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Icarus 277 (2016) 342–353
Contents lists available at ScienceDirect
Icarus
journal homepage: www.elsevier.com/locate/icarus
Influence of mineralogy on the preservation of amino acids under
simulated Mars conditions
Renato dos Santos
a
, Manish Patel
b , c
, Javier Cuadros
d
, Zita Martins
a , ∗
a
Department of Earth Science and Engineering, Imperial College London, South Kensington Campus, London SW7 2AZ, UK
b
Department of Physical Sciences, The Open University, Milton Keynes MK7 6AA, UK
c
Space Science and Technology Division, Rutherford Appleton Laboratory, Harwell, Oxfordshire, UK
d
Department of Earth Sciences, The Natural History Museum, London SW7 5BD, UK
a r t i c l e i n f o
Article history:
Received 14 December 2015
Revised 18 May 2016
Accepted 19 May 2016
Available online 27 May 2016
Keywo rds:
Mars
Mineralogy
Solar radiation
a b s t r a c t
The detection of organic molecules associated with life on Mars is one of the main goals of future life-
searching missions such as the ESA-Roscosmos ExoMars and NASA 2020 mission. In this work we studied
the preservation of 25 amino acids that were spiked onto the Mars-relevant minerals augite, enstatite,
goethite, gypsum, hematite, jarosite, labradorite, montmorillonite, nontronite, olivine and saponite, and
on basaltic lava under simulated Mars conditions. Simulations were performed using the Open Univer-
sity Mars Chamber, which mimicked the main aspects of the martian environment, such as temperature,
UV radiation and atmospheric pressure. Quantification and enantiomeric separation of the amino acids
were performed using gas-chromatography-mass spectrometry (GC–MS). Results show that no amino
acids could be detected on the mineral samples spiked with 1 μM amino acid solution (0.1 μmol of
amino acid per gram of mineral) subjected to simulation, possibly due to complete degradation of the
amino acids and/or low extractability of the amino acids from the minerals. For higher amino acid con-
centrations, nontronite had the highest preservation rate in the experiments in which 50 μM spiking
solution was used (5 μmol/g), while jarosite and gypsum had a higher preservation rate in the exper-
iments in which 25 and 10 μM spiking solutions were used (2.5 and 1 μmol/g), respectively. Overall,
the 3 smectite minerals (montmorillonite, saponite, nontronite) and the two sulfates (gypsum, jarosite)
preserved the highest amino acid proportions. Our data suggest that clay minerals preserve amino acids
due to their high surface areas and small pore sizes, whereas sulfates protect amino acids likely due to
their opacity to UV radiation or by partial dissolution and crystallization and trapping of the amino acids.
Minerals containing ferrous iron (such as augite, enstatite and basaltic lava) preserved the lowest amount
of amino acids, which is explained by iron (II) catalyzed reactions with reactive ox ygen species gener-
ated under Mars-like conditions. Olivine (forsterite) preserved more amino acids than the other non-clay
silicates due to low or absent ferrous iron. Our results show that D- and L-amino acids are degraded
at equal rates, and that there is a certain correlation between preservation/degradation of amino acids
and their molecular structure: alkyl substitution in the α-carbon seem to contribute towards amino acid
stability under UV radiation. These results contribute towards a better selection of sampling sites for the
search of biomarkers on future life detection missions on the surface of Mars.
©2016 The Authors. Published by Elsevier Inc.
This is an open access article under the CC BY license ( http://creativecommons.org/licenses/by/4.0/ ).
1. Introduction
The detection of organic molecules associated with extra-
terrestrial life has been primarily focused on Mars due to its
proximity to Earth, evidences of a congenial past environment and
potential to support microbial life ( Westall et al., 2013 ). Increasing
evidence from NASA’s Opportunity and Curiosity rovers obtained at
different locations indicates that the Red Planet could have indeed
∗Corresponding author.
E-mail address: z.martins@imperial.ac.uk (Z. Martins).
supported life at the surface in the past (
Arvidson et al., 2014;
Grotzinger et al., 2014 ). Furthermore, the detection of silica-rich
deposits by the Spirit rover in the Gusev crater is also an indi-
cation of an environment able to support life ( Des Marais 2010;
Ruff et al., 2011; Squyres et al., 2008 ). It is also plausible that
life developed underground and biomarkers reached the surface
( Michalski et al., 2013 ). Despite this, the environmental conditions
that prevail now on Mars’ surface are not congenial to life or to the
preservation of biomarkers. Two of the factors contributing to the
harsh current martian environmental conditions are the thin at-
mosphere and the absence of a significant magnetosphere ( Fairén
http://dx.doi.org/10.1016/j.icarus.2016.05.029
0019-1035/© 2016 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license ( http://creativecommons.org/licenses/by/4.0/ ).
R. dos Santos et al. / Icarus 277 (2016) 342–353 343
Fig. 1. Powder X-Ray diffraction patterns of hematite (Fe
2
O
3
). The figures indicate the d-spacing of the several peaks in angstroms. The intensity increase at ∼10 °2
θis
produced by the X-ray fluorescence of Fe.
et al., 2010 ), resulting in the inability to attenuate the intensity of
the multiple forms of solar radiation that reach the planet, such
as UV radiation, galactic cosmic rays and solar energetic particles
( Cockell et al., 20 0 0; Hassler et al., 2014 ). As a result, the martian
regolith is exposed to intense levels of radiation, contributing to
the reactivity of the soil which may destroy potential martian life
and degrade organic molecules ( Dartnell et al., 2007; Quinn et
al., 2013 ). UV radiation leads to the formation of radical species
(e.g. reactive oxygen species such as superoxide and hydroxyl
radicals) by photochemical processes, which cause degradation of
any potential organic compounds present on Mars ( Benner et al.,
20 0 0; Georgiou et al., 2007, Georgiou et al., 2015; Yen et al., 20 0 0 ).
Amino acids, which are the building blocks of proteins and consid-
ered important target molecules in future life-searching missions
( Parnell et al., 2007 ), are known to be subjected to degradation
by UV radiation ( Garry et al., 2006; Noblet et al., 2012 ). A 1.5-year
exposure of glycine and serine to Mars-like surface UV radiation
conditions in low-Earth orbit resulted in complete degradation of
these organic molecules ( Noblet et al., 2012 ).
In order to maximize the chances of finding biomarkers on
Mars, we must determine the most suitable conditions to preserve
them. Preservation of organic molecules on Mars is thought to be
favored in subsurface environments, and also through associations
with specific minerals that may confer protection from the harsh
surface conditions ( Kminek and Bada, 2006; Summons et al., 2011 ,
and references therein; Poch et al., 2015 ). Despite the unfavorable
conditions that are found at the surface, indigenous chlorinated hy-
drocarbons were recently detected on Mars by the Sample Anal-
ysis at Mars (SAM) instrument on-board Curiosity ( Freissinet et
al., 2015 ). The successful detection of organic molecules on sam-
ples from Mars’ surface exposed to ionizing radiation and oxidative
conditions suggests that: 1) the preservation of organic molecules
may not be limited to subsurface environments, and 2) organic
biomarkers may be found on the surface if associated with specific
minerals.
In this paper we examine the preservation under simulated
Mars-like conditions of amino acids that were spiked onto 11
minerals and onto basaltic lava, which are all present on the mar-
tian surface ( Ehlmann and Edwards, 2014 ). The simulations were
performed using a custom-built Mars environmental simulation
chamber at the Open University (OU), Milton Keynes, UK. This
facility permits multiple aspects of the martian environment to
be simulated, including temperature, UV radiation, atmospheric
pressure and composition. Analyses of the amino acids extracted
from the mineral surfaces after the experiments were performed
by gas chromatography-mass spectrometry (GC-MS). Our results
are particularly relevant for future in situ life-detection missions,
such as the ESA-Roscosmos ExoMars 2018 rover and the NASA
Mars 2020 mission, highlighting which minerals may be the most
suitable to protect amino acids from the harsh environmental
conditions found at the martian surface.
