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Biomineralization and Biosequestration Mechanisms at Life's Upper Temperatures: A Reappraisal using Novel CryoEM Techniques


EMSL Project ID
48552

Abstract

Though microbes can indirectly and metabolically transform, sequester, and transport (i) ions, (ii) organic and inorganic complexes, and (iii) precipitates via a wide range of mechanisms, implementation challenges remain as to how these attributes can be used in subsurface bioremediation strategies. Until we have a fundamental understanding of the composition of subsurface communities and their intrinsic capabilities to interact with and alter their environment, and acquire the tools and methodologies required to monitor how subsurface processes affect the fate of toxic metals and contaminants, the practice of subsurface bioremediation will continue to be an empirical one (Leeson et al., 2005). An alternate approach to expanding current bioremediation strategies involves actualistic studies in environments considered analogs for subsurface regimes. Such analog environments, like hot springs, can be accessed routinely to facilitate ongoing investigations of the mechanisms by which extremophile biofilm communities mobilize or sequester contaminants and toxic elements (e.g., heavy metals) from indigenous hydrothermal fluids. Some of the closest modern relatives of Earth’s most ancient ancestors, which lived in heavy metal-rich hydrothermal regimes, occupy the highest temperature regions of active hot springs (Stetter, 2006). Such studies could pave the way for more sophisticated efforts to identify and harness proteins involved in sequestering toxic elements. A fundamental aspect of such an approach is the ability to document microbe-mineral interactions over time and in natural settings during field and laboratory-based experiments. EMSL scientists are at the forefront of efforts to elucidate how key bacterial soil populations (e.g., Shewanella) interact with their environment in the critical zone of Earth’s regolith (Fredrickson et al., 2002; Marshall et al., 2006; Reardon, 2010). This proposal seeks to advance the study of hightemperature organisms with regard to their ability to assist in heavy-metal sequestration. The application of cryoEM (electron microscope) techniques developed recently at EMSL, along with a variety of PNNL instruments suited to the interrogation of geomicrobial specimens, will be essential for initiation of this project. CryoEM specimen preparation and imaging/analysis techniques optimized at EMSL by Dohnalkova et al. (personal communication) enable the direct study of ultrastructural, intracellular, and extracellular sites where inorganic and organic complexes, minerals, and mineraloids accumulate in association with microbial biofilm communities. Biofilms consist of benthic communities encased in extracellular polymeric substances (EPS) they exude, which, due to the high absorptive capacity of EPS, can sequester organic and inorganic constituents from the environment and facilitate a range of microbe-mineral interactions (e.g., Decho et al., 2005). It has been recognized for some time that the EPS of thermophile and hyperthermophile communities play a key role in sequestering mineraloids in silica-depositing hot springs (Cady and Farmer, 1996, see CV). Such microbe-mineral interactions facilitate the accumulation of laminated hydrothermal deposits (e.g., Handley et al, 2008). Recently, we found (with the use of conventional EM specimen preparation techniques) that fibrils in the integral glycocalyx of thermophilic biofilm EPS can serve as a loci for opaline silica accumulation (Hugo, Cady and Smythe, 2011, reference when listed in review in Geomicrobiology Journal (now published) on CV). We have also discovered a thermophilic organism in an iron-depositing hot spring that sequesters iron-oxides within the periplasmic space of its cells (Parenteau and Cady, 2010, see CV). It has been suggested to us (A.L. Reysenbach, personal communication), that this inherent capability––in which an organism extracts a metal ion from its environment, sequesters it via precipitation of a metal oxide in its periplasmic space, and remains viable in the environment––may be more widespread than previously recognized. Given that (i) hyperthermophilic and thermophilic biofilms were some of the earliest microbial communities to inhabit our planet, (ii) such communities evolved and thrived in heavy metal-rich ecosystems, and (iii) new “mineral formers” are still being discovered in subsurface analog environments like hot springs, it is likely that some members of such communities have inherent “toxic element” sequestration capabilities, yet unrecognized, that evolved to aid in their survival and could ultimately be harnessed for bioremediation purposes. The ability to apply cryoEM techniques recently optimized at EMSL-PNNL and investigate with state-of-the art chemical imaging tools and EMs at EMSL-PNNL and Portland State University (PSU) are timely in this regard.

Project Details

Start Date
2014-08-04
End Date
2014-09-30
Status
Closed

Team

Principal Investigator

Sherry Cady
Institution
Environmental Molecular Sciences Laboratory

Team Members

Richard Castenholz
Institution
University of Oregon

Christopher Anderton
Institution
Environmental Molecular Sciences Laboratory

James Evans
Institution
Environmental Molecular Sciences Laboratory

Libor Kovarik
Institution
Pacific Northwest National Laboratory

Hailan Piao
Institution
Washington State University Tri-Cities

Zihua Zhu
Institution
Environmental Molecular Sciences Laboratory

Alice Dohnalkova
Institution
Environmental Molecular Sciences Laboratory

Bruce Arey
Institution
Pacific Northwest National Laboratory