Articles

https://doi.org/10.1038/s41893-021-00709-3

Selective extraction of uranium from seawater

with biofouling-resistant polymeric peptide
Yihui Yuan1,3, Qiuhan Yu1,3, Meng Cao1, Lijuan Feng1, Shiwei Feng1, Tingting Liu1, Tiantian Feng1,
Bingjie Yan1, Zhanhu Guo2 and Ning Wang   1 ✉

Nuclear power could continue to be a reliable and carbon-free energy source at least from a near-term perspective. In addition
to the safety issues, another risk that may threaten the sustainability of this technology is the uranium supply disruption. As
opposed to the land-based deposits, the ocean contains 1,000 times more uranium reserves and provides a more abundant
resource for uranium. However, due to the very low concentration and presence of many other metal ions as well as the accu-
mulation of microorganisms, the development of uranium extraction technology faces enormous challenges. Here we report
a bifunctional polymeric peptide hydrogel that shows not only strong affinity to and selectivity for uranium in seawater but
also remarkable resistance against biofouling. Detailed characterizations reveal that the amino acid in this peptide material
serves as the binding ligand, and uranyl is exclusively bound to the oxygen atoms. Benefiting from its broad-spectrum anti-
microbial activity, the present polymeric adsorbent can inhibit the growth of approximately 99% of marine microorganisms.
Measurements in natural seawater show that this peptide material delivers an impressive extraction capacity of 7.12 mg g−1 and
can be reused. This work opens a new direction for the design of low-cost and sustainable materials for obtaining nuclear fuel.

N
uclear power could play a role in transitioning the energy
supply towards carbon neutrality as it does not contribute
to the generation of greenhouse gases1–3. As uranium is the
main fuel for nuclear reactors, its access matters to the sustainability
of this green technology. With nuclear power generation expected
to increase over the coming decades, access to this unconventional
reserve is a matter of energy security. At present, the primary source
of uranium is the terrestrial ore, which is estimated to contain 7.6
million tons of uranium and can empower the nuclear power indus-
try for only limited years, not even considering the growing con-
sumption rates4. In addition, the global distribution of terrestrial
uranium mineral resources is spatially imbalanced5. Eight coun-
tries with the largest uranium reserves account for more than 80%
of total resources. As a result, seeking unconventional sources of
uranium is of great importance to extend the time horizon of raw
material supply requirements. The ocean is estimated to contain
1,000 times more uranium than the land and would be an enormous
alternative resource as long as the technological development allows
for recovery of uranium at competitive costs6–8. Furthermore, more
than 75% of the world’s countries are more ocean than land, further
suggesting the feasibility of the strategy.
To utilize this inexhaustible resource, capturing uranium using
adsorbents has proved to be an effective approach9–13. Various
adsorbents have been reported with varying performance, includ-
ing organic polymers, metal organic frameworks, covalent organic
frameworks and biological substances6,14–18. However, there is no
straightforward solution because the low uranium concentration
(3.3 ppb)19, the coexisting metal ions20 and the marine biofoul-
ing21 make the separation of uranium from seawater complicated
and limit the capacity of uranium extraction. For example, the
most widely used amidoxime-group-based adsorbent suffers from
the competing uptake of vanadium present in natural seawa-
ter22–24. Biofouling is another key factor that degrades the uranium
extraction capacity by up to 30% and passivates the adsorbents,
which deteriorates the reusability and increases the economic cost
for the technology25,26. Therefore, the development of functional
uranium binding materials with both selectivity and antibiofouling
activity is crucial for enhancing the efficiency of uranium extraction
from natural seawater27.
To enhance the selectivity for uranium, various functional
groups and nano-structures have been reported15,28. For example,
biogenic protein is found to exhibit high specific uranium adsorp-
tion and has been used in the development of uranium adsorbent29.
However, these functional moieties do not inhibit biofouling. To
address the issue, an antimicrobial agent is usually introduced30–32.
Unfortunately, the addition does not boost uranium adsorption
but instead reduces the uranium adsorption capacity in simulated
seawater without biofouling31. Inspired by the bifunctionality of
bacterial strain UUS-1 in uranium immobilization and in marine
biofouling control33, we seek to explore polypeptides, which repre-
sent a large family of materials with antimicrobial activity and appli-
cations for microbial biological control34,35. We show that a biosafe
omiganan peptide36 (OP, ILRWPWWPWRRK-NH2) exhibits broad
antimicrobial activity and can bind uranium species tightly. Further
cross-linking this water-soluble peptide into polymeric peptide
hydrogel PPH-OP enables extraordinary uranium extraction capac-
ity (7.12 mg g−1) and high uranium selectivity in natural seawater.
The amino acids provide a large number of accessible active sites for
the coordination of uranium. Operation in natural seawater reveals
that the accumulation of marine microorganisms is largely sup-
pressed as a result of the intrinsic antimicrobial properties.
Results
Synthesis and characterization. By screening the database of anti-
microbial peptides, we observed that omiganan, a cationic antibiotic
peptide often used in the control of bacterial and fungal pathogens36,

