Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation

The study of the role that fungi have played and are playing in fundamental geological processes can be termed ‘geomycology’ and this article seeks to emphasize the fundamental importance of fungi in several key areas. These include organic and inorganic transformations and element cycling, rock and mineral transformations, bioweathering, mycogenic mineral formation, fungal–clay interactions, metal–fungal interactions, and the significance of such processes in the environment and their relevance to areas of environmental biotechnology such as bioremediation. Fungi are intimately involved in biogeochemical transformations at local and global scales, and although such transformations occur in both aquatic and terrestrial habitats, it is the latter environment where fungi probably have the greatest influence. Within terrestrial aerobic ecosystems, fungi may exert an especially profound influence on biogeochemical processes, particularly when considering soil, rock and mineral surfaces, and the plant root–soil interface. The geochemical transformations that take place can influence plant productivity and the mobility of toxic elements and substances, and are therefore of considerable socio-economic relevance, including human health. Of special significance are the mutualistic symbioses, lichens and mycorrhizas. Some of the fungal transformations discussed have beneficial applications in environmental biotechnology, e.g. in metal leaching, recovery and detoxification, and xenobiotic and organic pollutant degradation. They may also result in adverse effects when these processes are associated with the degradation of foodstuffs, natural products, and building materials, including wood, stone and concrete. It is clear that a multidisciplinary approach is essential to understand fully all the phenomena encompassed within geomycology, and it is hoped that this review will serve to catalyse further research, as well as stimulate interest in an area of mycology of global significance.     

Metal accumulation by fungi: Applications in environmental biotechnology

Summary Fungi can accumulate metal and radionuclide species by physico-chemical and biological mechanisms including extracellular binding by metabolites and biopolymers, binding to specific polypeptides and metabolism-dependent accumulation. Biosorptive processes appear to have the most potential for environmental biotechnology. Biosorption consists of accumulation by predominatly metabolism-independent interactions, such as adsorptive or ion-exchange processes: the biosorptive capacity of the biomass can be manipulated by a range of physical and chemical treatments. Immobilized biomass retains biosorptive properties and possesses a number of advantages for process applications. Native or immobilized biomass can be used in fixed-bed, air-lift or fluidized bed bioreactors; biosorbed metal/radionuclide species can be removed for reclamation and the biomass regenerated by simple chemical treatments.     

Use of molecular techniques in bioremediation

In a practical sense, biotechnology is concerned with the production of commercial products generated by biological processes. More formally, biotechnology may be defined as "the application of scientific and engineering principles to the processing of material by biological agents to provide goods and services" (Cantor, 2000). From a historical perspective, biotechnology dates back to the time when yeast was first used for beer or wine fermentation, and bacteria were used to make yogurt. In 1972, the birth of recombinant DNA technology moved biotechnology to new heights and led to the establishment of a new industry. Progress in biotechnology has been truly remarkable. Within four years of the discovery of recombinant DNA technology, genetically modified organisms (GMOs) were making human insulin, interferon, and human growth hormone. Now, recombinant DNA technology and its products--GMOs are widely used in environmental biotechnology (Glick and Pasternak, 1988; Cowan, 2000). Bioremediation is one of the most rapidly growing areas of environmental biotechnology. Use of bioremediation for environmental clean up is popular due to low costs and its public acceptability. Indeed, bioremediation stands to benefit greatly and advance even more rapidly with the adoption of molecular techniques developed originally for other areas of biotechnology. The 1990s was the decade of molecular microbial ecology (time of using molecular techniques in environmental biotechnology). Adoption of these molecular techniques made scientists realize that microbial populations in the natural environments are much more diverse than previously thought using traditional culture methods. Using molecular ecological methods, such as direct DNA isolation from environmental samples, denaturing gradient gel electrophoresis (DGGE), PCR methods, nucleic acid hybridization etc., we can now study microbial consortia relevant to pollutant degradation in the environment. These techniques promise to provide a better understanding and better control of environmental biotechnology processes, thus enabling more cost effective and efficient bioremediation of our toxic waste and contaminated environments.     

