SUMMARY Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

Microbial Surface Colonization and Biofilm Development in Marine Environments

Aquatic surface chemistry: Edited by Werner Stumm. Wiley, New York. 1987. $69.95 (ISBN 0471822951)

Many iron (Fe) redox processes that were previously assumed to be purely abiotic, such as photochemical Fe reactions, are now known to also be microbially mediated. Owing to this overlap, discerning whether biotic or abiotic processes control Fe redox chemistry is a major challenge for geomicrobiologists and biogeochemists alike. Therefore, to understand the network of reactions within the biogeochemical Fe cycle, it is necessary to determine which abiotic or microbially mediated reactions are dominant under various environmental conditions. In this Review, we discuss the major microbially mediated and abiotic reactions in the biogeochemical Fe cycle and provide an integrated overview of biotic and chemically mediated redox transformations.

The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle

Geobacter species specialize in making electrical contacts with extracellular electron acceptors and other organisms. This permits Geobacter species to fill important niches in a diversity of anaerobic environments. Geobacter species appear to be the primary agents for coupling the oxidation of organic compounds to the reduction of insoluble Fe(III) and Mn(IV) oxides in many soils and sediments, a process of global biogeochemical significance. Some Geobacter species can anaerobically oxidize aromatic hydrocarbons and play an important role in aromatic hydrocarbon removal from contaminated aquifers. The ability of Geobacter species to reductively precipitate uranium and related contaminants has led to the development of bioremediation strategies for contaminated environments. Geobacter species produce higher current densities than any other known organism in microbial fuel cells and are common colonizers of electrodes harvesting electricity from organic wastes and aquatic sediments. Direct interspecies electron exchange between Geobacter species and syntrophic partners appears to be an important process in anaerobic wastewater digesters. Functional and comparative genomic studies have begun to reveal important aspects of Geobacter physiology and regulation, but much remains unexplored. Quantifying key gene transcripts and proteins of subsurface Geobacter communities has proven to be a powerful approach to diagnose the in situ physiological status of Geobacter species during groundwater bioremediation. The growth and activity of Geobacter species in the subsurface and their biogeochemical impact under different environmental conditions can be predicted with a systems biology approach in which genome-scale metabolic models are coupled with appropriate physical/chemical models. The proficiency of Geobacter species in transferring electrons to insoluble minerals, electrodes, and possibly other microorganisms can be attributed to their unique "microbial nanowires," pili that conduct electrons along their length with metallic-like conductivity. Surprisingly, the abundant c-type cytochromes of Geobacter species do not contribute to this long-range electron transport, but cytochromes are important for making the terminal electrical connections with Fe(III) oxides and electrodes and also function as capacitors, storing charge to permit continued respiration when extracellular electron acceptors are temporarily unavailable. The high conductivity of Geobacter pili and biofilms and the ability of biofilms to function as supercapacitors are novel properties that might contribute to the field of bioelectronics. The study of Geobacter species has revealed a remarkable number of microbial physiological properties that had not previously been described in any microorganism. Further investigation of these environmentally relevant and physiologically unique organisms is warranted.

Geobacter: The Microbe Electric's Physiology, Ecology, and Practical Applications

Mercury is a potent neurotoxin for humans, particularly if the metal is in the form of methylmercury. Mercury is widely distributed in aquatic ecosystems as a result of anthropogenic activities and natural earth processes. A first step toward bioaccumulation of methylmercury in aquatic food webs is the methylation of inorganic forms of the metal, a process that is primarily mediated by anaerobic bacteria. In this Review, we evaluate the current state of knowledge regarding the mechanisms regulating microbial mercury methylation, including the speciation of mercury in environments where methylation occurs and the processes that control mercury bioavailability to these organisms. Methylmercury production rates are generally related to the presence and productivity of methylating bacteria and also the uptake of inorganic mercury to these microorganisms. Our understanding of the mechanisms behind methylation is limited due to fundamental questions related to the geochemical forms of mercury that persist in an...

Mechanisms Regulating Mercury Bioavailability for Methylating Microorganisms in the Aquatic Environment: A Critical Review

Pyrite is a key mineral in the global biogeochemical cycles of sulfur and iron, yet its anaerobic microbial oxidation has eluded geochemists and microbiologists for decades. Recent reports indicated that anaerobic oxidation of pyrite is occurring, but the mechanism remains unclear. Here, we provide evidence for the capability of Thiobacillus denitrificans to anaerobically oxidize a putatively nanosized pyrite particle fraction with nitrate as electron acceptor. Nanosized pyrite was readily oxidized to ferric iron and sulfate with a rate of 10.1 μM h–1. The mass balance of pyrite oxidation and nitrate reduction revealed a closed recovery of the electrons. This substantiates a further “missing lithotrophy” in the global cycles of sulfur and iron and emphasizes the high reactivity of nanominerals in the environment.

