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Chemical Geology 21

Mg–silica precipitation in fossilization mechanisms of sand tufa

endolithic microbial community, Mono Lake (California)

Virginia Souza-Egipsya,*, Jacek Wierzchosb, Carmen Ascasoc, Kenneth H. Nealsona

aDepartment of Earth Sciences, University of Southern California, 3651 Trousdale Parkway, Los Angeles, CA 90089-0740, USAbServei de Microscopia Electronica, Universitat de Lleida, Rovira Roure 44, Lleida 25198, Spain

cCentro Ciencias Medioambientales, CSIC, Serrano 115 bis, Madrid 28006, Spain

Received 15 April 2004; received in revised form 5 November 2004; accepted 16 December 2004

Abstract

The detection of Mg–silica associated with endolithic biofilms of cyanobacteria and bacterial communities living in lake

shore sand tufa formations in Mono Lake (California) has been observed using scanning electron microscopy with

backscattered electron imaging (SEM–BSE) and energy-dispersive X-ray spectroscopy (EDS). Mg accumulated in cell walls of

living cyanobacteria is interpreted to promote Mg-silicification with structural preservation while non-cyanobacterial

prokaryotes are not fossilized. However, extracellular polymeric substances around the living communities were prominent

as nucleation sites for authigenic mineral precipitation: a Mg–silicate served to stabilize the biofilm remains. Further diagenesis

of these textures resulted in occlusion of the cytoplasm pore spaces by carbonate precipitates. This precipitate damaged the

microfossil structures but the Mg–silica fabric was still present. The paleontological significance of Mg–silica precipitates as a

possible biosignature of the former presence of endolithic biofilms is addressed.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Cyanobacteria; Silica precipitation; Biomineralization; Tufa

1. Introduction

Two different approaches have been identified in

the study of the fossilization mechanisms of micro-

organisms and the study of the Earth’s earliest life

forms (Konhauser et al., 2003). In one side, laboratory

0009-2541/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.chemgeo.2004.12.004

* Corresponding author. Present address: Centro de Astrobiologıa

CSIC-INTA, Ctra. Torrejon a Ajalvir Km 4, Torrejon de Ardoz

28850, Madrid, Spain. Tel.: +34 91 520 64 08; fax: +34 91 520 1074.

E-mail address: souzaev@inta.es (V. Souza-Egipsy).

studies using metabolic different microorganisms will

describe the preservation potential of specific micro-

organisms and the mechanisms of fossilization under

controlled conditions. And on the other side, the study

of the fossilization mechanisms of natural microbial

communities will provide the description of specific

fossilization mechanisms depending on the environ-

ment under study. These fossilization mechanisms

may depend also on the post-fossilization alteration

processes responsible for the final structure of the

geological deposits.

7 (2005) 77–87

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–8778

Current knowledge of fossils of microorganisms,

as traces of microbial activity on ancient Earth, tends

to be scarce in comparison to the wealth of

information available for present living microbial

biofilm and mat-building communities. The study of

such modern mat systems has led to the ability to

relate the basic physiological activities to structural

components and fabrics (Gerdes et al., 1993).

However, the physiological changes that occur upon

death and decay are much less well known. This lack

of knowledge of lithification and microfossil forma-

tion on the various components of diverse mat

communities is a major impediment bridging the

gap between the modern ecosystems and fossil

records (Walter et al., 1992). One of the steps needed

to reach such an understanding is the study of the

geobiological processes as they occur. We thus

present in this paper an in situ approach to the study

of the mineralogical changes related with the decay,

fossilization, and diagenic processes in an endolithic

microbial community.