2. Materials and methods
2.1. Minerals and XRD characterization
Eleven mineral samples were used in this work: augite (A), en-
statite (E), goethite (G), gypsum (Gy), hematite (H), jarosite (J),
labradorite (L), montmorillonite (M), nontronite (N), olivine (O)
and saponite (S). Basaltic lava (B) was also used. They were all se-
lected as representing abundant mineral phases on Mars ( Ehlmann
and Edwards, 2014 ). Augite, jarosite, labradorite, nontronite, and
saponite were purchased from Richard Tayler ( http://richardtayler.
co.uk , Cobham, Surrey, UK). Enstatite, goethite and olivine were
obtained from the Natural History Museum collection (NHM, Lon-
don), all of them unregistered specimens in the NHM collection.
The basaltic lava is a specimen collected in Mauna Loa (Hawaii) at
the point of lava quenching and donated by Joe Michalski. Gypsum
and hematite were purchased from Sigma Aldrich. The montmoril-
lonite is SAz-1 (smectite-rich rock of volcanic origin) described in
Cuadros (2002) .
Minerals were ground to powder by hand with a mortar and
pestle and they were analyzed with X-ray diffraction (XRD) at
the NHM, in order to determine their purity and structure. They
were side-loaded to avoid preferred orientation of particles and
analyzed in the range 3–80 °2 θusing a PANanalytical X’Pert Pro
diffractometer operated at 45 kV and 40 mA, with Cu K αradiation,
divergence slit of 0.25 °, Soller slits of 1.146 °and a solid-state
X’Celerator detector covering an angle of 2.1 °. The basaltic lava
contains the following mineral phases in the estimated order
of abundance: volcanic glass, pyroxene, olivine, and labradorite.
Jarosite is of the natrojarosite variety. Olivine is forsterite. The
augite and enstatite contain some traces of amphibole; the non-
tronite and montmorillonite contain traces of quartz; the other
minerals are pure at the XRD detection level. Fig. 1 shows the
X-ray pattern of hematite as an example.
2.2. Chemicals and tools
The pipette tips and eppendorfs used in this work were bought
sterile. Hydrochloric acid (37 wt. %), and high performance liquid
chromatography (HPLC)-grade water were purchased from Sigma-
Aldrich. Sodium hydroxide was purchased from Riedel-de Haen.
Aluminium hydroxide and 2-aminoheptanoic acid ( > 97%) were
purchased from Fluka. AG 50W-X8 resin (10 0–20 0 mesh) was
acquired from Bio-Rad. HPLC-grade dichloromethane (DCM) was
344 R. dos Santos et al. / Icarus 277 (2016) 342–353
Fig. 2. Mars Chamber simulator located at the Open University (left) and the experimental setup inside the chamber showing the amino acid-spiked minerals (right).
purchased from Fisher Scientific. Copper turnings used for sulfur
removal were purchased from BDH. The 25 amino acids used
in the experiments were: α-aminoisobutyric acid ( α-AIB); D,L-
isovaline; D,L-alanine; D,L-valine; glycine; D,L-norvaline; D,L- β-
aminoisobutyric acid (D,L- β-AIB); D,L- β-aminobutyric acid (D,L- β-
ABA); β-alanine; D,L-leucine; D,L-norleucine; γ-aminobutyric acid
( γ-ABA); D,L-aspartic acid; D,L-glutamic acid and 6-aminohexanoic
acid (6-AHA). The amino acid L-2-aminoheptanoic acid (L-2-AHA)
was not subjected to the simulation experiments and was used as
internal standard for the GC-MS analysis. All the amino acid stan-
dards were purchased from Sigma-Aldrich, except D,L-isovaline,
which was bought from Acros Organics. The trifluoroacetic an-
hydride isopropanol (TFAA-IPA) derivatization kit was obtained
from Alltech. All glass tools and ceramics used were sterilized by
wrapping in aluminum foil and heating in a furnace for at least 3
h at 500 °C.
2.3. Spiking of amino acids
A stock solution of 0.005 M concentration was prepared for
each of the 25 amino acids. One milliliter of each amino acid
stock solution was used to prepare a spiking solution containing an
equimolar mixture of the 25 amino acids. Four of these solutions
were prepared with final concentrations of 50, 25, 10 and 1 μM
of each amino acid. The spiking solutions containing 1, 10, 25 and
50 μM concentrations of each amino acid were labeled as solution
1, 2, 3 and 4, respectively. Concentrations were chosen by adapt-
ing the protocols from Parbhakar et al (2007) and Cuadros et al.
(2009) . These authors show that at low amino acid concentrations
the mechanism of amino acid adsorption on smectite is a simple
exchange with interlayer cations, whereas at higher amino acid
concentration physical interaction between amino acid molecules
become important. In the present work we wanted to be in the
low-amino acid concentration (i.e. much lower than 0.025 M) in or-
der to avoid amino acid interaction with other amino acids.
Approximately 30 mg of each mineral sample described in
Section. 2.1 were weighed in Pyrex test tubes. Three milliliters of
each of the solutions described above (1–4) were transferred into
12 test tubes, each containing one of the minerals.
The experiments containing the minerals and the spiking so-
lutions were named by the respective mineral initial provided in
Section. 2.1 , followed by the number of the solution. For exam-
ple, augite spiked with solution 1 (i.e., 1 μM of each amino acid)
was labeled as A1, while augite samples labeled as A2, A3 and A4
were spiked with solution 2, 3 and 4, respectively. Using this la-
beling procedure, the experiments carried out include basaltic lava
(with experiments B1, B2, B3 and B4), enstatite (E1, E2, E3 and E4),
goethite (G1, G2, G3 and G4), gypsum (Gy1, Gy2, Gy3 and Gy4),
hematite (H1, H2, H3 and H4), montmorillonite (M1, M2, M3 and
M4), nontronite (N1, N2, N3 and N4), olivine (O1, O2, O3 and O4)
and saponite (S1, S2, S3 and S4). Jarosite was only used in exper-
iments 3 and 4, resulting in a total of two samples (J3 and J4).
Labradorite was only used in experiments 1, 2 and 3 (L1, L2 and
L3).
All the test tubes containing the mineral samples and the spik-
ing solutions were flame sealed and placed in an orbital shaker
(Heidolph Polymax 1040) for 24 h at 50 revolutions per minute
(rpm) in order to let amino acids adsorb onto the mineral surfaces.
The outside of the test tubes was rinsed with HPLC grade water
and cracked open. The content of the test tubes was dried under a
flow of nitrogen (i.e., the spiking solution was dried in contact with
the mineral). Thus, the 1, 10 , 25 and 50 μM solutions correspond
to 0.1, 1, 2.5 and 5 μmol/g of the amino acids on the minerals,
respectively.
Control experiments were prepared by repeating the same pro-
cedure described in this section with a second set of samples. The
first set of samples was used to perform the Mars chamber sim-
ulations, while the second set was used as controls (i.e., samples
that were spiked but not subjected to the Mars simulation).
2.4. Mars chamber simulations
The spiked mineral standards were transferred into 14 mm di-
ameter metallic sample cups and placed inside a Mars chamber
simulator at the Open University, Milton Keynes, UK ( Fig. 2 ). The
sample cups were pre-sterilized by heat at 500 °C for 4 h. The
thickness of the deposits was approximately 1 mm in order to
avoid any self-shielding issues. The sample cups were placed on
a custom-made cold plate, to enable the cooling of the samples to
Mars-relevant temperatures. Copper shielding was provided to the
edges of the plate to define a cold zone, and the external faces of
the plate and shields were insulated to provide an efficient sample
cooling zone. The cooling plate was connected to a liquid nitro-
gen supply, with thermal valves providing control over the sample
R. dos Santos et al. / Icarus 277 (2016) 342–353 345
Fig. 3. UV lamp spectrum and modeled UV spectrum expected at the martian surface.
temperature. Temp eratu re was monitored using an array of ther-
mocouples mounted on the sample plate. The resulting sample
configuration is shown in Fig. 2 (right). The chamber contained
a Xe light source at the top of the chamber using a fused silica
window (to ensure good UV transmission) providing direct illu-
mination of the sample area with a UV spectrum similar to that
encountered on the surface of Mars (e.g. Patel et al., 2002 ). The
lamp output, along with a typical modeled UV irradiance expected
at the surface of Mars at local noon (taken from Patel et al., 2002 )
is shown in Fig. 3 . After setting the samples in the chamber and
previous to the experiments, the pressure was reduced to a vac-
uum ( < 1 mbar) for > 10 min and at room temperature. This en-
sures that there is no air and no water vapor in the atmosphere.
