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Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403
BACKGROUND: Bacteria have been reported to exhibit complicated morphological colony patterns on solid media, depending on intracellular, and extracellular factors such as motility, cell propagation, and cell-cell interaction. We isolated the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 (P...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8365994/ https://www.ncbi.nlm.nih.gov/pubmed/34399691 http://dx.doi.org/10.1186/s12866-021-02183-5 |
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author | Yamamoto, Hiroki Fukasawa, Yuki Shoji, Yu Hisamoto, Shumpei Kikuchi, Tomohiro Takamatsu, Atsuko Iwasaki, Hideo |
author_facet | Yamamoto, Hiroki Fukasawa, Yuki Shoji, Yu Hisamoto, Shumpei Kikuchi, Tomohiro Takamatsu, Atsuko Iwasaki, Hideo |
author_sort | Yamamoto, Hiroki |
collection | PubMed |
description | BACKGROUND: Bacteria have been reported to exhibit complicated morphological colony patterns on solid media, depending on intracellular, and extracellular factors such as motility, cell propagation, and cell-cell interaction. We isolated the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 (Pseudanabaena, hereafter), that forms scattered (discrete) migrating colonies on solid media. While the scattered colony pattern has been observed in some bacterial species, the mechanism underlying such a pattern still remains obscure. RESULTS: We studied the morphology of Pseudanabaena migrating collectively and found that this species forms randomly scattered clusters varying in size and further consists of a mixture of comet-like wandering clusters and disk-like rotating clusters. Quantitative analysis of the formation of these wandering and rotating clusters showed that bacterial filaments tend to follow trajectories of previously migrating filaments at velocities that are dependent on filament length. Collisions between filaments occurred without crossing paths, which enhanced their nematic alignments, giving rise to bundle-like colonies. As cells increased and bundles aggregated, comet-like wandering clusters developed. The direction and velocity of the movement of cells in comet-like wandering clusters were highly coordinated. When the wandering clusters entered into a circular orbit, they turned into rotating clusters, maintaining a more stable location. Disk-like rotating clusters may rotate for days, and the speed of cells within a rotating cluster increases from the center to the outmost part of the cluster. Using a mathematical modeling with simplified assumption we reproduced some features of the scattered pattern including migrating clusters. CONCLUSION: Based on these observations, we propose that Pseudanabaena forms scattered migrating colonies that undergo a series of transitions involving several morphological patterns. A simplified model is able to reproduce some features of the observed migrating clusters. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02183-5. |
format | Online Article Text |
id | pubmed-8365994 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-83659942021-08-17 Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 Yamamoto, Hiroki Fukasawa, Yuki Shoji, Yu Hisamoto, Shumpei Kikuchi, Tomohiro Takamatsu, Atsuko Iwasaki, Hideo BMC Microbiol Research Article BACKGROUND: Bacteria have been reported to exhibit complicated morphological colony patterns on solid media, depending on intracellular, and extracellular factors such as motility, cell propagation, and cell-cell interaction. We isolated the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 (Pseudanabaena, hereafter), that forms scattered (discrete) migrating colonies on solid media. While the scattered colony pattern has been observed in some bacterial species, the mechanism underlying such a pattern still remains obscure. RESULTS: We studied the morphology of Pseudanabaena migrating collectively and found that this species forms randomly scattered clusters varying in size and further consists of a mixture of comet-like wandering clusters and disk-like rotating clusters. Quantitative analysis of the formation of these wandering and rotating clusters showed that bacterial filaments tend to follow trajectories of previously migrating filaments at velocities that are dependent on filament length. Collisions between filaments occurred without crossing paths, which enhanced their nematic alignments, giving rise to bundle-like colonies. As cells increased and bundles aggregated, comet-like wandering clusters developed. The direction and velocity of the movement of cells in comet-like wandering clusters were highly coordinated. When the wandering clusters entered into a circular orbit, they turned into rotating clusters, maintaining a more stable location. Disk-like rotating clusters may rotate for days, and the speed of cells within a rotating cluster increases from the center to the outmost part of the cluster. Using a mathematical modeling with simplified assumption we reproduced some features of the scattered pattern including migrating clusters. CONCLUSION: Based on these observations, we propose that Pseudanabaena forms scattered migrating colonies that undergo a series of transitions involving several morphological patterns. A simplified model is able to reproduce some features of the observed migrating clusters. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02183-5. BioMed Central 2021-08-16 /pmc/articles/PMC8365994/ /pubmed/34399691 http://dx.doi.org/10.1186/s12866-021-02183-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Yamamoto, Hiroki Fukasawa, Yuki Shoji, Yu Hisamoto, Shumpei Kikuchi, Tomohiro Takamatsu, Atsuko Iwasaki, Hideo Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title | Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title_full | Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title_fullStr | Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title_full_unstemmed | Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title_short | Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 |
title_sort | scattered migrating colony formation in the filamentous cyanobacterium, pseudanabaena sp. nies-4403 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8365994/ https://www.ncbi.nlm.nih.gov/pubmed/34399691 http://dx.doi.org/10.1186/s12866-021-02183-5 |
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