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Raman spectroscopic analysis of arctic nodules: Relevance to the

astrobiological exploration of Mars

Article in Analytical and Bioanalytical Chemistry · September 2011

DOI: 10.1007/s00216-011-5385-5 · Source: PubMed

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Anal Bioanal Chem (2011) 401:2927–2933
DOI 10.1007/s00216-011-5385-5

ORIGINAL PAPER

Raman spectroscopic analysis of arctic nodules: relevance

to the astrobiological exploration of Mars
Susana E. Jorge-Villar & Howell G. M. Edwards &
Liane G. Benning & AMASE 2004 team

Received: 13 June 2011 / Revised: 31 August 2011 / Accepted: 31 August 2011 / Published online: 23 September 2011
# Springer-Verlag 2011

Abstract The discovery of small, spherical nodules termed Keywords Raman spectroscopy . Nodules . Extremophiles .
‘blueberries’ in Gusev Crater on Mars, by the NASA rover Scytonemin . Carotenoids . AMASE
Opportunity has given rise to much debate on account of
their interesting and novel morphology. A terrestrial
analogue in the form of spherical nodules of similar Introduction
size and morphology has been analysed using Raman
spectroscopy; the mineralogical composition has been The search for life signatures in early evolutionary
determined and evidence found for the biological processes informs the origins of life arising from a prebiotic
colonisation of these nodules from the spectral signatures world [1]. In our terrestrial geological history, the recognition
of cyanobacterial protective biochemical residues such of the presence of fossilised relict cyanobacterial organisms
as scytonemin, carotenoids, phycocyanins and xantho- through their morphological traces is a key factor in the
phylls. This is an important result for the recognition of so-called ‘top-down’ approach to an understanding of
future sites for the planned astrobiological exploration the early biological colonisation and the prebiological
of planetary surfaces using remote robotic instrumentation in chemistry of the evolving geosphere.
the search for extinct and extant life biosignatures and Cyanobacterial colonisation of geological substrates
for the expansion of putative terrestrial Mars analogue has been identified in our earliest terrestrial geological
geological niches and morphologies. formations, extending from about 3.8 Gy, and it is clear
that an understanding of the survival strategies and
S. E. Jorge-Villar (*) protection mechanisms being adopted by these organisms can
Area Geodinamica Interna, Facultad de Humanidades y provide some important clues as to the conditions that were
Educacion, Universidad de Burgos,
Calle Villadiego,
operating on early Earth and in their adaptation to the
09001 Burgos, Castille y Leon, Spain changing evolutionary conditions [2, 3].
e-mail: [email protected] The survival of cyanobacterial extremophiles in stressed
terrestrial environments is fundamentally dependent upon
S. E. Jorge-Villar
e-mail: [email protected]
their synthesis of a specialised suite of protective biochemicals
in response to desiccation; low-wavelength high-energy
H. G. M. Edwards radiation insulation; extremes of pH, temperature and
Centre for Astrobiology and Extremophiles Research, pressure and high concentrations of toxic heavy metal
School of Life Sciences, University of Bradford,
Bradford BD7 1DP,
ions [4–6]. Our understanding of the roles of these
West Yorkshire, UK chemical protectants reveals a sophistication in design
e-mail: [email protected] for specific functions; for example, the ultraviolet radiation
screening effectiveness of scytonemin in cyanobacterial
L. G. Benning
School of Earth and Environment, University of Leeds,
sheaths which selectively absorbs in the UVA, UVB and
Leeds LS2 9JT, UK UVC regions of the electromagnetic spectrum whilst
e-mail: [email protected] permitting the transmission of the longer-wavelength
2928 S. E. Jorge-Villar et al.