Then, the chamber was pressurized at 6 mbar with a mixture of
95% CO
2
and 5% N
2
, mimicking the approximate Mars pressure en-
vironment. The very dry conditions established by the initial vac-
uum treatment and the simulated Mars atmosphere (water vapor
partial pressure is nominally zero) eliminated adsorbed water from
the mineral surfaces. Complete removal of adsorbed water is likely
not obtained, unless the samples are sufficiently heated. Thermal
cycling of the sample (to simulate the potential diurnal thermal
cycle of Mars, e.g. Kieffer et al., 1977 ) was performed, with a cy-
cle from –80 °C to + 20 °C of 2 h duration repeated throughout
the exposure. During thermal cycling the samples were exposed
to UV, and overnight the samples were maintained at room tem-
perature with no UV. The samples received a total of 28 h of real-
time continuous UV illumination. On Mars, the diurnal profile of
UV irradiance encountered at the surface exhibits a bell-shaped
profile (such as demonstrated in Patel et al., 2002 ), therefore the
local noon irradiance represents a peak irradiance and the UV lev-
els throughout the rest of the day are significantly lower. Given
the higher irradiance level of the lamp as shown in Fig. 3 , coupled
with the effect of a diurnal light curve profile, the lab irradiance of
28 h is calculated to correspond to a martian equivalent UV dose
of approximately 6.5 days. Upon completion, the chamber was re-
stored to ambient conditions before removal of the samples from
the chamber.
2.5. Extraction, derivatization and GC-MS analyses of amino acids
After the Mars simulation, amino acids were extracted from the
minerals and derivatized according to the procedure described by
Martins et al. (2011, 2015 and references therein). A step to remove
sulfur was performed between the desalting and derivatization,
by using copper turnings (activated in a 10% HCl solution). The
activated copper turnings were added to V-vials containing the
desalted amino acid sample residues, brought up with 1 mL of
HPLC grade water, and left overnight. The copper turnings were
then removed and the V-vials were dried under a flow of N
2
. The
derivatized amino acids were dissolved in 75 μL of DCM.
The GC-MS analyses were performed using a Perkin Elmer
Clarus 580 gas chromatograph/Clarus SQ 8S mass spectrometer.
The amino acids were separated using two Agilent Chirasil L-Val
capillary columns (each 25 m, inner diameter 0.25 mm, film thick-
ness 0.12 μm) connected by a zero dead-volume connector. Helium
was used as carrier gas with a 1 mL/min flow. GC injector temper-
ature was set at 220 °C. Automatic splitless mode was used for in-
jection and the oven programme was: 1) 35 °C for 10 min; 2) 2 °C
per minute increase until 80 °C, hold for 5 min; 3) 1 °C per minute
increase until 100 °C; and 4) 2 °C per min increase until 200 °C,
hold for 10 min (total run time 117. 5 min). Temperatures for the
transfer line and the MS ion source were set at 220 °C and 230 °C,
respectively.
346 R. dos Santos et al. / Icarus 277 (2016) 342–353
Fig. 4. Single ion GC-MS chromatograms (25 to 85 min) of the derivatized (N-TFA, O-isopropyl) amino acids extracted from control sample G4 (goethite spiked with solution
4, but not subjected to the Mars simulation; chromatograms pointing upwards) and corresponding sample G4 (goethite spiked with solution 4 and analyzed after the Mars
chamber simulations; chromatograms pointing downwards). All single ions chromatograms are in the same scale. 1)
α-AIB; 2) D,L-isovaline; 3) D-alanine; 4) L-alanine; 5)
D-valine; 6) L-valine; 7) glycine; 8) D-norvaline; 9) D-
β-AIB; 10) L- β-AIB; 11) D- β-ABA; 12) β-alanine; 13) L- β-ABA; 14) L-norvaline; 15) D-leucine; 16) D-norleucine; 17)
L-leucine; 18) L-norleucine; 19 ) D-2-aminoheptanoic acid (internal standard); 20)
γ-ABA; 21) L-2-aminoheptanoic acid (L-2-AHA, internal standard); 22) D-aspartic acid; 23)
L-aspartic acid; 24) 6-AHA; 25) D-glutamic acid; 26) L-glutamic acid.
The identification of amino acids was achieved by comparing
the retention times and mass fragmentation patterns of the amino
acids present in the samples with those obtained from known
amino acid standard mixtures. The amino acid detection limit of
the GC-MS was verified to be approximately 3 parts per billion
(ppb). Typical GC-MS chromatograms from simulated G4 sample
and respective control are provided in Fig. 4 . Amino acids were
quantified by peak area integration of the corresponding ion frag-
ment, which were then converted to abundances using calibration
curves. These were created by plotting the ratio of the amino acid
standard/internal standard target ion peak area versus the mass of
amino acid standard injected into the column.
2.6. Brunauer–Emmett–Teller (BET) analyses
Brunauer–Emmett–Teller (BET) analyses were performed to
measure the surface area and pore size of the 11 minerals and
basaltic lava used in this work. These two variables are likely to be
the most relevant for amino acid adsorption and protection from
UV radiation because they have an important control on amino
acid distribution and arrangement on the mineral surface and on
physical shielding. Prior to analysis, approximately 0.5 g of all
samples were outgassed overnight at 353 K, under high vacuum.
Measurements were performed using a Micrometrics TriStar 30 0 0
gas adsorption analyzer, using N
2
as adsorptive gas. Measurements
were made in the relative pressure (P/P
0
) range from 0.01 up to
0.99. Final results were calculated using 9 equilibrium points in
the P/P
0
range between 0.03 and 0.20 (all linear regressions had
a correlation coefficient higher than 0.999).
3. Results
3.1. Degradation of amino acids under simulated Mars conditions
The fraction of extractable amino acids preserved after expo-
sition to simulated Mars surface conditions was calculated as the
ratio A/A0 (%), where A is the amount of each amino acid that was
not degraded and successfully extracted after the Mars Chamber
experiment, and A0 is the total amount of amino acid extracted
from the correspondent control (i.e., equivalent samples, prepared
in the same conditions, but not exposed in the Mars Chamber). The
amount of the amino acids extracted from the controls is an effec-
tive way to ascertain whether a lack of detection of amino acids
in a tested sample is due to degradation or to low extraction. The
lack of amino acid detection in both exposed sample and corre-
spondent control suggests that the lack of detection in the former
cannot be attributed to degradation induced by the simulated mar-
tian environmental conditions.
The fractions of amino acids extracted from the control samples
(i.e. [A0]/initial amino acid in the spiking solution) were calculated.
They ranged from 0 (no amino acids were detected in augite A1,
basalt lava B1 and nontronite N1) to 86%, 13 to 100%, 0 to 96%,
and 0 to 92% for experiments 1, 2, 3, and 4, respectively. Fig. 5
shows the average A/A0 ratios (in %) obtained for the 25 amino
acids that were used in experiments 2, 3 and 4. These values were
calculated from the individual A/A0 (%) obtained for each of the 25
amino acids (individual A/A0 ratios are shown in Tables 1–3 ).
Results from experiment 1 (i.e., minerals spiked with solution
containing 1 μM of each amino acid; not presented) show that
no amino acids were detected in any of the exposed samples (the
amino acid detection limit of the GC-MS is ∼3 ppb). In the con-
R. dos Santos et al. / Icarus 277 (2016) 342–353 347
Fig. 5. Summary of the average A/A0 amino acid ratios (in %) obtained after the simulation experiments in the Mars Chamber, where A is the amount of amino acids that
were not degraded and extracted after the simulation, and A0 is the total amount of amino acids extracted from the corresponding controls. Average values presented in
this figure were calculated using all the A/A0 ratios obtained for each of the 25 amino acids that were spiked in a given experiment found in Tabl es 1–3 . The lack of bars in
basaltic lava and enstatite for experiment 2 means complete degradation of
amino acids. Labradorite and jarosite were not used in experiments 4 and 2, respectively.
