Sci. Rep. Kanazawa Univ.
Vol.53, p.39-54, 200939

Bacterial Contribution to Precipitation ofManganese Nodules in Freshwater Environments:
An Electron Microscope Study ofExperimental Biomineralization by Cultured Bacteria
Kazue TAZAKI and Tatsuya HATTORI
Graduate School of Natural Science and Technology, Kanazawa University, Kakuma, Kanazawa,
Ishikawa 920-1192, Japan
E-mail: Kazue Tazaki: kazuet@kenroku.kanazawa-u.ac.jp
Phone: +81−76−264−6512
Fax: +81−76−264−6545
Abstract : Bacterial mineralization processes in the manganese cycle can be traced using
manganese oxide (MnOx) nodules and Mn-oxidizing bacteria. A laboratory simulation
experiment showed evidence of an organic contribution to manganese precipitation in freshwaterat pH 7-8 and in an Eh range from −24 to +200 mV. Glass slides that were kept in a beaker withnatural fresh water and river sediments for half a month were found to be coated by a brownmaterial. These manganese nodules were doughnut-shaped holdfasts of colonized bacteria
produced under photosynthetic conditions. These manganese mineral formation processes arecomposed of MnOx precipitation as well as bacterial activity and were studied by optical
microscopy, scanning electron microscopy, energy dispersive X-ray analysis and transmission
electron microscopy. Atomic absorption was used for the initial chemical analysis of the riverwater. The water contained high amounts of dissolved manganese whereas the sediments had no
manganese oxide minerals as determined by XRD analysis. The well-developed nodules aremainly poorly crystalline manganese oxides that associate with hydrated iron oxides and with a
Leptothrix discophora − like bacteria. EDX semi-quantitative analyses of the holdfasts indicatedthat iron precipitation occurred on the glass slides at an early stage. Manganese precipitation
occurred later during the iron precipitation and declined within 11 days. The mobilization andprecipitation paths for the dominant manganese in fresh water indicates the possible quick
formation of manganese nodules whose appearance is dependent on the specific biochemical
environment during oxidation and substitution of Mn2+. Experimental results indicated that thesemanganese nodules had a biogeochemical origin rather than an inorganic origin in freshwater.
Keywords: Bacteria, manganese nodules, freshwater, SEM, TEM.

Introduction
MnOx precipitation occurs in various environments such as in deep-sea sediments,
Mn-bearing ground water, lakes, streams and wetlands. Many microorganisms have theability to accumulate Fe and Mn from their external environments, especially from aquatic40

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

environments. Biomineralization in acid mine effluent revealed crystallized minerals ofiron and mixtures of manganese oxide (Mann and Fyfe, 1984, 1985, 1989; Mann et al.,
1992; Skinner and Fitzpatrick, 1992; Tanaka et al., 1994; Thamdrup et al., 1994; Snowball,
1994; Emerson and Revsbech, 1994 a). The dissolution and precipitation of manganese,
under natural conditions, is primarily mediated by microorganisms (Beveridge and Murray,
1976; Chapnick et al., 1982; Burdige and Kepkay, 1983; Ferris et al., 1988; Schmidt andRobbins, 1992; Robbins et al., 1992). In particular, manganese is largely oxidized by the“iron bacteria” group which precipitate amorphous or microcrystalline oxides and oxyhydroxides on their sheaths and holdfasts. Oxidation of manganese by bacteria occurs formany reasons and one of these serves to reduce the dissolved manganese content to below
toxic levels. Manganese precipitates as MnO2 in the form of angstrom-sized platelets(Nealson and Tebo, 1980; Beveridge and Fyfe, 1985; Doyle and Marquis, 1994).
Laboratory studies have provided evidence that “iron bacteria” commonly associated withneutral pH iron seep are responsible for most iron oxidation and that the presence offerrous iron appears to stimulate the growth of Lepthothrix ochracea and Gallionella spp.
(Emerson and Revesbech, 1994 b).
In this study, a laboratory simulation was undertaken to search for micrometer-sizedmanganese-bearing nodules that may have formed during several stages of precipitation
within half a month. We thus investigated a low-grade manganese-bearing fresh water
system to understand the role of bacteria.
Materials and methods
Samples for the laboratory simulation of water and sediments were collected fromthree spots at a pond close to Kanazawa University. Small streams run into this pond andbrownish microbial mats are found on the surface of river sediments. Three sediment
samples that were composed of clay sized grains (sample A), silt sized grains (sample B)
and sandy grains (sample C) were placed in separate glass beakers. Modern manganeseprecipitating iron bacteria were cultured in these glass beakers containing river water andsediments at pH 7-8 under photosynthetic conditions. A cover glass slide that was kept inwater for a few weeks to a few months at room temperature was used to observe
precipitated materials on the surface (Fig. 1 A). The initial river water, after removal of the>0.5 μm fraction using membrane filter paper (Fig. 1 B), was analyzed by atomic
absorption. The elemental composition of the water was as follows: Mn 1.03 ppm, Fe 0.25
ppm, Ca 76.00 ppm and K 18.00 ppm, at pH 6.5 − 6.8.
Initial sediments (Fig. 1 C) that were used in the three beakers were analyzed by Xray powder diffraction and showed mainly quartz and feldspars. No iron oxide minerals,
manganese oxide minerals or clay minerals were found in bulk samples as shown in Fig. 2.
Figure 1 E shows that a floater was used for glass cover slide A, and D is a lid for the
beaker.
The brownish bacterial colony on the glass slides that were coated with manganeseKazue TAZAKI and Tatsuya HATTORI

