Literature DB >> 29269839

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

Yoshiaki Kinosita1,2, Yoshitomo Kikuchi3, Nagisa Mikami4, Daisuke Nakane4, Takayuki Nishizaka4.   

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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Mesh:

Year:  2017        PMID: 29269839      PMCID: PMC5864224          DOI: 10.1038/s41396-017-0010-z

Source DB:  PubMed          Journal:  ISME J        ISSN: 1751-7362            Impact factor:   10.302


  36 in total

Review 1.  The flagellum in bacterial pathogens: For motility and a whole lot more.

Authors:  Bonnie Chaban; H Velocity Hughes; Morgan Beeby
Journal:  Semin Cell Dev Biol       Date:  2015-11-03       Impact factor: 7.727

2.  A Periplasmic Polymer Curves Vibrio cholerae and Promotes Pathogenesis.

Authors:  Thomas M Bartlett; Benjamin P Bratton; Amit Duvshani; Amanda Miguel; Ying Sheng; Nicholas R Martin; Jeffrey P Nguyen; Alexandre Persat; Samantha M Desmarais; Michael S VanNieuwenhze; Kerwyn Casey Huang; Jun Zhu; Joshua W Shaevitz; Zemer Gitai
Journal:  Cell       Date:  2017-01-12       Impact factor: 41.582

3.  Unitary step of gliding machinery in Mycoplasma mobile.

Authors:  Yoshiaki Kinosita; Daisuke Nakane; Mitsuhiro Sugawa; Tomoko Masaike; Kana Mizutani; Makoto Miyata; Takayuki Nishizaka
Journal:  Proc Natl Acad Sci U S A       Date:  2014-05-27       Impact factor: 11.205

4.  Movement of microorganisms in viscous environments.

Authors:  H C Berg; L Turner
Journal:  Nature       Date:  1979-03-22       Impact factor: 49.962

5.  Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis.

Authors:  Yanling Wang; Anne K Dunn; Jacqueline Wilneff; Margaret J McFall-Ngai; Stephen Spiro; Edward G Ruby
Journal:  Mol Microbiol       Date:  2010-09-29       Impact factor: 3.501

6.  Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the Stinkbug Gut.

Authors:  Jiyeun Kate Kim; Ho Jin Lee; Yoshitomo Kikuchi; Wataru Kitagawa; Naruo Nikoh; Takema Fukatsu; Bok Luel Lee
Journal:  Appl Environ Microbiol       Date:  2013-06-07       Impact factor: 4.792

7.  NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association.

Authors:  Seana K Davidson; Tanya A Koropatnick; Renate Kossmehl; Laura Sycuro; Margaret J McFall-Ngai
Journal:  Cell Microbiol       Date:  2004-12       Impact factor: 3.715

8.  Direct observation of rotation and steps of the archaellum in the swimming halophilic archaeon Halobacterium salinarum.

Authors:  Yoshiaki Kinosita; Nariya Uchida; Daisuke Nakane; Takayuki Nishizaka
Journal:  Nat Microbiol       Date:  2016-08-26       Impact factor: 17.745

9.  Insect's intestinal organ for symbiont sorting.

Authors:  Tsubasa Ohbayashi; Kazutaka Takeshita; Wataru Kitagawa; Naruo Nikoh; Ryuichi Koga; Xian-Ying Meng; Kanako Tago; Tomoyuki Hori; Masahito Hayatsu; Kozo Asano; Yoichi Kamagata; Bok Luel Lee; Takema Fukatsu; Yoshitomo Kikuchi
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-31       Impact factor: 11.205

10.  Swimming behavior of the monotrichous bacterium Pseudomonas fluorescens SBW25.

Authors:  Liyan Ping; Jan Birkenbeil; Shamci Monajembashi
Journal:  FEMS Microbiol Ecol       Date:  2013-02-12       Impact factor: 4.194

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  21 in total

1.  Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture.

Authors:  Tsubasa Ohbayashi; Ryo Futahashi; Mia Terashima; Quentin Barrière; Florian Lamouche; Kazutaka Takeshita; Xian-Ying Meng; Yasuo Mitani; Teruo Sone; Shuji Shigenobu; Takema Fukatsu; Peter Mergaert; Yoshitomo Kikuchi
Journal:  ISME J       Date:  2019-02-11       Impact factor: 10.302

Review 2.  Bacterial Vivisection: How Fluorescence-Based Imaging Techniques Shed a Light on the Inner Workings of Bacteria.

Authors:  Alexander Cambré; Abram Aertsen
Journal:  Microbiol Mol Biol Rev       Date:  2020-10-28       Impact factor: 11.056

Review 3.  Housing microbial symbionts: evolutionary origins and diversification of symbiotic organs in animals.

Authors:  Angela E Douglas
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-10       Impact factor: 6.237

4.  Bacterial physiology: It's a wrap for Burkholderia flagella.

Authors:  Ursula Hofer
Journal:  Nat Rev Microbiol       Date:  2018-01-15       Impact factor: 60.633

5.  Host-symbiont specificity determined by microbe-microbe competition in an insect gut.

Authors:  Hideomi Itoh; Seonghan Jang; Kazutaka Takeshita; Tsubasa Ohbayashi; Naomi Ohnishi; Xian-Ying Meng; Yasuo Mitani; Yoshitomo Kikuchi
Journal:  Proc Natl Acad Sci U S A       Date:  2019-10-21       Impact factor: 11.205

6.  Burkholderia insecticola triggers midgut closure in the bean bug Riptortus pedestris to prevent secondary bacterial infections of midgut crypts.

Authors:  Yoshitomo Kikuchi; Tsubasa Ohbayashi; Seonghan Jang; Peter Mergaert
Journal:  ISME J       Date:  2020-03-23       Impact factor: 10.302

7.  Microbial interactions in the mosquito gut determine Serratia colonization and blood-feeding propensity.

Authors:  Elena V Kozlova; Shivanand Hegde; Christopher M Roundy; George Golovko; Miguel A Saldaña; Charles E Hart; Enyia R Anderson; Emily A Hornett; Kamil Khanipov; Vsevolod L Popov; Maria Pimenova; Yiyang Zhou; Yuriy Fovanov; Scott C Weaver; Andrew L Routh; Eva Heinz; Grant L Hughes
Journal:  ISME J       Date:  2020-09-07       Impact factor: 10.302

Review 8.  The role of microbial motility and chemotaxis in symbiosis.

Authors:  Jean-Baptiste Raina; Vicente Fernandez; Bennett Lambert; Roman Stocker; Justin R Seymour
Journal:  Nat Rev Microbiol       Date:  2019-05       Impact factor: 60.633

9.  Modeling of lophotrichous bacteria reveals key factors for swimming reorientation.

Authors:  Jeungeun Park; Yongsam Kim; Wanho Lee; Sookkyung Lim
Journal:  Sci Rep       Date:  2022-04-20       Impact factor: 4.996

10.  Prevalence of an Insect-Associated Genomic Region in Environmentally Acquired Burkholderiaceae Symbionts.

Authors:  Patrick T Stillson; David A Baltrus; Alison Ravenscraft
Journal:  Appl Environ Microbiol       Date:  2022-04-18       Impact factor: 5.005

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