The Development of Fungal Networks in Complex Environments

Fungi are of fundamental importance in terrestrial ecosystems playing important roles in decomposition, nutrient cycling, plant symbiosis and pathogenesis, and have significant potential in several areas of environmental biotechnology such as biocontrol and bioremediation. In all of these contexts, the fungi are growing in environments exhibiting spatio-temporal nutritional and structural heterogeneities. In this work, a discrete mathematical model is derived that allows detailed understanding of how events at the hyphal level are influenced by the nature of various environmental heterogeneities. Mycelial growth and function is simulated in a range of environments including homogeneous conditions, nutritionally-heterogeneous conditions and structurally-heterogeneous environments, the latter emulating porous media such as soils. Our results provide further understanding of the crucial processes involved in fungal growth, nutrient translocation and concomitant functional consequences, e.g. acidification, and have implications for the biotechnological application of fungi.     

Geomicrobiology of the ocean crust: a role for chemoautotrophic Fe-bacteria

The delicate balance of the major global biogeochemical cycles greatly depends on the transformation of Earth materials at or near its surface. The formation and degradation of rocks, minerals, and organic matter are pivotal for the balance, maintenance, and future of many of these cycles. Microorganisms also play a crucial role, determining the transformation rates, pathways, and end products of these processes. While most of Earth's crust is oceanic rather than terrestrial, few studies have been conducted on ocean crust transformations, particularly those mediated by endolithic (rock-hosted) microbial communities. The biology and geochemistry of deep-sea and sub-seafloor environments are generally more complicated to study than in terrestrial or near-coastal regimes. As a result, fewer, and more targeted, studies usually homing in on specific sites, are most common. We are studying the role of endolithic microorganisms in weathering seafloor crustal materials, including basaltic glass and sulfide minerals, both in the vicinity of seafloor hydrothermal vents and off-axis at unsedimented (young) ridge flanks. We are using molecular phylogenetic surveys and laboratory culture studies to define the size, diversity, physiology, and distribution of microorganisms in the shallow ocean crust. Our data show that an unexpected diversity of microorganisms directly participate in rock weathering at the seafloor, and imply that endolithic microbial communities contribute to rock, mineral, and carbon transformations.     

Fate of metallic engineered nanomaterials in constructed wetlands: prospection and future research perspectives

Metallic engineered nanomaterials (ENMs) undergo various transformations in the environment which affect their fate, toxicity and bioavailability. Although constructed wetlands (CWs) are applied as treatment systems for waste streams potentially containing metallic ENMs, little is known about the fate and effects of ENMs in CWs. Hence, literature data from related fields such as activated sludge wastewater treatment and natural wetlands is used to predict the fate and effects of ENMs in CWs and to analyze the risk of nanomaterials being released from CWs into surface waters. The ENMs are likely to reach the CW (partly) transformed and the transformations will continue in the CW. The main transformation processes depend on the type of ENM and the ambient environmental conditions in the CW. In general, ENMs are expected to undergo sorption onto (suspended) organic matter and plant roots. Although the risk of ENMs being released at high concentrations from CWs is estimated low, caution is warranted because of the estimated rise in the production of these materials. As discharge of (transformed) ENMs from CWs during normal operation is predicted to be low, future research should rather focus on the effects of system malfunctions (e.g. short-circuiting). Efficient retention in the CW and increasing production volumes in the future entail increasing concentrations within the CW substrate and further research needs to address possible adverse effects caused.     

BMRI-2, Rossendorf/Dresden, Germany (30 August - 1 September 2000)

Clearly, there is much left to be understood about microbial processes and interactions with metals, but much progress has been made, and the multidisciplinary approach of groups who are studying both the microbial populations and the chemistry of biotransformations of metals by bacteria will ensure rapid progress in our understanding of these issues. Several major points from different speakers summarize this meeting and are usefully reiterated at this point: Toxic metal ions, unlike organic pollutants, are immutable, and their bioavailability is a critical feature of their toxicity. The mobility, transport and fate of toxic metals and radionuclides in the environment are dependent on chemical and geochemical processes in which micro-organisms are intimately involved. Metals can be mobilized as well as immobilized by microorganisms. Metal/radionuclide valencies and chemical properties are critical to their environmental mobility. Bacterial- or fungal-metal interactions will be complicated by the presence of other pollutants. The identification of bacteria from environmental samples should not rely on one methodology, as these have been shown to be biased. Sonja Selenska-Pobell organized both BMRI-1 in 1998 and BMRI-2, which had well over 100 participants from Europe, Russia, USA and Japan in attendance. Thirty-one oral presentations were given, and over 30 posters were displayed over two poster sessions. BMRI-3 is provisionally planned for 2002 at GBF, Braunschweig, Germany.     