41

Fig. 1. A schematic diagram of the laboratory experiment.
Manganese-precipitating iron bacteria were studied
in beakers with fresh river water (B) and sediments(C) under photosynthetic conditions at pH 7.2 - 8.1.
The cover glass slide (A) keeps the water in for a
few weeks to a few months at room temperature. D;a lid of filter paper, E; a float for the glass slide.

Fig. 2. X-ray powder diffraction patterns of initial sediment bulk samples from three spots in a pond near
Kanazawa University. A; clay sized grains (sample A), B; silt sized grains (sample B), C; sandy
grains (sample C).

42

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteriaoxide minerals were observed using an optical microscope, a JEOL JSM-5200 scanningelectron microscope (SEM) equipped with a PV 9800 STD energy dispersion system and a
JEOL JEM 2000 EX transmission electron microscope (TEM). The pH and Eh of the water
were measured using a pH meter (Horiba M-8) and an Eh meter (Horiba D-13).
Mineralogical compositions of the brown materials on the slide cover glasses were
determined using a Rigaku X-ray powder diffractometer (XRD) (CuKα radiation).
Results
pH, Eh and XRD results
The water pH for all three beakers ranged from 7.2 to 8.1 and the water temperature
ranged from 15 to 24°
C during the experiment (Fig. 3). All samples A, B and C showed agradual increase in pH within 13 days. The Eh of the water in all three beakers ranged from−24 to +200 mV. The brownish material that precipitated on the cover glass slides after 13days contained a large amount of calcite (3.9, 3.0, 2.5, 2.29, 2.09 Å) and mica clay
minerals (10-9, 4.7-4.5, 3.3-3.2 Å) in all three samples A, B and C (Fig. 4). Sample A
produced a higher amount of mica clay minerals compared with samples B and C. Sample
B showed a strong refraction for crystalline calcite. No crystalline manganese or iron oxideminerals were found by XRD for these initial samples. Calcite and mica clay minerals
found in the precipitates originated from the elements in the beaker water. XRD patterns of
the thick brown precipitates showed a large background and this suggests the presence oflarge amounts of amorphous and/or organic materials. Based on SEM-EDX data and TEM
electron diffraction patterns, the amorphous or poorly crystallized precipitates are
identified as Mn-Fe rich materials. The brown to red colors of the precipitates are due toferrihydrite, goethite and lepidocrocite.

Fig. 3. pH values and water temperature of fresh water in all three beakers A, B and C during 13 days
aging. The three sediment samples of A, B and C are the same as in Fig. 2.

Kazue TAZAKI and Tatsuya HATTORI

43

Fig. 4. X-ray powder diffraction patterns of the brown precipitated holdfasts on the cover glass slidefrom all three beakers A, B and C. Cal; calcite.

