & Ruslan Abdullin & Tatyana Tourova & Vitaly Kadnikov & Andrey Mardanov & Nikolai Ravin & Denis Grouzdev & Andrey Poltaraus & Ste, 2020. "Ultramicrobacteria from Nitrate- and Radionuclide-Contaminated Groundwater," Sustainability, MDPI, vol. 12(3), pages 1-27, February.
    13. Zhongyi Lu & Runyue Xia & Siyu Zhang & Jie Pan & Yang Liu & Yuri I. Wolf & Eugene V. Koonin & Meng Li, 2024. "Evolution of optimal growth temperature in Asgard archaea inferred from the temperature dependence of GDP binding to EF-1A," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    14. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Nancy O. Nou & Jonathan K. Covington & Dengxun Lai & Xavier Mayali & Cale O. Seymour & Juliet Johnston & Jian-Yu Jiao & Steffen Buessecker & Damon Mosier & Alise R. Muok & Nicole Torosian & Allison M., 2024. "Genome-guided isolation of the hyperthermophilic aerobe Fervidibacter sacchari reveals conserved polysaccharide metabolism in the Armatimonadota," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Minjia Zheng & Linran Wen & Cailing He & Xinlan Chen & Laiting Si & Hao Li & Yiting Liang & Wei Zheng & Feng Guo, 2024. "Sequencing-guided re-estimation and promotion of cultivability for environmental bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Steffen Buessecker & Marike Palmer & Dengxun Lai & Joshua Dimapilis & Xavier Mayali & Damon Mosier & Jian-Yu Jiao & Daniel R. Colman & Lisa M. Keller & Emily St. John & Michelle Miranda & Cristina Gon, 2022. "An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Bin Ma & Caiyu Lu & Yiling Wang & Jingwen Yu & Kankan Zhao & Ran Xue & Hao Ren & Xiaofei Lv & Ronghui Pan & Jiabao Zhang & Yongguan Zhu & Jianming Xu, 2023. "A genomic catalogue of soil microbiomes boosts mining of biodiversity and genetic resources," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    19. Matthew Herdman & Buse Isbilir & Andriko Kügelgen & Ulrike Schulze & Alan Wainman & Tanmay A. M. Bharat, 2024. "Cell cycle dependent coordination of surface layer biogenesis in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Zhirui Zeng & Huahui Chen & Huan Yang & Yufei Chen & Wei Yang & Xi Feng & Hongye Pei & Paula V. Welander, 2022. "Identification of a protein responsible for the synthesis of archaeal membrane-spanning GDGT lipids," Nature Communications, Nature, vol. 13(1), pages 1-9, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47750-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.