Intraspecific traits change biodiversity effects on ecosystem functioning under metal stress

Studies investigating the impacts of biodiversity loss on ecosystem processes have often reached different conclusions, probably because insufficient attention has been paid to some aspects including (1) which biodiversity measure (e.g., species number, species identity or trait) better explains ecosystem functioning, (2) the mechanisms underpinning biodiversity effects, and (3) how can environmental context modulates biodiversity effects. Here, we investigated how species number (one to three species) and traits of aquatic fungal decomposers (by replacement of a functional type from an unpolluted site by another from a metal-polluted site) affect fungal production (biomass acumulation) and plant litter decomposition in the presence and absence of metal stress. To examine the putative mechanisms that explain biodiversity effects, we determined the contribution of each fungal species to the total biomass produced in multicultures by real-time PCR. In the absence of metal, positive diversity effects were observed for fungal production and leaf decomposition as a result of species complementarity. Metal stress decreased diversity effects on leaf decomposition in assemblages containing the functional type from the unpolluted site, probably due to competitive interactions between fungi. However, dominance effect maintained positive diversity effects under metal stress in assemblages containing the functional type from the metal-polluted site. These findings emphasize the importance of intraspecific diversity in modulating diversity effects under metal stress, providing evidence that trait-based diversity measures should be incorporated when examining biodiversity effects.     

Emerging high-throughput approaches to analyze bioremediation of sites contaminated with hazardous and/or recalcitrant wastes

Sustainable development requires the promotion of environmental management and a constant search for new technologies to treat a wide range of aquatic and terrestrial habitats contaminated by increasing anthropogenic activities. Bioremediation, i.e. the elimination of natural or xenobiotic pollutants by living organisms, is an environmentally friendly and cost-effective alternative to physico-chemical cleanup options. However, the strategy and outcome of bioremediation in open systems or confined environments depend on a variety of physico-chemical and biological factors that need to be assessed and monitored. In particular, microorganisms are key players in bioremediation applications, yet their catabolic potential and their dynamics in situ remain poorly characterized. To perform a comprehensive assessment of the biodegradative potential of a contaminated site and efficiently monitor changes in the structure and activities of microbial communities involved in bioremediation processes, sensitive, fast and large-scale methods are needed. Over the last few years, the scientific literature has revealed the progressive emergence of genomic high-throughput technologies in environmental microbiology and biotechnology. In this review, we discuss various high--throughput techniques and their possible--or already demonstrated-application to assess biotreatment of contaminated environments.     

Mineral-microbe interactions: biotechnological potential of bioweathering

Mineral-microbe interaction has been a key factor shaping the lithosphere of our planet since the Precambrian. Detailed investigation has been mainly focused on the role of bioweathering in biomining processes, leading to the selection of highly efficient microbial inoculants for the recovery of metals. Here we expand this scenario, presenting additional applications of bacteria and fungi in mineral dissolution, a process with novel biotechnological potential that has been poorly investigated. The ability of microorganisms to trigger soil formation and to sustain plant establishment and growth are suggested as invaluable tools to counteract the expansion of arid lands and to increase crop productivity. Furthermore, interesting exploitations of mineral weathering microbes are represented by biorestoration and bioremediation technologies, innovative and competitive solutions characterized by economical and environmental advantages. Overall, in the future the study and application of the metabolic properties of microbial communities capable of weathering can represent a driving force in the expanding sector of environmental biotechnology.     