The endolithic mode of life includes several differ-

ent ecological niches: chasmoendoliths and cryptoen-

doliths occupy preexisting fissures and structural

cavities in the rocks, whereas euendoliths penetrate

the rock by etching (Golubic et al., 1981). The

morphological description of the community structure

of microorganisms colonizing the inside of lithic

materials, and solid interfaces has presented enormous

technical challenges; challenges that have often dis-

couraged scientific involvement and delayed our

understanding of these complex systems. Recently,

new approaches based on scanning electron micro-

scopy operated in backscattered electron mode (SEM–

BSE) combined with an auxiliary X-ray energy-

dispersive spectroscopy (EDS) has been implemented

for the study of lithobiontic microbial communities

(Wierzchos and Ascaso, 1994, 2001; Ascaso and

Wierzchos, 1994). This technique permits the chem-

ical characterization of mineral features, and the

observation of the ultrastructural characteristic of the

cells without the need to remove them from their

microenvironment. Indeed, this in situ microscopic

method permits both the description of the living

community and the associated mineralization pro-

cesses, as well as the study of the mineralogical

changes associated with diagenetic events. This allows

one to interpret the microfossil structures from extant

microbial communities in the context of biominerali-

zation processes occurring in living and dying micro-

bial ecosystems, according to taphonomic principles as

suggested by Golubic and Seong-Joo (1999).

In this study we have applied such approaches to

the knowledge of the ultrastructure of the endolithic

communities from the shores of an alkaline salt lake at

California. Mono Lake is famous for the tufa towers

(Council and Benneth, 1993; Scholl and Taft, 1964)

but tufa deposits also occur as pavements of calcite

impregnate sands and silts beneath and adjacent to the

shoreline in areas saturated with brine (Rieger, 1992).

In this article we report the results of studies of sand

tufa microbial endolithic community dynamic pro-

cesses in situ. It is our long-term goal to be able to

recognize signs of past life in geological materials.

Through the description of the living and degradation

sequences of modern cyanobacteria and bacteria

endolithic communities it should be possible to

reconstruct the information lost during the selective

process of preservation, fossilization, and diagenesis

in the geological record.

2. Materials and method

Pieces of sand tufa from Navy Beach (southern

shore lake) were cut with a chisel and collected in

clean and sterile plastic bags. The samples were kept

cold (5 8C) and in the dark until processing. The

samples were processed for scanning electron micro-

scopy following the method published previously

(Ascaso and Wierzchos, 1994; Wierzchos and

Ascaso, 1994) with the following modifications:

they were chemically fixed with 2.5% glutaraldehyde

in filter-sterilized (0.2 Am) lake water. All samples

were then rinsed in filter sterilized lake water, and

post-fixed in 2% osmium tetroxide. During dehy-

dration with an ethanol series, samples were con-

trasted with saturated 70% ethanol uranyl acetate.

The samples were embedded in LR-White embed-

ding medium. Once polymerized the blocks were cut

transversally using a diamond saw, fine polished and

examined under a scanning electron microscope with

backscattered electron (BSE) detector plus an auxil-

iary X-ray energy-dispersive spectroscopy (EDS)

microanalytical system. Transverse sections of the

polished surfaces of the rocks were examined using a

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–87 79

DSM 940 A Zeiss SEM equipped with a BSE

detector and a Link ISIS microanalytical EDS

system. Prior to observation the samples were carbon

coated with a Polaron CA508 evaporation PSC

equipment. EDS operating conditions were as

follows: 08 tilt angle, 358 take-off angle (EDS), 15

kV acceleration potential, 10 or 25 (EDS) mm

working distance, and 1–5 nA specimen current.

For EDS semiquantitative point analysis following

internal standards were used: quartz for O and Si,

magnesium oxide for Mg, alumina for Al, and

wollastonite for Ca, respectively.