State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, P. R. China. 2Integrated Composites Laboratory (ICL),
1

Department of Chemical and Biomolecular Engineering, University of Tennessee, Knoxville, TN, USA. 3These authors contributed equally: Yihui Yuan,
Qiuhan Yu. ✉e-mail: wangn02@hainanu.edu.cn

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Articles Nature Sustainability

a b

Cross-linking

c d
140 Pseudo-second-order model
Pseudo-first-order model 140
4 ppm
120
8 ppm
16 ppm
100 120

qt (mg g–1)
qt (mg g–1)

80

100
60

Data
40
Freundlich model fitting
80
Langmuir model fitting
20

10 20 30 40 50 60 70 80 8 16 24 32 40 48
Time (min) Ce (ppm)

e 105 f
1.0
Selectivity
Excess
104 0.8
Selectivity/excess in sample

Fraction of bound uranium

Kd = 3.35 nM
3
10 0.6

102 0.4

101 0.2

100
Na+ K+ Ca2+ Mg2+ Fe3+ Co2+ Cu2+ Ni2+ VO3– 10–5 10–4 10–3 10–2 10–1
Coexisting ions Total carbonate concentration (M)

Fig. 1 | Characterization and uranium adsorption capacity of PPH-OP. a, Morphology of the wet hydrogel PPH-OP after cross-linking process. b, Scanning
electron microscope image of dry hydrogel PPH-OP. The scale bar represents 1 μm. c, Kinetics for uranium adsorption and the fitting of the data.
qt, uranium adsorption capacity (q) at the contact time (t). d, Fitting of the equilibrium adsorption isotherms. Ce, the initial concentration of uranium.
e, Binding selectivity to uranium in 100-times concentrated seawater. f, Binding affinity to uranium against carbonate group. The error bars indicate the
standard deviation (n = 3).

showed the highest uranium adsorption capacity and high antibacte-
rial activity with both Gram-positive (G+) and Gram-negative (G–)
bacteria (Supplementary Table 1 and Fig. 1). Omiganan kills the
microbe by disrupting the cytoplasmic membranes of the microor-
ganism, which subsequently results in the depolarization and death
of the microorganism37,38. The three-dimensional structure of pep-
tide omiganan is similar to that of peptide CP-1139, except for the
replacement of one arginine with two lysines (Supplementary Fig. 2).
To extract uranium from the aqueous environment, the
water-soluble peptide omiganan was covalently cross-linked into
polymeric peptide hydrogel PPH-OP using glutaraldehyde as the
cross-linker (Supplementary Fig. 3). After the polymerization pro-
cess, the hydrogel shows a brown colour (Fig. 1a). The formed dry
hydrogel exhibits a rather porous structure with pores on the wall
(Fig. 1b). The analysis of the viscoelastic property shows that the pep-
tide hydrogel exhibits higher storage modulus (G′) than loss modu-
lus (G″) within the linear viscoelastic region, indicating the high
stiffness and viscoelastic properties of the hydrogel (Supplementary
Fig. 4). The hydrogel also maintains high compressive strength of
11.19 MPa and tensile strength of 1.18 MPa (Supplementary Figs. 5

