The role of microbes in accretion, lamination and early lithification of modern marine stromatolites

Abstract

For three billion years, before the Cambrian diversification of life, laminated carbonate build-ups called stromatolites were widespread in shallow marine seas. These ancient structures are generally thought to be microbial in origin and potentially preserve evidence of the Earth's earliest biosphere. Despite their evolutionary significance, little is known about stromatolite formation, especially the relative roles of microbial and environmental factors in stromatolite accretion. Here we show that growth of modern marine stromatolites represents a dynamic balance between sedimentation and intermittent lithification of cyanobacterial mats. Periods of rapid sediment accretion, during which stromatolite surfaces are dominated by pioneer communities of gliding filamentous cyanobacteria, alternate with hiatal intervals. These discontinuities in sedimentation are characterized by development of surface films of exopolymer and subsequent heterotrophic bacterial decomposition, forming thin crusts of microcrystalline carbonate. During prolonged hiatal periods, climax communities develop, which include endolithic coccoid cyanobacteria. These coccoids modify the sediment, forming thicker lithified laminae. Preservation of lithified layers at depth creates millimetre-scale lamination. This simple model of modern marine stromatolite growth may be applicable to ancient stromatolites.

Full text

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The role of microbes in accretion,
lamination and early lithi®cation
of modern marine stromatolites
R. P. Reid*, P. T. Visscher², A. W. Decho³, J. F. Stolz§, B. M. Beboutk,
C. Dupraz*, I. G. Macintyre¶, H. W. Paerl#, J. L. Pinckney**,
L. Prufert-Beboutk, T. F. Steppe#& D. J. DesMaraisk
*MGG-RSMAS, University of Miami, 4600 Rickenbacker Causeway, Miami,
Florida 33149, USA
²Department of Marine Sciences, University of Connecticut, Groton,
Connecticut 06340, USA
³School of Public Health, University of South Carolina, Columbia,
South Carolina 29208, USA
§Department of Biological Sciences, Duquesne University, Pittsburgh,
Pennsylvania 15282, USA
kNASA Ames Research Centre, Moffett Field, California 94035, USA
¶National Museum of Natural History, Smithsonian Institution,
Washington DC 20560, USA
#Institute of Marine Sciences, University of North Carolina, Morehead City,
North Carolina 28557, USA
** Department of Oceanography, Texas A&M University, College Station,
Texas 77843, USA
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For three billion years, before the Cambrian diversi®cation of life,
laminated carbonate build-ups called stromatolites were wide-
spread in shallow marine seas1,2. These ancient structures are
generally thought to be microbial in origin and potentially
preserve evidence of the Earth's earliest biosphere1±3. Despite
their evolutionary signi®cance, little is known about stromatolite
formation, especially the relative roles of microbial and environ-
mental factors in stromatolite accretion1,3. Here we show that
growth of modern marine stromatolites represents a dynamic
balance between sedimentation and intermittent lithi®cation of
cyanobacterial mats. Periods of rapid sediment accretion, during
which stromatolite surfaces are dominated by pioneer com-
munities of gliding ®lamentous cyanobacteria, alternate with
hiatal intervals. These discontinuities in sedimentation are char-
acterized by development of surface ®lms of exopolymer and
subsequent heterotrophic bacterial decomposition, forming thin
crusts of microcrystalline carbonate. During prolonged hiatal
periods, climax communities develop, which include endolithic
coccoid cyanobacteria. These coccoids modify the sediment,
forming thicker lithi®ed laminae. Preservation of lithi®ed layers
at depth creates millimetre-scale lamination. This simple model
of modern marine stromatolite growth may be applicable to
ancient stromatolites.
The only known examples of stromatolites presently forming in
open marine environments of normal seawater salinity are on the
margins of Exuma Sound, Bahamas4±6. Our study focused on well-
laminated build-ups at Highborne Cay (768499W, 2 48439N) as
potential analogues of ancient stromatolites extending back to the
Precambrian. Highborne Cay stromatolites form in the back reef
zone of an algal-ridge fringing reef complex that extends 2.5 km
along the eastern shore of the island, facing Exuma Sound7. Surface
waters have a salinity of 36± 37 parts per thousand and are saturated
with respect to both aragonite and calcite. Stromatolites form as
intertidal and subtidal build-ups, shoreward of the algal ridge.
