Article
https://doi.org/10.1038/s41467-024-49237-6
Primordial aqueous alteration recorded in
water-soluble organic molecules from the
carbonaceous asteroid (162173) Ryugu
A list of authors and their af
fi
liations appears at the end of the paper
We report primordial aqueous alteratio
nsignaturesinwater-solubleorganic
molecules from the carbonaceous aster
oid (162173) Ryugu by the Hayabusa2
spacecraft of JAXA. Newly identi
fi
ed low-molecular-weig
ht hydroxy acids (HO-
R-COOH) and dicarboxylic
acids (HOOC-R-COOH), such as glycolic acid, lactic
acid, glyceric acid, oxalic acid, and succi
nic acid, are predominant in samples
from the two touchdown locations at Ryug
u. The quantitative and qualitative
pro
fi
les for the hydrophilic molecules between the two sampling locations
shows similar trends within the order
of ppb (parts per billion) to ppm (parts
per million). A wide variety of structural isomers, including
α
-and
β
-hydroxy
acids, are observed among the hydrophilic molecules. We also identify pyruvic
acid and dihydroxy and tricar
boxylic acids, which are biochemically important
intermediates relevant to molecular evolution, such as the primordial TCA
(tricarboxylic acid) cycle. Here, we
fi
nd evidence that the asteroid Ryugu
samples underwent substantial aqueo
us alteration, as revealed by the pre-
sence of malonic acid during keto
–
enol tautomerism in t
he dicarboxylic acid
pro
fi
le.Thecomprehensivedatasuggestthepresenceofaseriesforwater-
soluble organic molecules in the regolith of Ryugu and evidence of signatures
in coevolutionary aqueous alteration between water and organics in this car-
bonaceous asteroid.
Pristine samples from the near-Earth asteroid (162173) Ryugu returned
to Earth by the Hayabusa2 spacecraft provided a valuable opportunity
to reveal the organic astrochemistry preserved for over 4.6 billion
years in the Solar System
1
–
4
. This unique opportunity for investigating
primordial organic molecules illuminates several scienti
fi
ccontexts
involving carbonaceous asteroids, including the following
questions
5
–
7
:
–
WhatistheroleofcarbonaceousasteroidsintheSolarSystemhis-
tory?
–
What are the origins and characteristics of the light elements, e.g.,
carbon (C), nitrogen (N), hydrogen (H), oxygen (O), and sulfur (S)?
–
What do their isotopic compositions reveal?
–
How do they record the primordial organic evolution on the aster-
oid?
–
Is the nature of molecular chirality symmetric or asymmetric?
–
How do interactions between water, organic matter, and minerals
affect chemical diversity?
To address these important scienti
fi
c questions, the
Hayabusa2 soluble organic matter (SOM) team
6
evaluated aggregate
fi
ne grain samples from the
fi
rst and second touchdown sites (here-
after, TD1 and TD2); hence, the bulk chemistry data from these two
sample collections are averaged representative values for the surface
(A0106) and possibly subsurface (C0107) environments (i.e., TD2 was
near the arti
fi
cial crater, for which the depth was ~1.7 meters below
ground level
8
) of Ryugu (Fig.
1
). For further insight at the organic
molecular level, the SOM team determined the
fi
rst answers to these
questions based on carbon (C), nitrogen (N), hydrogen (H), oxygen
Received: 16 September 2023
Accepted: 29 May 2024
Check for updates
e-mail:
takano@jamstec.go.jp
Nature Communications
| (2024) 15:5708
1
1234567890():,;
1234567890():,;
(O), sulfur (S) elements and their isotopic pro
fi
les
6
,
9
,
10
, monocarboxylic
acids
6
, amino acids and their molecular chirality
6
,
11
,
12
, pyrimidine
nucleobase and N-heterocycles
6
,
9
, primordial salts and sulfur-bearing
labile molecules between the organic and inorganic interfaces
10
, ali-
phatic hydrocarbons and polycyclic aromatic hydrocarbons (PAHs)
13
,
14
,
comprehensive organic molecular pro
fi
les
6
,
15
, molecular growth
signatures
16
, and sub-mm scale spatial imaging for organic homo-
geneity and heterogeneity in the mineral assemblage
6
,
17
. According to
Fourier transform-ion cyclotron resonance mass spectrometry (FT-
ICR/MS) analysis, the SOM from Ryugu samples contained highly
diverse organic molecules (~20,000 species) in the solvent extracts
6
,
15
.
