Ultrastructure of ellipsoidal magnetotactic multicellular prokaryotes depicts their complex assemblage and cellular polarity in the context of magnetotaxis

Abstract

Magnetotactic multicellular prokaryotes (MMPs) consist of unique microorganisms formed by genetically identical Gram-negative bacterial that live as a single individual capable of producing magnetic nano-particles called magnetosomes. Two distinct morphotypes of MMPs are known: spherical MMPs (sMMPs) and ellipsoidal MMPs (eMMPs). sMMPs have been extensively characterized, but less information exists for eMMPs. Here, we report the ultrastructure and organization as well as gene clusters responsible for magnetosome and flagella biosynthesis in the magnetite magnetosome producer eMMP Candidatus Magnetananas rongchenensis. Transmission electron microscopy and focused ion beam scanning electron microscopy (FIB-SEM) 3D reconstruction reveal that cells with a conspicuous core-periphery polarity were organized around a central space. Magnetosomes were organized in multiple chains aligned along the periphery of each cell. In the partially sequenced genome, magnetite-related mamAB gene and mad gene clusters were identified. Two cell morphologies were detected: irregular elliptical conical 'frustum-like' (IECF) cells and H-shaped cells. IECF cells merge to form H-shaped cells indicating a more complex structure and possibly a distinct evolutionary position of eMMPs when compared with sMMPs considering multicellularity.

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes

“…Here, we used HPF/FS, for the first time, in combination with TEM and fluorescence confocal microscopy to study the ultrastructure of MMPs. As previously reported (Leao et al, 2017) but with more detail, we observed the conspicuous periphery-core architecture ( Fig. 3A, B, C, E and G), an axisymmetrical arrangement of cells along the eMMP longitudinal axis (Fig.…”

“…B). Interestingly, the genes involved in magnetosome biosynthesis are well conserved among uni‐ and multicellular MTB from the Deltaproteobacteria class (Leao et al ., ). This result cannot distinguish between acquisitions by non‐magnetic multicellular microbes of magnetosome coding genes via horizontal gene transfer from evolution of MMPs from unicellular magnetotactic Deltaproteobacteria .…”

“…Previously, we have reported the architecture of ellipsoidal MMPs using fluorescence microscopy, transmission electron microscope (TEM), scan electron microscope (SEM) and focused ion beam SEM (FIB-SEM) (Zhou et al, 2012;Chen et al, 2015Chen et al, , 2016Leao et al, 2017). Approximately 40-80 cells arrange in interlacing circles with a pineapple-like ellipsoidal morphology.…”

Culture‐independent characterization of a novel magnetotactic member affiliated to the Beta class of the Proteobacteria phylum from an acidic lagoon

“…Because the cytoplasmic pH in MTB collected from the acidic sediment was close to neutral in all MTB morphotypes (except for the intracellular granules produced by some MTB) as evidenced by the intracellular pH assay, these organisms likely have an efficient mechanism of maintaining the intracellular pH close to neutrality as do known acidophiles (Dopson et al, 2017). Lipid, sulfur and phosphorus-rich granules are commonly described in MTB (Lefèvre et al, 2010;Lefèvre et al, 2012;Leão et al, 2017). All these granules can have an acidic pH depending on the storaged compound(s) chemical form.…”

Effect of applied magnetic fields on motility and magnetotaxis in the uncultured magnetotactic multicellular prokaryote ‘CandidatusMagnetoglobus multicellularis’

“…Several MMP species have been described at the level of 'Candidatus', most of them showing spherical shapes, and a few exhibiting ellipsoidal morphologies. Despite morphological differences, they show coherent phylogeny, structure, life cycle and behaviour (Keim et al, 2004a;Abreu et al, 2007;Zhou et al, 2012;Chen et al, 2015;Kolinko et al, 2014;Zhang et al, 2014;Chen et al, 2016;Leão et al, 2017). MMPs are motile only when forming the multicellular ensemble, whereas detached cells are immotile and probably dead .…”