photosynthetically active radiation (PAR) that is necessary destructive analysis of specimen, ease of sample examination
for the operation of chlorophyll in photosynthetic colonies. that does not involve any physical or chemical surface
Other protectants, such as trehalose, which is synthesised in preparation and an ability to collect data from both biological
Antarctic cyanobacterial mats colonising salt-rich lakes and mineralogical entities in association.
[5, 6], are dualistic in their roles; trehalose is used as a Although, specifically, there is no single terrestrial
water-replacement intracellular molecule which also Mars analogue site, the examination of a range of
combats osmotic stress caused by abnormally large closely related extremophilic scenarios is therefore of
concentrations of soluble salts such as calcium chloride. potential relevance to the diverse situations that may be
Similarly, a range of carotenoids can serve as light-harvesting expected on Mars. The current study was undertaken on
pigments and also as cellular DNA damage repair agents the geological and possible biological composition of
under stressed conditions [4]. spherical nodular structures found in sedimentary terrestrial
It is generally accepted that life started on Earth 3.8 Gya, rocks; the presence of residual protective biochemicals
when the environmental conditions on the surface were in such an ecological niche could be indicative of early
drastically different to the current situation. At that time, it life signatures [22] in extraterrestrial morphologies such
was predicted that Mars had similar conditions to those as the ‘blueberries’ found in Gusev Crater on Mars.
pertaining on Earth, and this has led to the idea that life
could also have appeared on Mars [7–10]. As the external
conditions were changing on early Mars, as on Earth, Experimental
organisms needed to adapt to new habitats and colonise
even the most extreme niches using a range of response Raman spectroscopy
strategies. Those organisms that were able to survive in
such hostile environments can be considered to have left Spectra were collected using a Renishaw inVia Raman
signatures of their presence on Mars; it is fundamentally Spectrometer with a dedicated Leica DMLM microscope,
important, therefore, to the understanding of these complex using ×20 and ×50 objectives. The laser wavelength used
processes to analyse the terrestrial analogues of possible was in the near-infrared at 785 nm for analysing both the
Mars scenarios [11–14]. host minerals and the organic protectant biomolecules
Cold deserts, such as Antarctica or the Arctic, have been produced by the cyanobacterial colonies. With a 10-s
proposed as the closest Martian analogues on Earth [15]. exposure time, a range of between 20 and 80 accumulations
The extremely low temperatures, dry atmospheres, strong were achieved for improving signal-to-noise ratios in the
UV-radiation isolation, low nutrient availability or long spectra. The laser power was operated at values between
periods without sunlight have not been obstacles in the 0.1 to 10 mW, depending on the compound analysed; for
adaptation and proliferation of several different types of those specimens where there was a high risk of thermal
microorganisms. The survival adaptations of microorganisms degradation occurring, such as iron oxides, hydrated
in these environments necessarily use both inorganic and minerals or biomolecules, the lower laser power and
organic strategies [16–18], especially involving a wide range spectral irradiance were used, whereas when there was a
of radiation protective pigments [19, 20]. low risk of inducing structural changes, higher laser powers
Laser Raman spectroscopy is being adopted by National and spectral irradiance were selected for collecting spectra
Aeronautics and Space Administration (NASA) and to minimise the acquisition times.
European Space Agency (ESA) as a part of an
analytical instrumentation suite for Mars surface explo- Specimens
ration, including the ExoMars mission scheduled for
2018 which will deploy one or two rovers on the Samples were collected from the Ebbaelva sandstone
surface of Mars; the rover(s) will sample the Martian formation in Billeffjord (Svalbard, Norway), during the
atmosphere, searching for water and interrogating the AMASE 2004 expedition (Arctic Mars Analogue Svalbard
subsurface geology with ground-penetrating radar and Expedition). The main outcrop shown in Fig. 1 was made
will be using a variety of analytical instrumentation for up of a white laminated sandstone, which was dotted with
the recognition of extinct and extant life signatures in small hemispherical depressions of around 1 cm diameter
association with a detailed geological and mineralogical and 0.5 cm in depth; a sample from this outcrop containing
survey. The particular characteristics of Raman spectroscopy fresh surfaces and these spherical structures (which we
that make this technique a valuable instrument for the termed “negative nodules”) were analysed; a second sample
unambiguous identification of biological, biogeological and collected from the underside of a ledge from the sandstone
geological signatures [21] are primarily those of non- (Fig. 2) contained ‘positive nodules’ which appeared as
Raman spectroscopic analysis of arctic nodules 2929

