Gliding motility driven by individual cell-surface movements in a multicellular filamentous bacteriumChloroflexus aggregans

Abstract

Chloroflexus aggregans is an unbranched multicellular filamentous bacterium having the ability of gliding motility. The filament moves straightforward at a constant rate, ∼3 μm sec(-1) on solid surface and occasionally reverses the moving direction. In this study, we successfully detected movements of glass beads on the cell-surface along long axis of the filament indicating that the cell-surface movement was the direct force for gliding. Microscopic analyses found that the cell-surface movements were confined to a cell of the filament, and each cell independently moved and reversed the direction. To understand how the cellular movements determine the moving direction of the filament, we proposed a discrete-time stochastic model; sum of the directions of the cellular movements determines the moving direction of the filament only when the filament pauses, and after moving, the filament keeps the same directional movement until all the cells pause and/or move in the opposite direction. Monte Carlo simulation of this model showed that reversal frequency of longer filaments was relatively fixed to be low, but the frequency of shorter filaments varied widely. This simulation result appropriately explained the experimental observations. This study proposed the relevant mechanism adequately describing the motility of the multicellular filament in C. aggregans.

Cryo-Electron Tomography Reveals the Complex Ultrastructural Organization of Multicellular Filamentous Chloroflexota (Chloroflexi) Bacteria

“…Chloroflexales bacteria also possess extracellular appendages such as pili. Long pili have been previously reported in C. aggregans and C. islandicus (Fukushima, 2016;Gaisin et al, 2017). Here, we show that they were also present in R. castenholzii and "Ca.…”

“…It resembled typical bacterial chemoreceptor arrays (Briegel et al, 2009). Previously, Fukushima et al suggested that C. aggregans was capable of aerotaxis (Fukushima, 2016), and a chemotaxis system in Chloroflexales has been predicted by genomic analysis (Wuichet and Zhulin, 2010). These previous findings and the images of chemoreceptor-like arrays presented here show that Chloroflexales bacteria are adapted to active translocation in their environment.…”

“…The results presented here allow for a deeper understanding of the cell biology of Chloroflexales , as well as Chloroflexota bacteria in general. Particularly, these data provide new information to the debate surrounding the organization of the cell envelope in Chloroflexota ( Sutcliffe, 2011 ; Cavalier-Smith and Chao, 2020 ), the mechanism of their motility and adherence ( Fukushima et al, 2016 ; Fukushima, 2016 ), and finally on the multicellular organization of the phototrophic bacteria.…”

Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

“…These Tepidiforma isolates are the only three members of the Chloroflexota known to possess flagella. Many cultivated members of the Chloroflexota are considered non-motile (e.g., 7,33,34 ), although gliding motility in this phylum is well known, particularly in the filamentous Chloroflexia 9,[35][36][37][38] . Despite these observations based on isolates of Chloroflexota, environmental genomics studies have improved representation of the diversity across the phylum and revealed flagellar gene clusters in some Chloroflexota genomes 16,35,[39][40][41] .…”

Tree of motility – A proposed history of motility systems in the tree of life

“…Wartel, Brochier-Armanet, & Mignot, 2015;Mercier & Mignot, 2016;Nan, McBride, Chen, Zusman, & Oster, 2014) typified by the A motility of Myxococcus xanthus (Figure 1; type 3) (Agrebi et al, 2015;Mercier & Mignot, 2016;Nan et al, 2014), the gliding motility of Bacteroidetes (Figure 1; type 4) (McBride & Nakane, 2015;Nakane, Sato, Wada, McBride, & Nakayama, 2013;Wada, Nakane, & Chen, 2013) represented by Flavobacterium johnsoniae, and the surface motion of thermophilic filamentous bacteria Chloroflexus aggregans classified as phylum Chloroflexi (Figure 1; type 5) (Fukushima, Morohoshi, Hanada, Matsuura, & Haruta, 2016;Hanada, Shimada, & Matsuura, 2002). Spirochete swimming is a variation of the flagellar swimming described above, but achieves a smooth motion by placing flagella inside the outer membrane, in the periplasmic space (Figure 1; type 1b) (Charon et al, 2012;Charon & Goldstein, 2002;Li et al, 2000;Takabe, Kawamoto, Tahara, Kudo, & Nakamura, 2017).…”