Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments

Abstract

Biodiversity of benthic eukaryotic microorganisms in highly acidic (pH ≤ 3.5) aquatic environments is limited to species that have developed strategies to tolerate elevated concentrations of H + and dissolved metals and low nutrients levels that commonly characterize these environments. To survive adverse conditions, some algae, protozoa, and fungi have developed mechanisms to make their cell membranes impermeable to protons and maintain cytosolic pH at near neutral levels; others have developed a cell boundary mechanism that blocks H + ions from entering the cell. High concentrations of heavy metals are also toxic, adversely impacting growth by disrupting physiological, biochemical, or metabolic processes. Some algae, fungi, and protozoans are able to tolerate high metal concentrations via metal complexation outside the cell, extracellular binding and precipitation of metals, reduced metal uptake, increased metal efflux, and detoxification or compartmentalization of metals within the cell. In acidic environments, benthic eukaryotic microorganisms form biofilm communities in which they are the dominant members numerically and ecologically. Eukaryotedominated benthic communities produce heterogeneous microenvironments that vary spatially and temporally in their physicochemical character. The eukaryotes in these biofilms can be considered ecosystem engineers as they directly or indirectly modulate the availability of resources to other species within the biofilm. These eukaryote-dominated communities may play a significant role in mediating their environment by actively and passively contributing to metal attenuation through various processes of biosorption and via formation of laminated organosedimentary structures, which may be used as analogs for similar structures in the rock record.

Euglenoid flagellates: A multifaceted biotechnology platform

“…The most conspicuous feature of this AMD system is the presence of Fe-rich stromatolites overlain by E. mutabilis-dominated biofilms. It has been proposed that E. mutabilis directly or indirectly produced stromatolites through phototactic and aerotactic activities by binding Fe and Al chemical precipitates that periodically covered the biofilms, in a way similar to stromatolite-building prokaryotes in marine settings (Brake et al, 2002;Brake and Hasiotis, 2010).…”

Watershed-Scale Fungal Community Characterization along a pH Gradient in a Subsurface Environment Cocontaminated with Uranium and Nitrate

“…Fungi are known to be metal resistant and occur in abundance in acidic, metal-rich environments observed in terrestrial ecosystems, such as aquifers (e.g., see references 14 and 15); thus, they could play an important role in contaminant transformation in the subsurface of U.S. DOE sites. Traits that favor the survival of fungi under the extreme conditions found in the radionuclide-contaminated acidic subsurface include facultative anaerobic growth, resistance to acidic pH, resistance to toxic metals, spore formation, and in some cases, radiation-enhanced growth (14,16). Additionally, previous research has also demonstrated a role of fungi in denitrification (17,18).…”

“…To our knowledge, the occurrence of fungi has been described for few pristine and contaminated aquifers (28,29), and the community composition of these microbial eukaryotes in subsurface environments remains poorly characterized. We hypothesized that the structure and composition of the subsurface fungal community are impacted by the subsurface pH gradient across the contaminated watershed and that this group of organisms contributes significantly to in situ denitrification in the contaminated subsurface, in part due to a greater tolerance of acidity by many fungi relative to that by bacteria (14,15). Thus, the objective of this study was to interrogate subsurface fungal communities through a close coupling of microbiological and biogeochemical approaches.…”

Speciation of bioaccumulated uranium(VI) by Euglena mutabilis cells obtained by laser fluorescence spectroscopy

“…Thus, there is only limited information available on the immobilization behavior of eukaryotes or microbial biofilms on metal removal in AMD environments [11,12]. However, biofilm communities, containing large amounts of eukaryotes, may play a significant role in mediating their environment by actively and passively contributing to metal attenuation through various processes of biosorption and via formation of laminated organosedimentary structures [13]. Some representatives of the euglenoids -which contain about 44 free-living genera and more than 800 species [14] -e.g.…”

“…In this study, for the first time the bioaccumulation of uranium by Euglena mutabilis, a eukaryotic organisms often observed in microbial communities forming biofilms and mats in AMD environments [13,15] was investigated by laser-induced fluorescence spectroscopy (LIFS) at pH 3 and 4. This technique has superior sensitivity for fluorescent metal ions, e.g.…”