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Nature Sustainability
and 6). Contributing to the high cross-linking density, the hydrogel
shows no significant swelling behaviour after being soaked in water
for 24 h (Supplementary Fig. 7). The nuclear magnetic resonance
analysis shows that a chemical bond was formed between the amino
group in the peptide and the aldehyde oxygen (Supplementary
Fig. 8). The Brunauer, Emmett and Teller specific surface area anal-
ysis of the dry hydrogel suggests that the dry hydrogel maintains a
surface area of 17.97 m2 g−1, which is higher than that of many of the
adsorbents used for uranium extraction (Supplementary Fig. 9)8,40.
The pore size analysis reveals that the dry hydrogel of PPH-OP con-
tains macro-pores of various sizes (Supplementary Fig. 10). These
properties imply that PPH-OP is suitable for use in uranium extrac-
tion from seawater.
Uranium adsorption in simulated seawater. The uranium adsorp-
tion capacity of PPH-OP is then measured in 8 ppm uranium-spiked
simulated seawater. At pH 8.0, a value close to that of natural seawa-
ter (pH 8.3), PPH-OP maintains a uranium adsorption capacity as
high as 103.85 mg g−1, which is higher than that of most biological
uranium adsorbents29,41,42 (Supplementary Fig. 11). Moreover, the
adsorption capacity can be retained for pH ranging from 3.0 to 9.0.
The optimal condition for uranium adsorption is pH 6.0, which is
attributed to the electrostatic attraction of the positive peptide to
the negative [UO2(CO3)3]4− in simulated seawater. PPH-OP shows a
short time of 70 min to reach equilibrium (Fig. 1c), faster than most
previously reported uranium adsorbents, which usually take a few
days to saturate43. After reaching the equilibrium, PPH-OP realizes
uranium adsorption capacities of 76.35, 129.16 and 139.47 mg g−1 in
simulated seawater with uranium concentrations of 4 ppm, 8 ppm
and 16 ppm, respectively, at pH 6.0. The adsorption behaviour anal-
ysis of PPH-OP can be fitted with the pseudo-second-order model,
suggesting the chemical nature of the adsorption rather than a phys-
ical interaction. On the basis of the maximum uranium adsorption
capacity together with the molecular weights of peptide omiganan
(1,779 Da) and uranium (238 Da), it is estimated that each peptide
binds one uranium atom. The equilibrium adsorption isotherms of
PPH-OP fit well with the Freundlich adsorption model but not the
Langmuir adsorption model (Fig. 1d).
Selective uranium adsorption. To assess the selectivity of PPH-OP
for uranium over other possible ions, including V, Fe, Co, Ni and
Cu, the concentrations of uranium and these five cations are
increased to 100 times the typical level in natural seawater
whereas the concentrations of Na, K, Mg and Ca are not changed
(Supplementary Table 2). In the presence of various concen-
trated ions, PPH-OP shows a high uranium adsorption capacity
of 86.95 mg g−1 within 2 h and a high enrichment index of 89.17
for uranium, while other metals rarely are adsorbed (Fig. 1e,
Supplementary Fig. 12 and Table 3). Vanadium is the closest spe-
cies to uranium in seawater in terms of ion charge and size and
shows higher affinity for the amidoxime-group-based adsorbent
than uranium10. PPH-OP shows 94.86 times higher enrichment
with uranium than with vanadium, indicating the extraordinarily
high selectivity of the adsorbent. The binding competitive assay
shows that even with a 1,000-fold excess, most metal ions, includ-
ing vanadium, cannot compete with uranium (Supplementary
Fig. 13). Another factor that affects the uranium adsorption capac-
ity is the binding affinity of the adsorbent. The uranium exists
mainly as [UO2(CO3)3]4− in natural seawater, and the adsorbent
needs to compete with the carbonate group for the uranyl ion. The
competition of the adsorbent and the carbonate group for ura-
nyl is determined, and the result shows that the adsorbent main-
tained a low dissociation constant (Kd) of 3.35 nM to uranyl in a
carbonate-existing environment, which indicated the high binding
affinity of PPH-OP to uranium (Fig. 1f). The X-ray photoelectron
spectroscopy (XPS) spectra show the characteristic peak of U4f in
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Articles
uranium-bound PPH-OP, confirming the adsorption of uranium by
the hydrogel (Supplementary Fig. 14).
Antibiofouling activity of PPH-OP. The antifouling activity of the
peptide before and after the polymerization process is measured by
testing its rates of inhibition of the G+ strain Staphylococcus aureus,
the G− strain Escherichia coli, the marine strain Vibrio vulnificus,
the marine chlorella strain Chlorella sorokiniana, the cyanobacteria
strain Synechococcus elongatus and the diatom strain Nitzschia clo-
sterium. The result shows that, before the polymerization process,
omiganan shows 91.0%, 93.3%, 98.6%, 93.4%, 98.4% and 92.6%
inhibition of the tested microbial strains S. aureus, E. coli, V. vul-
nificus, C. sorokiniana, S. elongatus and N. closterium, respectively
(Fig. 2a,b and Supplementary Fig. 15). After polymerization,
PPH-OP exhibits only a slight reduction in antimicrobial activity,
and high inhibition rates of 89.9%, 93.2%, 96.6%, 91.8%, 96.9% and
90.1% are observed against the tested microbial strains S. aureus,
E. coli, V. vulnificus, C. sorokiniana, S. elongatus and N. closterium,
respectively, suggesting the polymerization process has little influ-
ence on the antimicrobial activity. In addition, PPH-OP shows
99.1% inhibition of the growth of the marine microbial community
from natural seawater. The higher antimicrobial ability against the
marine microorganism community is attributed to the lower micro-
bial concentration in natural seawater. In consideration of the broad
antimicrobial activity, PPH-OP would highly efficiently control
marine biofouling during the practical application.
We further assessed the influence of biofouling on the ura-
nium adsorption using 8 ppm uranium-spiked natural seawater.
Comparing with filtered natural seawater where the marine micro-
organisms and the particle contaminates have been removed, the
adsorbent soaked in non-filtered natural seawater loses only 4.08%
adsorption capacity, suggesting that marine biofouling is no lon-
ger a limiting factor (Fig. 2c). Further measurements under high
microbial concentration conditions reveal that the concentration
of 103 CFU ml−1 microbial V. vulnificus strain causes only a 10.32%
decrease in uranium adsorption capacity (Supplementary Fig. 16),
which is significantly lower than that of the material without antibi-
ofouling activity, which shows 36.04% reduced uranium adsorption
capacity because of biofouling31.
Extraction of uranium from natural seawater. The uranium extrac-
tion capacity of PPH-OP has also been determined in natural seawa-
ter by using a column cyclic adsorption system31. In the non-filtered
natural seawater containing marine microorganisms, PPH-OP
extracts 21.57% of the uranium and reaches a high adsorption
capacity of 7.12 mg g−1 within 3 weeks (Fig. 2d and Supplementary
Table 4). This hydrogel is among the best-performing adsorbents
merely in terms of uranium extraction capacity. What is important,
although few adsorbents exhibit higher uranium extraction capac-
ity, their capacities were tested in biofouling-removed seawater, and
PPH-OP shows the highest capacity among known hydrogel adsor-
bents with antibiofouling activity in natural seawater. By compari-
son, the uranium adsorption capacity of PPH-OP in filtered natural
seawater increases by 6.71% to 7.63 mg g−1, indicating that the influ-
ence of marine microorganisms is nearly negligible. In natural sea-
water, PPH-OP also shows a high selectivity of uranium against the
other competing metal cations, including a 10-fold selectivity of
vanadium compared with state-of-the-art adsorbents utilizing ami-
doxime group, which show only 0.19- to 0.33-times selectivity23,44
while PPH-OP shows 2.64-times selectivity of uranium against
vanadium.
Reusability. Reusability is critical for the adsorbent in natural
seawater. The result shows that using 100 mM ethylene diamine
tetraacetic acid (EDTA, pH 8.0)29, more than 99% of the bound ura-
nium can be eluted from PPH-OP within 30 min (Supplementary
Articles Nature Sustainability