Results reported here pertain to the subtidal stromatolites, which
grow in depths of less than 1 m at mean low tide and form ridges and
columnar heads up to half a metre high (Fig. 1).
Surfaces of Highborne Cay stromatolites are covered with cyano-
bacterial mats. Examination of these mats using a variety of
integrated geological and microbiological techniques reveals
variations in microbial community structure and composition.
Extensive ®eld sampling over a two-year period revealed three
mat types, representing a continuum of growth stages with minimal
seasonal variability (Fig. 2).
Type 1: About 70% of all mats examined consist of a sparse
population of the ®lamentous cyanobacterium Schizothrix sp.8.
Schizothrix ®laments are generally vertically orientated and are
entwined around carbonate sand grains (Fig. 2a and b).
Type 2: Approximately 15% of mats show development of
calci®ed bio®lms, which appear as thin crusts of microcrystalline
carbonate (micrite) at the uppermost surface of the mat (Fig. 2c and
d). These ®lms are about 20±60 mm thick; they drape over and
bridge interstitial spaces between sand grains. Silt-sized carbonate
particles, such as tunicate spicules, are commonly embedded in the
®lms. Cyanobacterial ®laments are present, but are not abundant
in the bio®lms, which are comprised mainly of copious amounts
of amorphous exopolymer, metabolically diverse heterotrophic
microorganisms9±11 and aragonite needles. Needle-shaped aragonite
crystals, approximately 1 mm in length, form spherical aggregates
2±5mm in diameter and are embedded in the exopolymer matrix
(Fig. 2e). Bacteria are abundant and are commonly observed at the
edges of the aragonite spherules (Fig. 3). A sparse to moderately
dense population of Schizothrix underlies the exopolymer bio®lm
(Fig. 2c).
Type 3: The remaining 15% of mats are characterized by an
abundant population of the coccoid cyanobacterium Solentia sp.
and randomly-orientated Schizothrix ®laments below a calci®ed
bio®lm (Fig. 2f and g). Solentia is an endolith, which bores into
carbonate sand grains. These bored grains appear grey when viewed
in plane polarized light in a petrographic microscope (Fig. 2f),
contrasting with the golden-brown colour of unbored grains (Figs
2a and c). The microbored grains are often fused at point contacts
and appear `welded' together (Fig. 2f and g).
The variations in surface mats described above represent changes
in microbial community structure and activity in response to
intermittent sedimentation. Type 1 mats, characterized by a
sparse population of Schizothrix ®laments, resemble pioneer
communities12, which dominate during periods of sediment accre-
tion. Formation of these mats during intervals of rapid sedimenta-
tion is documented by ®eld observations showing that accretion
rates of one grain-layer per day produce mats with Type 1 fabrics.
The activities of Schizothrix, in particular, photosynthetic produc-
tion of exopolymer, are crucial in the accretion process. Flume
studies show that sand grains, which settle from suspension when
¯ow rate is low, adhere to mucous-like exopolymer (B.M.B.,
unpublished video recordings). These `trapped' grains are subse-
quently bound by ®laments and exopolymer as Schizothrix moves
upward to the sediment surface. Populations of diatoms and other
eukaryotes are minor to absent in these accreting mats8,13,14 indicat-
ing that, contrary to previous reports15,16, eukaryotic organisms are
not required for the trapping and binding of coarse-grained sedi-
ment. Aragonite precipitation is inhibited during this stage through
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Figure 1 Shallow subtidal stromatolites, Highborne Cay, Bahamas. a, Extensive columnar
build-ups. b, Vertical section showing lamination; scale bar, 2 cm.
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calcium ion binding by exopolymer and low-molecular-weight
organic acids excreted by Schizothrix11.
