High Resolution Imaging to Characterize the Structure and
Biogeochemical Function of Microbial Biofilms
Matthew J. Marshall, Alice C. Dohnalkova, David W. Kennedy, Bruce W. Arey, and
James K. Frederickson
Pacific Northwest National Laboratory, Richland, WA 99354
Direct examination of natural and engineered environments has revealed that the
majority of microorganisms in these systems live in structured communities termed
biofilms. In addition to microbial cells, biofilms are comprised of a poorly characterized
organic matrix commonly referred to as extracellular polymeric substance (EPS) that may
play roles in facilitating microbial interactions and biogeochemical reactions including
extracellular electron transfer. In our previous communications, we have examined the
composition of EPS produced by Shewanella oneidensis MR-1 during uranium [U(VI)]
biotransformation and the formation of reduced, extracellular uraninite [U(IV)O
2
]
nanoparticles [1]. Using a combination of transmission electron microscopy (TEM),
synchrotron-based, micro X-ray fluorescence (μ-XRF) imaging, and high-resolution
immuno-TEM, a highly-hydrated 3d bacterial EPS containing redox-active, extracellular
electron transfer proteins was found to be produced during microbial metal reduction [1,2].
The juxtaposition of extracellular electron transfer proteins and nanoparticulate uraninite
suggested that EPS played a key role in metal capture and precipitation and, possibly,
extracellular electron transfer. Therefore, understanding how biofilm EPS functions and
interacts with inorganic substrates such as metal ions and mineral surfaces connects the
molecular-scale biogeochemical processes to those at the microorganism-level and
provides insight to how microorganisms influence larger, pore-scale biogeochemical
reactions.
Our current view of mineral-biofilm interactions has arisen from 2-dimensional images
of 3-dimensional structures. Although a 3-dimensional structure of hydrated biofilm can
readily be visualized using confocal laser scanning microscopy (CLSM), the relatively low
resolution fails to resolve the fine scale interactions of EPS with minerals or newly formed
nanoparticles (Fig.1). We have begun to employ cryogenic (cryo) sample processing to
visualize specimens in the EM while fully preserved in their frozen-hydrated state.
Preliminary experiments demonstrated that the cryoTEM produced dramatically improved
cell architecture relative to the traditional TEM (Fig. 1). We have also begun to use
cryoTEM to examine fully hydrated EPS. In these studies, we observed that EPS has an
amorphous texture with low contrast due to sparse electron density. Notably, EPS
visualization was enhanced in preliminary experiments where Shewanella cells were
exposed to U(VI) (Fig. 1D). We speculate that addition of electron dense uranyl ions for
bioreduction experiments provides a fortuitous contrasting agent for EPS; presumably due
the binding of uranyl and/or U(IV) with EPS.
We have developed a protocol for cryo-preservation and cryoSEM visualization of
biofilms [2]. Our preliminary experiments demonstrated that we can successfully cryo-
preserve relatively large pieces of biomass in a nearest-to-native, frozen-hydrated state.
Our data suggested that the hydrated biofilm-associated EPS was significantly more
extended than presumed (Fig. 2). We explored the underlying biofilm using the cryo-
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doi:10.1017/S1431927611002170
Microsc. Microanal. 17 (Suppl 2), 2011
© Microscopy Society of America 2011
https://doi.org/10.1017/S1431927611002170
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