PerspectiveGeochemistry

What Biogenic Minerals Tell Us

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Science  12 Mar 2004:
Vol. 303, Issue 5664, pp. 1618-1619
DOI: 10.1126/science.1095177

Biogenic minerals [HN1] are generally those formed in the presence of biological cells (mainly bacteria; see the figure) and structures outside cells (1). These minerals, which come in a variety of types and shapes, are often small (on the order of nanometers) and occur in close association with the bacterial cell wall [HN2]. Several studies (27) have shown such an association [HN3] in natural samples taken from a wide range of environments, as well as in synthetic samples produced under laboratory conditions that mimic natural conditions. Some studies have also reported the formation of biogenic minerals inside microbial cells (8, 9) [HN4]. Although the occurrence of biogenic minerals in natural environments is well documented, the exact formation mechanisms are still poorly understood. A clear understanding of these mechanisms is essential in order to assess how bacteria interact with metals in present and ancient environments. In addition, a clear demonstration that bacteria can template mineral crystallization is also crucial because it might lead to the development of new tools in the search for evidence of past life on Earth and other planets.

Bacterial oxides. Transmission electron microscopy (TEM) image shows natural bacterial exopolymers covered with poorly ordered iron oxides. The sample was collected in the oxic sediments of a neutral-pH freshwater lake. The arrows indicate the position of very thin crystals of iron oxides on the cell wall and within the extracellular exopolymers. The elongated fine crystals appear to be covered by a more amorphous form of iron oxide.

Many researchers accept that bacteria can trigger mineral formation under saturation conditions through active reactions (from physiological and metabolic activity) and passive reactions (from surface reactivity of the cell wall or extracellular structures such as exopolymers) (1), but the reasons why bacteria favor or promote mineral nucleation are still unclear. One general explanation is that bacteria do so to prevent cell entombment and death by mineral metabolic by-products. Even though the survival of microbial cells is a logical explanation, an alternative is reported on page 1656 of this issue by Chan et al. (10) [HN5]. These authors propose that neutrophilic iron-oxidizing bacteria [HN6] promote the formation of elongated iron oxide minerals (identified as akaganeite) [HN7] onto extracellular polymers (polysaccharides) [HN8] in order to enhance metabolic energy generation.

Chan et al. analyzed natural biominerals in an iron oxide-encrusted biofilm [HN9] collected in a flooded mine. With the help of high-resolution synchrotron spectromicroscopy [x-ray photoemission electron microscopy (X-PEEM) and x-ray absorption near-edge structure (XANES)] [HN10] and high-resolution transmission electron microscopy (HRTEM) [HN11], they were able to show that microbially produced polysaccharides can template the nucleation of pseudo-single crystals (that is, having the appearance of single crystal structure) of akaganeite (with aspect ratios of about 1000:1). Unlike previous electron microscopy studies that showed bacteria-mineral associations and concluded that bacteria were likely involved in mineral formation (2, 3, 5, 7), the study by Chan et al. clearly shows the presence of a microbially derived organic-rich template for iron oxide formation. The clever use of carbon K-edge XANES analysis indicates a strong similarity between the spectra of synthetic acidic polysaccharides and the natural mineralized filaments.

The authors were also able to reproduce the formation of iron-rich filaments and elongated akaganeite crystals under laboratory conditions. Scanning transmission x-ray microscopy (STXM) [HN12] and spectral analyses confirmed the presence of mineralized filaments rich in iron and carbon in an alginate [HN13] solution mixed with ferric iron. Additional syntheses with a mixture of polysaccharides rich in carboxylic groups revealed the presence of elongated akaganeite crystals with smaller aspect ratios than those found in the natural sample. The combination of high-quality HRTEM images and XANES analysis provides compelling evidence that organic exopolymers secreted by bacterial cells can indeed template the crystallization of iron oxides. As stated by the authors, the use of high spatial resolution tools and powerful mineralogical analysis to characterize samples containing mineralized organic structures should improve our understanding of biomineralization mechanisms.

