Abstract
The cell biology of Chloroflexota is poorly studied. We applied cryo-focused ion beam milling and cryo-electron tomography to study the ultrastructural organization of thermophilic Roseiflexus castenholzii and Chloroflexus aggregans, and mesophilic “Ca. Viridilinea mediisalina.” These species represent the three main lineages within a group of multicellular filamentous anoxygenic phototrophic Chloroflexota bacteria belonging to the Chloroflexales order. We found surprising structural complexity in the Chloroflexales. As with filamentous cyanobacteria, cells of C. aggregans and “Ca. Viridilinea mediisalina” share the outer membrane-like layers of their intricate multilayer cell envelope. Additionally, cells of R. castenholzii and “Ca. Viridilinea mediisalina” are connected by septal channels that resemble cyanobacterial septal junctions. All three strains possess long pili anchored close to cell-to-cell junctions, a morphological feature comparable to that observed in cyanobacteria. The cytoplasm of the Chloroflexales bacteria is crowded with intracellular organelles such as different types of storage granules, membrane vesicles, chlorosomes, gas vesicles, chemoreceptor-like arrays, and cytoplasmic filaments. We observed a higher level of complexity in the mesophilic strain compared to the thermophilic strains with regards to the composition of intracellular bodies and the organization of the cell envelope. The ultrastructural details that we describe in these Chloroflexales bacteria will motivate further cell biological studies, given that the function and evolution of the many discovered morphological traits remain enigmatic in this diverse and widespread bacterial group.
Highlights
There are only two groups of filamentous multicellular phototrophic bacteria: a polyphyletic group of filamentous cyanobacteria and green non-sulfur bacteria, which belong to the Cyanobacteria and Chloroflexota (Chloroflexi) phyla, respectively
“Ca. Viridilinea mediisalina,” C. aggregans, and R. castenholzii, showed a typical filamentous multicellular morphology when observed under an optical microscope (Figure 1A)
Our tomograms revealed that both “Ca. Viridilinea mediisalina” and C. aggregans showed an obvious didermlike cell envelope, whereas the organization of the cell envelope was different in R. castelholzii
Summary
There are only two groups of filamentous multicellular phototrophic bacteria: a polyphyletic group of filamentous cyanobacteria and green non-sulfur bacteria, which belong to the Cyanobacteria and Chloroflexota (Chloroflexi) phyla, respectively. Despite green non-sulfur bacteria and filamentous cyanobacteria being phylogenetically distant lineages that have many differences in their biology, Cryo-ET on Chloroflexi their phenotypes often share many significant similarities that are adapted to specific ecological niches. Their multicellular filaments often form a dense “fabric” of cyanobacterial mats or biofilms (Bauld and Brock, 1973; Doemel and Brock, 1977; Ley et al, 2006; Gaisin et al, 2015). 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 on the multicellular organization of the phototrophic bacteria
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