Article

Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body

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Abstract

A bean bug symbiont, Burkholderia sp. RPE64, selectively colonizes the gut crypts by flagella-mediated motility: however, the mechanism for this colonization remains unclear. Here, to obtain clues to this mechanism, we characterized the swimming motility of the Burkholderia symbiont under an advanced optical microscope. High-speed imaging of cells enabled the detection of turn events with up to 5-ms temporal resolution, indicating that cells showed reversal motions (θ ~ 180°) with rapid changes in speed by a factor of 3.6. Remarkably, staining of the flagellar filaments with a fluorescent dye Cy3 revealed that the flagellar filaments wrap around the cell body with a motion like that of a ribbon streamer in rhythmic gymnastics. A motility assay with total internal reflection fluorescence microscopy revealed that the left-handed flagellum wound around the cell body and propelled it forward by its clockwise rotation. We also detected periodic-fluorescent signals of flagella on the glass surface, suggesting that flagella possibly contacted the solid surface directly and produced a gliding-like motion driven by flagellar rotation. Finally, the wrapping motion was also observed in a symbiotic bacterium of the bobtail squid, Aliivibrio fischeri, suggesting that this motility mode may contribute to migration on the mucus-filled narrow passage connecting to the symbiotic organ.

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Acknowledgements

The authors thank R. Kamiya and T. E.F. Quax for preparing the manuscript, and T. Minamino and Y.V. Morimoto for supplying E. coli K-12 W3110. This study was supported in part by a grant from the Funding Program for Next-Generation World-Leading Researchers (no. LR033 to T.N.) from the Japan Society for the Promotion of Science, by a Grant-in-Aid for Scientific Research on Innovative Areas “Harmonized Supramolecular Motility Machinery and Its Diversity” (to T.N.) and “Fluctuation & Structure” (no.26103527 to T.N.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and the Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI (grant number 15H05638 for Y. Kikuchi). Y. Kinosita was the recipient of a JSPS Fellowship for Japan Junior Scientists (15J12274) and Postdoctral Fellowship for Research Abroad.

Author contributions

Y Kinosita, Y Kikuchi, DN, and TN designed the research; Y. Kinosita performed the research; NM developed a framework for analyzing a reorientation event, Y Kinosita and TN constructed the optical setup and microscope; Y Kinosita, Y Kikuchi and TN wrote the paper.

Author information

Author notes

    • Yoshiaki Kinosita

    Present address: Institute for Biology II, Freiburg University, Freiburg, Germany

Affiliations

  1. Department of Physics, Gakushuin University, 1-5-1 Mejiro, Toshima-ku, Tokyo, 171-8588, Japan

    • Yoshiaki Kinosita
    • , Nagisa Mikami
    • , Daisuke Nakane
    •  & Takayuki Nishizaka
  2. Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology, Sapporo, 062-8517, Japan

    • Yoshitomo Kikuchi

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Conflict of interest

The authors declare that they have no competing interests.

Corresponding authors

Correspondence to Yoshiaki Kinosita or Yoshitomo Kikuchi.

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