Chan et al. also propose a novel mechanism for the formation of crystals on bacterial exopolymers. They hypothesize that the oxidation of ferrous iron by iron-oxidizing bacteria increases the pH [HN14] gradient across the cell membrane. The generation of protons near the cell wall is then thought to enhance the proton motive force [HN15] and thus increase the energy-generating potential of the cell. This interesting hypothesis raises the possibility that bacteria do profit from encrusting themselves with various minerals (especially precipitation reactions leading to a pH gradient) because it allows them not only to survive, but also to gain useful energy in sometimes hostile or extreme environments.

Finally, a better understanding of the mechanisms leading to crystal nucleation on organic templates in natural environments and better characterization of such minerals might allow us to identify specific characteristics unique to biogenic minerals. Such characteristics could then become very helpful in the search for biosignatures in ancient environments on Earth and other planets. This is especially important for the NASA astrobiology program, which aims to learn how to recognize signatures of life on other worlds (11) [HN16]. The present and upcoming missions to Mars [HN17] have already generated a lot of interest among the general public and in the scientific community. With more research such as that of Chan et al. (10), we may soon be able to ascertain whether life existed or still exists on other worlds. But with the lessons learned from the famous Martian meteorite (12) [HN18], we must keep in mind that it is difficult to differentiate between biotic and abiotic mechanisms. With care, it should be possible to distinguish one from the other and apply our newly gained knowledge to samples returned from Mars or other planets.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

Dictionaries and Glossaries

A Chemistry & Environmental Dictionary is provided by EnvironmentalChemistry.com.

D. Glick's Glossary of Biochemistry and Molecular Biology is made available by Portland Press.

Web Collections, References, and Resource Lists

The Google Directory provides links to geochemistry and environmental microbiology resources.

The Yahoo Directory provides links to geochemistry and microbiology Internet resources.

Links for Mineralogists includes a section on geochemistry.

The Mineralogical Society of America offers a collection of mineral-related links.

Geochemistry on the World Wide Web is a collection of Internet resources made available by the Department of Earth and Atmospheric Sciences, Cornell University.

Online Texts and Lecture Notes

R. Foust, Department of Chemistry, Northern Arizona University, offers lecture notes for a course on environmental chemistry.

D. Clark, Department of Microbiology, Southern Illinois University, provides lecture notes for a course on the physiology and biochemistry of microorganisms.

W. White, Department of Earth and Atmospheric Sciences, Cornell University, makes available in PDF format his geochemistry textbook.

Lecture slides (in PDF format) are made available for a course on environmental microbiology at the University of Ottawa.

General Reports and Articles

The 14 February 2003 issue of Science had a Perspective by L. A. Warren and M. E. Kauffman titled “Microbial geoengineers.”

The 10 May 2002 issue had a review by D. K. Newman and J. F. Banfield titled “Geomicrobiology: Elucidation of the molecular-scale interactions that underpin biogeochemical systems.”

The 18 May 2001 issue had a Perspective by D. K. Newman titled “How bacteria respire minerals” about a report in that issue by S. K. Lower, M. F. Hochella Jr., and T. J. Beveridge titled “Bacterial recognition of mineral surfaces: Nanoscale interactions between Shewanella and alpha-FeOOH.”

A course on environmental geochemistry at Texas A&M University makes available in PDF format the May 1999 Reviews in Geophysics article by P. O'Day titled “Molecular environmental geochemistry.”

The NSF Nanoscale Science and Technology Web site makes available in PDF format the report of a 2002 nanogeoscience workshop.

J. L. Kirschvink, Division of Geological and Planetary Sciences, California Institute of Technology, makes available in PDF format a book chapter by J. L. Kirschvink and J. Hagadorn titled “The grand unified theory of biomineralization.”

Numbered Hypernotes

1. Biogenic minerals. An introduction to biomineralization is provided by the Biomineralization Web page of the Département des Sciences de la Terre, Université Paris-Sud, France. Wat on Earth, a publication of the Department of Earth Science, University of Waterloo, Canada, had an article by G. Ferris on biomineralization titled “Microbes to minerals.” The Laboratory of Intelligent Interfaces, School of Chemistry, Seoul National University, offers a presentation on biomineralization. J. F. Banfield, Department of Earth and Planetary Science, University of California, Berkeley, offers an illustrated presentation titled “Biomineralization of Fe oxides and ZnS at the Tennyson mine, WI.”