a b
Marine bacteria Chlorella Cyanobacterium Peptide PPH-OP
100

Control 80

Inhibition rate (%)

60

Peptide
40

20

PPH-OP 0

li

m
la
us

ia

m
co

cu

el
er

to
iu
re

or
ifi

er

ia
ct
E.

au

ln

D
hl
ba

ct
vu

ba
S.

e
V.

in

no
ar

ya
M

C
c d 8
110

100 7
4.08% 6.71%
90 6
7
80 5 6

qt (mg g–1)
qt (mg g–1)

qe (mg g–1)
5
70 4 4
3
60 3
2
50 2 1
0
40 1 U V Fe Cu Zn
Filtered seawater Filtered natural seawater
Non-filtered seawater
30 0 Non-filtered natural seawater

10 20 30 40 50 60 70 80 90 0 1 2 3
Time (min) Time (week)

Fig. 2 | Antibiofouling activity and uranium extraction capacity in natural seawater. a, Antimicrobial activity. b, Inhibition activity against microbial
strains. c, Influence of the marine microbial community on uranium adsorption capacity in 8 ppm uranium-spiked natural seawater. d, Uranium extraction
from natural seawater. The inset item indicates the metal selectivity of PPH-OP in natural seawater. qe, adsorbed uranium at equilibration adsorption. The
error bars indicate the standard deviation (n = 3).