Type 2 mats represent a more mature12,17 surface community
characterized by development of a continuous surface ®lm of
exopolymer. This mat type develops during quiescent periods
when sedimentation ceases and mats begin to lithify. Formation
during calm periods is indicated by carbonate silt, such as tunicate
spicules, which is commonly entrapped in the surface ®lms but is
characteristically lacking in Type 1 mats. Mesocosm manipulations
suggest that continuous surface bio®lms form in a matter of days.
These surface ®lms support heterotrophic activity of both aerobic
and anaerobic bacteria9,11, which metabolize the low-molecular-
weight organic compounds and the labile fraction of the amorphous
exopolymer10,11. Sulphate reduction takes place despite the presence
of oxygen at the surface and sulphate-reducing bacteria account for
a signi®cant fraction (30± 40%) of the organic carbon consumption
by the community9,10. This bacterial activity promotes aragonite
precipitation as evidenced by microscale observations that high
rates of sulphate reduction coincide with micritic crusts18.In
addition, microautoradiography of radiolabelled organic matter
shows a close association between bacteria and aragonite needles
(H.W.P., unpublished data). The net result of these processes is
calci®cation of the bio®lm and formation of a thin micritic crust.
When additional carbonate sand is accreted onto the stromatolite,
this surface-coating ®lm persists into the subsurface as a nearly
continuous thin sheet of micritic cement.
Longer hiatal periods allow formation of Type 3 mats, which are
more fully developed than Type 2 mats and include an abundant
population of the coccoid cyanobacterium Solentia sp. These
Solentia-rich mats represent the `climax' community of the stro-
matolite system (Fig. 2). Excretion products of Solentia and
Schizothrix support high rates of bacterial respiration10,12. Micro-
scopy and culture experiments have revealed an unusual process of
boring and in®lling associated with Solentia19,20. Boreholes are
®lled in with aragonite as Solentia advances19,20. Moreover, as
Solentia crosses between grains at point contacts, in®lling of the
microbored tunnels obliterates grain boundaries and grains become
fused together (Fig. 2g). Observations of organic matter in some
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Figure 2 Dominant prokaryotic communities on stromatolite surfaces. Cycling between
communities, indicated by large arrows, is a response to intermittent sedimentation (see
text). a,b, Pioneer community: ®lamentous cyanobacteria (arrows) bind carbonate sand
grains. c±e, Bacterial bio®lm community: a continuous sheet of amorphous exopolymer
(arrows, c,d) with abundant heterotrophic bacteria (Fig. 3) forms uppermost surface;
aragonite needles precipitate within this surface ®lm (e). f,g, Climax community: a
surface bio®lm overlies ®lamentous cyanobacteria and endolith-infested grains, which
appear grey and are fused (arrow, f). Precipitation in tunnels that cross between grains
leads to welding (g). a,c,f, Petrographic thin sections, plane polarized light;
cyanobacteria are stained with methylene blue. b,d,e,g, Scanning electron microscope
images. Scale bars: a,b,c,f, 100 mm; d,50mm; e,5mm; g,10mm.
Figure 3 Scanning laser confocal microscope image of a surface bio®lm. Bacteria (red
¯uorescence) are abundant and show an intimate association with carbonate precipitates
(blue auto¯uorescence). Large, uncalci®ed ®lament in upper left is Schizothrix sp. Sample
is stained with propidium iodide; scale bar, 5 mm.
© 2000 Macmillan Magazines Ltd

boreholes, together with high sulphate reduction activity in these
layers18 indicates that, as in Type 2 mats, heterotrophic activity may
be important in the precipitation process. In contrast to the
conventional view that microboring is principally a destructive
process8,21, the microboring and in®lling processes associated with
Solentia activity in these mats is a constructive process. This process
fuses grains together to create laterally cohesive carbonate crusts.
These crusts persist into the subsurface and provide structural
support for the growth and long-term preservation of the stroma-
tolite. Field and laboratory studies show that layers of fused
microbored grains are formed in periods of weeks to months19.As
Solentia is a photosynthetic microorganism, such prolonged periods
of microboring activity can only be sustained when this population
remains at the surface during long hiatal periods. Even longer hiatal
periods result in a community succession to eukaryotic algal
communities, which do not form laminated structures8,14.