2. The bacterial cell wall. An introduction to bacterial cell walls is provided by the Companion Web Site of the third edition of Biochemistry by Mathews, van Holde, and Ahern. G. Kaiser, Community College of Baltimore County, Catonsville Campus, provides a presentation on bacterial cell walls for a microbiology course. D. Clark offers lecture notes on the cell envelope for a course on the physiology and biochemistry of microorganisms.

3. Small mineral particles on bacterial cell walls. The November-December 1998 issue of the American Mineralogist had an article (PDF format) by D. Fortin, F. G. Ferris, and S. D. Scott titled “Formation of Fe-silicates and Fe-oxides on bacterial surfaces in samples collected near hydrothermal vents on the Southern Explorer Ridge in the northeast Pacific Ocean” (2). The 4 August 2000 issue of Science had a report by J. F. Banfield et al. titled “Aggregation-based crystal growth and microstructure development in natural iron oxyhydroxide biomineralization products” (4) and an Enhanced Perspective by A. P. Alivisatos titled “Naturally aligned nanocrystals.” The June 1999 issue of Applied and Environmental Microbiology had an article by D. Emerson, J. V. Weiss, and J. P. Megonigal titled “Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants” (5).

4. Formation of biogenic minerals within cells. The 4 January 2002 issue of Science had a report by S. Glasauer, S. Langley, and T. J. Beveridge titled “Intracellular iron minerals in a dissimilatory iron-reducing bacterium” (8).

5. Clara S. Chan, Bradley H. Frazer, and Jillian F. Banfield are in the Department of Earth and Planetary Science, University of California, Berkeley. Gelsomina De Stasio is in the Department of Physics and at the Synchrotron Radiation Center, University of Wisconsin. Susan A. Welch (formerly in the Department of Geology and Geophysics, University of Wisconsin) is at the Research School of Earth Sciences and CRC LEME, Australian National University, Canberra. Maria V. Nesterova (formerly in the Department of Geology and Geophysics, University of Wisconsin) is in the Department of Chemistry and Biochemistry, Montana State University. Marco Girasole is in the Scanning Probe Microscopy Department, Istituto di Struttura della Materia, Rome. Sirine Fakra is at the Molecular Environmental Science Beamline, Advanced Light Source, Lawrence Berkeley National Laboratory.

6. Iron-oxidizing bacteria. The Biochemical Periodic Table, provided by the University of Minnesota Biocatalysis/Biodegradation Database, provides information about iron. C. Hagedorn, Department of Crop and Soil Environmental Sciences, Virginia Tech, makes available an information page about the iron-oxidizing bacteria Leptothrix, prepared as a student project for a course on environmental microbiology. Photomicrographs of bacteria that precipitate iron and manganese are include in a U.S. Geological Survey publication titled “How to collect and see the microbial community that fixes iron and manganese in the natural environment.”

7. Information on akaganeite is provided by the Mineralogy Database.

8. Polysaccharides. Polysaccharide is defined by the Britannica Concise Encyclopedia. An entry on polysaccharides is included in the Biochemistry Companion Web site. An introduction to polysaccharides is provided by P. von Sengbusch's Botany online.

9. Biofilms. The December 2000 issue of Microbiology and Molecular Biology Reviews had a review article by M. E. Davey and G. A. O'Toole titled “Microbial biofilms: From ecology to molecular genetics.” The September 2003 issue of Applied and Environmental Microbiology had an article by J. R. Lawrence et al. titled “Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms.”

10. High-resolution synchrotron spectromicroscopy (X-PEEM and XANES). The UK Surface Analysis Forum Web site provides an introduction to NEFAXS (near edge x-ray absorption fine structure) and XANES (x-ray absorption near-edge structure). The Synchrotron Radiation Center (SRC) at the University of Wisconsin makes available in PDF format a presentation titled “Geomicrobiology research with spectromicroscopy at SRC.” G. De Stasio provides a presentation on the principles of x-ray spectromicroscopy and the SPHINX and MEPHISTO instruments used at SRC by the De Stasio group. The Mobile X-ray PhotoElectron Emission Microscope (X-PEEM) Web page of S. Urquhart, Department of Chemistry, University of Saskatchewan, provides an introduction (in PDF format) to X-PEEM. Rigaku/MSC provides information about XANES. The Soft X-Ray Spectroscopy Group at the Daresbury Synchrotron Radiation Source provides an introduction to NEXAFS and XANES. L. Kipp, Institut für Experimentelle und Angewandte Physik, Kiel, Germany, offers a presentation on X-ray absorption spectroscopy.