Fig. 1 Photograph showing the general aspect of the Ebbaelva Fig. 3 Red and yellowish-green chasmoliths and the green endolithic
sandstone outcrop and the ‘negative nodules’ (©Storvik/AMASE) community on the third rock sample analysed (©Storvik/AMASE)

spherical convex structures together with a brownish Results and discussion

weathered crust. In this second sample, the fresh host rock,
the brownish crust as well as the inside of one of these Host rock substrate and brown crust
positive nodules were analysed.
Finally, from the same outcrop, another sample was The main component of the fresh rock was quartz, with
collected (Fig. 3), and this exhibited one endolithic characteristic Raman bands at 205, 261, 355 and 463 cm−1
(organisms living inside a host rock) and two more (Fig. 4, A); in addition, signatures at 141, 200, 393, 511 and
superficial chasmolithic (microorganisms living inside a 636 cm−1 are characteristic of anatase (Fig. 4, D); the 701-
rock fissure) communities. The endolithic organisms and 262-cm−1 bands have been assigned to muscovite and
appeared as a continuous bluish-green band, at about those at 506 and 477 cm−1 to a feldspar. Raman spectra of
1 cm depth below the surface, while the two chasmolithic small brown crystals, which appeared dispersed in the fresh
communities were present as patches of yellowish-green rock matrix, showed signatures at 170, 290, 721 and
and red-coloured communities covering small cracks in the 1092 cm−1 and thus were unambiguously assigned to
rock close to the endolith band. ankerite, a calcium-iron carbonate (Fig. 4, C). Furthermore,
a white powdery phase was found under microscopic
examination, filling the rock pores and acting as a cement;
its Raman spectrum showed signatures at 413, 491, 617,
668, 1007 and 1135 cm−1 which are unambiguously
assigned to gypsum (Fig. 4, B).

2500000

(A)
Intensity (arbitrary units)

2000000
(B)

(C)
1500000
(D)

1000000 (E)

1200 1000 800 600 400 200

Wavenumber (cm-1)
Fig. 2 Photograph of the sample collected from below a ledge of the
sandstone showing the ‘positive nodules’ and the brownish surface Fig. 4 Raman spectra acquired on the fresh rock: A Gypsum and
crust (©Storvik/AMASE) quartz; B gypsum; C ankerite; D anatase and E gypsum and hematite
2930 S. E. Jorge-Villar et al.

In this sample, one spectrum shows two broad may be a step in the mobilisation process for iron
signatures at 1335 and 1590 cm−1, which have been through the rock.
attributed to amorphous carbon. Since there are coal mines In terms of organic molecules in the chasmolith, the
in Spitsbergen, it is possible that these particles may be a presence of the 1515; 1154; 1002 and 980 cm−1 Raman
consequence of aerial contamination, but their presence bands were assigned to canthanxanthin (Fig. 5, A and B).
could also be the result of the degradation of organic Although the position of the stretching mode C=C
carbonaceous compounds. double-bond band at 1515 cm−1 could be also related
In the brownish crust, again, quartz and gypsum were with betacarotene, analyses carried out in our laboratory
detected, but no signatures of ankerite were observed; with commercial standard betacarotene showed that there
however, new Raman bands at 224, 292, 408 and 612 cm−1 was no Raman band at 980 cm−1 for pure betacarotene,
appeared in the spectra (Fig. 4, E) are characteristic of and this weak broad signature at 980 cm−1 only appears
haematite, which could be responsible for the red when this compound has been degraded because of its
colour. One of the spectra collected from this crust exposure to atmospheric conditions. As this signature
gave a rather weak band at 1050 cm−1, which can be appears in the Raman spectra of the red chasmolith and
assigned to a lead carbonate (cerussite or hydrocerussite). always together with the 1515-cm−1 band, we therefore
The absence of ankerite on the rock surface could be prefer a canthaxanthin assignment. Apart from canthaxanthin,
ascribed to weathering processes which could have the peaks at 1509; 1153 and 1005 cm−1 are attributable to a
converted the ankerite to haematite. different carotenoid, probably astaxanthin (Fig. 5, A). A very
broad signature, centred at 1330 cm−1, which always appears
Red chasmolithic community associated with these carotenoid bands in the Raman spectra,
can be assigned to chlorophyll.
The red chasmolith was a small patch (Fig. 3) of 2 cm
wide situated on a crack around 5 mm below the surface Yellowish-green chasmolith
crust but not in contact with it. Several analyses were
carried out at points across this area, and despite the clear The yellowish-green chasmolithic colony was found adja-
presence of a red colouration in the surface crust, no cent to the red chasmolith described above but situated
Raman signals of haematite were found in this red further away from the rock surface (Fig. 3). Apart from
chasmolith area; however, limonite, FeO(OH)n(H2O), quartz and gypsum, the Raman spectra show signatures at
was clearly identified by its Raman signatures at 204, 1524; 1155 and 1007 cm−1 assignable to a carotenoid,
295, 391, 550 and 692 cm−1. It is interesting to point out possibly lutein (Fig. 6). Although numerous Raman
here that, despite a large number of analyses that have spectroscopic analyses were acquired from this area, only
been carried out in our laboratory involving different this carotenoid was observed. However, in many spectra the
endolithic and chasmolithic organisms, we have not found clear signatures at 1438; 1388; 1325; 1285; 1225; 1185;
in our studies any of those communities in the rock matrix 1069; 1048; 916; 756; 744 and 514 cm−1 were character-
itself directly related with haematite. It appears that if istic of chlorophyll (Fig. 6).
haematite was originally present in the bulk rock matrix It is of interest that no signatures of any iron oxide were
before colonisation, it has always been chemically found in this region despite its closeness to the surface and
mobilised to external areas around the colony [16, 23].
In the specimens we have previously studied, as found
here, the crust is often enriched with haematite itself 550000

and/or goethite, showing a different colour to that of the

Intensity (arbitrary units)

500000
fresh rock. It has been already reported that haematite,
(A)
Fe2O3, acts as an UV radiation screen [23] and, since this 450000
(A)

sample was collected at 79° North, this strategy could (B)

(B) (B)

have been useful for avoiding DNA damage caused by 400000

(B)

the high UV radiation insolation levels experienced near

the terrestrial poles. It is not clear why limonite should 350000

be associated with the microbial communities and what (A)

(A)

role this mineral plays, if any, for the survival of the 1500 1400 1300 1200 1100 1000 900 800
endolith/chasmolith communities. It is possible that Wavenumber (cm-1)
limonite is a weathering product of the haematite Fig. 5 Raman spectrum collected on the red chasmolithic community
observed in the surface crust, a process that may have showing broad bands of carotene: A, canthanxanthin and astaxanthin;
been enhanced by the biological colonisation and that it B, canthaxanthin
Raman spectroscopic analysis of arctic nodules 2931

1800000
Positive nodule
1700000
Intensity (arbitrary units)

1600000 As in all other rock samples analysed in this study, quartz

1500000 and gypsum (Fig. 8, B) were found as the main components
1400000
also on the inside of the positive nodule; however, rutile
and anatase were also identified (Fig. 8, C). It is interesting
1300000
to note that, in the bulk rock, no signals of rutile were
1200000 observed in any of the Raman spectra, whereas anatase was
1100000 found.
1600 1400 1200 1000 800 600 400 200
However, among the organic compounds found on the
Wavenumber (cm-1) inside surface of the convex positive nodule, apart from a
carotenoid (probably lutein) and chlorophyll, for the first
Fig. 6 Raman spectrum of chlorophyll, carotene and gypsum time in this set of samples, the cyanobacterial radiation
achieved on the yellowish-green chasmolith
protectant biomolecule scytonemin was unambiguously
identified from its Raman bands at 1709; 1631; 1605;
its direct contact with the red chasmolith where limonite 1591; 1555; 1520; 1384; 1324; 1285; 1245; 1171; 1154;
has been clearly identified (Fig. 3). 1097; 983; 889; 830; 754; 677 and 569 cm−1 (Fig. 8, A).

