Characterization of swimming motility in a marine unicellular cyanobacterium
Characterization of swimming motility in a marine unicellular cyanobacterium
Date
1988-04
Authors
Willey, Joanne M.
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DOI
10.1575/1912/4317
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Cyanobacteria
Abstract
The structural mechanism, behavior, energetics and functional
significance of the unique swimming motility displayed by some oceanic
isolates of the cyanobacterium Synechococcus was investigated. A variety
of analytical techniques confirmed that these strains swam
through liquids without flagella or flagellar-like appendages. No
extracellular structures were observed in a broad range of cell preparations
examined by transmission electron microscopy (TEM), or by
high-intensity dark field microscopy. The possibility that a structure
might be present that eluded visualization was eliminated by the
lack of motility-dependent amplitude spectra, the absence of discrete
circulation of microspheres around the cell body and the
inability of shearing forces to arrest motility. TEM and gel
electrophoretic analysis of spheroplasts, cell wall-enriched fractions
from motile and nonmotile strains, and cell material collected following
the application of a flagellar hook-basal body complex isolation
technique to a motile Synechococcus strain provided no further evidence
of a structure or protein unique to motile strains.
The motile Synechococcus strains represent the only
cyanobacterium reported to date capable of swimming rather than
gliding motility. Swimming behavior was characterized by several
features: between 50 - 80% of cells were actively motile during
loyarithmic phase of growth, with speeds that ranged from 5 - 40 um
s-1 the average speed was 13 um s-1. Swimming patterns were
entirely random, consistent with the absence of bacterial flagella.
Synechococcus motility resembled flagellar-mediated motility in that
thrust (forward motion) was accompanied by torque (cell rotation) as
demonstrated by i) dividing cells which swam with the daughter cells
at an angle, ii) individual cells that were sometimes seen to rotate
end over end at a rate of 3 to 5 rev s-1, iii) polystyrene beads
attached to the cell body served as a point of reference as the cell
rotated concomitant with translocation and iv) cells attached to the
coverslip or slide spun about one pole at an average rate of 1 rev
s-1. When observed in the same plane of focus, 50% of the cells
spun clockwise and 50% spun counterclockwise, but unlike flagellated
cells, Synechococcus was never seen to change direction of rotation,
as would be predicted if the cell body were rotating as a single unit
and the motility apparatus were incapable of reversing direction of
rotation. This motility apparatus appeared to operate at a constant
torque, as indicated by the relationship between swimming speeds and
the fluidity of the surrounding medium.
Investigation of the energetics of motility in Synechococcus
WH8ll3 demonstrated that swimming was sodium coupled. There was a
specific sodium requirement such that cells were immotile at external
sodium concentrations below 10 mM, with speeds increasing with
increasing sodium to a maximum speed at 150 to 250mM sodium, pH 8.0
to 8.5. The sodium motive force increased similarly, but other
energetic parameters including proton motive force, electrical potential,
and the proton and sodium diffusion gradients lacked correlation
to levels of motility. When components of the sodium motive force
were diminished by monensin or carbonyl cyanide m-chlorophenyl-hydrazone,
motility was arrested. Motility was independent of the
magnitude of internal ATP pools, which were depleted to 2% of control
values without affecting cell motility. These results suggest that
the direct source of energy for Synechococcus motility is a sodium
motive force, and that the devise driving motility is located in the
cytoplasmic membrane, as is the case for flagellated bacteria.
The ecological role of Synechococcus motility was explored and
several lines of evidence indicated that cells lacked behavioral
photoresponses but were able to detect and respond to very low concentrations
of simple nitrogenous compounds. When 23 compounds were
tested in spatial gradients established in blind well chemotaxis chambers,
cells displayed positive chemoresponses only when placed in
gradients of NH4Cl, NaN03, urea, glycine and alanine. Cells
also failed to respond in chambers which lacked gradients due to the
presence of only seawater or an equal distribution of chemoeffector,
demonstrating that a gradient was required to elicit a response. The
apparent threshold levels of 10-10 M - 10-9 M for Synechococcus
chemoresponses are 4 to 5 orders of magnitude lower than those for
most other bacteria and place them in the range of ecological significance.
The presence of chemotaxis in this oceanic cyanobacterium may
help support the notion that nutrient enriched microaggregates may
play an important role in picoplankton nutrient dynamics.
Description
Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution April 1988
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Citation
Willey, J. M. (1988). Characterization of swimming motility in a marine unicellular cyanobacterium [Doctoral thesis, Massachusetts Institute of Technology and Woods Hole Oceanographic Institution]. Woods Hole Open Access Server. https://doi.org/10.1575/1912/4317