Fig. 17). The continuous adsorption–desorption measurement
reveals that on average the degradation of uranium adsorption
capacity and antibacterial activity are only 2.54% and 1.58%, respec-
tively, after each reuse cycle (Supplementary Fig. 18). After being
reused for five cycles, the peptide hydrogel still maintains integrated
macrostructure and microstructure, which confirms the structural
stability of PPH-OP (Supplementary Fig. 19).
Discussion
To understand the uranium uptake mechanism in PPH-OP, com-
bined XPS, extended X-ray absorption fine-structure (EXAFS)
spectroscopy and density functional theory (DFT) calculations are
performed. The XPS analysis reveals that the uranium adsorbed by
the peptide exists in the forms of U4f 7/2 and U4f 5/2 with binding
energies of 382.2 eV and 393.1 eV, respectively, which are increased
compared with the binding energies of uranium in uranyl nitrate
(Supplementary Figs. 20 and 21). The increases of the binding ener-
gies indicate the transfer of the electrons during the coordination
process. The results of EXAFS analysis and DFT calculations show
that, except for two axial oxygens from the uranyl ion, the uranium
atom is detected to coordinate with two additional oxygen atoms,
which derive from the carbonyl group of amino acid residual Arg11
and Lys12, with bond lengths of 2.45 Å and 2.27 Å, respectively (Fig.
3 and Supplementary Table 5). These oxygen atoms form double
bonds with the carbon atoms and can provide the coordination
bonds with electrons. The DFT calculations show that the ura-
nium atom is coordinated to the oxygen atoms from the amino acid
residues with the adsorption energy being negative (−2.29 eV),
which should allow for tight uranyl binding (Fig. 3c). The analysis
of the electron density reveals that the functional oxygen atoms in
the peptide form low potential space that is attractive to the posi-
tively charged uranyl ion (Supplementary Fig. 22). The analysis of
the partial density of states of the uranium atom and the oxygen
atom in the uranium-loaded peptide shows that the U4f orbital
hybridizes with the O2p orbital to form the coordination structure.
Comparing with the coordination mechanism of the amidoxime
group, the PPH-OP shows a smaller coordination spatial structure
with shorter bond lengths15,45, which can enhance the adsorption
energy of the peptide to uranyl ion and is the reason for the higher
selectivity and binding affinity. PPH-OP also shows a different
coordination mechanism from that of protein super uranyl-binding
protein, which needs three α-helixes to form the specific structure
for uranyl binding29.
In addition to the high selectivity and affinity in enhancing ura-
nium extraction, the antibiofouling activity is the other factor that
boosts the uranium extraction (Fig. 4). Currently, several adsorbents
with antibiofouling activity have been developed (Supplementary
Table 4). However, the added antibiofouling substance is useless
for uranium adsorption. Because of the bifunctionality of the used
peptide, PPH-OP can realize high uranium extraction ability
as well as sustainable usage in natural seawater by resisting the
marine biofouling. Because of its reusability, PPH-OP can sustain
30 cycles and is calculated to realize a total extraction capacity of
150.76 mg g−1 (Supplementary Table 6). According to previous
reports, an adsorbent that has a uranium extraction capacity of
6 mg g−1 with an average loss of adsorption capacity less than by 3%

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Nature Sustainability Articles
a b

|X(R)| (Å–3)
k 2X(k)

2 4 6 8 10 12 0 1 2 3 4 5 6
k (Å–1) R (Å)

c H
2.27 Å
N
Lys12 2.45 Å
C
O
U Arg10

Arg11

Fig. 3 | EXAFS analysis and DFT calculations of the uranium binding mechanism. a, The k2-weighted χ(k) data and the fitting result. b, The R-space
analysis and the fitting result. The grey lines indicate the experimental data. The red, orange and green lines indicate the fitted k2-weighted χ(k) data, the
fitted Fourier-transformed k2-weighted data and the fitted data of the real space component, respectively. c, DFT calculations of the uranium adsorption
mechanism. The bond lengths of U–O are shown.