Endolithic community Negative nodule

The endolithic community appeared as a continuous bluish- Finally, a series of analyses of the negative (concave)
green band about 1 cm below the surface crust (Fig. 3). Two nodule (Fig. 1) was carried out. Compared with the rock
different types of carotenoid have been detected here, the matrix, the only newly identified phase here was calcite,
first one with signatures at 1517; 1155; 1005 and 984 cm−1 with characteristic bands at 1086; 711; 281 and 154 cm−1.
is assignable to canthaxanthin, and the second carotenoid, Together with quartz, rutile and haematite as mineral
with Raman bands at 1525; 1156 and 1004 cm−1, was components, bands of a carotenoid (1524; 1157 and
identified as lutein. However, in contrast to the chasmolithic 1004 cm−1) and chlorophyll indicate that these nodules
communities, in the endolith associated with both these were colonised by microorganisms. Not anatase, ankerite,
carotenes, clear Raman bands at 1628; 1581; 1465; 1371; or any of the other protective biomolecules noted above
1339; 1284; 1240; 1109; 1053; 972; 823; 667 and 505 cm−1 were detected in the Raman spectra of these negative
that were assigned to c-phycocyanin were identified nodules.
(Fig. 7). C-phycocyanin is a light-harvesting accessory
pigment important in photosynthetic processes when weak
sunlight is a limiting factor, such as in dark niches; the Conclusions
synthesis of c-phycocyanin could therefore be a necessity
for this particular endolithic community where only Raman spectroscopy is a powerful analytical tool that can
minimal polar sunlight reaches the colony at depths in the be used to distinguish among a large variety of mineral
rock matrix.

3000000
Intensity (arbitrary units)

1000000 2500000 (A)

Intensity (arbitrary units)

900000
2000000
800000
(B)
700000 1500000

600000 (C)
1000000
500000
1800 1600 1400 1200 1000 800 600 400 200
1800 1600 1400 1200 1000 800 600 400 200 Wavenumber (cm-1)
Wavenumber (cm-1)
Fig. 8 Raman spectra acquired from the inside of the positive nodule:
Fig. 7 Raman spectrum of c-phycocyanin, carotene and quartz from A scytonemin, chlorophyll, carotene and quartz; B gypsum; C anatase
the endolithic community and rutile
2932 S. E. Jorge-Villar et al.