Table. 1
Summary of the individual A/A0 ratios (in %) obtained for experiment 2 (spiking solution, 10
μM of each amino acid) where A is the amount of the remaining amino acids
detected in simulated samples and A0 is the amount of amino acids detected in the control.
Individual amino acid Augite Basaltic Enstatite Goethite Gypsum Hematite Labradorite Montmorillonite Nontronite Olivine Saponite
(A/A0) vs mineral (A2) lava (B2) (E2) (G2) (Gy2) (H2) (L2) (M2) (N2) (O2) (S2)
α-AIB 3 ±1 0
a 0
a 9 ±0 17 ±1 0
a 0
a 42 ±4 18 ±2 22 ±1 18 ±7
D,L-isovaline
b 3 ±1 0
a 0
a 7 ±0 12 ±1 5 ±2 0
a 34 ±3 12 ±1 14 ±1 14 ±5
D-alanine 0
a 0
a 0
a 0
a 24 ±2 0
a 0
a 40 ±4 25 ±2 16 ±1 19 ±6
L-alanine 0
a 0
a 0
a 0
a 20 ±2 0
a 0
a 34 ±3 22 ±2 16 ±2 15 ±5
D- valine 2 ±0 0
a 0
a 4 ±0 32 ±2 3 ±0 9 ±1 30 ±2 18 ±2 14 ±1 15 ±5
L- valine 2 ±0 0
a 0
a 5 ±0 30 ±1 4 ±1 8 ±0 31 ±2 19 ±1 13 ±1 12 ±4
glycine 0
a 0
a 0
a 0
a 54 ±4 0
a 0
a 68 ±5 51 ±5 22 ±1 18 ±5
D-
β- AIB 0
a 0
a 0
a 0
a 49 ±2 0
a 0
a 32 ±3 29 ±3 26 ±3 0
a
L-
β- AIB 0
a 0
a 0
a 0
a 48 ±5 0
a 0
a 35 ±5 24 ±4 26 ±2 0
a
D-
β- ABA 0
a 0
a 0
a 0
a 56 ±3 0
a 0
a 35 ±3 29 ±6 17 ±1 19 ±6
L-
β- ABA 0
a 0
a 0
a 0
a 54 ±5 0
a 0
a 39 ±3 30 ±4 19 ±2 14 ±4
D- norvaline 0
a 0
a 0
a 0
a 50 ±3 0
a 10 ±2 33 ±1 23 ±1 15 ±1 15 ±4
L- norvaline 0
a 0
a 0
a 0
a 53 ±3 0
a 11 ±2 36 ±2 24 ±1 18 ±1 15 ±4
β-alanine 0
a 0
a 0
a 0
a 52 ±4 0
a 0
a 38 ±2 27 ±1 19 ±2 13 ±4
D- leucine 0
a 0
a 0
a 0
a 51 ±4 2 ±0 3 ±1 34 ±1 22 ±1 11 ±1 10 ±3
L- leucine 0
a 0
a 0
a 0
a 45 ±3 2 ±0 5 ±1 32 ±1 22 ±1 11 ±1 10 ±3
D- norleucine 0
a 0
a 0
a 0
a 43 ±4 0
a 7 ±0 18 ±2 12 ±1 13 ±1 17 ±8
L- norleucine 0
a 0
a 0
a 0
a 41 ±1 0
a 5 ±0 21 ±1 15 ±1 13 ±1 14 ±7
γ-ABA 0
a 0
a 0
a 0
a 66 ±4 0
a 0
a 32 ±2 28 ±3 26 ±2 19 ±6
D- aspartic acid 13 ±1 0
a 0
a 12 ±1 55 ±2 9 ±0 7 ±1 22 ±2 31 ±2 24 ±1 12 ±3
L- aspartic acid 14 ±1 0
a 0
a 14 ±1 59 ±3 10 ±0 8 ±0 25 ±1 34 ±2 26 ±2 13 ±4
6-AHA 0
a 0
a 0
a 0
a 40 ±3 0
a 0
a 22 ±1 25 ±1 25 ±1 20 ±5
D- glutamic acid 0
a 0
a 0
a 6 ±0 51 ±4 0
a 9 ±0 29 ±2 29 ±1 31 ±3 15 ±3
L- glutamic acid 0
a 0
a 0
a 6 ±0 49 ±3 0
a 9 ±1 25 ±2 26 ±2 32 ±3 14 ±4
a Complete degradation (A/A0 = 0).
b Enantiomeric separation not possible under chromatographic conditions.
trols, no amino acids were detected in augite (A1), basalt lava (B1)
and nontronite (N1). Hence, the lack of amino acid detection in the
A1, B1 and N1 experiments cannot be unequivocally interpreted as
caused by degradation. For the remaining minerals of experiment
1, amino acid degradation was observed. In the case of enstatite
(E1) all amino acids suffered complete degradation.
In experiment 2 (spiking solution containing 10 μM of each
amino acid), gypsum (Gy2) was the mineral that, on average,
preserved a greater proportion of amino acids, whereas amino
acids on enstatite (E2) and basaltic lava (B2) were completely de-
graded ( Fig. 5 and Table 1 ). Gypsum, olivine, montmorillonite and
nontronite were the only minerals that preserved all amino acids
( Table 1 ). Saponite prevented degradation of all amino acids except
D, L- β-AIB ( Table 1 ).
Results from experiment 3 (minerals spiked with a solution
containing 25 μM of each amino acid) showed that amino acids
were preserved (to different degrees) in all minerals ( Fig. 5 ). The
percentage of surviving amino acids for augite (A3), basaltic lava,
(B3) enstatite (E3), hematite (H3) and labradorite (L3) were be-
low 10% ( Fig. 5 and Table 2 ). On average, amino acids were
348 R. dos Santos et al. / Icarus 277 (2016) 342–353
Table. 2
Summary of the individual A/A0 ratios (in %) obtained for experiment 3 (spiking solution, 25
μM of each amino acid) where A is the amount of the remaining amino acids
detected in simulated samples and A0 is the amount of amino acids detected in the control.