Uranyl binding PPH-OP hydrogel Antibiofouling for uranium extraction from seawater48,49, the price for uranium
Arg10 extraction by using PPH-OP, which is among the best currently
available uranium adsorbents (Supplementary Table 7)8,11, is esti-
H+ mated to be $204.91–293.22 kg−1 uranium. By comparison, in past
H+
decades, the global uranium spot price ranged from $60 to $300 kg−1
(ref. 50). Thus, the extraction of uranium from seawater using
H+ PPH-OP is economically feasible.
Lys12 H+ In summary, this study screens a peptide to fabricate peptide
Arg11 hydrogel adsorbent for uranium extraction from natural seawater.
Because of the bifunctionality of the screened peptide, the peptide
hydrogel adsorbent shows both high uranium binding ability and
Uranium extraction
high antibiofouling activity. The uranium coordination mecha-
nism between peptide and uranium is also uncovered, which shows
that uranium coordinates with carbonyl oxygen in the peptide
and endows the adsorbent with high binding selectivity and affin-
ity to uranium against the other coexisting metals with more than
1,000-fold excess. Because of the high uranium adsorption capacity,
high selectivity, high binding affinity and high antibiofouling activity,
PPH-OP achieves a high uranium extraction capacity of 7.12 mg g−1
Peptide omiganan Uranyl ion Live microorganism in natural seawater, which is the highest among the hydrogel ura-
Glutaraldehyde Interfering ions Dead microorganism nium adsorbents with antifouling activity, indicating that PPH-OP
is a promising adsorbent for use in sustainable uranium extraction.
Fig. 4 | Schematic diagram of the uranyl binding and antibiofouling The uranium coordination structure in PPH-OP would also open
mechanisms of PPH-OP. The cross-linking among peptides and the a new direction for designing biomolecular-mimetic materials for
viability of the microorganism are shown. low-cost and sustainable utilization of marine uranium resources.

after each reuse process would be suitable for economic uranium
extraction from seawater8,46. Chemicals used in the fabrication of
adsorbent dominate the adsorbent cost, which represents 58–83%
of the total cost for uranium extraction from seawater. The cost of
amino acid, which is the main component of peptide synthesis, is
estimated to be $11 kg−1, and the cost for amino acid is 42.9% of the
total cost for peptide synthesis47. Thus, the cost for the main chemi-
cals for uranium extraction is appropriately $170.07 kg−1 uranium.
On the basis of the theory used in estimating the techno-economics
Methods
Preparation of polymeric peptide hydrogel. First, 100 mg peptide was dissolved
in 500 µl phosphate buffer saline, then 125 µl glutaraldehyde with a mass fraction
of 25% was added to the solution to a final concentration of 5%, and afterwards it
was placed in a constant temperature water bath at 70 °C for 15 min. Finally, the
formed polymerized product was freeze-dried in a freeze vacuum oven for 10 h to
determine the dry weight.
Characterization of materials. The concentrations of uranium and interfering
metals were measured by inductively coupled plasma optical emission
spectrometer (ICP-OES) and inductively coupled plasma mass spectrometry
(ICP-MS). An X-ray photoelectron spectrometer equipped with an Al Kα radiation

