Geobiology (2007) DOI: 10.1111/j.1472-4669.2007.00117.x
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd 1
Blackwell Publishing Ltd ORIGINAL ARTICLES Sulfate-reducing bacteria exopolymeric substances
Exopolymeric substances of sulfate-reducing bacteria:
Interactions with calcium at alkaline pH and implication for
formation of carbonate minerals
O. BRAISSANT,
1
A. W. DECHO,
2
C. DUPRAZ,
1,3
C. GLUNK,
3
K. M. PRZEKOP
1
AND
P. T. VISSCHER
1
1
Center for Integrative Geosciences, University of Connecticut, 354 Mansfield Road, U-2045 Storrs, CT 06269, USA
2
Arnold School of Public Health, University of South Carolina, 800 Sumter St., Columbia, SC 29208, USA
3
Institut de Géologie et d’Hydrogéologie, University of Neuchâtel, Rue Emile Argand 158, CH-2009 Neuchâtel, Switzerland
ABSTRACT
Sulfate-reducing bacteria (SRB) have been recognized as key players in the precipitation of calcium carbonate
in lithifying microbial communities. These bacteria increase the alkalinity by reducing sulfate ions, and consuming
organic acids. SRB also produce copious amounts of exopolymeric substances (EPS). All of these processes
influence the morphology and mineralogy of the carbonate minerals. Interactions of EPS with metals, calcium
in particular, are believed to be the main processes through which the extracellular matrix controls the
precipitation of the carbonate minerals. SRB exopolymers were purified from lithifying mat and type cultures,
and their potential role in CaCO
3
precipitation was determined from acid-base titrations and calcium-binding
experiments. Major EPS characteristics were established using infrared spectroscopy and gas chromatography
to characterize the chemical functional groups and the sugar monomers composition. Our results demonstrate
that all of the three SRB strains tested were able to produce large amounts of EPS. This EPS exhibited three main
buffering capacities, which correspond to carboxylic acids (pK
a
= 3.0), sulfur-containing groups (thiols, sulfonic
and sulfinic acids – pK
a
= 7.0 –7.1) and amino groups (pK
a
= 8.4 –9.2). The calcium-binding capacity of these
exopolymers in solution at pH 9.0 ranged from 0.12g
Ca
g
EPS
–1
–0.15 g
Ca
g
EPS
–1
. These results suggest that SRB
could play a critical role in the formation of CaCO
3
in lithifying microbial mats. The unusually high sulfur content,
which has not been reported for EPS before, indicates a possible strong interaction with iron. In addition to
changing the saturation index through metabolic activity, our results imply that SRB affect the rock record
through EPS production and its effect on the CaCO
3
precipitation. Furthermore, EPS produced by SRB may
account for the incorporation of metals (e.g. Sr, Fe, Mg) associated with carbonate minerals in the rock record.
Received 23 February 2007; accepted 4 July 2007
Corresponding author: O. Braissant, Tel.: +1 860 405 92 40; fax: +1 860 405 91 53; e-mail:
Olivier.braissant@uconn.edu
INTRODUCTION
Seawater is supersaturated with respect to calcium carbonate,
but precipitation does not occur spontaneously due to various
inhibiting factors. These factors include the high hydratation
energies of Ca
2+
and Mg
2+
(Slaughter & Hill, 1991), ion-
pairing with sulfate, and presence of organic ligands that binds
Ca
2+
and Mg
2+
(Wright & Oren, 2005). In lithifying microbial
mats (i.e. where calcium carbonate precipitates are found), the
metabolic activity of sulfate-reducing bacteria (SRB), which
are abundant in mats (Canfield & DesMarais, 1991; Fründ &
Cohen, 1992; Visscher et al ., 1992), is believed to enhance
calcium carbonate precipitation (Visscher et al ., 2000; Dupraz
et al ., 2004; Baumgartner et al ., 2006). The activity of SRB
affects the formation of carbonate minerals in several ways.
Firstly, sulfate reduction results in a pH increase, affecting
the saturation index and thus directly the precipitation of
carbonate minerals (Lyons et al ., 1984; Walter et al ., 1993;
Visscher & Stolz, 2005). Secondly, when SRB use low
molecular weight organic acids (e.g. lactate, acetate) as electron
donors for growth, the availability of free calcium ions may
increase due to the removal of carboxylic acids binding
calcium (Bosak, 2005; Dupraz & Visscher, 2005). Thirdly, by
removing sulfate ions from solution, SRB alter the kinetic