Individual amino acid Augite Basaltic Enstatite Goethite Gypsum Hematite Jarosite Labradorite Monmorillonite Nontronite Olivine Saponite
(A/A0) vs mineral (A3) lava (B3) (E3) (G3) (Gy3) (H3) (J3) (L3) (M3) (N3) (O3) (S3)
α-AIB 16 ±1 2 ±0 8 ±1 22 ±2 0
a 5 ±1 43 ±4 6 ±1 17 ±2 12 ±1 12 ±1 20 ±1
D,L-isovaline
b 13 ±2 2 ±0 6 ±1 21 ±2 0
a 5 ±1 44 ±4 5 ±1 13 ±1 11 ±1 8 ±1 22 ±2
D-alanine 6 ±1 3 ±1 5 ±1 21 ±3 11 ±1 6 ±1 32 ±2 7 ±1 24 ±2 15 ±2 13 ±1 17 ±1
L-alanine 5 ±0 2 ±0 4 ±0 18 ±2 7 ±1 5 ±1 28 ±2 6 ±1 21 ±1 11 ±1 12 ±1 15 ±1
D- valine 7 ±0 3 ±1 5 ±1 24 ±2 15 ±2 8 ±1 47 ±3 8 ±1 22 ±2 16 ±2 17 ±1 24 ±2
L- valine 7 ±0 3 ±0 5 ±0 24 ±1 12 ±1 8 ±1 46 ±2 7 ±0 20 ±1 13 ±1 15 ±1 20 ±2
Glycine 0
a 0
a 0
a 31 ±3 22 ±2 7 ±1 28 ±4 9 ±1 40 ±2 19 ±2 18 ±2 15 ±1
D-
β- AIB 0
a 0
a 0
a 29 ±2 23 ±3 0
a 42 ±5 19 ±2 25 ±2 31 ±3 20 ±2 18 ±2
L-
β- AIB 0
a 0
a 0
a 33 ±2 27 ±3 0
a 37 ±5 19 ±2 28 ±2 30 ±3 20 ±3 17 ±1
D-
β- ABA 0
a 0
a 0
a 28 ±1 20 ±1 7 ±0 32 ±4 9 ±1 24 ±2 24 ±2 20 ±2 15 ±1
L-
β- ABA 0
a 0
a 0
a 29 ±2 23 ±2 8 ±1 31 ±3 9 ±1 26 ±2 24 ±3 20 ±2 13 ±1
D- norvaline 6 ±0 3 ±1 5 ±1 29 ±2 20 ±2 9 ±0 50 ±3 8 ±0 26 ±2 20 ±1 23 ±1 24 ±2
L- norvaline 7 ±0 4 ±1 6 ±0 32 ±2 23 ±1 10 ±1 51 ±3 9 ±1 30 ±2 19 ±2 26 ±2 21 ±1
β-Alanine 0
a 0
a 0
a 28 ±2 24 ±2 5 ±0 24 ±2 10 ±1 31 ±2 24 ±2 17 ±1 12 ±1
D- Leucine 5 ±0 3 ±0 5 ±0 29 ±1 25 ±1 7 ±0 32 ±3 5 ±0 18 ±1 13 ±1 21 ±1 12 ±0
L- Leucine 5 ±0 3 ±0 5 ±0 28 ±1 24 ±1 7 ±0 29 ±1 5 ±0 19 ±1 12 ±1 19 ±1 11 ±0
D- norleucine 6 ±1 5 ±0 5 ±0 26 ±1 23 ±1 8 ±1 42 ±2 8 ±0 18 ±2 18 ±1 20 ±2 20 ±1
L- norleucine 9 ±1 5 ±0 5 ±0 29 ±1 25 ±1 7 ±1 45 ±1 7 ±0 22 ±2 17 ±1 23 ±1 20 ±1
γ-ABA 0
a 0
a 0
a 37 ±2 38 ±5 10 ±1 78 ±3 10 ±1 23 ±1 39 ±2 21 ±1 18 ±2
D- aspartic acid 5 ±0 5 ±0 6 ±0 35 ±3 33 ±2 12 ±1 32 ±3 10 ±0 16 ±1 32 ±3 26 ±1 16 ±1
L- aspartic acid 6 ±0 7 ±0 7 ±1 40 ±2 37 ±2 14 ±1 34 ±4 11 ±1 19 ±1 35 ±3 28 ±1 18 ±1
6-AHA 0
a 0
a 0
a 35 ±3 33 ±3 8 ±1 0
a 12 ±1 18 ±1 28 ±2 20 ±1 22 ±2
D- glutamic acid 0
a 5 ±0 7 ±0 40 ±4 32 ±2 8 ±1 40 ±4 11 ±0 15 ±1 32 ±2 26 ±1 23 ±2
L- glutamic acid 0
a 5 ±0 6 ±1 37 ±4 30 ±2 8 ±1 38 ±2 10 ±0 13 ±1 29 ±2 25 ±1 22 ±2
a Complete degradation (A/A0 = 0).
b Enantiomeric separation not possible under chromatographic conditions.
preserved most efficiently in jarosite (J3). Basaltic lava (B3) pre-
served the smallest amount of amino acids ( Fig. 5 ).
The simulations using the minerals that were spiked with the
50 μM solution (experiment 4) reveal that nontronite (N4) pre-
served, on average, the largest proportion of amino acids ( Fig. 5 ).
The lowest percentage of surviving amino acids were found in
augite (A4), basaltic lava (B4) and hematite (H4), with A/A0 values
of 11%, 9% and 9%, respectively ( Fig. 5 ).
In addition, our results indicate that amino acid enantiomers
are degraded in the same degree (individual preservation ra-
tios obtained for D- and L-amino acids enantiomers are pro-
vided in Tables 1–3 ). The average A/A0 calculated for all D and
L enantiomers preserved after experiment 4 were 20.0 ±1.1 % and
20.4 ±1.1%, respectively. In experiment 3, D-amino acids had an
average A/A0 of 16. 5 ±1.2%, while L enantiomers had an aver-
age A/A0 of 16. 7 ±1.2%. Similarly, the average A/A0 ratios for D
and L-amino acids obtained for experiment 2 were 17.3 ±1.9% and
17.1 ±1.9%, respectively.
3.2. BET analyses
The results obtained for the surface areas and pore sizes of the
11 minerals and basaltic lava used in the simulations are provided
in Table 4 . Surface area values range from 0.22 m
2
/g (for basaltic
lava) up to 129.01 m
2
/g (for montmorillonite). Pore size values
range from 5.17 nm in saponite up to 21.04 nm in olivine.
4. Discussion
The preservation from UV-induced degradation of amino acids
spiked onto minerals is likely dependant on multiple factors. Here
we analyze the results obtained from the simulations in light of
the effect of 1) the structure of amino acids and 2) the physi-
cal/chemical features of the minerals that were used, in particular
their ferric/ferrous iron content, surface area and pore size.
4.1. Effect of the amino acid structure
Decarboxylation induced by UV photolysis has been proposed
as one of the main destruction pathways of amino acids ( Bertrand
et al., 2015; Boillot et al., 2002; Ehrenfreund et al., 2001; Johns and
Seuret, 1970 ; ten Kate et al., 2005 ). Boillot et al. (2002) verified
that L-leucine was subjected to decarboxylation under UV radia-
tion. Furthermore, Ehrenfreund et al. (2001) suggested this mech-
anism to explain the destruction of amino acids such as glycine,
alanine, α-aminoisobutyric acid and β-alanine under simulated
conditions in interstellar gas and interstellar icy grains. Decarboxy-
lation of amino acids by UV radiation results in the formation of a
radical in the α-carbon atom ( Ehrenfreund et al., 2001 ). The stabil-
ity of the radical is dependent on the substituents bonded to the
α-carbon atom. Alkyl substituent groups attached to the α-carbon
atom contribute towards the stability of the resulting alkyl amine
radical that forms after UV-induced decarboxylation and prolong
the life of the amino acid ( ten Kate et al., 2005 ). Therefore, we
should expect that glycine (the simplest amino acid, with two
hydrogen atoms bonded to the α-carbon) would be more degraded
and have the lowest surviving ratios after the Mars-conditions sim-
ulation experiments. In fact, Li and Brill (2003) have shown that
glycine has the highest relative aqueous decarboxylation rate when
compared to the protein amino acids leucine, isoleucine, valine and
alanine. In addition, we would expect that the amino acids more
resistant to UV radiation and less prone to decarboxylation would
be α-aminoisobutyric and isovaline, which are doubly substituted
in the α-carbon. A group of our results agree with the overall
effect of substitution in the α-carbon described above ( Tables 1–3 ).
For instance, glycine was less preserved than α-aminoisobutyric
and isovaline in all augite, basaltic lava, enstatite and jarosite
experiments 2, 3 and 4 ( Tables 1–3 ). However, it is evident that
the alkyl substituent groups are not the only factor contributing
towards the stability of the amino acids. If that was the case, then
isovaline and α-aminoisobutyric would be the most stable amino
acids in our experiments and the ones with the highest A/A0
values, which is not observed in our results. Other amino acid
R. dos Santos et al. / Icarus 277 (2016) 342–353 349
Table. 3
Summary of the individual A/A0 ratios (in %) obtained for experiment 4 (spiking solution, 50
μM of each amino acid) where A is the amount of the remaining amino acids
detected in simulated samples and A0 is the amount of amino acids detected in the control.