Naraoka et al.
6
reported organic molecular diversity from initial
bulk (IB) to insoluble organic matter (IOM) in a sequential extraction
process using hydrophilic to hydrophobic solvents. In this report, we
determine the molecular diversity of polar organic molecules extracted
from the
fi
rst contact between hot wate
r and pristine Ryugu samples
Article
https://doi.org/10.1038/s41467-024-49237-6
Nature Communications
| (2024) 15:5708
2
and report the unique color characteristics of the sequentially extracted
fractions with systematic variations in their
13
C- and
15
N-isotopic pro
fi
les.
If indigenous water
–
organic interactions occurred in the history of the
asteroid, the signatures of parent
body aqueous alteration could have
been recorded in these hydrophilic organic molecules (Fig.
2
).
To decipher the chemical evolution that occurred in surface and
subsurface samples
1
,
2
,
18
, we comprehensively evaluated highly diverse
hydrophilic organic molecules using capillary electrophoresis (CE)
with high-resolution mass spectrometry (HRMS). We used this mole-
cular information to interpret the aqueous alteration processes that
asteroid Ryugu has experienced to complement the study by Naraoka
et al., who reported organic molecular diversity from initial bulk (IB) to
insoluble organic matter (IOM) in the sequential extraction process.
Results and discussion
Identi
fi
cation of water-extractable molecules and diverse
structural isomers
The Ryugu A0106 and C0107 samples (~10 mg each) were subjected to
hot water extraction in sealed ampoules at 105 °C for 20 h for the
present study
6
(see Methods). This extraction targeting water-
extractable compounds followed previous reports (e.g., hydroxy
acids
19
,
20
;). We
fi
rst identi
fi
ed highly diverse hydroxy acids and
hydrophilic molecular groups in hot water extracts by CE-HRMS
(Fig.
2
). Figure
3
A shows the baseline resolution of representative
hydroxy acids and other molecules from the hot water extracts iden-
ti
fi
ed with reference standards (Murchison meteorite; Methods). We
determined each molecule by migration time (MT) and the exact mass
corresponding to the monoisotopic mass
9
. Short-chain hydroxy acids
(e.g., glycolic acid, HO-CH
2
-COOH; lactic acid, CH
3
-CH(OH)-COOH;
and glyceric acid, HO-CH
2
-CH(OH)-COOH) were predominant in
aggregate samples of A0106 and C0107 from Ryugu (Fig.
3
B).
Within the concentration range of 10 ppb to 10
3
ppb [i.e., parts per
billion (ppb) as nanograms (ng) hydroxy acid per gram (g) of extracted
Ryugu sample] (Table S1), structural isomers of hydroxy acids and
molecular abundance were determined. The concentration of lactic acid
(C
3
), which is more abundant than glycolic acid (C
2
), is consistent with
previous reports on the Murchison meteorite
19
,
20
. Among these homo-
logs of hydroxy acids, we also identi
fi
ed molecules potentially relevant to
chemical evolution (e.g., pyruvic acid, C
3
H
4
O
3
; mevalonic acid, C
6
H
12
O
4
;
and citric acid, C
6
H
8
O
7
). Since these molecules are important precursors
in diverse molecular evolution
21
, demonstrating their presence on the
carbonaceous asteroid Ryugu is signi
fi
cant. Speci
fi
cally, these molecules
are biochemically crucial and are intermediate substrates of the lipid
synthesis pathway and Krebs cycle. Chemically reactive hydroxy acids
(e.g., glycolic acid) may play an important role in molecular evolution for
the formation of primary carbon chains
22
. Furthermore, there may be a
connection pathway between hydr
oxy acids and formose reaction-
derived IOM
23
as side products
24
.
