IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37638-y.html
   My bibliography  Save this article

Previously uncharacterized rectangular bacterial structures in the dolphin mouth

Author

Listed:
  • Natasha K. Dudek

    (Stanford University School of Medicine
    University of California, Santa Cruz
    Quantori)

  • Jesus G. Galaz-Montoya

    (Stanford University)

  • Handuo Shi

    (Stanford University
    Stanford University School of Medicine)

  • Megan Mayer

    (SSRL, SLAC National Accelerator Laboratory
    Harvard Medical School)

  • Cristina Danita

    (Stanford University)

  • Arianna I. Celis

    (Stanford University School of Medicine)

  • Tobias Viehboeck

    (University of Vienna
    University of Vienna)

  • Gong-Her Wu

    (Stanford University)

  • Barry Behr

    (Stanford University School of Medicine)

  • Silvia Bulgheresi

    (University of Vienna)

  • Kerwyn Casey Huang

    (Stanford University
    Stanford University School of Medicine
    Chan Zuckerberg Biohub)

  • Wah Chiu

    (Stanford University
    Stanford University School of Medicine
    SSRL, SLAC National Accelerator Laboratory)

  • David A. Relman

    (Stanford University School of Medicine
    Stanford University School of Medicine
    Chan Zuckerberg Biohub
    Veterans Affairs Palo Alto Health Care System)

