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Dissociation and Re-Aggregation of Multicell-Ensheathed Fragments Responsible for Rapid Production of Massive Clumps of Leptothrix Sheaths

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ABSTRACT

Species of the Fe/Mn-oxidizing bacteria Leptothrix produce tremendous amounts of microtubular, Fe/Mn-encrusted sheaths within a few days in outwells of groundwater that can rapidly clog water systems. To understand this mode of rapid sheath production and define the timescales involved, behaviors of sheath-forming Leptothrix sp. strain OUMS1 were examined using time-lapse video at the initial stage of sheath formation. OUMS1 formed clumps of tangled sheaths. Electron microscopy confirmed the presence of a thin layer of bacterial exopolymer fibrils around catenulate cells (corresponding to the immature sheath). In time-lapse videos, numerous sheath filaments that extended from the periphery of sheath clumps repeatedly fragmented at the apex of the same fragment, the fragments then aggregated and again elongated, eventually forming a large sheath clump comprising tangled sheaths within two days. In this study, we found that fast microscopic fragmentation, dissociation, re-aggregation and re-elongation events are the basis of the rapid, massive production of Leptothrix sheaths typically observed at macroscopic scales.

No MeSH data available.


SEM and TEM images of cells encased with the sheath cultured in SGP. (A) surface of the cell chain covered with a thin immature sheath of woven fibrils; (B) thin layers (corresponding to immature sheaths) (arrows) across an intervening space away from the cells. Inset shows wavy cell surfaces with globular projections (arrowhead) and an immature sheath of woven fibrils.
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biology-05-00032-f002: SEM and TEM images of cells encased with the sheath cultured in SGP. (A) surface of the cell chain covered with a thin immature sheath of woven fibrils; (B) thin layers (corresponding to immature sheaths) (arrows) across an intervening space away from the cells. Inset shows wavy cell surfaces with globular projections (arrowhead) and an immature sheath of woven fibrils.

Mentions: SEM indicated that surfaces of chained cells were covered with aggregated woven fibrils (Figure 2A), and TEM demonstrated that the chained cells were surrounded by a thin (ca. 50 nm) layer of nearly parallel fibrils (Figure 2B, arrows). A few globular projections (Figure 2B, inset) emerged from the cell surface, consistent with the previous observation in a one-day culture of OUMS1 of a globular and/or thread-like secretion on the surface of the outer membrane of the bacterial cell [14]; these secreted bodies form an immature sheath skeleton comprising aggregated and intermingled fibrils [8]. The surface structure of the sheath in the SEM image appeared to be winkled and shrunk, whereas in the TEM image the surface appeared rather flat. These differing images between the two types of electron microscopy could be due to artifacts created by sample preparation protocols; Dolnalkova et al. [15] emphasized that polymer collapse induced by dehydration could lead to inaccurate spatial relationships and thus affect conclusions regarding the nature of interactions between microbial extracellular polymers and their environment.


Dissociation and Re-Aggregation of Multicell-Ensheathed Fragments Responsible for Rapid Production of Massive Clumps of Leptothrix Sheaths
SEM and TEM images of cells encased with the sheath cultured in SGP. (A) surface of the cell chain covered with a thin immature sheath of woven fibrils; (B) thin layers (corresponding to immature sheaths) (arrows) across an intervening space away from the cells. Inset shows wavy cell surfaces with globular projections (arrowhead) and an immature sheath of woven fibrils.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5037351&req=5

biology-05-00032-f002: SEM and TEM images of cells encased with the sheath cultured in SGP. (A) surface of the cell chain covered with a thin immature sheath of woven fibrils; (B) thin layers (corresponding to immature sheaths) (arrows) across an intervening space away from the cells. Inset shows wavy cell surfaces with globular projections (arrowhead) and an immature sheath of woven fibrils.
Mentions: SEM indicated that surfaces of chained cells were covered with aggregated woven fibrils (Figure 2A), and TEM demonstrated that the chained cells were surrounded by a thin (ca. 50 nm) layer of nearly parallel fibrils (Figure 2B, arrows). A few globular projections (Figure 2B, inset) emerged from the cell surface, consistent with the previous observation in a one-day culture of OUMS1 of a globular and/or thread-like secretion on the surface of the outer membrane of the bacterial cell [14]; these secreted bodies form an immature sheath skeleton comprising aggregated and intermingled fibrils [8]. The surface structure of the sheath in the SEM image appeared to be winkled and shrunk, whereas in the TEM image the surface appeared rather flat. These differing images between the two types of electron microscopy could be due to artifacts created by sample preparation protocols; Dolnalkova et al. [15] emphasized that polymer collapse induced by dehydration could lead to inaccurate spatial relationships and thus affect conclusions regarding the nature of interactions between microbial extracellular polymers and their environment.

View Article: PubMed Central - PubMed

ABSTRACT

Species of the Fe/Mn-oxidizing bacteria Leptothrix produce tremendous amounts of microtubular, Fe/Mn-encrusted sheaths within a few days in outwells of groundwater that can rapidly clog water systems. To understand this mode of rapid sheath production and define the timescales involved, behaviors of sheath-forming Leptothrix sp. strain OUMS1 were examined using time-lapse video at the initial stage of sheath formation. OUMS1 formed clumps of tangled sheaths. Electron microscopy confirmed the presence of a thin layer of bacterial exopolymer fibrils around catenulate cells (corresponding to the immature sheath). In time-lapse videos, numerous sheath filaments that extended from the periphery of sheath clumps repeatedly fragmented at the apex of the same fragment, the fragments then aggregated and again elongated, eventually forming a large sheath clump comprising tangled sheaths within two days. In this study, we found that fast microscopic fragmentation, dissociation, re-aggregation and re-elongation events are the basis of the rapid, massive production of Leptothrix sheaths typically observed at macroscopic scales.

No MeSH data available.