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

Abstract

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.

The dgc2 gene encoding di-guanylate cyclase suppresses both motility and biofilm formation in the filamentous cyanobacterium Leptolyngbya boryana

“…S3C) indicate the passage of wandering comets. Although comet-like clusters in Pseudanabaena was proposed to be a pioneer in traveling to virgin area on the solid surface (18), in L. boryana comet-like cluster was observed to move exclusively on already existing passages. Their speed of movement is not constant, and some clusters were observed to collapse suddenly.…”

“…Many of the disks rotated steadily over 400 min as indicated by periodically fluctuating profile on the kymograph as is observed for Pseudanabaena sp. NIES-4403 (18) On the other hand, disk-like clusters in Paenibacillus sp. NAIST15-1 immediately stops rotating after forming large vortices (22).…”

“…In Oscillatoria and N. punctiforme, especially, staining of the trajectory of the filaments as they pass through with india ink has been established to show remaining mucus-like substance on trails (9, 42; 43; ). The presence of EPS was confirmed in N. punctiforme and Pseudanabaena using fluorescent dye-conjugated lectin subunits, RCA-120 (9,18). Thus, we examined both the india ink assay and the RCA-120 staining in L. boryana.…”

“…We recently reported that the filamentous cyanobacterium, Pseudanabaena sp. NIES-4403 (hereafter, Pseudanabaena) generates highdensity migrating clusters, which were categorized into comet-like wandering and disk-like rotating clusters (18). The combination of these wandering and rotating clusters has been reported in Bacillus (19, 20; ), Paenibacillus vortex in the presence of mitomycin C (21), and in Paenibacillus sp.…”

“…NAIST15-1 (22). Our previous observations suggested in Pseudanabaena that the following processes are key to generate the wandering and rotating clusters: (1) follow-up motion of bacterial filaments via polysaccharide secretion or groove formation on the solid-phase surface, (2) formation of bundles with nematic alignment, (3) formation of comet-like clusters accompanied by the creation of a cover of filaments at the tip in the direction of travelling, (4) formation of rotating disks by spontaneous self-tracking of comet-like clusters, and (5) transition based on collisions between different types of clusters (18). Nevertheless, molecular details of generating these colony patterns remain largely unknown: genetic study has been limited to Paenibacillus sp.…”