Scattered migrating colony formation in the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403

Hiroki Yamamoto,Hideo Iwasaki,Shumpei Hisamoto,Yuki Fukasawa,Yu Shoji,Tomohiro Kikuchi,Atsuko Takamatsu

doi:10.1186/s12866-021-02183-5

Abstract

BackgroundBacteria 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.ResultsWe 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.ConclusionBased 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.

Highlights

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 refer to migrating clusters consisting of high-density bacterial filaments that maintain their unity with a constant comet-like shape and move basically in a straight line while occasionally changing direction as wandering clusters
We describe the morphology of colony pattern formation based on the collective behaviors of the filamentous cyanobacterium, Pseudanabaena sp

Summary

Introduction

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. A moving cluster consisting of high-density filaments that maintains a high degree of unity and continues to move in a rotational motion forming a circular orbit is called a (disk-like) rotating cluster. These colony patterns have been analyzed in detail, mainly in Bacillus and Paenibacillus species. Myxococcus xanthus is a bacterium that forms large moving clusters such as vortices, bundled circular patterns, side-by-side clusters, and rafts [15, 16] In this species, EPS associated with the pilus [17, 18] and its trail [19] and its ability to reverse directions [16, 20] have been suggested to contribute to cluster formation via cell-cell interaction

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Conclusion