Laminations in the fossilized part of the stromatolites represent a
chronology of former surface mats (Fig. 4). Stromatolite laminae
are most easily observed on water-washed, cut surfaces where
lithi®ed layers stand out in relief (Fig. 4a). Although lamination is
readily apparent in hand samples, it has a subtle expression in
petrographic thin sections. Detailed microstructural analyses show,
however, that the lithi®ed layers have two distinct petrographic
appearances (Fig. 4b). These laminae correspond to (1) thin crusts
of micrite, 10 ±60 mm thick (blue lines in Fig. 4b and c), and (2)
layers of fused, microbored grains infested with Solentia sp.; these
layers are 1±2mm thick (orange lines in Fig. 4b and d) and underlie
micritic crusts. Light microscopy combined with scanning electron
microscopy shows that the thin crusts are identical in thickness,
composition and texture to the calci®ed bio®lms described above;
they are also similar in thickness to micritic laminae in many ancient
stromatolites3,22. In addition, microstructural features of the layers
of fused, microbored grains are identical to those formed by the
climax community described above.
Lithi®ed layers, which represent former surfaces of mats, show a
millimetre-scale distribution. This is indicated by petrographic
analyses of the upper several centimetres of 37 stromatolites con-
taining 453 micritic crusts and 174 microbored layers. The micritic
crusts form at intervals averaging 1 ±2 mm. Distances between tops
of layers of fused, microbored grains show two modes, one at 2±
3 mm and a second at 4 ±5 mm. Typical marine cements, such as
acicular fringes of aragonite, are notably absent during these early
stages of growth. Thus, the lithi®ed mats provide initial structural
support for the development of laminated build-ups with topo-
graphic relief.
To our knowledge, this is the ®rst study to de®ne a speci®c set of
mechanisms that link lamination in marine stromatolites to a
dynamic balance between sedimentation, a succession of pro-
karyotic communities and early lithi®cation. Integration of detailed
geological and microbiological analyses of stromatolites in a
modern marine system has shown that the structure and composi-
tion of surface mats alter in response to intermittent sedimentation
and that mats lithify during hiatal periods. Lithi®cation depends on
two fundamentally important microbial processes: photosynthetic
production by cyanobacteria and heterotrophic respiration by
bacteria. A laminated microstructure is formed by precipitation of
laterally continuous sheets of micrite in surface bio®lms, which are
formed during frequent discontinuties in sedimentation. In some
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Figure 4 Lamination and microstructure in stromatolite subsurface. Lithi®ed layers
representing former surface mats form at 1 ±2 mm intervals. a, Water-washed vertical
section showing lithi®ed laminae, which stand out in relief. b, Low magni®cation thin-
section photomicrograph of boxed area in ashowing the distribution of lithi®ed layers.
Blue lines represent micritic crusts (c); orange lines represent welded, micritized grains
(d). c, Thin-section photomicrograph of a micritic crust; these crusts represent calci®ed
bio®lms (Type 2 mats). d, Thin-section photomicrograph of a layer of microbored, fused
grains, which underlie a micritic crust; these layers represent former climax communities
(Type 3 mats). c,d, Plane polarized light. Scale bars: b, 10 mm; c,d, 100 mm.
© 2000 Macmillan Magazines Ltd

cases, thicker layers of fused grains form below these bio®lms in
response to microboring activities and precipitation, probably
resulting from polymer degradation in boreholes.
These ®ndings provide insight into the role of microbes in
stromatolite accretion, lamination and lithi®cation. Although
most researchers agree that, ``microbial mats and their associated
sediments must be lithi®ed early in order to be preserved in the
record as stromatolites''1, the proposed mechanisms and precise
timing of early lithi®cation have been ``vigorously debated''1.
