Terminal Electron Acceptors Influence the Quantity and Chemical Composition of Capsular Exopolymers Produced by Anaerobically Growing Shewanella spp.
Andrew L. Neal,*,† Steven N. Dublin‡, Jeanette Taylor‡, David J. Bates§, Justin L. Burns§, Robert Apkarian‡, and Thomas J. DiChristina§
Savannah River Ecology Laboratory, The University of Georgia, Aiken, South Carolina 29802, The Integrated Microscopy and Microanalytical Facility, Emory University, Atlanta, Georgia 30322, and School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332
Abstract
Bacterial exopolymers perform various roles, including acting as a carbon
sink, a protective layer against desiccation or antimicrobial agents,
or a structural matrix in biofilms. Despite such varied roles, little
is known about the heterogeneity of bacterial exopolymer production under
varying growth conditions. Here we describe experiments designed to characterize
the quantity and quality of exopolymers produced by two commonly studied
members of the widely distributed genus Shewanella. Electrokinetic,
spectroscopic, and electron microscopic techniques were employed to demonstrate
that cell surfaces of Shewanella oneidensis MR-1 (electrophoretic
softness, lower case Lambda -1, range from 0.4 to 2.6 nm) are
associated with less extracellular polymeric material than surfaces of
Shewanella putrefaciens 200R ( lower case Lambda -1
range from 1.6 to 3.0 nm). Both species exhibit similar responses to changes
in electron acceptor with nitrate- and fumarate-grown cells producing
relatively little exopolymer compared to trimethylamine N-oxide (TMAO)-grown
cells. In S. oneidensis, the increase in exopolymers has no apparent
effect upon cell-surface fixed charge density (-7.7 to -8.7 mM), but for
S. putrefaciens a significant drop in fixed charge density is observed
between fumarate/nitrate-grown cells (-43 mM) and TMAO-grown cells (-20.8
mM). For both species, exopolymers produced during growth on TMAO have
significant amide functionality, increasing from approximately 20-25%
of C-containing moieties in nitrate-grown cells to over 30% for TMAO-grown
cells (determined from X-ray photoelectron spectroscopy). The increased
exopolymer layer associated with TMAO-grown cells appears as a continuous,
convoluted layer covering the entire cell surface when viewed by low-temperature,
high-resolution scanning electron microscopy. Such significant changes
in cell-surface architecture, dependent upon the electron acceptor used
for growth, are likely to influence a variety of cell interactions, including
aggregation and attachment to surfaces, and the binding of aqueous metal
species.
** To whom correspondence should be addressed. Savannah River Ecology
Laboratory, The University of Georgia, PO Drawer E, Aiken, SC 29802. E-mail:
neal@srel.edu. Phone: (803)725 5341.
† The University of Georgia
‡ Emory University
§
Georgia Institute of Technology
SREL Reprint #2998
Neal, A. L., S. N. Dublin, J. Taylor, D. J. Bates, J. L. Burns, R. P. Apkarian and T. J. DiChristina. 2007. Terminal Electron Acceptors Influence the Quantity and Chemical Composition of Capsular Exopolymers Produced by Anaerobically Growing Shewanella spp. Biomacromolecules 8: 166-174.