Individual amino acid Augite Basaltic Enstatite Goethite Gypsum Hematite Jarosite Montmorillonite Nontronite Olivine Saponite
(A/A0) vs mineral (A4) lava (B4) (E4) (G4) (Gy4) (H4) (J4) (M4) (N4) (O4) (S4)
α-AIB 38 ±4 22 ±1 27 ±3 34 ±3 27 ±1 9 ±0 27 ±3 33 ±4 36 ±2 11 ±2 11 ±1
D,L-isovaline
b 34 ±5 23 ±1 26 ±2 33 ±3 27 ±1 9 ±0 31 ±3 24 ±3 40 ±2 8 ±1 8 ±0
D-alanine 21 ±3 10 ±1 22 ±2 26 ±2 21 ±2 9 ±0 26 ±2 34 ±3 31 ±2 11 ±1 15 ±1
L-alanine 17 ±2 8 ±1 19 ±2 22 ±2 17 ±2 9 ±1 22 ±2 30 ±3 27 ±2 9 ±1 12 ±2
D- valine 15 ±2 16 ±1 39 ±2 26 ±2 22 ±1 8 ±1 22 ±1 26 ±2 46 ±2 16 ±1 19 ±1
L- valine 14 ±1 14 ±1 37 ±2 26 ±2 20 ±1 9 ±1 24 ±1 24 ±1 44 ±2 14 ±1 17 ±1
glycine 0
a 4 ±0 4 ±1 26 ±1 29 ±2 13 ±1 18 ±2 41 ±4 42 ±1 15 ±2 20 ±1
D-
β- AIB 0
a 0
a 18 ±2 24 ±2 22 ±2 8 ±0 20 ±2 28 ±1 30 ±5 20 ±2 25 ±2
L-
β- AIB 0
a 0
a 18 ±2 25 ±1 26 ±2 9 ±0 19 ±1 31 ±1 31 ±3 23 ±1 28 ±1
D-
β- ABA 0
a 7 ±0 23 ±2 20 ±1 19 ±1 7 ±0 16 ±1 25 ±1 34 ±1 15 ±1 23 ±1
L-
β- ABA 0
a 9 ±1 25 ±3 21 ±1 23 ±2 7 ±0 17 ±1 24 ±2 30 ±2 17 ±1 21 ±1
D- norvaline 14 ±1 15 ±1 48 ±1 29 ±1 23 ±1 9 ±1 24 ±1 28 ±1 57 ±3 18 ±1 24 ±1
L- norvaline 16 ±1 17 ±1 53 ±3 32 ±2 25 ±1 11 ±1 26 ±1 30 ±2 55 ±3 20 ±1 26 ±1
β-Alanine 0
a 0
a 15 ±2 20 ±1 24 ±1 15 ±1 15 ±1 29 ±2 21 ±1 14 ±1 16 ±1
D- leucine 9 ±1 11 ±0 35 ±2 23 ±1 17 ±1 9 ±1 24 ±1 17 ±1 31 ±4 16 ±1 17 ±0
L- leucine 9 ±1 11 ±0 30 ±3 25 ±1 17 ±1 10 ±1 24 ±2 17 ±1 28 ±3 14 ±1 16 ±0
D- norleucine 14 ±1 15 ±1 54 ±2 20 ±2 23 ±1 8 ±0 23 ±2 19 ±1 54 ±3 18 ±1 20 ±1
L- norleucine 12 ±1 16 ±1 59 ±3 24 ±2 25 ±1 10 ±0 26 ±1 22 ±1 52 ±2 20 ±1 22 ±1
γ-ABA 0
a 7 ±1 11 ±1 18 ±1 32 ±2 6 ±0 11 ±1 22 ±1 37 ±3 21 ±2 17 ±1
D- aspartic acid 13 ±1 4 ±0 18 ±2 21 ±1 28 ±1 13 ±1 14 ±1 16 ±1 55 ±3 17 ±1 17 ±2
L- aspartic acid 15 ±1 5 ±0 22 ±2 23 ±1 30 ±1 15 ±1 16 ±1 18 ±1 62 ±4 19 ±1 21 ±2
6-AHA 0
a 0
a 9 ±0 16 ±1 28 ±1 7 ±1 9 ±1 17 ±1 29 ±1 20 ±1 16 ±1
D- glutamic acid 9 ±1 3 ±0 11 ±1 23 ±1 34 ±1 9 ±1 20 ±2 14 ±1 54 ±6 24 ±2 14 ±1
L- glutamic acid 9 ±1 4 ±0 10 ±1 21 ±1 34 ±1 7 ±1 17 ±1 12 ±1 55 ±4 24 ±1 13 ±1
a Complete degradation (A/A0 = 0).
b Enantiomeric separation not possible under chromatographic conditions.
Tabl e 4
Qualitative information on the iron content and its valence, as well as the surface
area and pore size values from BET analyses for the minerals used in the Mars
chamber simulations.
Iron content BET analyses
Surface area (m
2
/g) Pore size
a
(nm)
Augite low Fe
2 + 1.19 ±0.01 12.91
Basaltic Lava medium Fe
2 + 0.22 ±0.01 14. 79
Enstatite medium Fe
2 + 0.50 ±0.01 14. 40
Goethite high Fe
3 + 2.13 ±0.01 17.7 8
Gypsum no iron 2.25 ±0.01 12.01
Hematite high Fe
3 + 4.91 ±0.04 11. 51
Jarosite high Fe
3 + 4.98 ±0.01 13. 25
Labradorite no iron 0.27 ±0.01 17.11
Montmorillonite low Fe
3 + 129.01 ±0.41 5.89
Nontronite high Fe
3 + 26.76 ±0.24 7.3 6
Olivine no iron 0.23 ±0.01 21.04
Saponite no iron
b 37.26 ±0.35 5.17
a Average pore width.
b Assessed from the XRD pattern.
structural and chemical factors (molecule dimensions and shape,
pKa values, etc.) will affect the way of interaction or adsorption
between the mineral surface and the amino acid. These factors
probably also play a role in the stabilization of amino acids against
UV light, but their complexity is beyond the scope of this article.
We observed that D and L amino acids were equally degraded
in the simulations ( Tables 1–3 ). This lack of enantiomeric pref-
erence regarding UV-induced degradation is consistent with the
observations of Orzechowska et al. (2007) for D,L-aspartic acid,
D,L-glutamic acid and D,L-phenylalanine.
4.2. Effects from the mineral features
The minerals can act as protectors of the amino acids from the
UV radiation in several ways. First of all, the opacity of the mineral
to UV radiation is a protection factor. Opacity increases approxi-
mately with the increasing average atomic number of the mineral.
For the minerals investigated here, Fe is the only element with
electrons in d orbitals, and is a much greater absorber of UV ra-
diation than any of the other elements. Thus, as a good approxi-
mation, the presence of Fe can be considered the dominant factor
controlling opacity to UV radiation. However, ferrous Fe promotes
iron (II) catalyzed reactions that degrade organic molecules, and
this is an important effect to be considered here. Other mineral
protecting factors are a high specific surface area and small aver-
age pore space, both of which should allow for a greater proportion
of the adsorbed amino acids to be protected from direct UV radia-
tion. Table 4 provides the information on the above characteristics
that can guide our discussion of their effect in the Mars simulation
experiments. The chemical character of specific mineral adsorption
sites may also have an effect in determining amino acid stability
but they should be considered in conjunction with the chemical
characteristics of the individual amino acid and are not discussed
here.
4.2.1. Role of iron
Iron is a transition metal with UV-photoprotective properties
( Olson and Pierson, 1986 ). The amount of ferric iron was found to
be correlated with the ability of minerals to confer protection from
UV-radiation ( Hoang-Minh et al., 2010 ) and the protective role of
ferric iron against UV radiation has been verified by Pierson et al.
(1993), Gómez et al. (2003) and Gauger et al. (2015) . In clay min-
erals, ferric iron increases the absorbance of UV radiation ( Chen
et al., 1979 ). Similarly, for sulfates, the opacity to UV radiation in-
creases much from gypsum to jarosite ( Martinez-Frias et al., 2006 ).
In our experiments, two ferric iron-rich minerals, jarosite and non-
tronite ( Table 4 ) had the highest amino acid preservation in exper-
iments 3 and 4, respectively ( Fig. 5 ). Within the smectite group,
montmorillonite and nontronite preserved more amino acids than
saponite, probably due to the absence of Fe in saponite ( Table 4 ).
The absence of Fe in saponite was inferred from X-ray diffraction
data, because the position of the 060 peak at 1.534 ˚
A indicates that
Fe
3 +
is not present in any significant amount ( Brown and Brindley,
198 0 ). Poch et al. (2015) have suggested that nontronite not only
350 R. dos Santos et al. / Icarus 277 (2016) 342–353
protects amino acids from UV light by shielding but that there
is also a stabilizing interaction between the clay and the amino
acids. These interactions perhaps help to dissipate absorbed energy
or facilitate photodissociated molecules to recombine ( Poch et al.,
2015 ).