Abstract

Much remains to be explored regarding the diversity of uncultured, host-associated microbes. Here, we describe rectangular bacterial structures (RBSs) in the mouths of bottlenose dolphins. DNA staining revealed multiple paired bands within RBSs, suggesting the presence of cells dividing along the longitudinal axis. Cryogenic transmission electron microscopy and tomography showed parallel membrane-bound segments that are likely cells, encapsulated by an S-layer-like periodic surface covering. RBSs displayed unusual pilus-like appendages with bundles of threads splayed at the tips. We present multiple lines of evidence, including genomic DNA sequencing of micromanipulated RBSs, 16S rRNA gene sequencing, and fluorescence in situ hybridization, suggesting that RBSs are bacterial and distinct from the genera Simonsiella and Conchiformibius (family Neisseriaceae), with which they share similar morphology and division patterning. Our findings highlight the diversity of novel microbial forms and lifestyles that await characterization using tools complementary to genomics such as microscopy.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37638-y
    DOI: 10.1038/s41467-023-37638-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37638-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37638-y?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. Sammy Nyongesa & Philipp M. Weber & Ève Bernet & Francisco Pulido & Cecilia Nieves & Marta Nieckarz & Marie Delaby & Tobias Viehboeck & Nicole Krause & Alex Rivera-Millot & Arnaldo Nakamura & Norbert , 2022. "Evolution of longitudinal division in multicellular bacteria of the Neisseriaceae family," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Dongying Wu & Philip Hugenholtz & Konstantinos Mavromatis & Rüdiger Pukall & Eileen Dalin & Natalia N. Ivanova & Victor Kunin & Lynne Goodwin & Martin Wu & Brian J. Tindall & Sean D. Hooper & Amrita P, 2009. "A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea," Nature, Nature, vol. 462(7276), pages 1056-1060, December.
    3. Taiki Katayama & Masaru K. Nobu & Hiroyuki Kusada & Xian-Ying Meng & Naoki Hosogi & Katsuyuki Uematsu & Hideyoshi Yoshioka & Yoichi Kamagata & Hideyuki Tamaki, 2020. "Isolation of a member of the candidate phylum ‘Atribacteria’ reveals a unique cell membrane structure," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    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. David Burstein & Lucas B. Harrington & Steven C. Strutt & Alexander J. Probst & Karthik Anantharaman & Brian C. Thomas & Jennifer A. Doudna & Jillian F. Banfield, 2017. "New CRISPR–Cas systems from uncultivated microbes," Nature, Nature, vol. 542(7640), pages 237-241, February.
    6. Birgit Luef & Kyle R. Frischkorn & Kelly C. Wrighton & Hoi-Ying N. Holman & Giovanni Birarda & Brian C. Thomas & Andrea Singh & Kenneth H. Williams & Cristina E. Siegerist & Susannah G. Tringe & Kenne, 2015. "Diverse uncultivated ultra-small bacterial cells in groundwater," Nature Communications, Nature, vol. 6(1), pages 1-8, May.
    7. Christopher T. Brown & Laura A. Hug & Brian C. Thomas & Itai Sharon & Cindy J. Castelle & Andrea Singh & Michael J. Wilkins & Kelly C. Wrighton & Kenneth H. Williams & Jillian F. Banfield, 2015. "Unusual biology across a group comprising more than 15% of domain Bacteria," Nature, Nature, vol. 523(7559), pages 208-211, July.
    8. Karthik Anantharaman & Christopher T. Brown & Laura A. Hug & Itai Sharon & Cindy J. Castelle & Alexander J. Probst & Brian C. Thomas & Andrea Singh & Michael J. Wilkins & Ulas Karaoz & Eoin L. Brodie , 2016. "Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    9. Elisabeth M. Bik & Elizabeth K. Costello & Alexandra D. Switzer & Benjamin J. Callahan & Susan P. Holmes & Randall S. Wells & Kevin P. Carlin & Eric D. Jensen & Stephanie Venn-Watson & David A. Relman, 2016. "Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    10. Raphaël Méheust & David Burstein & Cindy J. Castelle & Jillian F. Banfield, 2019. "The distinction of CPR bacteria from other bacteria based on protein family content," Nature Communications, Nature, vol. 10(1), pages 1-12, 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. Kelly J. Whaley-Martin & Lin-Xing Chen & Tara Colenbrander Nelson & Jennifer Gordon & Rose Kantor & Lauren E. Twible & Stephanie Marshall & Sam McGarry & Laura Rossi & Benoit Bessette & Christian Baro, 2023. "O2 partitioning of sulfur oxidizing bacteria drives acidity and thiosulfate distributions in mining waters," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. 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.
    3. 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.
    4. Zongzhi Wu & Tang Liu & Qian Chen & Tianyi Chen & Jinyun Hu & Liyu Sun & Bingxue Wang & Wenpeng Li & Jinren Ni, 2024. "Unveiling the unknown viral world in groundwater," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. 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).
    6. 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.
    7. Marie C. Schoelmerich & Lynn Ly & Jacob West-Roberts & Ling-Dong Shi & Cong Shen & Nikhil S. Malvankar & Najwa Taib & Simonetta Gribaldo & Ben J. Woodcroft & Christopher W. Schadt & Basem Al-Shayeb & , 2024. "Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Yunxi Liu & R. A. Leo Elworth & Michael D. Jochum & Kjersti M. Aagaard & Todd J. Treangen, 2022. "De novo identification of microbial contaminants in low microbial biomass microbiomes with Squeegee," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Feiyu Zhao & Tao Zhang & Xiaodi Sun & Xiyun Zhang & Letong Chen & Hejun Wang & Jinze Li & Peng Fan & Liangxue Lai & Tingting Sui & Zhanjun Li, 2023. "A strategy for Cas13 miniaturization based on the structure and AlphaFold," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. 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.
    11. 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.
    12. Morten Kam Dahl Dueholm & Marta Nierychlo & Kasper Skytte Andersen & Vibeke Rudkjøbing & Simon Knutsson & Mads Albertsen & Per Halkjær Nielsen, 2022. "MiDAS 4: A global catalogue of full-length 16S rRNA gene sequences and taxonomy for studies of bacterial communities in wastewater treatment plants," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Danielle Miller & Adi Stern & David Burstein, 2022. "Deciphering microbial gene function using natural language processing," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Xianzhe Gong & Álvaro Rodríguez Río & Le Xu & Zhiyi Chen & Marguerite V. Langwig & Lei Su & Mingxue Sun & Jaime Huerta-Cepas & Valerie Anda & Brett J. Baker, 2022. "New globally distributed bacterial phyla within the FCB superphylum," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    15. Boris Kantor & Bernadette O’Donovan & Joseph Rittiner & Dellila Hodgson & Nicholas Lindner & Sophia Guerrero & Wendy Dong & Austin Zhang & Ornit Chiba-Falek, 2024. "The therapeutic implications of all-in-one AAV-delivered epigenome-editing platform in neurodegenerative disorders," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. S. Emil Ruff & Pauline Humez & Isabella Hrabe Angelis & Muhe Diao & Michael Nightingale & Sara Cho & Liam Connors & Olukayode O. Kuloyo & Alan Seltzer & Samuel Bowman & Scott D. Wankel & Cynthia N. Mc, 2023. "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. 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.
    18. 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.
    19. 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.
    20. Daniela S. Aliaga Goltsman & Lisa M. Alexander & Jyun-Liang Lin & Rodrigo Fregoso Ocampo & Benjamin Freeman & Rebecca C. Lamothe & Andres Perez Rivas & Morayma M. Temoche-Diaz & Shailaja Chadha & Nata, 2022. "Compact Cas9d and HEARO enzymes for genome editing discovered from uncultivated microbes," Nature Communications, Nature, vol. 13(1), pages 1-11, 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:14:y:2023:i:1:d:10.1038_s41467-023-37638-y. 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.