3. Results

The living sand tufa endolithic communities at the

shores of the lake were present in the sediment

covered with a crust of salts (Fig. 1a). Some of these

sediments are currently exposed due to the decrease in

the level of the lake (Fig. 1b) and it was possible to

observe that the precipitation of carbonates induces

Fig. 1. (a) General view of the sand tufa formation on the shores of the lake

of the lake level.

the preservation of the upper part of the sediment and

some columnar structures while other areas were

easily weathered. The detail image of the sand tufa

indicates that this crytoendolithic community is

confined to an exact area below the surface and has

a constant thickness of 1–2 mm (lines in Fig. 2a). The

sediment grains below the living community were

loose, while in the upper part they were attached to

each other through the carbonate precipitate (white

square in Fig. 2b). Fig. 2c is an image obtained with

the scanning electron microscope (SEM) operating in

backscattered electron (BSE) emission mode. The

BSE signal is strongly dependent on the mean atomic

number of the target (Joy, 1991) so that the image not

only reveals different contrasts of inorganic particles

but also allows the identification of microorganisms

by staining with heavy metals. The grey areas marked

with the stars are areas were the biofilm is present

between the brilliant sand particles (SP). In some

areas a precipitate was observed between the sand

particles and the biofilm (arrows Fig. 2c). The biofilm

in the area marked with a white square is magnified in

. (b) General view of the exposed sand tufa formations after receding

Fig. 2. (a) Optical image of the endolithic sand tufa community. Area between lines indicates situation of the endolithic green community. Width

of the image is 2 cm. (b) SEM–BSE general view of the sand tufa. White square area magnified in panel c. Bar=1 mm. (c) SEM–BSE image of

the polished cross-section. Stars indicate distribution of the biofilm. White square indicates living biofilm area magnified in panel d. Black

square indicates magnified area in Fig. 6a. Arrows indicate calcium carbonate precipitate around sand particles (SP). Bar=500 Am. (d) Detailed

image of the aspect of the biofilm. Living cells appear brilliant due to the presence of uranyl acetate and osmium tetroxide fixatives (L),

decaying cells exhibit a less brilliant interior (D), fossils remains as cell walls (F). Bar=20 Am. (e) Detailed image of the living cyanobacteria

(cb) and the bacteria cells (b) among them. Bar=10 Am. (f) Silica digital mapping distribution in panel d. (g) Magnesium digital mapping

distribution in panel d.

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–8780

Fig. 2d. The living biofilm is composed of unicellular

and filamentous cyanobacteria (cb) and bacterial (b)

communities. The living cyanobacterial cells (L)

exhibit a brilliant interior, whereas the decaying ones

(D) show much less contrasted cytoplasm, and it was

collapsed and detached from the cell walls. A detail

image of the biofilm shows the relation between

bacteria cells (b in Fig. 2e) and living cyanobacteria

cells (cb in Fig. 2e). Only the remains of the

cyanobacteria cell walls can be recognized fossilized

in the biofilm (F in Fig. 2d) due to the accumulation

of silica–magnesium precipitate. The EDS and digital

mappings of silica and magnesium were similar (Fig.

2f and g) in the area shown in Fig. 2d and showed a

Fig. 3. Comparison of the Mg and Si composition (EDS wt.%) of

deposits present between sand particles (arrows in Fig. 2c), and

mineral deposits associated with live (L in Fig. 2d), decaying (D in

Fig. 2d), and fossil cyanobacteria cell walls (F in Fig. 2d). The fossil

remains and the precipitate around sand particles have a higher

amount of silica than the decaying cells. Living cells have no

detectable amount of silica and almost the same amount of

magnesium as the decaying cells.

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–87 81

sequence in the permineralization of the cell walls

related to the post-mortem processes in the biofilm.

Note that an increased amount of mineral precipitate

Fig. 4. SEM–BSE image (a) and digital mapping of the different precipi

(Fig. 1b). (b) Magnesium map; (c) aluminum; (d) silica; (e) potassium

(asterisk in Fig. 5A) that correspond to areas with the presence of remains

and Mg (arrows in panel B and white square in A).

was observed in the areas corresponding to the

cyanobacteria decayed cell walls (star in Fig. 2f).

Silica and magnesium were also uniformly distributed

around the extracellular polymeric substances (arrow

Fig. 2f).

Semiquantitative point EDS analysis of the element

concentrations in weight percent (wt %) established

that the levels of Mg and Si were different in the

mineral deposits associated with live, decaying, and

fossil cells (Fig. 3). The living cells showed the

presence of Mg, with little or no Si, while the

decaying cells contained an increased amount of Si,

often equal to or greater than the amount of Mg.

Fossilized cell walls had a higher proportion of Si than

Mg, with ratios similar to those found precipitated in

the Mg–silica matrix among sand particles in the

endolithic community area (stars in Fig. 4).

The sand tufa consists mostly of calcite-cemented

pumice sand, formed in beach sediments near the

shore of the lake saturated with brine. The digital

tates among the sand particles in the exposed sand tufa formation

; (f) calcium. Among sand particles there are Mg–Si precipitates

of biofilm. Around the sand particles there is a precipitation of Ca

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–8782

mapping of the area near the surface also showed

other precipitates among the sand particles (stars Fig.

4a) formed of Mg–silica (Fig. 4b, d). The coatings

around the sand particles were formed from a mix of

magnesium and calcium (arrows Fig. 4b, f). A

detailed study of these coatings (square Fig. 4a) with

Linescan distribution of Ca and Mg (Fig. 5) showed a

banded pattern indicating different episodic precip-

itation reflecting differences in the solution around the

sediments. The low-magnesium calcite precipitate

was present around most of the sand particles and

around Mg–silica areas formerly colonized by living

biofilm.

Fig. 5. SEM–BSE magnified image of the area marked with a white square

the transect indicate in the image. The precipitation around the sand partic

pattern in the image and compositional analysis.

In some zones in the endolithic microbial com-

munity, life, and/or decaying cells were not observed

(Fig. 6a corresponds to magnified black square from

Fig. 2c). The size of the voids in the Mg–silica

precipitate can be related to the space occupied by the

cytoplasm of the cyanobacteria. Since the voids are

observed to be empty, permineralization of the interior

of the cells does not occur, only the cell walls had

been effectively fossilized and were present inside a

matrix of Mg–silica precipitate. The presence of the

matrix surrounding the cell wall remains indicates that

the bacterial extracellular polymers were effective at

binding ions from solution and serving as nucleation

in Fig. 4a with Linescan of Ca (black line) and Mg (grey line) around

les has a variable proportion of Mg and Ca as shown by the banding

Fig. 6. SEM–BSE images of the biofilm fossil remains in the sand tufa sediment (Fig. 1a). (a) Magnified area from black square in Fig. 2c. The

remains of the cell walls are immersed in a matrix of magnesium and silica. Most of the remains have the interior empty but outer edge

structures (white arrows) are becoming filled with calcium carbonate precipitated. In some areas (black arrow) the precipitated is penetrating the

matrix. Small images are the digital mapping of the elements Mg (b), Si (c), and Ca (d) present in the same area of the image. Bar=20 Am.

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–87 83

surfaces for mineral formation. The digital mappings

of Mg and Si in the area shown in Fig. 6a had a

similar distribution (Fig. 6b and c). One important

Fig. 7. SEM–BSE images of the biofilm fossil remains in the exposed sa

particle (white arrow on the upper left corner). The fossil remain was becom

the lower part of the image). Remains of the cyanobacterial cell walls (bl

indicates the presence of the Mg–silica biologically induced mineral prec

factor in the fossilization process observed in this

environment is that there were changes in the

bioinduced mineralized materials with time. This

nd tufa sediment (Fig. 1b). (a) Calcium carbonate around the sand

ing surrounded by a new ring of calcite precipitate (white arrow on

ack arrow). Chemical composition (digital mapping, panels b, c, d)

ipitate. Bar=20 Am.

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–8784

aspect is related with the physico-chemical conditions

of the environment, as there is a close contact with the

surrounding lake water and ions present. Silicification

of the cyanobacteria cell walls does not seem to

permanently preserve the microbial remnants; after

the cytoplasmic decay, the area became infiltrated

with calcium carbonate. Fig. 6 shows how part of the

empty cytoplasmatic spaces were starting to be filled

with a calcium carbonate precipitate (white arrows in

Fig. 6a) and was in other areas the growth of the new

carbonate crystals were displacing the Mg–silica

matrix (black arrow in Fig. 6a).

The calcite precipitation is a periodic process that

affects the surface of the sand particles and

permineralized biofilm remains (Fig. 4). On older

formations such as the exposed shore sediments

(Fig. 1b), we found some fossil microbialites. In

Fig. 7a there was a ring of calcium carbonate

around the sand particle (white arrow on the upper

left corner), and over this there was a fossil remain

of the biofilm that was becoming surrounded by a

new ring of calcite precipitate (white arrow on the

lower part of the image). Between these two

coatings, in the Mg–silica precipitate, it was possible

to distinguish the remains of the cyanobacterial cell

walls (black arrow Fig. 7a). However, the deposit of

calcium carbonate around the remains of the fossil

biofilm area was inducing the damage of the fossil

remains. In some areas the cell wall structure was

not present anymore, although the chemical compo-

sition (digital mapping in Fig. 7b, c) indicates the

presence of the Mg–silica biologically induced

mineral precipitate.

4. Discussion

The adsorption of magnesium in dead or decaying

cell structures and organic matter is an important

factor to take into account in the preservation potential

of the microorganism and extracellular polymers at

Mono Lake. Our observations indicate a biological

influence in the presence of Mg–silica precipitates.

There is a correlation between areas of biofilm

presence and Mg adsorption and finally Mg–silica

complexation. With this in situ approach it was

possible to see that the Mg2+ adsorption process was

related to decay and post-mortem processes at the

cyanobacteria cell walls. It has been demonstrated that

bacteria and cyanobacteria have the ability to bind and

to complex metallic cations (Beveridge and Fyfe,

1985; Beveridge, 1989; Schultze-Lam et al., 1993;

Benning et al., 2004). The possible inhibition of the

autocatalytic degradion activity of the cyanobacteria

by magnesium can be explained by data which show

that autolysis tend to be inhibited by other metal

cations (Ferris et al., 1988). Differences in the size and

cell wall structure between cyanobacteria and other

bacteria during the process of fossilization might

explain the different affinity to Mg2+ and thus the

absence of visual remains of smaller bacteria in the

sediment. Recently, Mg–Si permineralization of cell

walls was reported as a possible explanation for the

preservation of green algae remains in subfossil

microbialites of Lake Satonda (Arp et al., 2003).

Schultze-Lam et al. (1996) noted that Gram-positive

bacteria have a higher metal-binding capacity than

Gram-negative bacteria and this aspect has implica-

tions in the fossilization potential as shown in

experimental silicification studies (Westall et al.,

1995; Toporski et al., 2002) and in geothermal hot

springs (Schultze-Lam et al., 1995; Jones and Renaut,

1997; Konhauser et al., 2001). The extent to which the

cells were degraded by their own autocatalytic

enzymes effectively determined whether intact struc-

tures conforming to the original morphology can be

silicified and preserved in the sediments.

Mono Lake is a high pH alkaline lake where at pH

above 9 the solubility of amorphous silica rises sharply

due to the formation of silicate ion (Govett, 1961):

SiðOHÞ4 þ ðOHÞ�YSiOðOHÞ�3 þ H2O

Proposed silicification models at neutral pH ranges

(Leo and Barghoorn, 1976) consider polysilicic acid

as the agent in petrification by means of the attach-

ment of silica molecules to available groups; further

polymerization will lead to the formation of a

precipitate. Recent laboratory experiments demonstra-

ted that neutral undersaturated solutions of Si dis-

played low affinity and did not nucleate onto

cyanobacteria surfaces (Yee et al., 2003). However,

experiments conducted with ferrihydrite-coated cya-

nobacteria significantly increased the rate of Si

removal from the solutions (Yee et al., 2003). In our

field site the pH induces the formation of silica ions

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–87 85

that are available to react with the decaying cyano-

bacteria with Mg2+ onto the surfaces. A similar

process should happen into the extracellular poly-

meric substances around decaying biofilms. Recent

studies on the formation of subfossil microstromatolic

crusts suggested that a primary carbonate mineral may

have been replaced by the amorphous Mg–Si layers

present in the microbialites (Arp et al., 2003).

