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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.


(A) time-lapse images of aggregation of multicell-ensheathed fragments. The aggregated fragments increased in number with time (older: red; younger: yellow arrowheads). These aggregated fragments developed into visible sheath clumps within the next 4–5 h. Note that a fragment (arrow) began to elongate again, nearly doubling in length within about 1 h 40 min (frames b and e); (B) TEM image of the fragments covered with sheath layers.
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biology-05-00032-f005: (A) time-lapse images of aggregation of multicell-ensheathed fragments. The aggregated fragments increased in number with time (older: red; younger: yellow arrowheads). These aggregated fragments developed into visible sheath clumps within the next 4–5 h. Note that a fragment (arrow) began to elongate again, nearly doubling in length within about 1 h 40 min (frames b and e); (B) TEM image of the fragments covered with sheath layers.

Mentions: To understand whether these moving multicell-ensheathed fragments were involved in sheath clump formation, we monitored the moving multicell-ensheathed fragments around the sheath clump at 5 min intervals for 20 h (see Video S2 in the Supplemental Material). At a seemingly random time, the motile multicell-ensheathed fragments gradually aggregated to form a clump of fragments (Figure 5A, red and yellow arrowheads) that increased in number within 10–20 min. Once in the clump, the fragments notably began to elongate again (Figure 5, arrows). The number of cells in a fragment increased from six (Figure 5A (b), arrow) to at least 11 (Figure 5A (e)) within 1 h 38 min, amounting to sheath fragment elongation of approximately 0.15 µm/min. Such rapid elongation of multicell-ensheathed fragments plausibly reflects the rapid cell proliferation of Leptothrix species. These observations agree with earlier reports on rapid cell proliferation (0.28 µm/min) and sheath elongation (0.01–0.04 µm/min) of L. ochracea [5] and L. cholodnii [7]. TEM observations confirmed the presence of sheaths around these moving multicell-ensheathed fragments (Figure 5B).


Dissociation and Re-Aggregation of Multicell-Ensheathed Fragments Responsible for Rapid Production of Massive Clumps of Leptothrix Sheaths
(A) time-lapse images of aggregation of multicell-ensheathed fragments. The aggregated fragments increased in number with time (older: red; younger: yellow arrowheads). These aggregated fragments developed into visible sheath clumps within the next 4–5 h. Note that a fragment (arrow) began to elongate again, nearly doubling in length within about 1 h 40 min (frames b and e); (B) TEM image of the fragments covered with sheath layers.
© Copyright Policy
Related In: Results  -  Collection

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

biology-05-00032-f005: (A) time-lapse images of aggregation of multicell-ensheathed fragments. The aggregated fragments increased in number with time (older: red; younger: yellow arrowheads). These aggregated fragments developed into visible sheath clumps within the next 4–5 h. Note that a fragment (arrow) began to elongate again, nearly doubling in length within about 1 h 40 min (frames b and e); (B) TEM image of the fragments covered with sheath layers.
Mentions: To understand whether these moving multicell-ensheathed fragments were involved in sheath clump formation, we monitored the moving multicell-ensheathed fragments around the sheath clump at 5 min intervals for 20 h (see Video S2 in the Supplemental Material). At a seemingly random time, the motile multicell-ensheathed fragments gradually aggregated to form a clump of fragments (Figure 5A, red and yellow arrowheads) that increased in number within 10–20 min. Once in the clump, the fragments notably began to elongate again (Figure 5, arrows). The number of cells in a fragment increased from six (Figure 5A (b), arrow) to at least 11 (Figure 5A (e)) within 1 h 38 min, amounting to sheath fragment elongation of approximately 0.15 µm/min. Such rapid elongation of multicell-ensheathed fragments plausibly reflects the rapid cell proliferation of Leptothrix species. These observations agree with earlier reports on rapid cell proliferation (0.28 µm/min) and sheath elongation (0.01–0.04 µm/min) of L. ochracea [5] and L. cholodnii [7]. TEM observations confirmed the presence of sheaths around these moving multicell-ensheathed fragments (Figure 5B).

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.