Historically, early lithi®cation was attributed to abiotic processes
of submarine cementation23,5 or to calci®cation of cyanobacterial
sheaths24 related to photosynthetic activity. More recently, attention
has shifted to heterotrophic bacterial decomposition of cyano-
bacterial sheaths in subsurface, aphotic zones25,26. Although ®eld
studies have documented bacterial precipitation of micrite on the
sheaths of dead cyanobacteria in the subsurface of laminated
microbial mats in tidal ¯ats25,27, these mats do not form fully lithi®ed
laminae and stromatolitic build-ups. We argue that growth of
laminated microbial structures with topographic relief, such as
those that dominated the fossil record for three billion years,
depends on penecontemporaneous lithi®cation of surface mats.
This lithi®cation process occurs by decomposition of an amorphous
matrix of bacterial exopolymer (not sheath material) in the photic
zone across the stromatolite surface. Similar processes of precipita-
tion within the amorphous exopolymer matrix of bio®lms, rather
than on cyanobacterial sheaths, offer an additional mechanism to
account for the paucity of preserved microfossils in Precambrian
stromatolites, which is typically ascribed to recrystallization and/or
rapid degradation of sheaths1,26,28. The potential role that climax
microbial communities, functionally equivalent to the endolithic
coccoid cyanobacterial communities in modern marine stromato-
lites, may have played in the growth and lithi®cation of ancient
stromatolites remains to be evaluated. M
Methods
This study combined a range of geological, microbial and chemical analyses. An extensive
®eld program was conducted during January and June 1997, and March and August 1998.
Physicochemical indices of stromatolite mats were determined in situ, primarily with O
2
,
sulphide, pH needle electrodes (0.8 mm outer diameter)9, whereas microstructural,
chemical and microbial analyses and incubations were done in the laboratory at the ®eld
site and in home institutions. Mat communities and microstructural features were
identi®ed using a variety of microscope techniques (light, scanning electron, transmission
electron, and scanning laser confocal29) and microbial populations were enumerated using
epi¯uorescence microscopy counts9, most-probable number enumerations9,10 and mole-
cular phylogenetic techniques. Microbial activities were assessed using depth pro®les
measured with microelectrodes9and radioisotope incubations using
3
H,
14
C and
35
S (refs
9, 10 and 30). Heterotrophic activity was also studied with microautoradiography of
labelled organic matter uptake30. Microscale distribution of sulphate reduction was
assessed using Ag foil coated with
35
SO
2-
4
(ref. 18). Exopolymer distribution and
production were evaluated by physical and chemical extractions and
14
C-bicarbonate
experiments, respectively11. Other methods used are described elsewhere9,10,11,13,29,30.
Received 17 April; accepted 26 May 2000.
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Acknowledgements
D. A. Dean prepared petrographic thin sections; T. Kawaguchi provided confocal images;
N. Pinel analysed layer distribution. Numerous students assisted in ®eld and laboratory
studies. Logistical ®eld support was provided by the crew of the RV Calanus and
Highborne Cay management. This study is a contribution to the Research Initiative on
Bahamian Stromatolites Project and International Geological Correlation Project Biose-
dimentology of Microbial Buildups. Funding for this research was provided by the US
National Science Foundation, Ocean Sciences Division and NASA's Exobiology Program.
Correspondence and requests for materials should be addressed to R.P.R.
(e-mail: preid@rsmas.miami.edu).
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Ant-like task allocation and
recruitment in cooperative robots
Michael J. B. Krieger*², Jean-Bernard Billeter³& Laurent Keller*
*Institute of Ecology, University of Lausanne, BB, 1015 Lausanne, Switzerland
³Laboratoire de micro-informatique, Swiss Federal Institute of Technology,
1015 Lausanne, Switzerland
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One of the greatest challenges in robotics is to create machines
that are able to interact with unpredictable environments in real
time. A possible solution may be to use swarms of robots behaving
in a self-organized manner, similar to workers in an ant colony1±5.
Ef®cient mechanisms of division of labour, in particular series±
parallel operation and transfer of information among group
members6, are key components of the tremendous ecological
success of ants7,8. Here we show that the general principles regu-
lating division of labour in ant colonies indeed allow the design of
²Present address: Department of Entomology and Department of Microbiology, University of Georgia,
Athens, Georgia 30602, USA.
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