Anaerobic, Nitrate-Dependent Oxidation of Pyrite Nanoparticles by Thiobacillus denitrificans

The use of nanoscale ferrihydrite particles, which are known to effectively enhance microbial degradation of a wide range of contaminants, represents a promising technology for in situ remediation of contaminated aquifers. Thanks to their small size, ferrihydrite nanoparticles can be dispersed in water and directly injected into the subsurface to create reactive zones where contaminant biodegradation is promoted. Field applications would require a detailed knowledge of ferrihydrite transport mechanisms in the subsurface, but such studies are lacking in the literature. The present study is intended to fill this gap, focusing in particular on the influence of flow rate and ionic strength on particle mobility. Column tests were performed under constant or transient ionic strength, including injection of ferrihydrite colloidal dispersions, followed by flushing with particle-free electrolyte solutions. Particle mobility was greatly affected by the salt concentration, and particle retention was almost irreversible under typical salt content in groundwater. Experimental results indicate that, for usual ionic strength in European aquifers (2 to 5 mM), under natural flow condition ferrihydrite nanoparticles are likely to be transported for 5 to 30 m. For higher ionic strength, corresponding to contaminated aquifers, (e.g., 10 mM) the travel distance decreases to few meters. A simple relationship is proposed for the estimation of travel distance with changing flow rate and ionic strength. For future applications to aquifer remediation, ionic strength and injection rate can be used as tuning parameters to control ferrihydrite mobility in the subsurface and therefore the radius of influence during field injections.

http://www.soilmech.polito.it/content/download/186/954/version/1/file/2012+Tosco.pdf

Transport of Ferrihydrite Nanoparticles in Saturated Porous Media: Role of Ionic Strength and Flow Rate

The biodegradation of organic pollutants in aquifers is often restricted to the fringes of contaminant plumes where steep countergradients of electron donors and acceptors are separated by limited dispersive mixing. However, long-distance electron transfer (LDET) by filamentous 'cable bacteria' has recently been discovered in marine sediments to couple spatially separated redox half reactions over centimeter scales. Here we provide primary evidence that such sulfur-oxidizing cable bacteria can also be found at oxic-anoxic interfaces in aquifer sediments, where they provide a means for the direct recycling of sulfate by electron transfer over 1-2-cm distance. Sediments were taken from a hydrocarbon-contaminated aquifer, amended with iron sulfide and saturated with water, leaving the sediment surface exposed to air. Steep geochemical gradients developed in the upper 3 cm, showing a spatial separation of oxygen and sulfide by 9 mm together with a pH profile characteristic for sulfur oxidation by LDET. Bacterial filaments, which were highly abundant in the suboxic zone, were identified by sequencing of 16S rRNA genes and fluorescence in situ hybridization (FISH) as cable bacteria belonging to the Desulfobulbaceae. The detection of similar Desulfobulbaceae at the oxic-anoxic interface of fresh sediment cores taken at a contaminated aquifer suggests that LDET may indeed be active at the capillary fringe in situ.

Long-distance electron transfer by cable bacteria in aquifer sediments.

Microbial iron reduction is considered to be a significant subsurface process. The rate-limiting bioavailability of the insoluble iron oxyhydroxides, however, is a topic for debate. Surface area and mineral structure are recognized as crucial parameters for microbial reduction rates of bulk, macroaggregate iron minerals. However, a significant fraction of iron oxide minerals in the subsurface is supposed to be present as nanosized colloids. We therefore studied the role of colloidal iron oxides in microbial iron reduction. In batch growth experiments with Geobacter sulfurreducens, colloids of ferrihydrite (hydrodynamic diameter, 336 nm), hematite (123 nm), goethite (157 nm), and akaganeite (64 nm) were added as electron acceptors. The colloidal iron oxides were reduced up to 2 orders of magnitude more rapidly (up to 1,255 pmol h 1 cell 1 ) than bulk macroaggregates of the same iron phases (6 to 70 pmol h 1 cell 1 ). The increased reactivity was not only due to the large surface areas of the colloidal aggregates but also was due to a higher reactivity per unit surface. We hypothesize that this can be attributed to the high bioavailability of the nanosized aggregates and their colloidal suspension. Furthermore, a strong enhancement of reduction rates of bulk ferrihydrite was observed when nanosized ferrihydrite aggregates were added. Dissimilatory iron reduction is an important anaerobic respiration process in anoxic subsurface environments. However, the reactivity of ferric iron is mostly limited by the reduction kinetics of the poorly soluble, extracellular iron minerals. Electron transfer from microorganisms to iron oxides can occur via direct contact or by electron shuttling compounds (46). Trans

Julian Bosch

Papers

Anaerobic, Nitrate-Dependent Oxidation of Pyrite Nanoparticles by Thiobacillus denitrificans

Transport of Ferrihydrite Nanoparticles in Saturated Porous Media: Role of Ionic Strength and Flow Rate

Long-distance electron transfer by cable bacteria in aquifer sediments.

Nanosized Iron Oxide Colloids Strongly Enhance Microbial Iron Reduction

Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation.