Microbial mats are ecosystems that arguably greatly affected the conditions of the biosphere on Earth through geological time. These laminated organosedimentary systems, which date back to >
3.4 Ga ...bp, are characterized by high metabolic rates, and coupled to this, rapid cycling of major elements on very small (mm-µm) scales. The activity of the mat communities has changed Earth's redox conditions (i.e. oxidation state) through oxygen and hydrogen production. Interpretation of fossil microbial mats and their potential role in alteration of the Earth's geochemical environment is challenging because these mats are generally not well preserved.
Preservation of microbial mats in the fossil record can be enhanced through carbonate precipitation, resulting in the formation of lithified mats, or microbialites. Several types of microbially-mediated mineralization can be distinguished, including biologically-induced and biologically influenced mineralization. Biologically-induced mineralization results from the interaction between biological activity and the environment. Biologically-influenced mineralization is defined as passive mineralization of organic matter (biogenic or abiogenic in origin), whose properties influence crystal morphology and composition. We propose to use the term organomineralization
sensu lato as an umbrella term encompassing biologically influenced and biologically induced mineralization. Key components of organomineralization
sensu lato are the “alkalinity” engine (microbial metabolism and environmental conditions impacting the calcium carbonate saturation index) and an organic matrix comprised of extracellular polymeric substances (EPS), which may provide a template for carbonate nucleation. Here we review the specific role of microbes and the EPS matrix in various mineralization processes and discuss examples of modern aquatic (freshwater, marine and hypersaline) and terrestrial microbialites.
Intertidal marine systems are highly dynamic systems which are characterized by periodic fluctuations in environmental parameters. Microbial processes play critical roles in the remineralization of ...nutrients and primary production in intertidal systems. Many of the geochemical and biological processes which are mediated by microorganisms occur within microenvironments which can be measured over micrometer spatial scales. These processes are localized by cells within a matrix of extracellular polymeric secretions (EPS), collectively called a “microbial biofilm”. Recent examinations of intertidal systems by a range of investigators using new approaches show an abundance of biofilm communities. The purpose of this overview is to examine recent information concerning the roles of microbial biofilms in intertidal systems. The microbial biofilm is a common adaptation of natural bacteria and other microorganisms. In the fluctuating environments of intertidal systems, biofilms form protective microenvironments and may structure a range of microbial processes. The EPS matrix of biofilm forms sticky coatings on individual sediment particles and detrital surfaces, which act as a stabilizing anchor to buffer cells and their extracellular processes during the frequent physical stresses (e.g., changes in salinity and temperature, UV irradiation, dessication). EPS is an operational definition designed to encompass a range of large microbially-secreted molecules having widely varying physical and chemical properties, and a range of biological roles. Examinations of EPS using Raman and Fourier-transform infared spectroscopy, and atomic-force microscopy suggest that some EPS gels possess physical and chemical properties which may hasten the development of sharp geochemical gradients, and contribute a protective effect to cells. Biofilm polymers act as a sorptive sponge which binds and concentrates organic molecules and ions close to cells. Concurrently, the EPS appear to localize extracellular enzyme activities of bacteria, and hence contribute to the efficient biomineralization of organics. At larger spatial scales, the copious secretion of specific types of EPS by diatoms on the surfaces of intertidal mudflats may stabilize sediments against resuspension. Biofilms exert important roles in environmental- and public health processes occurring within intertidal systems. The sorptive properties of EPS effectively chelate toxic metals and other contaminants, which then act as an efficient trophic-transfer vehicle for the entry of contaminants into food webs. In the water column, biofilm microenvironments in suspended flocs may form a stabilizing refugia that enhances the survival and propagation of pathogenic (i.e., disease-causing) bacteria entering coastal waters from terrestrial and freshwater sources. The EPS matrix affords microbial cells a tremendous potential for resiliency during periods of stress, and may enhance the overall physiological activities of bacteria. It is emphasized here that the influences of small-scale microbial biofilms must be addressed in understanding larger-scale processes within intertidal systems.
Sulfate reducing bacteria (SRB) have existed throughout much of Earth's history and remain major contributors to carbon cycling in modern systems. Despite their importance, misconceptions about SRB ...are prevalent. In particular, SRB are commonly thought to lack oxygen tolerance and to exist only in anoxic environments. Through the last two decades, researchers have discovered that SRB can, in fact, tolerate and even respire oxygen. Investigations of microbial mat systems have demonstrated that SRB are both abundant and active in the oxic zones of mats. Additionally, SRB have been found to be highly active in the lithified zones of microbial mats, suggesting a connection between sulfate reduction and mat lithification. In the present paper, we review recent research on SRB distribution and present new preliminary findings on both the diversity and distribution of δ-proteobacterial SRB in lithifying and non-lithifying microbial mat systems. These preliminary findings indicate the unexplored diversity of SRB in a microbial mat system and demonstrate the close microspatial association of SRB and cyanobacteria in the oxic zone of the mat. Possible mechanisms and further studies to elucidate mechanisms for carbonate precipitation via sulfate reduction are also discussed.
Extracellular polymeric secretions (EPS) that are produced by cyanobacteria represent potential structuring agents in the formation of marine stromatolites. The abundance, production, and degradation ...of EPS in the upper layers of a microbial mat forming shallow subtidal stromatolites at Highborne Cay, Bahamas, were determined using
14C tracer experiments and were integrated with measurements of other microbial community parameters. The upper regions of a Type 2 Reid, R.P., Visscher, P.T., Decho, A.W., Stolz, J., Bebout, B., MacIntyre, I.G., Dupraz, C., Pinckney, J., Paerl, H., Prufert-Bebout, L., Steppe, T., Des Marais, D., 2000. The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature (London) 406, 989–992 stromatolite mat exhibited a distinct layering of alternating “green” cyanobacteria-rich layers (Layers 1 and 3) and “white” layers (Layers 2 and 4), and the natural abundance of EPS varied significantly depending on the mat layer. The highest EPS abundance occurred in Layer 2. The production of new EPS, as estimated by the incorporation of
14C-bicarbonate into EPS, occurred in all layers examined, with the highest production in Layer 1 and during periods of photosynthesis (i.e., daylight hours). A large pool (i.e., up to 49%) of the total
14C-bicarbonate uptake was released as low molecular-weight (MW) dissolved organic carbon (DOC). This DOC was rapidly mineralized to CO
2 by heterotrophic bacteria. EPS degradation, as determined by the conversion of
14C-EPS to
14CO
2, was slowest in Layer 2. Results of slurry experiments, examining O
2 uptake following additions of organic substrates, including EPS, supported this degradation trend and further demonstrated selective utilization by heterotrophs of specific monomers, such as acetate, ethanol, and uronic acids. Results indicated that natural EPS may be rapidly transformed post-secretion by heterotrophic degradation, specifically by sulfate-reducing bacteria, to a more-refractory remnant polymer that is relatively slow to accumulate. A mass balance analysis suggested that a layer-specific pattern in EPS and low-MW DOC turnover may contribute to major carbonate precipitation events within stromatolites. Our findings represent the first estimate of EPS turnover in stromatolites and support an emerging idea that stromatolite formation is limited by a delicate balance between evolving microbial activities and environmental factors.
Climate‐induced stressors, such as changes in temperature, salinity, and pH, contribute to the emergence of infectious diseases. These changes alter geographical constraint, resulting in increased ...Vibrio spread, exposure, and infection rates, thus facilitating greater Vibrio‐human interactions. Multiple efforts have been developed to predict Vibrio exposure and raise awareness of health risks, but most models only use temperature and salinity as prediction factors. This study aimed to better understand the potential effects of temperature and pH on V. vulnificus and V. parahaemolyticus planktonic and biofilm growth. Vibrio strains were grown in triplicate at 25°, 30°, and 37°C in 96 well plates containing Modified Seawater Yeast Extract modified with CaCl2 at pH's ranging from 5 to 9.6. AMiGA software was used to model growth curves using Gaussian process regression. The effects of temperature and pH were evaluated using randomized complete block analysis of variance, and the growth rates of V. parahaemolyticus and V. vulnificus were modeled using the interpolation fit on the MatLab Curve Fitting Toolbox. Different optimal conditions involving temperature and pH were observed for planktonic and biofilm Vibrio growth within‐ and between‐species. This study showed that temperature and pH factors significantly affect Vibrio planktonic growth rates and V. parahaemolyticus biofilm formation. Therefore, pH effects must be added to the Vibrio growth modeling efforts to better predict Vibrio risk in estuarine and coastal zones that can potentially experience the cooccurrence of Vibrio and harmful algal bloom outbreak events.
Plain Language Summary
Changes in temperature, salinity, and pH are increasing Vibrio‐human interactions in coastal communities. Multiple efforts have been developed to predict Vibrio risk, mainly using temperature and salinity measurements. However, more comprehensive models are needed to help inform decision‐makers on how to better design policies and create public health awareness. This study looks at how temperature and pH could affect the growth of the potential human bacterial pathogens, V. vulnificus and V. parahaemolyticus. Vibrio strains were grown in triplicate at different temperatures in acidic, neutral, and alkaline conditions (different pH ranges). The effects of temperature and pH were evaluated using randomized complete block analysis of variance, and the growth rates of V. parahaemolyticus and V. vulnificus were modeled using the MatLab Curve Fitting Toolbox. This study found different optimal conditions for free‐living and aggregated Vibrio growth within and between species. In addition, this study showed that temperature and pH factors significantly impact Vibrio growth. Overall, the pH effects must be added to the Vibrio growth modeling efforts to have a more comprehensive model and to better predict Vibrio risk in climate change scenarios.