Optical microscope observations
The cover glass slides of both thick-bedded and thin-bedded brownish precipitating
materials showed the microstructure of bacterial colony holdfasts which had a black andbrown doughnut shape and were 5-50 μm in diameter as seen using optical microscopy(Fig. 5). From sample beaker C, the diameter of these doughnuts became larger withexperimental time as shown in Fig. 5 A (3 days), B (5 days), C (7 days) and D-E (11 days).
In the initial experimental stages, brownish iron materials containing filamentous and/or
coccoidal microorganisms precipitated on glass surfaces (Fig. 5 A). Later in theexperiments black opaque manganese materials precipitated near the center of thedoughnuts (Fig. 5 C, D) and these materials completely covered the doughnuts when theexperiments neared completion (Fig. 5 E). The black materials became concentrated andformed spherical manganese nodules as the experiments progressed. The black color ofmanganese can easily be distinguished from the brown iron materials using optical
microscopy. The observed microstructure of the holdfasts at the initial stage of theexperiments revealed nucleation, distribution and radial growth of coccoidal (Leptothrix
discophora ‐ like) bacterial colonies (Fig. 6).

44

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

Fig. 5. Optical micrographs of holdfasts and colonized bacteria on the cover glass slide in beaker A. The
brown or black-coated holdfasts with manganese oxide minerals that transmitted light can notpass through. A; 3 day old sample showing small doughnut-shaped holdfasts with filamentous
and/or coccoidal colonies, B; 5 day old sample showing the radial growth of doughnuts‐shaped
holdfasts, C; 7 day old samples showing concentrated opaque manganese materials in the center,
D and E; 11 day old samples showing heavily condensed manganese nodules.

Kazue TAZAKI and Tatsuya HATTORI

45

Fig. 6. Optical micrograph of a doughnut-shaped holdfast at the initial stage showing bacterial colonies.

SEM observations
SEM micrographs showing various formation stages of the manganese nodules (Fig.
7) from their early stages (A) to their matured stages (B) were taken from a cover glass
slide that had been kept in water for 1-3 weeks. The holdfasts have a 1-5 μm hole in theircenters from where bacteria emerged. Mature holdfasts have a rounded morphology and ahole at their centers (Fig. 7 B). Holdfasts that were still intact became more doughnut
shaped with attached filaments. The holdfasts that were kept on a slide in water during along-term experiment precipitated manganese nodules that were so thick and high the hole
was almost filled with colonized precipitates (Fig. 8). The centers of the doughnut-shaped
holdfasts were 10 μm in diameter and were found to concentrate manganese oxidematerials (Fig. 8 B, C). Small amounts of Si, K and Ca were due to cover glass slide
components.
TEM observations
Both SEM and TEM micrographs revealed that the bacterial holdfasts were coatedwith thin films (Figs. 9 and 10). TEM observations especially revealed the microstructureof these doughnut-shaped holdfasts and showed that films and spheres were attached. Mnrich materials were found around the bacterial cell which indicates that Mn-precipitation
continues after the initial deposit on the cell wall (Fig. 9 A, B). The bacterium wascharacterized by the intense development of granular manganese aggregates at the cell wall
and within the internal structure (Fig. 9 C). TEM micrographs as shown in Fig. 10 A shows
the microstructure of the doughnut-shaped holdfasts wherein a bacterium cell is situated in
the center where films and spheres are attached. The holdfasts were composed of thick,mesh-like films and spheres that show electron diffraction of diffuse rings at 2.76, 2.18 and46

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

Fig. 7. SEM micrographs of holdfasts on the cover glass slide showing formation processes ofmanganese nodules. A; early formation stage, B; doughnut shaped holdfasts.

1.56 Å, suggesting a mixture of Mn and Fe oxide minerals are present (Fig. 10 B inset C).
The highly dense spheres of nm-size are manganese nodules. Some electron diffraction
spots were due to calcite and quartz d-spacings.
EDX analysis
The chemical composition of the doughnut-shaped holdfasts from all three beakers A,
B and C after 3, 5, 7 and 11 days are given in Table 1. An EDX analysis of the doughnutshaped holdfasts indicated that Si, K, Ca and Fe are its major components. Both Si and Ca
are most likely accounted for by considering the entrapped particles of quartz, calcite andclay minerals. The Si concentration in the holdfasts did not have the same chemicaltendency in the three beakers.
A semi-quantitative area analysis, without a standard sample, was done with EDX andthis showed the chemical tendency of the doughnut-shaped holdfasts with experimental
time. The small amounts of Na, Mg, Al, P, S, Cl, K and Ti were found to be unchanged
with experimental time whereas Ca, Mn and Fe gradually increased in all beakers. Holdfast

Kazue TAZAKI and Tatsuya HATTORI

47

Table 1. Semi-quantitative chemical analyses of doughnut-shaped holdfasts in all three beakers A, B andC at 3, 5, 7 and 11 days of aging using EDX analysis without a standard. The unit ofmeasurement is wt%.