Endophytic microorganisms—promising applications in bioremediation of greenhouse gases

Bioremediation is a technique that uses microbial metabolism to remove pollutants. Various techniques and strategies of bioremediation (e.g., phytoremediation enhanced by endophytic microorganisms, rhizoremediation) can mainly be used to remove hazardous waste from the biosphere. During the last decade, this specific technique has emerged as a potential cleanup tool only for metal pollutants. This situation has changed recently as a possibility has appeared for bioremediation of other pollutants, for instance, volatile organic compounds, crude oils, and radionuclides. The mechanisms of bioremediation depend on the mobility, solubility, degradability, and bioavailability of contaminants. Biodegradation of pollutions is associated with microbial growth and metabolism, i.e., factors that have an impact on the process. Moreover, these factors have a great influence on degradation. As a result, recognition of natural microbial processes is indispensable for understanding the mechanisms of effective bioremediation. In this review, we have emphasized the occurrence of endophytic microorganisms and colonization of plants by endophytes. In addition, the role of enhanced bioremediation by endophytic bacteria and especially of phytoremediation is presented.     

Microbial formation and transformation of organometallic and organometalloid compounds

Abstract: Microbial formation and transformation of organometallic and organometalloid compounds comprise significant components of biogeochemical cycles for the metals mercury, lead and tin and the metalloids arsenic, selenium, tellurium and germanium. Methylated derivatives of such elements can arise as a result of chemical and biological mechanisms and this frequently results in altered volatility, solubility, toxicity and mobility. The major microbial methylating agents are methylcobalamin (CH₃CoB₁₂), involved in the methylation of mercury, tin and lead, and S -adenosylmethionine (SAM), involved in the methylation of arsenic and selenium. Evidence for the methylation of other toxic metal(loid)s is sparse. Biomethylation may result in metal(loid) detoxification since methylated derivatives may be excreted readily from cells, are often volatile and may be less toxic, e.g. organoarsenicals. However, for mercury, low yields of methylated derivatives and the existence of more efficient resistance mechanisms, e.g. reduction of Hg²⁺ to Hg⁰, suggest a lower significance in detoxification. Bioalkylation has only been characterised in detail for arsenic. Microorganisms can accumulate organometal(loid)s, a phenomenon relevant to toxicant transfer to higher organisms. As well as bioaccumulation, many microorganisms are capable of the degradation and detoxification of organometal(loid) compounds by, e.g. demethylation and dealkylation. Several organometal(loid) transformations have potential for environmental bioremediation.     

Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects

 High concentrations of heavy metals in soil have an adverse effect on micro-organisms and microbial processes. Among soil microorganisms, mycorrhizal fungi are the only ones providing a direct link between soil and roots, and can therefore be of great importance in heavy metal availability and toxicity to plants. This review discusses various aspects of the interactions between heavy metals and mycorrhizal fungi, including the effects of heavy metals on the occurrence of mycorrhizal fungi, heavy metal tolerance in these micro-organisms, and their effect on metal uptake and transfer to plants. Mechanisms involved in metal tolerance, uptake and accumulation by mycorrhizal hyphae and by endo- or ectomycorrhizae are covered. The possible use of mycorrhizal fungi as bioremediation agents in polluted soils or as bioindicators of pollution is also discussed. Accepted: 23 June 1997     

Neutrophilic Iron-Oxidizing Bacteria in the Ocean: Their Habitats,Diversity, and Roles in Mineral Deposition,Rock Alteration,and Biomass Production in the Deep-Sea