Although in our samples low-Mg calcite was present

around the sand particles, it was absent from the area

where the biofilm was present. Therefore, in high-pH

alkaline water–sand interface, Mg–silica precipitation

is induced on the surface of the cyanobacteria and

extracellular polymeric substances during the decay-

ing processes of the biofilm.

The particular distribution of Mg–silica precipita-

tion on the sediment indicates the biological influence

in the formation. Chemical Mg–hydroxysilicate pre-

cipitation is likely to occur in carbonate-containing

siliceous sediments because the CaCO3 dissolution

helps to maintain pH values near 8 (Kent and Kastner,

1985), a hydrated amorphous Mg–Si phase was

reported to form within sediments in other alkaline

lakes (Spencer et al., 1985). However in the sand tufa

formations it is not homogeneously distributed. This

precipitate only occurs in the area where the living or

decaying biofilm was present. In the search of the first

fossil record of microorganisms that lived on Earth,

and in the search of life or its fossil record on Mars, it

might be possible to find minerals formed by, or in

association with microorganisms. Previous studies

have proved the present of oxyhydroxides precipitates

associated with living bacteria in Antarctic sandstones

(Wierzchos et al., 2003). When the bacteria died, the

biogenecity of these precipitates was assessed through

the special distribution and morphological features

presented in contrast to the surrounding minerals. This

was an example of how bacteria can template mineral

crystallization, resulting in biosignatures of evidence

of past life in the sediments.

In contrast with the heterogeneity in the distribu-

tion of the Mg–silica precipitates, the distribution of

low magnesium calcite coatings around the sediment

particles presents a homogenous distribution. The

banding pattern, shown with the linescan analysis,

indicates variations in the solutions during time.

Variation in Ca2+ and Mg2+ content in the coatings

around sand particles is probably the result of

pronounced seasonality with stronger evaporation

during summer in front of conditions in the winter

rainy season. Recently, Eggins et al. (2004) have

shown a similar banding in the tests of Orbulina

universa, a foraminifera. They explain the bandings

as a consequence of the day–night variations in pH

due to the activity of the algal symbionts. The same

process can be happening around the area where the

biofilm is present in the sand tufa. The activity of the

biofilm can induce microenvironmental variations in

the pore water around the grains resulting in differ-

ences of Mg/Ca precipitation.

During diagenesis, physico-chemical alteration of

the fossil remains occurred. Similar processes were

also observed by Oehler (1976) during the exper-

imental fossilization of cyanobacteria filaments in

synthetic chert. In those experiments, morphological

alterations of the fossil remains occurred due to quartz

crystallization, as radial expansion of growing quartz

spherulites displaced the cyanobacterial-mineralized

material. In the sand tufa formation, the continuous

precipitation of calcite also provokes the alteration of

the fossil remains. In some areas of the sand tufa, the

Mg–Si precipitates show no evidence for a former

presence of cyanobacteria or bacteria dominated

biofilms. However, the shape and spatial distribution

of these precipitates indicates the presence of micro-

bial communities in the sand tufa. The in situ study of

the diagenetic changes that induce physico-chemical

alterations of microfossils have a clear importance in

the recognition of the fossil remains of biofilms in

geological material.

5. Conclusions

The microenvironment around the endolithic com-

munities during the fossilization process influences

the fidelity of microbial preservation and also has an

increasing importance in paleoecological reconstruc-

tions of the microbial habitat. In Mono Lake sand tufa

formations the precipitation of calcite is a process that

creates coatings around the sand particles but calci-

fication is not happening around the living and

decaying microorganisms while they are alive. Post-

mortem events lead to the accumulation of Mg–silica

in the biofilm area, influencing the preservation and

formation of fossil remains. However, the preserva-

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–8786

tion potential of these structures is finally controlled

by the continuous precipitation of calcite in the

environment. The biosignature of the former presence

of an endolithic biofilm in sand tufa formations will

be the presence of Mg–silica precipitate between the

calcite and sand particles.

The study of in situ microbe–mineral interactions

revealed the transition between accumulations of

elements in the living biofilm to post-mortem

nucleation sites and the influence of the environ-

mental conditions in the preservation of the biosigna-

tures in the geological record.

Acknowledgements

We are grateful to Alicia Thompson (Center for

Electron Microscopy) and Dr. Frank Corsetti (Depart-

ment of Earth Sciences) at University of Southern

California for their assistance and support. Thanks are

due to Dr. Rafael Rodriguez Ochoa for helpful

comments and discussions. Dr. H. Sun kindly guided

in the collection of the samples. V. S-E was supported

by a post-doctoral grant Secretarıa de Estado de

Educacion y Universidades (Spain). The Spanish

MCyT supported the present research under project

REN2003-07366-CO2-02. [LW]

References

Arp, G., Reimer, A., Reitner, J., 2003. Microbialite formation in

seawater of increased alkalinity, Satonda Crater Lake, Indonesia.

J. Sediment. Res. 73 (1), 105–127.

Ascaso, C., Wierzchos, J., 1994. Structural aspects of the lichen–

rock interface using back-scattered electron imaging. Bot. Acta

107, 251–256.

Benning, L.G., Phoenix, V.R., Yee, N., Konhauser, K.O., 2004. The

dynamics of cyanobacterial silicification: an infrared micro-

spectroscopic investigation. Geochim. Cosmochim. Acta 68,

743–757.

Beveridge, T.J., 1989. Role of cellular design in bacterial metal

accumulation and mineralization. Annu. Rev. Microbiol. 43,

147–171.

Beveridge, T.J., Fyfe, W.S., 1985. Metal fixation by bacterial cell

walls. Can. J. Earth Sci. 22, 1893–1898.

Council, T.C., Benneth, P.C., 1993. Geochemistry of Ikaite

formation at Mono Lake, California: implications for the origin

of tufa mounds. Geology 21, 971–974.

Eggins, S.M., Sadekov, A., De Deckker, P., 2004. Modulation and

daily banding of Mg/Ca in Orbulina universa tests by simbiont

photosynthesis and respiration: a complication for seawater

thermometry. Earth Planet. Sci. Lett. 225, 411–419.

Ferris, F.G., Fyfe, W.S., Beveridge, T.J., 1988. Metallic ion binding

by Bacillus subtilis: implications for the fossilization of micro-

organism. Geology 16, 149–152.

Gerdes, G., Claes, M., Dunajtschik-Piewak, K., Krumbein, W.E.,

Reineck, H.E., 1993. Contribution of microbial mats to

sedimentary surface structures. Facies 29, 61–74.

Golubic, S., Seong-Joo, L., 1999. Early cyanobacteria fossil record:

preservation, palaeoenvironments and identification. Eur. J.

Phycol. 34, 339–348.

Golubic, S., Friedmann, I., Schneider, J., 1981. The lithobiontic

ecological niche, with special reference to microorganisms.

J. Sediment. Petrol. 51, 475–478.

Govett, G.J.S., 1961. Critical factors in the colorimetric determi-

nation of silica. Anal. Commun. 25, 69–80.

Jones, B., Renaut, R.W., 1997. Formation of silica oncoids around

geysers and hot springs at el Tatio northern Chile. Sedimentol-

ogy 44, 287–304.

Joy, D.C., 1991. An introduction to Monte Carlo simulation.

Scanning Microsc. 5, 329–337.

Kent, D.B., Kastner, M., 1985. Mg2+ removal in the system Mg2+

-amorphous SiO2–H2O by adsorption and Mg–hydroxylicate

precipitation. Geochim. Cosmochim. Acta 49, 1123–1136.

Konhauser, K.O., Phoenix, V.R., Bottrell, S.H., Adams, D.G., Head,

I.M., 2001. Microbial–silica interactions in Icelandic hot spring

sinter: possible analogues for some Precambrian siliceous

stromatolites. Sedimentology 48, 415–433.

Konhauser, K.O., Jones, B., Reysenbach, A.-L., Renault, R.W.,

2003. Hot spring sinters: key to understanding Earth’s earliest

life forms. Can. J. Earth Sci. 40, 1713–1724.

Leo, R.F., Barghoorn, E.S., 1976. Silicification of wood. Bot. Mus.

Leaf., Harv. Univ. 25, 1–47.

Oehler, J.H., 1976. Experimental studies in Precambrian paleonto-

logy: structural and chemical changes in blue green algae during

simulated fossilization in synthetic chert. Geol. Soc. Amer. Bull.

87, 117–129.

Rieger, T., 1992. Calcareous tufa formations, Searles Lake and

Mono Lake. Calif. Geol. 45, 99–109 (July/August).

Scholl, D.W., Taft, W.H., 1964. Algae, contributors to the formation

of calcareous tufa, Mono Lake, California. J. Sediment. Petrol.

34, 309–319.

Schultze-Lam, S., Thompson, J.L., Beveridge, T.J., 1993. Metal ion

immobilization by bacterial surfaces in fresh water environ-

ments. Water Pollut. Res. J. Can. 28, 51–81.

Schultze-Lam, S., Ferris, F.G., Konhauser, K.O., Wiese, R.G., 1995.

In situ silicification of an Icelandic hot spring microbial mat:

implications for microfossil formation. Can. J. Earth Sci. 32,

2021–2026.

Schultze-Lam, S., Fortin, D., Davis, B.S., Beveridge, T.J., 1996.

Mineralization of bacterial surfaces. Chem. Geol. 132, 171–181.

Spencer, R.J., Eugster, H.P., Jones, B.F., 1985. Geochemistry of

Great Salt Lake, Utah: II. Pleistocene–Holocene evolution.

Geochim. Cosmochim. Acta 49, 739–747.

Toporski, J.K.W., Steele, A., Westall, F., Thomas-Keprta, K.L.,

McKay, D.S., 2002. The simulated silicification of bacteria—

new clues to the modes and timing of bacteria preservation and

V. Souza-Egipsy et al. / Chemical Geology 217 (2005) 77–87 87

implications for the search for extraterrestrial microfossils.

Astrobiology 2, 1–26.

Walter, M.R., Bauld, J., Des Marais, D.J., Schopf, W.J., 1992. A

general comparison of microbial mats and microbial stroma-

tolites: bridging the gap between the modern and the fossil.

In: Schopf, W.J., Klein, C. (Eds.), The Proterozoic Biosphere:

A Multidisciplinary Approach. Cambridge University Press,

New York, pp. 335–338.

Westall, F., Boni, L., Guerzoni, M.E., 1995. The experimental

silicification of microorganisms. Palaeontology 38, 495–528.

Wierzchos, J., Ascaso, C., 1994. Application of back-scattered

electron imaging to the study of the lichen–rock interface.

J. Microsc. 175, 54–59.

Wierzchos, J., Ascaso, C., 2001. Life, decay and fossilisation of

endolithic microorganisms from the Ross Desert Antarctica:

suggestion for in situ further research. Polar Biol. 24,

863–868.

Wierzchos, J., Ascaso, C., Sancho, L.G., Green, A., 2003. Iron-rich

diagenetic minerals are biomarkers of microbial activity in

Antarctic rocks. Geomicrobiol. J. 20 (1), 15–24.

Yee, N., Phoenix, V.R., Konhauser, K.O., Benning, L.G., Ferris,

F.G., 2003. The effect of cyanobacteria on silica precipitation at

neutral pH: implications for bacterial silicification in geothermal

hot springs. Chem. Geol. 199, 83–90.