TY - JOUR
T1 - Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403
AU - Yamamoto, Hiroki
AU - Fukasawa, Yuki
AU - Shoji, Yu
AU - Hisamoto, Shumpei
AU - Kikuchi, Tomohiro
AU - Takamatsu, Atsuko
AU - Iwasaki, Hideo
N1 - Funding Information:
We thank the members of Iwasaki and Takamatsu laboratories and metaPhorest bioaesthetics platform for their valuable discussion, especially Keita Tanaka, Taku Saito and Taku Kimura for sharing preliminary results and Kazuma Toida for critical reading of the manuscript. We also thank Fumi Mori (National Institute for Environmental Studies) and Yu Hirose (Toyohashi University of Technology) for their help on the NIES culture collection.
Funding Information:
This work was supported by Grants-in-Aid from the Japanese Society for Promotion of Sciences (22520150, 25650111, 19 K21608 to HI; 23127511 and 25127717 to AT). The funding bodies had no role in the design of the study, collection, analysis, and interpretation of data and in writing the manuscript.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - 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.
AB - 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.
KW - Cell motility
KW - Collective behavior
KW - Colony pattern formation
KW - Cyanobacteria
UR - http://www.scopus.com/inward/record.url?scp=85113135856&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85113135856&partnerID=8YFLogxK
U2 - 10.1186/s12866-021-02183-5
DO - 10.1186/s12866-021-02183-5
M3 - Article
C2 - 34399691
AN - SCOPUS:85113135856
SN - 1471-2180
VL - 21
JO - BMC Microbiology
JF - BMC Microbiology
IS - 1
M1 - 227
ER -