In addition to the previously reported organic acids (e.g., formic
acid and acetic acid
6
) and nitrogen heterocycles
9
,wealsoidenti
fi
ed a
new group of diverse carboxylic acids (i.e., monocarboxylic acids for
aliphatic, aromatic, unsaturated, and keto acids; Figs.
2
,
3
and
Tables S1, S2) and nitrogen (N)-bearing molecules, including amines
(e.g., urea, CH
4
N
2
O; and glycocyamine, C
3
H
7
N
3
O
2
), hydroxy- and
N-heterocyclic indoles (e.g., dihydroxyindole, C
8
H
7
NO
2
;andhydro-
xyindole, C
8
H
7
NO), in hot water extracts. Thus, we suggest that the
spectroscopic signals of hydroxyl groups (-OH) and amino/imino
groups (-NH) in the infrared spectra (chambers A and C
2
; A0106 and
C0107,
9
; grain-scale and surface observation; Fig. S13, cf.
17
,
25
:) include a
substantial amount of intramolecular -OH and -NH moieties originat-
ing from the series of polar organic molecules in the present study.
Aqueous alteration signatures and keto
–
enol tautomerism
Aliphatic dicarboxylic acids (e.g., C
2
, oxalic acid; C
3
, malonic acid; C
4
,
succinic acid; C
5
, glutamic acid; and C
6
, adipic acid) are de
fi
ned as
organic compounds bearing two carboxyl groups (-COOH) with an
aliphatic backbone. We detected dicarboxylic acids (e.g., oxalic acid,
malonic acid, succinic acid, glutaric acid, adipic acid, malic acid, and
maleic acid) within the concentration range of 10 ppb to 10
3
ppb
(Table S1; Fig.
4
A). Previous reports have suggested that the relative
concentration of malonic acid (HOOC-CH
2
-COOH) in the dicarboxylic
acid group is sensitive properties by the process of keto
–
enol
tautomerization
26
,
27
. Laboratory-based malonic acid formation has
been compared with the extraterrestrial origin of dicarboxylic acids
from tautomerization
28
. Enol malonic acid is presumed to decompose
faster than other dicarboxylic acids because it produces a thermo-
dynamically unstable carbon
‒
carbon double bond (i.e., HO-C = CH-,
vinyl alcohol group
29
–
31
) during aqueous alteration as follows:
HOOC
CH
2
COOH with H
2
O
!ð
HO
Þ
2
C=CH
COOH
(
)
HOOC
CH = C
ð
OH
Þ
2
Hence, the formation of two vinyl alcohol groups on the intra-
molecular malonic acid is probably more reactive (chemically
unstable) than that of other dicarboxylic acids (Fig.
4
A, B). After
unstable equilibrium is eventually reached under aqueous conditions
at higher temperatures
32
,
33
,keto
–
enol tautomerism induces dec-
arboxylation to form acetic acid (CH
3
COOH) and carbon dioxide (CO
2
)
as end products (Fig.
4
B). Hence, a substantial concentration of acetic
acid
6
can result from chemical cleavage of the secondary acetogenic
process via malonic acid. Therefore, we suggest that malonic acid
(mole%) is a molecular signature of the aqueous alteration process
recorded in the asteroid Ryugu. In fact, the relative abundance of
malonic acid is an order of magnitude lower than that of CM meteor-
ites (e.g., Murchison and Murray, as shown in Fig.
4
A), suggesting a
different aqueous history.
The systematics of hydrophilic molecules at two sampling
locations on Ryugu
The systematics for elemental and organic chemical surveys, includ-
ing CNHOS and hydrophilic molecular groups, were compiled to
formulate the TD1 and TD2 diagrams (Fig.
5
). Within these overviews
of surface and potential subsurface sample pro
fi
les
1
,
2
,
18
,weevaluated
Fig. 1 | Pro
fi
les of samples obtained from asteroid (162173) Ryugu and various
observation photographs from kilometer to micrometer scales. A
Ryugu pho-
tograph taken with the Optical Navigation Camera Telescopic (ONC-T). The photo
was taken on August 31, 2018. Credit: JAXA, Univ. Tokyo etc.