Of the two Fe oxides in our experiments, goethite had a good
protection effect in experiments 3 and 4, as expected, but low in
experiment 2, while hematite protection was always low ( Fig. 5 ).
These results highlight the fact that protection against UV radiation
is controlled by a variety of phenomena. Watts et al., (1997) found
that the combinations of hematite and hydrogen peroxide promote
degradation of organic compounds. Goethite is also known to be
a catalyst for iron (II) catalyzed reactions ( Lin and Gurol, 1998 ),
which contributes to the degradation of organic molecules. It is
then possible that minerals where Fe is very abundant may pro-
mote electronic interactions between Fe atoms and adsorbed or-
ganic substances that cause their degradation. Thus, their overall
effect of protection against UV is a balance between the electronic
transfer effect and the UV-shielding effect.
4.2.2. Role of ferrous iron
Ferrous iron is known to degrade organic molecules in Mars-
like conditions through iron (II) catalyzed reactions ( Benner et al.,
20 0 0; Garry et al., 2006 ). Adsorbed water was removed from the
mineral surfaces in our Mars chamber simulation experiments due
to the low water vapor partial pressure (nominally zero), although
traces may have remained in the smectites as these are the most
hygroscopic of the minerals. Structural water or hydroxyls are not
removed using our experimental procedure, but this is not relevant
here because no mineral with ferrous iron contained structural
water. For these reasons, iron (II) catalyzed reactions in our exper-
iments most probably only involved ferrous iron in the minerals
and the amino acids. Thus, it can be expected that minerals with
ferrous Fe will have a degradation effect in our experiments.
The balance between the degradation effect of Fe
2 + and the UV-
shielding effect of Fe will decide which of the two is manifested
experimentally. Interestingly, Olson and Pierson (1986) observed
that ferrous iron absorbs less UV radiation than ferric iron be-
tween 200 and 400 nm (the UV-range used in our simulations),
and Chen et al. (1979) found that the UV absorption of nontronite
decreased when ferric iron was reduced to ferrous iron. Therefore,
the protective effect of Fe appears to be less effective in the case
of ferrous iron. In our study, the generally low amount of surviv-
ing amino acids from the minerals containing ferrous Fe, augite,
basaltic lava and enstatite ( Table 4 ) is in agreement with ferrous
iron being an important contributor for amino acid degradation
under simulated Mars conditions. The basaltic lava includes three
mineral phases containing ferrous iron: olivine, pyroxene and
glass. The olivine used in this work is forsterite (Mg variety) ac-
cording to XRD data and has little or no ferrous iron, which would
explain the high amino acid preservation in comparison to augite,
enstatite and basaltic lava. This explanation is compatible with the
higher amino acid preservation in enstatite for experiment 4 ( Fig.
5 ). The enstatite in our study is of the bronzite type, with low
ferrous Fe content (10–30% FeSiO
3
in the MgSiO
3
–FeSiO
3
series).
4.2.3. Surface area and pore size
According to Moores et al. (2007) , the variation in small-scale
geometries in the martian surface such as pits, trenches and over-
hangs would produce significant attenuation effects on the inci-
dent UV flux, and create safe spots for organisms and organic
molecules to be preserved. A similar principle can be applied at
the micro-scale for the minerals used in this work. Irregularities on
the mineral surfaces will also create sites where organic molecules
may be adsorbed and preserved from UV radiation. Higher surface
areas in a mineral indicate smaller particle size and/or a higher
amount of irregularities in the surface, both of which generate a
higher number of sites where organic molecules can be protected
from direct exposure to UV light.
In adsorption experiments, the key variable of the solid phase
is the surface area: the larger the surface, the more adsorbate can
be accommodated. Particle size is related to surface area, but is
not the key variable, because surface area depends also on other
variables. In our study, all the amino acid was forced to adsorb on
the mineral surfaces and so there is no dependence between total
amounts of amino acid adsorbed and surface area. The dependence
is on how the amino acids were adsorbed and where, plus on the
configuration of mineral particles in the well during the experi-
ment, all of which affect exposure to radiation and resilience to it.
In addition to the surface area, the size of the pores should also
influence the degradation of amino acids under a high flux of UV-
radiation. Pores provide a site where organic molecules may be
protected against radiation. The photoprotective effect conferred by
the pores should be inversely correlated with their respective size.
The range of pore size measured by BET is provided in Table 4 . If
all amino acids were able to penetrate the whole range of pores
existent in our minerals, this would result that the smaller pores
would create a more shielded environment for organic molecules
by limiting the amount of UV influx in the site. On the contrary,
bigger pores would let more radiation penetrate and induce more
degradation.
From our results we observe that nontronite, montmorillonite
and saponite were the minerals that had the highest surface areas
and the smaller pore sizes ( Table 4 ). Clay minerals of the smec-
tite group have large surface areas and the ability to adsorb or-
ganic molecules both in external surfaces and in the space between
the layers that make up the mineral structure (Mortland, 1970 ;
Raussel-Colom and Serratosa, 1987 ). This fact is in agreement with
the generally high amounts of amino acids preserved in nontronite,
montmorillonite and saponite when compared to the other miner-
als ( Fig. 5 ). With the clear exceptions of olivine and gypsum, the
minerals with lower surface areas and larger pore sizes than the
clays generally preserved less amino acids ( Table 4, Fig. 5 ). Olivine,
with a low surface area and the largest pore size, preserved more
amino acids than labradorite, hematite, augite and basaltic lava, all
of which have similar or larger surface areas and smaller pore sizes
( Table 4 ). This is one more example that no single variable can ex-
plain amino acid preservation on the mineral surfaces and all vari-
ables have to be considered together in order to approach a correct
interpretation.
4.3. Concentration effect
Overall, our results show that the concentration of amino acids
in the experiments had an influence on amino acid preservation.
The mineral displaying the highest photoprotective effect in each
experiment varied with the amount of amino acids that were
spiked into the minerals. Nontronite preserved the largest propor-
tion of amino acids in experiment 4, whereas jarosite and gypsum
did so in experiments 3 and 2, respectively ( Fig. 5 ). In experiments
2, 3 and 4 the general trend is that amino acid preservation ratio
increased with increasing spiking concentration. This was clearly
observed in augite, basaltic lava, enstatite, hematite, labradorite
and saponite ( Fig. 5 ), although gypsum and montmorillonite are
a clear exception to this trend, and the other minerals showed
no specific trend ( Fig. 5 ). However, if we consider that the low-
est preservations occur in experiment 1, the trend of increasing
preservation with increasing amino acid amounts in the mineral
surfaces appears more robust. We provide tentative explanations to
address these results that will need to be explored in future work.
The general increase of amino acid preservation with increasing
spiking concentration may be related to the type of sites where
R. dos Santos et al. / Icarus 277 (2016) 342–353 351
the amino acids were adsorbed. During the spiking procedure we
let amino acids to adsorb to the mineral surfaces for 24 h and
then the solution was evaporated. At lower concentrations of the
amino acids, they probably adsorbed on the most available sites.
As the concentration increased, probably the amino acids adsorbed
in less exposed sites and thus more protected. This effect may have
been enhanced by the experimental procedure. There are two ob-
vious stages in the adsorption process. During the first step (ad-
sorption in the suspension) the amount of water remains constant
and there was an approach to equilibrium between amino acid in
solution and in mineral sites. However, during the drying step the
amount of water decreased rapidly and so increased the amino
acid concentration in the existing water. This increasing concen-
tration may have forced adsorption into the less exposed sites as
the more exposed ones filled quickly.
Another plausible explanation for the increase of preserved
amino acid with increasing spiking concentration may be based
on the association of adsorbed amino acids on the mineral sur-
faces. As the amount of adsorbed amino acids increased, especially
as the water dried, the amino acids may have entered in contact
with each other more frequently on the mineral surface. Possible
interactions between amino acids adsorbed in nearby sites may in-
crease their stability and attenuate (in some way) the degradation
induced by UV-radiation. Alternatively, some of the amino acids
may have been adsorbed as aggregates, of which some molecules
were exposed and some were covered by other molecules. This dis-
position would result in increased protection of the amino acids
from UV radiation ( Poch et al., 2014 ). However, we do not think
that thick aggregates were likely to form given the low amino acid
concentrations (0.1–5 μmol/g) and the available mineral surface
(0.22–129 m
2
/g, Table 4 ).