48

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

Fig. 8. SEM micrographs of doughnut-shaped
holdfasts viewed from above (A), the side (B)and its EDX analysis (C) that shows Mn as amajor component.

Fig. 9. SEM micrographs (A, low magnification
image; B, high magnification image of
granules shown in A) and TEM
micrograph (C) reveals that bacteria in
the holdfast were coated by thin films.
Mn-rich material around the cell whichindicates that Mn precipitation continues
after an initial deposit on the cell wall.

Kazue TAZAKI and Tatsuya HATTORI

49

Fig. 10. TEM micrograph that demonstrates the microstructure of the doughnut-shaped holdfasts withbacterial cells situated within the center (A). TEM micrograph of thick films attached to thedoughnut-shaped holdfasts (B). High density spheres attached to the films are manganese nodules.
Diffused electron diffraction rings at 2.76, 2.18 and 1.56 Å (in set B) suggest that Mn-Fe oxideminerals are present.

concentrations of Mn and Fe in all three beakers A, B and C at 3, 5, 7 and 11 days areplotted in Fig. 11. The graph clearly indicates that the manganese content in all three
beakers increases whereas the iron content decreases. Sample A especially showed adramatic change in Mn and Fe counts, which is opposite to that found in the holdfast. For
samples B and C, both the Mn and Fe content were almost saturated within 7-11 days.

50

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

Fig. 11. Manganese and iron concentrations of doughnut-shaped holdfasts in the three beakers A, B andC after 3, 5, 7 and 11 days of aging.

Discussion
Formation processes of manganese nodules are very important for a better
understanding of the possible role of bacteria in the primary sedimentation process and inore-forming processes (Schmidt and Robbins, 1992; Konhauser et al., 1993). In this study,
bacterial mineralization processes were traced through manganese oxide (MnOx) nodules
by a laboratory simulation experiment. Results indicated that manganese nodules areformed biogeochemically rather than inorganically. Doughnut shaped bodies in thesemanganese ores resemble open-centered holdfasts of modern manganese-precipitating ironbacteria such as L. discophora (Schmidt and Robbins, 1992). The nodules consist of a
mixture of manganese oxide minerals and hydrated iron oxide minerals. This admixture ofiron and manganese is a typical modern microbial response and apparently also occurred in
the past. Hem and Lind (1983) reported on thermodynamic replacement conditions for Mn
and Fe phases in a diagram that depicted Eh, pH and Fe concentrations (Fig. 12). Our data
for this laboratory experiment is plotted in Fig. 12 (thick squares). In these reactions,manganese oxides and dissolved iron exchange electrons and manganese is reduced from
Mn4+ to Mn2+ (or Mn(OH)2). Pyrochroite normally precipitates under alkaline conditions.
Iron probably precipitates as ferrihydrite and replaces the mobilized manganese. New
manganese minerals such as manganite [MnO(OH)], groutite [Mn+3O(OH)], pyrolusite (BKazue TAZAKI and Tatsuya HATTORI

51

Fig. 12. The thermodynamic replacement conditions for Mn and Fe phases in a diagram depicting Eh,
pH and Fe concentrations; modified after Hem and Lind (1983). Our data is plotted as thicksquares.
-MnO2) etc. were formed much later in secondary ores by deep weathering processes. From
our results at higher than 0 mV (horizontal boundary; pH-independent) and at pH values
higher than 8 (vertical boundary; Eh-independent) manganese precipitation is gradually
increased, and the concentrations of both Fe and Mn in solution are directly related (Figs. 3,
11 and 12).
Mn oxide readily oxidizes ferrous Fe and pseudomorphs of Mn oxide were formed ona slide left in the test water during a long-term experiment (Golden et al., 1988). Iron may
be present in both a divalent and a trivalent ionic form. However, Fe2+ is stable over a muchlarger Eh and pH range than Fe3+. Generally, natural conditions restrict iron mobility to a
relatively acidic geochemical environment. In the reaction, manganese oxides anddissolved iron exchange electrons and manganese is reduced from Mn4+ to Mn2+.
Pyrochroite normally precipitates under alkaline conditions. Iron, on the other hand,probably precipitates as ferrihydrite and replaces the mobilized manganese (Pracejus andBolton, 1992).
In a natural river water system, living bacteria reproduce on surfaces and grow incolonies or as films of Mn-Fe oxide minerals. Schindler (1993) presented the dynamics of