B
Thermal image of
Ryugu from the thermal infrared imager (TIR). The observation indicates that the
lowest temperature in the blue section is estimated to be below
−
50 °C, whereas the
lowest temperature in the red section is estimated to be < 60 °C. Please see the
onsite data acquisition and temperature dynamics
74
,
75
. Credit: JAXA etc. The data
were collected on August 31, 2018.
C
The surface of the asteroid Ryugu and the
shadow of the Hayabusa2 spacecraft. The image was taken from ONC-W1 at an
altitude of 70 m. Date taken: 21 September 2018.
D
The 1st touchdown operation on
Ryugu with CAM-H imaging on 22 February 2019. The image was captured just
before touchdown during descent at an altitude of approximately 4.1 m. Credit:
JAXA.
E
Photograph of initial sample A0106 (38.4 mg)
6
from the asteroid Ryugu
during the 1st touchdown sampling
1
,
2
. A photograph of C0107 (37.5 mg) from the
2nd touchdown sampling is shown in Supplementary Fig. S1. The scale bar repre-
sents 1 mm (red line).
F
Reference photograph of the discolored and altered cross-
section of the Ryugu sample showing possible precipitates (e.g., C0041)
76
.
G
The
isotopic compositions of C, N, H, and S of the Ryugu aggregate samples for A0106
and C0107 are shown after compilation
6
,
9
,
10
. The isotopic compositions of
δ
13
C(
‰
vs. VPDB),
δ
15
N(
‰
vs. Air),
δ
D(
‰
vs. VSMOW) and
δ
34
S(
‰
vs. VCDT) are expressed
as international standard scales. By comparing the classi
fi
cation of carbonaceous
meteorites in the Solar System, the compiled data suggested that the Ryugu sample
has isotopic characteristics most similar to the petrologic type of CI chondrite
6
,
52
.
Article
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3
the average chemical composition and diversity of hydrophilic
molecules to determine whether there is potential organic hetero-
geneity or homogeneity in Ryugu. The total amount of CNHOS light
elements (
Σ
CNHOS) in the IB of A0106 and C0107 were ~21.3 wt%
6
and
~23.7 wt%
9
,respectively(Fig.
5
A). Then,
Σ
CNHOS in the IOM increased
by an order of magnitude (Fig.
5
B) because the inorganic matrix was
eliminated (cf. IOM description
34
).
The overall observations were plotted directly on or near the 1:1
line for hydroxy acids and other hydrophilic molecules (Fig.
5
C), water-
extractable amino acids and amines for the CHNO molecular series
6
,
11
(Fig.
5
D), and inorganic cations and anions
10
(Fig.
5
E). The detection of
N-bearing primary amine molecules (R-NH
2
), ammonium ions
(NH
4
+
)
6
,
10
,
11
and urea molecules [(NH
2
)
2
= CO] (Fig.
5
F) from Ryugu is an
important
fi
nding, not only as evidence of exogenous nitrogen carriers
but also as the most primitive chemical forms of nitrogen
35
,
36
.Ureaand
alkyl-urea groups (e.g., methyl-urea and alkyl-urea up to C
6
)mayalso
serve as reservoirs of involatile C, N, O, and H on the asteroid. Urea is
also an interesting organic reactive substrate that exhibits amphiphilic
Fig. 2 | Representative molecular structures of newly identi
fi
ed from Ryugu
aggregate samples (A0106 and C0107).
The hot water-extractable molecular
structures include
α
-hydroxy acids (e.g., glycolic acid, lactic acid, and
2-hydroxybutyric acid),
β
-hydroxy acids (e.g., glyceric acid, 3-hydroxybutyric acid,
mevalonic acid, and hydroxybenzoic acid), dicarboxylic hydroxy acids (e.g., malic
acid and citramalic acid), monocarboxylic acids (e.g., valeric acid, 4-oxovaleric acid,
5-oxohexanoic acid, tiglic acid, toluic acid, and cumic acid), dicarboxylic acids (e.g.,
oxalic acid, malonic acid, succinic acid, glutaric acid, adipic acid, and maleic acid),
tricarboxylic acid (e.g., citric acid), pyruvic acid and other nitrogen-bearing
hydrophilic molecules (e.g., urea, methylurea, glycocyamine = guanidinoacetic
acid, 6-hydroxynicotinic acid, isovalerylalanine, and dihydroxyindole). Notably,
some hydroxy acids and carboxylic acids have chiral centers with left
–
right sym-
metry, but those enantiomers are not discussed in the present report. Newly
identi
fi
ed cyclic sulfur compounds (S
6
,S
7
in this study; Supplementary informa-
tion) were also noted with the comparison of cyclic S
8
molecule
6
.