Gypsum is an interesting case in our experiments because
it has a large preservation rate while it has no Fe, and neither
its surface area nor its average pore size suggests an especially
protective capacity ( Table 4 ). In addition, gypsum preserved ap-
proximately two times more amino acids in experiment 2 than in
experiments 3 and 4 ( Fig. 5 ). Gypsum is a relatively soluble salt.
It is expected that gypsum was partially dissolved during the 24 h
contact with the spiking solution and that the dissolved gypsum
recrystallized during the drying step of the spiking protocol. It is
possible that recrystallization of dissolved calcium sulfate trapped
or surrounded amino acids that were adsorbed on the remaining
crystals. This putative entrapment of amino acids would have
likely increased protection. If this entrapment occurred, its effect
would probably have been more evident in the experiments using
less concentrated spiking solutions ( Fig. 5 ). This is because the
relative amount of amino acids that were adsorbed during the
24 h contact between the solution and the gypsum was higher (as
the total amino acid amount is lower, a greater proportion of it
adsorbs early), and then also a higher proportion of them could
be trapped by the crystallization during the later drying stage.
4.4. Implications for Mars exploration
In this work, clays and sulfate minerals proved to preserve, on
average, more amino acids from UV-induced degradation than sil-
icates, pyroxenes, iron oxides and feldspars. Precisely, the pres-
ence of clays and sulfate minerals on Mars is relevant in the as-
trobiology context because they indicate past habitable environ-
ments where water was present ( Downs et al., 2015, Squyres et
al., 2004 ). Clay minerals are associated with sites of accumulation
and preservation of organic molecules due to their high adsorption
capacity and their ability to preserve organic matter by stabiliz-
ing it and protecting it from oxidation (Mortland, 1970; Poch et al.,
2015; Raussel-Colom and Serratosa, 1987 ). Sulfate minerals, such
as jarosite and gypsum, may actually be opaque to UV radiation
and protect life and respective biomarkers ( Amaral et al., 2007;
Aubrey et al., 2006; Hughes and Lawley, 2003 ). Because clays of
the smectite group and sulfate minerals are (1) related to environ-
ments amenable to life and (2) good biomarker preservers, they
should be targeted for the detection of organic molecules in future
life-searching missions such as NASA’s 2020 mission.
Olivine of forsterite composition also preserved considerable
amounts of amino acids during the Mars simulation, despite its
low surface area and high pore size. Olivine (including low iron
varieties) is widely distributed on Mars ( Ody et al., 2013 ). Accord-
ing to our results, forsterite and perhaps other olivine minerals of
low Fe content might be considered good targets for the detec-
tion of life biomarkers on Mars, provided that there are geological
clues towards possible habitable environments. However, despite
the high amino acid preservation verified in our results, we believe
that olivine should be less relevant for life and organic biomarkers
searching missions due to its usual association with basaltic min-
erals that do not preserve high amounts of amino acids and high
weathering susceptibility by water ( Kuebler et al., 2003 ).
An important aspect of our experiments in relation to the
search for biomarkers on Mars is the mineral ability for amino
acid preservation at low amino acid content. Given the low
concentrations of organic matter expected on Mars, gypsum,
montmorillonite, nontronite, saponite and olivine appear as much
better candidates to preserve amino acid biomarkers than the
other minerals tested ( Fig. 5 ). This fact adds one more reason
to target smectite clays (nontronite, saponite, montmorillonite)
and gypsum on Mars. For these minerals, their protective ability
does not drop at 10 μM amino acid concentration, as appears to
happen with the other Mars-relevant minerals. To further support
our results, indigenous chlorinated hydrocarbons were detected by
the Curiosity rover in the Yellowknife Bay formation on Mars (in-
formally named the Sheepbed member), which contained ∼20 wt %
smectite clay ( Ming et al., 2014; Vaniman et al., 2014 ).
The amino acid standards used in this experiment ranged from
0.1 μmol/g of mineral to 5 μmol/g, i.e. ranged from ∼10 parts per
million (ppm) to 500 ppm for each amino acid present in the min-
eral matrix. This range of values is quite high when compared
to terrestrial Mars soil analogues. As an example, a typical Mars
soil analogue from Atacama and Arequipa have individual amino
acid concentration in the range of 1–10 ppb (e.g. Peeters et al.,
2009 ), while Mars soil analogues richer in amino acids, such as
Salten Skov and some Utah soils, range from 10 ppm to 50 ppm
(Martins et al., 2011; Peters et al., 2009 ). The abundances used in
this manuscript are higher than what it is expected to be present
on Mars, placing a limit of detection for the preservation of amino
acids under Mars conditions.
As a final note, UV irradiation on Mars is limited to the first
millimeters, but energetic particles (solar energetic particles (SEP)
and galactic cosmic rays (GCR)) can go deeper in the subsurface,
reach organic molecules and contribute to their degradation. A SEP
dose of 60 0–70 0 mGy/yr can reach the surface of Mars and pen-
etrate to around 10 cm, while GCR are typically capable of pen-
etrating up to 3 m into the subsurface ( Parnell et al., 2007 ) and
over geological time, deactivate spores and degrade organic species
( Dartnell et al., 2007 ). Therefore, future work should study the in-
fluence of the minerals on the preservation of organic molecules
under simulated Mars conditions using SEP and GCR.
5. Conclusions
We analyzed the UV-induced degradation of 25 amino acids
spiked onto augite, basaltic lava, enstatite, goethite, gypsum,
hematite, jarosite, labradorite, montmorillonite, nontronite, olivine
and saponite under simulated Mars conditions. The results indi-
cated that:
352 R. dos Santos et al. / Icarus 277 (2016) 342–353
(1) D- and L-enantiomers were degraded in the same extent in
all experiments.
(2) The proportion of amino acid preservation in each mineral
tends to increase with the concentration of amino acids in
the spiking solution. At the lowest concentration (1 μM or
each amino acid) no amino acids were recovered due to a
combination of complete degradation and low extractability.
(3) Results from the experiments at concentrations of 10, 25
and 50 μM (of each amino acid) show that, on average,
smectite clays (montmorillonite, nontronite and saponite),
sulfates (gypsum and jarosite) and olivine (forsterite) were
the minerals that preserved more amino acids. Augite,
basaltic lava, enstatite and hematite preserved the least
proportions of amino acids.
(4) For the interpretation of the results, several major variables
affecting protection from UV radiation were considered: a)
amino acid molecular structure and substitution in the α-
carbon; b) mineral opacity to UV light, driven mainly by Fe
content; c) large surface area and small average pore size are
likely to promote amino acid preservation; d) ferrous iron
content promotes iron (II) catalyzed reactions and thus dis-
sociation of amino acids. None of the above single variables
can fully explain our results, but most of them can be re-
lated to one or more of these variables.
(5) Our results indicate that rocks with abundant smectite
(montmorillonite, saponite, nontronite) and/or sulfates (gyp-
sum, jarosite) are very good targets to search for amino acid
biomarkers (and possibly other type of biomarkers) on Mars,
due to the preserving ability of the above minerals, even at
relatively low amino acid concentration (1 μmol/g). This ar-
gument is strengthened because the above minerals typically
form in environments amenable to life. As a result, future
missions that aim to detect organic molecules on the Red
planet, such as the NASA 2020 mission should consider tar-
geting locations rich in these minerals in order to maximize
the chances of finding preserved martian organic molecules.
Acknowledgments
Renato dos Santos is funded by a Janet Watson Scholarship. Zita
Martins is funded by a Royal Society University Research Fellow-
ship (grant UF080820 and grant UF130324). The authors acknowl-
edge financial support from STFC (grant ST/J001260/1 ). M. Patel ac-
knowledges funding from STFC grant ST/I003061/1 . We thank two
anonymous reviewers for their insightful comments.
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