The importance of metals to life has long been appreciated. Iron (Fe) is the fourth most abundant element overall, and the second most abundant element that is redox-active in near-surface aqueous habitats, rendering it the most important environmental metal. While it has long been recognized that microorganisms participate in the global iron cycle, appreciation for the pivotal role that redox cycling of iron plays in energy conservation among diverse prokaryotes has grown substantially in the past decade. In addition, redox reactions involving Fe are linked to several other biogeochemical cycles (e.g., carbon), with significant ecological ramifications. The increasing appreciation for the role of microbes in redox transformations of Fe is reflected in a recent surge in biological and environmental studies of microorganisms that conserve energy for growth from redox cycling of Fe compounds, particularly in the deep ocean. Here we highlight some of the key habitats where microbial Fe-oxidation plays significant ecological and biogeochemical roles in the oceanic regime, and provide a synthesis of recent studies concerning this important physiological group. We also provide the first evidence that microbial Fe-oxidizing bacteria are a critical factor in the kinetics of mineral dissolution at the seafloor, by accelerating dissolution by 6–8 times over abiotic rates. We assert that these recent studies, which indicate that microbial Fe-oxidation is widespread in the deep-sea, combined with the apparent role that this group play in promoting rock and mineral weathering, indicate that a great deal more attention to these microorganisms is warranted in order to elucidate the full physiological and phylogenetic diversity and activity of the neutrophilic Fe-oxidizing bacteria in the oceans.     

Quantitative Modeling of Microbial Population Responses to Chronic Irradiation Combined with Other Stressors

Microbial population responses to combined effects of chronic irradiation and other stressors (chemical contaminants, other sub-optimal conditions) are important for ecosystem functioning and bioremediation in radionuclide-contaminated areas. Quantitative mathematical modeling can improve our understanding of these phenomena. To identify general patterns of microbial responses to multiple stressors in radioactive environments, we analyzed three data sets on: (1) bacteria isolated from soil contaminated by nuclear waste at the Hanford site (USA); (2) fungi isolated from the Chernobyl nuclear-power plant (Ukraine) buildings after the accident; (3) yeast subjected to continuous γ-irradiation in the laboratory, where radiation dose rate and cell removal rate were independently varied. We applied generalized linear mixed-effects models to describe the first two data sets, whereas the third data set was amenable to mechanistic modeling using differential equations. Machine learning and information-theoretic approaches were used to select the best-supported formalism(s) among biologically-plausible alternatives. Our analysis suggests the following: (1) Both radionuclides and co-occurring chemical contaminants (e.g. NO₂) are important for explaining microbial responses to radioactive contamination. (2) Radionuclides may produce non-monotonic dose responses: stimulation of microbial growth at low concentrations vs. inhibition at higher ones. (3) The extinction-defining critical radiation dose rate is dramatically lowered by additional stressors. (4) Reproduction suppression by radiation can be more important for determining the critical dose rate, than radiation-induced cell mortality. In conclusion, the modeling approaches used here on three diverse data sets provide insight into explaining and predicting multi-stressor effects on microbial communities: (1) the most severe effects (e.g. extinction) on microbial populations may occur when unfavorable environmental conditions (e.g. fluctuations of temperature and/or nutrient levels) coincide with radioactive contamination; (2) an organism’s radioresistance and bioremediation efficiency in rich laboratory media may be insufficient to carry out radionuclide bioremediation in the field—robustness against multiple stressors is needed.     

Bioremediation of radioactive waste: radionuclide-microbe interactions in laboratory and field-scale studies

Given the scale of the contamination associated with 60 years of global nuclear activity, and the inherent high financial and environmental costs associated with invasive physical and chemical clean-up strategies, there is an unparalleled interest in new passive in situ bioremediation processes for sites contaminated with nuclear waste. Many of these processes rely on successfully harnessing newly discovered natural biogeochemical cycles for key radionuclides and fission products. Recent advances have been made in understanding the microbial colonization of radioactive environments and the biological basis of microbial transformations of radioactive waste in these settings.     

Enhancement of metal bioremediation by use of microbial surfactants

Metal pollution all around the globe, especially in the mining and plating areas of the world, has been found to have grave consequences. An excellent option for enhanced metal contaminated site bioremediation is the use of microbial products viz. microbial surfactants and extracellular polymers which would increase the efficiency of metal reducing/sequestering organisms for field bioremediation. Important here is the advantage of such compounds at metal and organic compound co-contaminated site since microorganisms have long been found to produce surface-active compounds when grown on hydrocarbons. Other options capable of proving efficient enhancers include exploiting the chemotactic potential and biofilm forming ability of the relevant microorganisms. Chemotaxis towards environmental pollutants has excellent potential to enhance the biodegradation of many contaminants and biofilm offers them a better survival niche even in the presence of high levels of toxic compounds.