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Fig. 3 | Representative hydrophilic molecular groups in hydroxy acid, dicar-
boxylic acid, and tricarboxylic acid in hot water extracts from Ryugu samples
(A0106 and C0107) and a reference sample (Murchison). A
High-resolution mass
electropherogram of capillary electrophoresis during the analysis of hot water
extracts (#7-1). The blank was composed of ultrapure water before hot water
extraction. Based on the migration time (min) and mass accuracy within ~1 ppm
(
μ
g/g) of the theoretical peak (
m/z
), we assigned each observed peak to the cor-
responding standard (Fig. S4).
B
Concentrations of representative hydroxy acids
determined in Ryugu aggregate samples. In this graph, dark blue and light blue
represent samples A0106 and C0107, respectively. These hydroxy acids and other
related hydrophilic molecules from fraction #7-1 (hot water extracts) are in ppb.
C
The analytical accuracy for the concentration of short-chain
α
-hydroxy acids (i.e.,
glycolic acid, lactic acid, 2-hydroxybutyric acid, and 2-hydroxyvaleric acid)
extracted from Murchison and Murray meteorites
19
(glycolic acid as 100%) is shown
for the same formulation.
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properties and behaves as a solid and/or liquid depending on tem-
perature and ambient physicochemical factors
22
,
37
. Regarding the
temperature constraint of Ryugu, Yokoyama et al. reported that sam-
ples from TD1 and TD2 remained below ~100 °C after aqueous altera-
tion until the present based on the abundance of structural water
38
.
To further describe the CI-like organic characteristics, the
hydrophilic molecules from Ryugu (A0106 and C0107) were compared
to CM-type chondrites from Murchison and Murray (Fig.
6
A).
According to the composition of amino acids found in the CI-type
meteorite Ivuna
39
, the properties of meteoritic amino acids were ver-
i
fi
ed for Ryugu with the same normalization (Fig.
6
B). Compared to the
CM2 chondrites of Murchison and Murray, CI-type carbonaceous
chondrites with parent bodies that h
ave experienced aqueous altera-
tion contain lower total amino acid abundances
39
,
40
.Inthiscontext,
Burton and coworkers reported that carbonaceous chondrites that
experienced high-temperature thermal alteration along with aqueous
alteration (e.g., CI type Y-980115; re-examination with
δ
15
Nofamino
acids
41
) have much lower amino acid abundances than CI Orgueil and
CM Murchison meteorites
40
,
42
). Distinct positive correlations were
observed in both concentration pro
fi
les above the 1:1 line, whereas the
principal component-2 (PC2) scores suggested that the concentration
of hydrophilic molecules was lower and that the history of aqueous
alteration differed between the Ryugu and CM samples (Fig.
6
C).
Therefore, we suggest that comprehensive surveys of meteoritic
amino acids of the CI and CM types are important for classifying
Ryugu
6
,
11
,
13
.
Stepwise
15
N depletion and
13
C depletion during solvent
extractions
The mass balance equation
1
for the initial bulk composition of organic
matter (normalized to 100% for IB as whole rock) in the Ryugu sample
is expressed as the sum of inorganic fractions
10
, soluble and insoluble
organic fractions through the following equation:
IB =
Σ
Inorganics +
Σ
SOM +
Σ
IOM
ð
1
Þ
Σ
SOM represents the sum of the components extracted in each
process of sequential extraction, whereas
Σ
IOM represents the sum of
the insoluble organic fractions, as detailed in previous literature
6
,
34
.We
investigated the nitrogen isotopic pro
fi
les during sequential solvent
extraction by hot water extracts (#7-1), formic acid extracts (#9), and
HCl extracts (#10) for Ryugu (A0106 and C0107) and the CI group
reference (Orgueil meteorite
9
,
10
)(Fig.