Key Points
Optimal growth conditions for Vibrio spp. depend on the life stage: planktonic or biofilm formation
Changes in pH and temperature in coastal areas may lead to a higher Vibrio‐human interaction and influence adaptative responses
pH effects must be included in Vibrio modeling efforts to predict Vibrio risk in zones with co‐occurrence of Vibrio and harmful algal blooms
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 CaCO3 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 (pKa = 3.0), sulfur‐containing groups (thiols, sulfonic and sulfinic acids – pKa = 7.0–7.1) and amino groups (pKa = 8.4–9.2). The calcium‐binding capacity of these exopolymers in solution at pH 9.0 ranged from 0.12gCa gEPS−1–0.15 gCa gEPS−1. These results suggest that SRB could play a critical role in the formation of CaCO3 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 CaCO3 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.
Microbial cells (i.e., bacteria, archaea, microeukaryotes) in oceans secrete a diverse array of large molecules, collectively called extracellular polymeric substances (EPSs) or simply
. These ...secretions facilitate attachment to surfaces that lead to the formation of structured '
' communities. In open-water environments, they also lead to formation of organic colloids, and larger aggregations of cells, called '
Secretion of EPS is now recognized as a fundamental microbial adaptation, occurring under many environmental conditions, and one that influences many ocean processes. This relatively recent realization has revolutionized our understanding of microbial impacts on ocean systems. EPS occur in a range of molecular sizes, conformations and physical/chemical properties, and polysaccharides, proteins, lipids, and even nucleic acids are actively secreted components. Interestingly, however, the physical ultrastructure of how individual EPS interact with each other is poorly understood. Together, the EPS matrix molecules form a three-dimensional architecture from which cells may localize extracellular activities and conduct cooperative/antagonistic interactions that cannot be accomplished efficiently by free-living cells. EPS alter optical signatures of sediments and seawater, and are involved in biogeomineral precipitation and the construction of microbial macrostructures, and horizontal-transfers of genetic information. In the water-column, they contribute to the formation of marine snow, transparent exopolymer particles (TEPs), sea-surface microlayer biofilm, and marine oil snow. Excessive production of EPS occurs during later-stages of phytoplankton blooms as an excess metabolic by product and releases a carbon pool that transitions among dissolved-, colloidal-, and gel-states. Some EPS are highly labile carbon forms, while other forms appear quite refractory to degradation. Emerging studies suggest that EPS contribute to efficient trophic-transfer of environmental contaminants, and may provide a protective refugia for pathogenic cells within marine systems; one that enhances their survival/persistence. Finally, these secretions are prominent in 'extreme' environments ranging from sea-ice communities to hypersaline systems to the high-temperatures/pressures of hydrothermal-vent systems. This overview summarizes some of the roles of exopolymer in oceans.
Bacteria are associated with mineralization and dissolution processes, some of which may enhance or compromise the physical stability of engineered structures. Examples include stabilization of ...sediment dikes, bioplugging, biogrouting, and self-healing of concrete and limestone structures. In contrast to ‘biologically controlled’ precipitation (
e.g. shells) of eukaryote organisms, microbial precipitation primarily results from two major processes: (1) ‘biologically induced’ precipitation, where microbial activities generate biogeochemical conditions that facilitate precipitation; and (2) ‘biologically influenced’ precipitation, where passive interactions of extracellular biopolymers and the geochemical environment drive precipitation. A common location for such biopolymers is the microbial ‘biofilm’ (
i.e. cells surrounded within a matrix of extracellular polymeric substances (EPS)). EPS biofilms occur commonly in both natural environments and many engineered surfaces. Emerging evidence now suggests that EPS inhibit, alter or enhance precipitation of calcium carbonate. Functional groups on EPS serve as initial nucleation sites, while other moieties function to control extent and types (
e.g. crystals vs. amorphous organominerals) of precipitation. Understanding how to control, or even manipulate, precipitation/dissolution processes within the confines of EPS matrices will influence long-term structural integrities of materials. The present overview explores properties of EPS, and their potentially destructive (dissolution) and constructive (precipitation) effects on precipitation. Initial insight is offered for understanding how biopolymers might be controlled for applied purposes.
Climate-induced stressors, such as changes in temperature, salinity, and pH, contribute to the emergence of infectious diseases. These changes alter geographical constraint, resulting in increased
...spread, exposure, and infection rates, thus facilitating greater
-human interactions. Multiple efforts have been developed to predict
exposure and raise awareness of health risks, but most models only use temperature and salinity as prediction factors. This study aimed to better understand the potential effects of temperature and pH on
and
planktonic and biofilm growth.
strains were grown in triplicate at 25°, 30°, and 37°C in 96 well plates containing Modified Seawater Yeast Extract modified with CaCl
at pH's ranging from 5 to 9.6. AMiGA software was used to model growth curves using Gaussian process regression. The effects of temperature and pH were evaluated using randomized complete block analysis of variance, and the growth rates of
and
were modeled using the interpolation fit on the MatLab Curve Fitting Toolbox. Different optimal conditions involving temperature and pH were observed for planktonic and biofilm
growth within- and between-species. This study showed that temperature and pH factors significantly affect
planktonic growth rates and
biofilm formation. Therefore, pH effects must be added to the
growth modeling efforts to better predict
risk in estuarine and coastal zones that can potentially experience the cooccurrence of
and harmful algal bloom outbreak events.
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