species even when they are in small amounts or just as Haematite, a mineral often responsible of the reddish
small particles on rock surfaces; these particulars make colouration of rocks and in our samples for the colour
Raman spectroscopy an ideal complementary payload to of the surface crust, was also present in the negative
XRD/XRF or other mineralogical instruments on future (concave) nodule, but it did not appear in the fresh rock
Mars missions. However, what makes Raman spectrometers matrix or in the red chasmolithic community, where
potentially an exceptional flight instrument for future limonite was the iron oxide identified based on the clear
“Search for life” missions to Mars is its high sensitivity Raman bands.
to vibrations from organic molecules even in complex Finally, in terms of biological signals, besides the
matrixes and—compared with other more destructive often-reported chlorophyll and carotenoids, noteworthy
tools—the fact that it can be used in situ with little are the two strategies adopted by microorganisms for
sample handling and preparation. protection from the harsh Arctic environment: (a) the
A major advantage of Raman spectroscopic analysis bluish-green endolith community, situated about 1 cm
is the ability to identify simultaneously both organic and below the rock surface, produced a light harvesting
inorganic compounds in the same specimen without pigment to compensate for the lower level of PAR that
undertaking any chemical pre-treatment; in these studies, reaches those depths inside the rock while (b) the
it was necessary to fracture the rock specimens to microorganisms inside the positive nodule produce
expose the endolithic strata and interior of the spherical scytonemin, an UV protective pigment exclusively
nodules, but no other form of mechanical treatment such synthesised by cyanobacteria.
as grinding, polishing or etching was undertaken or In our studies of samples collected during earlier
necessary for the Raman analyses. The identification of AMASE expeditions to the Norwegian Arctic, we
the mineralogical and key biomolecular components of analysed biological and mineral signatures in dark
the rock matrix was unambiguous even for compounds basaltic rocks [20], in fossil travertine terraces [25] or in
in admixture. algae and their associated mineral consortia living on
The specimens studied in this work were all sampled snow fields [26] and showed that similar protective
from the same outcrop, but they showed clear differences biomolecules were present. Among these, we often identified
both in the minerals and biological molecules present. specialised carotenoids (in many cases, the whole suite from
For example, ankerite was only found in the bulk rock betacarotene to astaxanthin), chlorophyll, scytonemin or c-
matrix; its absence from the surface crust or in places phycocyanin. With the use of in situ analyses by Raman
colonised by microbial communities could be attributed spectroscopy, some of these molecules were clearly identified
to weathering processes. The absence of ankerite signals even when no morphological microbial remnants were found
could also be related to the presence of haematite on by staining or high-resolution scanning electron microscopy
the surface, since ankerite could supply the iron [20]. Furthermore, Raman analyses carried out in our
necessary for the formation of haematite here. Furthermore, laboratory on endoliths from Antarctica also show similar
on the surface crust, and in association with the negative biomolecules [5, 16–18, 21, 22]. In all cases, both the
nodules, other carbonates have been identified, such as various bio- and geo-markers were unambiguously identified
lead carbonate and calcite. even when they appeared in complex mixtures.
Another interesting observation not described hitherto In the current study, some of the biomolecules
is the distribution of the titanium oxide polymorphs. In described in relation to the microorganisms found in
the bulk rock, only anatase was identified even from the the Ebbaelva sandstone samples were equivalent to
relatively large number of analyses carried out. Since previously reported biosignatures for microorganisms
both rutile and anatase give very strong and character- living under similar or other extreme environments [5,
istically distinct Raman signals, rutile is clearly either 6, 18–21]. In our case, the identified microbial signa-
absent in the fresh rock or is present in only very low tures indicate that microorganisms survived in extreme
amounts. However, rutile was found in association with cold, dry and high UV environments, and they have
the both types of nodules, but, significantly, rutile done this through various protective and adaptive
appears along with anatase in the positive nodule strategies against the hazardous conditions they live in,
whereas anatase was not identified in the negative for example, the use of haematite, carotenoids or
nodule. The thermal transformation of anatase to rutile scytonemin as UV radiation screen, carotenoids as free
has been reported [24], but this can also be affected radical quenching molecules or c-phycocyanins as light
through hydrothermal conditions and catalytic reactions harvesting compounds; similarly, in some cases, the
at high temperatures; it is noteworthy that hitherto there microorganisms used mineral covers or the rocks themselves
has been no reference to this conversion by microorganisms at (i.e. Fig. 3) as protective micro-environments which, at the
environmental temperatures. same time, act as a filter against harmful radiation and
Raman spectroscopic analysis of arctic nodules 2933

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Acknowledgements The work of S.E.J.V. was supported by Funda- Kluwer Academic, The Netherlands
ción Universidad de Burgos, Departamento de Didácticas Específicas 16. Jorge Villar SE, Edwards HGM, Cockell CS (2005) Analyst
(University of Burgos), Caja Burgos, Cámara de Comercio de Burgos 130:156–162
and Bodegas Martín Berdugo. L.G.B. acknowledges the funding 17. Jorge Villar SE, Edwards HGM, Wynn-Williams DD (2003) Int J
provided by the School of Earth and Environment, University of Astrobiol 1:349–355
Leeds, and the World University Network (WUN). H.G.M.E acknowl- 18. Edwards HGM, Moody CA, Jorge Villar SE, Wynn-Williams DD
edges funding from EPSRC for supporting the Raman analyses. (2005) Icarus 174:560–571
S.E.J.V. and L.G.B. also greatly acknowledge field, infrastructure and 19. Mueller DR, Vincent WF, Bonilla S, Laurion I (2005) FEMS
moral support from all members of the Arctic Mars Svalbard Analog Microbiol Ecol 53:73–87
Expedition 2004 (AMASE) team; without them, this work would not 20. Jorge Villar SE, Edwards HGM, Benning LG (2006) Icarus
have been possible. We would specifically like to thank Kjell Ove 184:158–169
Storvik who has taken the photographs of the rock samples used in 21. Jorge Villar SE, Edwards HGM (2006) Anal Bioanal Chem
this study. 384:100–113
22. Pullan D, Westall F, Hofmann B, Parnell J, Cockell CS, Edwards
HGM, Jorge Villar SE, Schröder C, Cressey G, Marinangeli L,
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