7
A). Interestingly, this validation
clearly showed that organic solvent extraction resulted in
15
N-enriched
pro
fi
les (e.g., hot water extracts; < +63.1
‰
and < +55.2
‰
vs. Earth
’
s
atmospheric air for A0106 and C0107, respectively) for each extrac-
table organic fraction during the sequential process. Therefore, the
nitrogen isotopic composition of the insoluble residue indicated that it
Fig. 4 | Evidence for aqueous alteration of the asteroid Ryugu revealed by
dicarboxylic acids and molecular tautomerism of malonic acid. A
Dicarboxylic
acid pro
fi
les (i.e., C
2
, oxalic acid; C
3
, malonic acid; C
4
, succinic acid; C
5
, glutaric acid;
C
6
, aspartic acid; C
7
, pimelic acid; and C
8
, suberic acid) for the Ryugu (A0106 and
C0107) and CM types (Murchison and Murray) normalized by oxalic acid as 100%.
B
Mechanism underlying keto
–
enol tautomerism of malonic acid (MA), which
converts a chemically stable keto form to an unstable enol- form in the aqueous
alteration process. The two enol- forms of the unstable MA tautomer are symmetric
and in fact identical molecule.
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was conversely depleted of
15
N-organic matter in the stepwise extrac-
tion (Fig.
7
B). We observed that the carbon isotopic composition of
the insoluble residues also tended to be
13
C-depleted down to
−
17.0 ± 0.2
‰
, as observed for
15
Npro
fi
les (down to +28.2 ± 3.8
‰
). This
observation (Fig.
7
B) agrees well with previous reports on the carbon
and nitrogen isotopic compositions of extractable SOM and refractory
IOM in Murchison
43
. In contrast, it is interesting to note that the sulfur
isotopic composition (
δ
34
S) converged to the VCDT scale (~0
‰
)before
and after solvent extraction. Within the SOM fraction, the normalized
nitrogen balance of each extract was high in the formic acid fraction,
indicating that the pink extracts (A0106 and C0107) contained a sub-
stantial amount of hydrophilic organic matter (Supplementary
Fig. 5 | Standardization to comparatively verify the elemental and hot water-
extractable molecular properties of samples from the 1st touchdown site (TD1)
and 2nd touchdown site (TD2) at Ryugu.
Notably, the Ryugu sample is of sci-
enti
fi
c value as a surface (TD1) and subsurface sample (TD2) from the carbonaceous
asteroid
1
,
18
. In this report, we evaluated the hydrophilic organic molecules in surface
aggregate (A0106) and subsurface aggregate (C0107) samples as follows.
A
Light
elements in IB samples for total C, N, H, and S and pyrolyzable O in wt%. Compi-
lation after the references
6
,
9
,
10
. The error arc indicates the standard deviation (1
σ
).
Here, we de
fi
ne IB as whole-rock bulk, which includes all inorganic matrices such as
silicates and carbonates, and IOM as the fraction that does not contain silicates
43
.
B
CNHOS contents in IOM (sample treatment
34
and measurement by the present
report) in wt% (Table S3).
C
Hydroxy acids, carboxylic acids and other newly
identi
fi
ed N-bearing hydrophilic molecules in this study obtained from fraction #7-1
(hot water extracts) in ppb. The molecular assignments and raw data pro
fi
les are
shown in Fig.
3
and Tables S1, S2, respectively.
D
Amino acids and amines from
fraction #7-1 (hot water extraction) in ppb. The data were compiled after the
references
6
,
11
. Please see the error notation in the diagram
11
.
E
Major inorganic
cations and anions from fraction #7-1 (hot water extracts) on the ppm scale. Please
see the report for ammonium ion detection (NH
4
+
, ~ 3 ppm; red diamond symbol)
and other important molecules associated with organic and inorganic pro
fi
les
10
.
The error notations in the diagram indicate 2
σ
after the reference.
F
Concentrations
of urea and alkyl-urea (i.e., methyl-urea, ethyl-urea, and other alkyl ureas up to C
6
-
urea) were measured in the present study.
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