Previously uncharacterized rectangular bacterial structures in the dolphin mouth

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 Chiu; David A Relman

doi:10.1038/s41467-023-37638-y

Previously uncharacterized rectangular bacterial structures in the dolphin mouth

Nat Commun. 2023 Apr 13;14(1):2098. doi: 10.1038/s41467-023-37638-y.

Authors

Natasha K Dudek^{1

2

3}, Jesus G Galaz-Montoya⁴, Handuo Shi^{4

5}, Megan Mayer^{6

7}, Cristina Danita⁴, Arianna I Celis⁵, Tobias Viehboeck^{8

9}, Gong-Her Wu⁴, Barry Behr¹⁰, Silvia Bulgheresi⁸, Kerwyn Casey Huang^{4

5

11}, Wah Chiu^{4

5

6}, David A Relman^{12

13

14

15}

Affiliations

¹ Department of Medicine, Stanford University School of Medicine, Stanford, CA, 94305, USA.
² Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, 95064, USA.
³ Quantori, Cambridge, MA, 02142, USA.
⁴ Department of Bioengineering, Stanford University, Stanford, CA, 94305, USA.
⁵ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, 94305, USA.
⁶ Division of CryoEM and Bioimaging, SSRL, SLAC National Accelerator Laboratory, Menlo Park, CA, 94025, USA.
⁷ Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, 02115, USA.
⁸ Department of Functional and Evolutionary Ecology, Environmental Cell Biology Group, University of Vienna, Vienna, Austria.
⁹ Division of Microbial Ecology, Center for Microbiology and Environmental Systems Science, and Vienna Doctoral School of Ecology and Evolution, University of Vienna, Vienna, Austria.
¹⁰ Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, CA, 94305, USA.
¹¹ Chan Zuckerberg Biohub, San Francisco, CA, 94158, USA.
¹² Department of Medicine, Stanford University School of Medicine, Stanford, CA, 94305, USA. relman@stanford.edu.
¹³ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, 94305, USA. relman@stanford.edu.
¹⁴ Chan Zuckerberg Biohub, San Francisco, CA, 94158, USA. relman@stanford.edu.
¹⁵ Infectious Diseases Section, Veterans Affairs Palo Alto Health Care System, Palo Alto, CA, 94304, USA. relman@stanford.edu.

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.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Animals
Bacterial Structures
Bottle-Nosed Dolphin*
In Situ Hybridization, Fluorescence
Mouth
Neisseriaceae* / genetics
RNA, Ribosomal, 16S / genetics

Substances

RNA, Ribosomal, 16S

Grants and funding

RM1 GM135102/GM/NIGMS NIH HHS/United States