52

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteriaa Bacillus colony growth. A young colony forms a round, convex body with a smooth orslightly matte surface and more or less sharp edges which can be described by Euclidean
geometry. Under appropriate conditions, colonies of bacilli, actinomycetes or clostridia andold colonies of other bacteria can develop into bizarre shapes with an irregular structuresuch as rough shrub-like radial sectors (Schindler, 1993). In the Bacillus model, an active
cell is randomly selected for each successive step of growth. A new cell is included into theset of active cells while the oldest cell is removed and thus the number of living cells
remains constant. A colony of bacteria is often simply regarded as a heap of
microorganisms (Tazaki, 1997). But the question of what a colony growth of bacteria thatform manganese nodules are remains. Factors that govern changes in cell morphology andmetabolic activity are not yet well defined. In this study, a laboratory simulation wasundertaken to find micrometer-size manganese nodules that were present at several stagesof formation within half a month. These produced manganese-bearing precipitates at pH 78 and Eh −24 to +200 mV suggesting growth up to ore-grade concentrations later on underbiochemical conditions in freshwater systems.
Conclusions
Manganese oxide (MnOx) nodules and Mn-oxidizing bacteria in a laboratory
simulation experiment showed evidence of an organic contribution to manganeseprecipitation in fresh water. We studied this behavior using an optical microscope, ascanning electron microscope, an energy dispersive X-ray analyzer and a transmission
electron microscope. Cover glass slides were kept in beakers with natural fresh water andsediments from a river were coated with brown-black materials, which were manganese
nodules of doughnut-shaped holdfasts of colonized bacteria. Doughnut-shaped bodies in
the manganese ores resembled open-centered holdfasts of modern manganese-precipitatingiron bacteria such as L. discophora. TEM and SEM observations revealed that manganesemineral formation processes occurred through the interaction of MnOx precipitation andbacterial activity. Under appropriate conditions, colonies of bacteria can develop roughradial forms with an amorphous or poorly crystallized structure. Electron diffraction
patterns showed that these nodules are composed of a mixture of manganese oxide andhydrated iron oxide minerals. An admixture of iron and manganese is a typical microbial
response at pH 7-8 and Eh −24 to+200 mV. Our laboratory simulation results indicated thatmanganese nodules are mainly produced biogeochemically rather than inorganically.
Acknowledgments
This work was supported by grants from the Ministry of Science, Culture and
Education of Japan to Kazue Tazaki.
References
Beveridge, T.J. and Murray, R.G.E. (1976) Uptake and retention of metals by cell walls ofKazue TAZAKI and Tatsuya HATTORI