11. HRTEM (high-resolution transmission electron microscopy). The Central Facility for Electron Microscopy, University of Nebraska, provides introductions to electron microscopy and to transmission electron microscope (TEM). The Center for High Resolution Electron Microscopy at Arizona State University provides an introduction to HRTEM. F. Ernst, Department of Materials Science and Engineering, Case Western Reserve University, offers a lecture presentation (in PDF format) on HRTEM for a course on advanced techniques of transmission electron microscopy. Microscopy.info provides links to Internet resources on electron microscope techniques and instrumentation.

12. STXM (scanning transmission x-ray microscopy). H. Ade, Department of Physics, North Carolina State University, offers a presentation on STXM. The Molecular Environmental Science Beamline Web page at the Advanced Light Source (ALS) provides a chart of the characteristics of STXM; a data sheet (in PDF format) is also available. The Hitchcock Group at McMaster University makes available a tutorial article about STXM by I. Koprinarov and A. P. Hitchcock titled “X-ray spectromicroscopy of polymers: An introduction for the non-specialist” (the document is also available as a PDF file) and a report on the operation of STXM at ALS.

13. Information on alginate is provided by CyberColloids Ltd. The August 2003 Protein Spotlight, a periodical electronic review from the Swiss-Prot group of the Swiss Institute of Bioinformatics, had an article on alginate by V. Baillie Gerritsen titled “Slime with a design.”

14. pH. An entry on pH is included in the Columbia Encyclopedia. C. R. Nave's HyperPhysics includes a section on pH. An introduction to pH is provided by Kimball's Biology Pages. A section on the biological aspects of pH is included in the pH Tutorial offered by the Department of Chemistry, University of British Columbia.

15. Proton motive force is defined in T. Paustian's Microtextbook and in D. Glick's Glossary of Biochemistry and Molecular Biology. D. Clark offers lecture notes on the electron transport chain and proton motive force for a course on the physiology and biochemistry of microorganisms. The 8 March 2002 issue of Science had a Perspective by D. Richardson and G. Sawers titled “PMF through the redox loop” about a Research Article in that issue by M. Jormakka et al. titled “Molecular basis of proton motive force generation: Structure of formate dehydrogenase-N.”

16. The NASA astrobiology program. The NASA Ames Research Center offers an astrobiology Web site. Goal 7 of the Astrobiology Road Map is “Determine how to recognize the signature of life on other worlds.” The NASA Astrobiology Institute provides a collection of Internet links. SpaceDaily makes available a 4 October 2000 article titled “Astrobiologists take interdisciplinary approach to biosignatures” and a 10 August 2000 article titled “Finding a rocky signature to life origins.” Astrobiology Web, a resource provided by SpaceRef.com, offers links to news and Internet resources related to astrobiology.

17. Mars missions. The Mars Exploration Program Web site is provided by NASA's Jet Propulsion Laboratory (JPL). The European Space Agency provides a presentation about a mission to search for life on Mars.

18. The famous Martian meteorite. The 16 August 1996 issue of Science had a Research Article by D. S. McKay et al. titled “Search for past life on Mars: Possible relic biogenic activity in Martian meteorite ALH84001” (12) and a News article by R. Kerr titled “Ancient life on Mars?” MarsNews.com offers a presentation about ALH84001 and life on Mars. The Mars Meteorites Web site at JPL provides photos of ALH84001 and Mars meteorite news. The Johnson Space Center's Meteorites from Mars Web site provides information about ALH84001 and a presentation on life on Mars. The Lunar and Planetary Institute offers a presentation titled “On the question of the Mars meteorite.” The January-February 1999 issue of Ad Astra magazine (a special issue on astrobiology) had an article by E. K. Gibson Jr., D. S. McKay, K. Thomas-Keprta, F. Westall, and C. A. Romanek titled “It's dead Jim. But was it ever alive?”

19. Danielle Fortin is in the Department of Earth Sciences, University of Ottawa.

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