Unique behavioral patterns of wandering colonies of Brevibacillus thermoruber on agar plates.

Brevibacillus thermoruber motile colony swarming swimming wandering colony

Journal

Journal of basic microbiology
ISSN: 1521-4028
Titre abrégé: J Basic Microbiol
Pays: Germany
ID NLM: 8503885

Informations de publication

Date de publication:
23 Apr 2024
Historique:
revised: 27 03 2024
received: 20 02 2024
accepted: 10 04 2024
medline: 23 4 2024
pubmed: 23 4 2024
entrez: 23 4 2024
Statut: aheadofprint

Résumé

Brevibacillus thermoruber strain Nabari cells grow as widely spreading dendritic colonies on reasoner's 2A-agar (1.5%) plates at around 55°C but as small motile colonies at 37°C. Motile colonies can be divided into colonies that move in straight or curved lines over long distances (wandering colonies), and colonies that rotate at a fixed location (rotating colonies). The addition of surfactant to the agar medium greatly increased the frequency of wandering colonies and facilitated the study of such colonies. The morphology of the wandering colonies varied: circular at the tip and pointed at the back, lemon-shaped with pointed ends, crescent-shaped, bullet-shaped, fish-like, and so on. A single colony may split into multiple colonies as it moves, or multiple colonies may merge into a single colony. The most surprising aspect of the movement of wandering colonies was that when a moving colony collides with another colony, it sometimes does not make a U-turn, but instead retreats straight back, as if bouncing back. The migration mechanisms of wandering colonies are discussed based on optical microscopic observations of swimming patterns of single cells in water and scanning electron microscopy of the arrangement of bacterial cells in wandering colonies.

Identifiants

pubmed: 38651780
doi: 10.1002/jobm.202400091
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e202400091

Informations de copyright

© 2024 Wiley‐VCH GmbH.

Références

Smibert RM, Krieg NR. Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR Editors. Methods for general and molecular bacteriology. Washington, DC: ASM Press; 1994. p. 607–654.
Bi S, Sourjik V. Stimulus sensing and signal processing in bacterial chemotaxis. Curr Opin Microbiol. 2018;45:22–29.
Colin R, Ni B, Laganenka L, Sourjik V. Multiple functions of flagellar motility and chemotaxis in bacterial physiology. FEMS Microbiol Rev. 2021;45:1–19.
Henrichsen J. Bacterial surface translocation: a survey and a classification. Bacteriol Rev. 1972;36:478–503.
Jose R, Singh V. Swarming in bacteria: a tale of plasticity in motility behavior. J Indian Inst Sci. 2020;100:515–524.
Belas R, Erskine D, Flaherty D. Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J Bacteriol. 1991;173:6279–6288.
Be'er A, Smith RS, Zhang HP, Florin EL, Payne SM, Swinney HL. Paenibacillus dendritiformis bacterial colony growth depends on surfactant but not on bacterial motion. J Bacteriol. 2009;191:5758–5764.
Cohen I, Ron IG, Ben‐Jacob E. From branching to nebula patterning during colonial development of the Paenibacillus alvei bacteria. Phys A Stat Mech Appl. 2000;286:321–336.
Fujikawa H, Matsushita M. Fractal growth of Bacillus subtilis on agar plates. J Phys Soc Jpn. 1989;58:3875–3878.
Ben‐Jacob E. From snowflake formation to growth of bacterial colonies II: cooperative formation of complex colonial patterns. Contemp Phys. 1997;38:205–241.
Kearns DB, Losick R. Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol. 2003;49:581–590.
Harshey RM, Matsuyama T. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface‐induced differentiation into hyperflagellate swarmer cells. Proc. Natl Acad Sci. 1994;91:8631–8635.
Köhler T, Curty LK, Barja F, van Delden C, Pechère JC. Swarming of Pseudomonas aeruginosa is dependent on cell‐to‐cell signaling and requires flagella and pili. J Bacteriol. 2000;182:5990–5996.
Zhang R, Turner L, Berg HC. The upper surface of an Escherichia coli swarm is stationary. Proc Natl Acad Sci. 2010;107:288–290.
Roberts JL. A new species of the genus Bacillus exhibiting mobile colonies on the surface of nutrient agar. J Bacteriol. 1935;29:229–237.
Shinn LE. A cinematographic analysis of the motion of colonies of B. alvei. J Bacteriol. 1938;36:419–422.
Kobayashi K, Kanesaki Y, Yoshikawa H. Genetic analysis of collective motility of Paenibacillus sp. NAIST15‐1. PLoS Genet. 2016;12:e1006387.
Ingham CJ, Jacob E. Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiol. 2008;8:36.
Sakka K, Kihira M, Kuhara W, Mochida A, Kimura T, Sakka M. Swarming behavior of a novel strain of Brevibacillus thermoruber. J Basic Microbiol. 2022;62:1475–1486.
Leifson E. Staining, shape, and arrangement of bacterial flagella. J Bacteriol. 1951;62:377–389.
Bray DF, Bagu J, Koegler P. Comparison of hexamethyldisilazane (HMDS), peldri II, and critical‐point drying methods for scanning electron microscopy of biological specimens. Microsc Res Tech. 1993;26:489–495.
Araujo JC. Comparison of hexamethyldisilazane and critical point drying treatments for SEM analysis of anaerobic biofilms and granular sludge. J Electron Microsc. 2003;52:429–433.
Bodour AA, Miller‐Maier RM. Application of a modified drop‐collapse technique for surfactant quantitation and screening of biosurfactant‐producing microorganisms. J Microbiol Meth. 1998;32:273–280.
Daniels R, Reynaert S, Hoekstra H, Verreth C, Janssens J, Braeken K, et al. Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli. Proc Natl Acad Sci. 2006;103:14965–14970.
Murray RGE, Elder RH. The predominance of counterclockwise rotation during swarming of Bacillus species. J Bacteriol. 1949;58:351–359.
Yamamoto H, Fukasawa Y, Shoji Y, Hisamoto S, Kikuchi T, Takamatsu A, et al. Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES‐4403. BMC Microbiol. 2021;21:227.
McCarter LL. Polar flagellar motility of the Vibrionaceae. Microbiol Mol Biol Rev. 2001;65:445–462.
DiLuzio WR, Turner L, Mayer M, Garstecki P, Weibel DB, Berg HC, et al. Escherichia coli swim on the right‐hand side. Nature. 2005;435:1271–1274.
Lauga E, DiLuzio WR, Whitesides GM, Stone HA. Swimming in circles: motion of bacteria near solid boundaries. Biophys J. 2006;90:400–412.

Auteurs

Kazuo Sakka (K)

Graduate School of Bioresources, Mie University, Tsu, Japan.

Masaki Kihira (M)

Iga Research Center, Mie University, Iga, Japan.

Wataru Kuhara (W)

Kinki Kankyo Service Co., Ltd., Nabari, Japan.

Akihiro Mochida (A)

Kinki Kankyo Service Co., Ltd., Nabari, Japan.

Satoru Ogawa (S)

Graduate School of Medicine, Mie University, Tsu, Japan.

Tetsuya Kimura (T)

Graduate School of Bioresources, Mie University, Tsu, Japan.

Makiko Sakka (M)

Graduate School of Bioresources, Mie University, Tsu, Japan.
Kinki Kankyo Service Co., Ltd., Nabari, Japan.

Classifications MeSH