53

Bacillus subtilis. Jour. Bacteriology, 127, 1502-1518.
Beveridge, T.J. and Fyfe, W.S. (1985) Metal fixation by bacterial cell wall. Can. J. Earth
Sci., 22, 1893-1898.
Burdige, D.J. and Kepkay, P.E. (1983) Determination of bacterial Mn oxidation rates in
sediments using an in situ dialysis technique. I. Laboratory studies. Geochimica et
Cosmochimica Acta, 47, 1907-1916.
Chapnick, S.D., Moore, W.S. and Nealson, K.H. (1982) Microbiologically mediatedmanganese oxidation in a fresh water lake. Limnological Oceanography, 27, 10041014.
Doyle, R.J. and Marquis, R.E. (1994) Elastic, flexible peptidoglycan and bacterial cell wall
properties. Trends in Microbiology, 2, 57-60.
Emerson, D. and Revsbech, N.P. (1994 a) Investigation of an iron-oxidizing microbial mat
community located near Aarhus, Denmark: Field studies. Applied and Environmental
Microbiology, 60, 4022-4031.
Emerson, D. and revsbech, N.P. (1994 b) Investigation of an iron oxidizing microbial mat
community located near Aarhus, Denmark: Laboratory studies. Applied andEnvironmental Microbiology, 60, 4032-4038.
Ferris F.G., Fyfe, W.S. and Beveridge, T.J. (1988) Metallic ion binding by Bacillus
subtilis: Implications for the fossilization of microorganisms. Geology, 16, 149-152.
Golden, D.C., Chen, C.C., Dixon, J.B. and Tokashiki, Y. (1988) Pseudomorphic
replacement of manganese oxides by iron oxides. Geoderma, 42, 199-211.
Hem, J.D. and Lind, C.J. (1983) Nonequilibrium models for predicting forms ofprecipitated manganese oxides. Geochemical et Cosmochimica Acta, 47, 2037-2046.
Konhauser, K.O., Fyfe, W.S., Ferris, F.G. and Beveridge, T.J. (1993) Metal sorption andmineral precipitation by bacteria in two Amazonian river systems: Rio Solimoes and
Rio Negro, Brazil. Geology, 21, 1103-1106.
Mann, H. and Fyfe, W.S. (1984) An experimental study of algal uptake of U, Ba, V, Co
and Ni from dilute solutions. Chemical Geology, 44, 385-398.
Mann, H. and Fyfe, W.S. (1985) Uranium uptake by algae: experimental and naturalenvironments. Can. J. Earth Sci., 22, 1899-1903.
Mann, H. and Fyfe, W.S. (1989) Metal uptake and Fe-, Ti-oxide biomineralization by
acidophilic microorganisms in mine-waste environments, Elliot Lake, Canada. Can. J.
Earth Sci., 26, 2731-2735.
Mann, H., Tazaki, K., Fyfe, W.S. and Kerrich, R. (1992) Microbial accumulation of ironand manganese in different aquatic environments: An electron optical study.
In: Biomineralization; Processes of iron an manganese. H.C.W. Skinner and R.W.
Fitzpatrick (Eds.), Catena Supplement, 21, 115-131.
Nealson, K.H. and Tebo, B. (1980) Structural features of manganese precipitating bacteria.
Origins of Life, 10, 117-126.
Pracejus, B. and Bolton, B.R. (1992) Interdependence of Mn, Fe, and clay mineral

54

Bacterial Contribution to Precipitation of Manganese Nodules in Freshwater Environments:
An Electron Microscope Study of Experimental Biomineralization by Cultured Bacteria

formation on Groote Eylandt, Australia: A model for modern and ancient weathering
environments. In: Biomineralization; Processes of iron and manganese. H.C.W.
Skinner and R.W. Fitzpatrick (Eds.), Catena Supplement, 21, 371-397.
Robbins, E.I., D’Agostino, J.P., Ostwald, J., Fanning, D.S., Carter, V. and Van Hoven, R.L.
(1992) Manganese nodules and microbial oxidation of manganese in the Huntley
Meadows wetland, Virginia, USA. In: Biomineralization; Processes of iron andmanganese. H.C.W. Skinner and R.W. Fitzpatrick (Eds.), Catena Supplement, 21, 179-202.
Schindler, J. (1993) Dynamics of Bacillus colony growth. Micro Biology, 1, 333-337.
Schmidt, F.G. and Robbins, E.I. (1992) New evidence of an organic contribution to
manganese precipitation in iron-formation and review of sedimentary conditions in
the Cuyuna north range, Minnesota. In: Biomineralization; Processes of iron andmanganese. H.C.W. Skinner and R.W. Fitzpatrick (Eds.), Catena Supplement, 21, 399-419.
Skinner, H.C.W. and Fitzpatrick, R.W. (1992) Iron and manganese biomineralization.
In: Biomineralization; Processes of iron and manganese. H.C.W. Skinner and R.W.
Fitzpatrick (Eds.), Catena Supplement, 21, 1-6.
Snowball, I.F. (1994) Bacterial magnetite and the magnetic properties of sediments in a
Swedish lake. Earth Planetary Science Letters, 126, 129-142.
Tanaka, A., Seyama, H. and Soma, M. (1994) Iron- and manganese-rich sediments as asindicator of hot spring activities at the bottom of Lake Mashu, Japan. Geochemical
Journal , 28, 289-306.
Tazaki, K. (1997) Biomineralization of layer silicates and hydrated Fe/Mn oxides in
microbial mats; An electron microscopical study. Clays and Clay Minerals, 45, 203212.
Thamdrup, B., Glud, R.N. and Hansen, J.W. (1994) Manganese oxidation and in situ
manganese fluxes from a coastal sediment. Geochimica et Cosmochimica Acta, 58,
2563-2570.