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Articles
source (1,487.6 eV) and hemispherical analyser with a pass energy of 30.00 eV
and an energy step size of 0.05 eV was used to analyse the elemental composition
and elemental electron binding energy of the materials. The viscoelastic property
was determined with a Discovery HR-2 rheometer. The EXAFS analysis was
performed at the BL14W1 substation of the Shanghai synchrotron radiation
facility by detecting with the Lytle detector. Zr foli (17,998 eV) was used as the
reference material for energy calibration, and data were analysed with the
software Athena and Artemis by using the structure of uranyl citrate as the
starting physical model.
Antibacterial activity assay. The antibacterial properties were determined by
using strains of E. coli, S. aureus, marine bacterium V. vulnificus, marine chlorella
C. sorokiniana, cyanobacteria S. elongatus and diatom N. closterium as indicator
strains. The exponential growth bacterial culture and algal culture were incubated
in the fresh liquid LB medium and BG-11 medium, respectively. The hydrogel
PPH-OP was added to the medium to the final concentration of 0.2 mg ml−1. After
cultivating at 37 °C for 3 h, the concentration of the microbe was determined.
To test the antibacterial activity of the hydrogel PPH-OP against the mixture
community of marine bacteria, the unfiltered seawater was used to replace the
culture of the tested microbe. The concentrations of the alga and bacterium were
determined with cell count technique and spread plate count method, respectively.
The inhibition rate (IR) was calculated using:
Ci − Ca
IR = × 100%
Ci
where Ca (CFU ml−1) represents the microbial concentration of culture treated
by PPH-OP, and Ci (CFU ml−1) refers to the microbial concentration of untreated
culture.
To further identify the antibacterial properties of the adsorbent and the effect
of bacterial concentration on the uranium adsorption performance, uranium
adsorption tests were carried out by using filtered and non-filtered uranium-spiked
natural seawater to mimic the biofouling and sterile environments. To assay the
influence of microbial concentration on the uranium adsorption capacity, the
bacteria V. vulnificus of different concentrations were added to the uranium-spiked
simulated seawater, and the uranium adsorption capacity was accordingly
determined.
Uranium adsorption capacity assay in simulated seawater. To determine the
optimal uranium adsorption pH, the pH of the simulated seawater (438.607 mM
sodium chloride and 2.297 mM sodium bicarbonate in deionized water) with
a uranium concentration of 8 ppm was adjusted by using sodium hydroxide or
hydrochloric acid. Then, the dry weight of 5 mg adsorbent was immersed in 100 ml
uranium-spiked simulated seawater of varying pH. After shaking at 120 rpm on a
constant temperature shaker at 25 °C for 2 h, the concentration of the uranium in
the uranium-spiked seawater was determined. The uranium adsorption capacity
was calculated by using:
(C0 − Ct ) × V
qt =
m
where qt (mg g−1) refers to the uranium adsorption capacity at the contact time
t, C0 (ppm) represents the initial uranium concentration, Ct (ppm) indicates the
uranium concentration at time t, V (l) refers to the volume of solution, and m (g) is
the mass of the used adsorbent.
Reusability assay. After washing the uranium-loaded adsorbent for three times
with deionized water, the dry weight of 5 mg once-used adsorbent was placed
into 30 ml 100 mM EDTA solution with vigorous stirring for 30 min. An aliquot
of eluent was removed every 3 min and the uranium concentration was tested by
ICP-OES. The elution efficiency (EF) was calculated as follows:
Cet × Vet
EF =
qe × m
where Cet (ppm) represents the uranium concentration of the eluent, and Vet (l)
refers to the volume of the eluent, qe (mg g−1) indicates the amount of adsorbed
uranium at equilibration adsorption, and m (g) is the mass of the used adsorbent.
The adsorbent after each elution was washed twice with deionized water and then
used for the next uranium adsorption–desorption cycle.
Metal ions competition assay. To test the selectivity of adsorbent to metal ions, the
concentrations of the elements U, V, Ni, Cu, Co and Fe were increased by 100 times
compared with their concentrations in natural seawater, and the concentrations of
Mg, K, Ca and Na were maintained as their concentrations in natural seawater. The
prepared 100-times coexisting ion-spiked seawater was further tested by ICP-MS
or ICP-OES to obtain the accurate concentrations. The adsorbent with a dry
weight of 4 mg was added to 1 l 100-times ions-spiked seawater and the adsorption
capacity to the metal ions were determined after incubating for 2 h with moderate
shaking. The enrichment index (K) is calculated by using:
Nature Sustainability
MPPH-OP
K= (4)
Maq
where MPPH-OP (mg g−1) is the concentration of metals in adsorbent at equilibrium
and Maq (mg g−1) is the concentration of metals in ion-spiked seawater at
equilibrium20. Adsorption selectivity was calculated using:
UPPH-OP MPPH-OP
Selectivity = / (5)
Uaq Maq
where UPPH-OP (mg g−1) is the concentration of uranium in adsorbent at equilibrium
and Uaq (mg g−1) is the concentration of uranium in ion-spiked seawater at
equilibrium.
To accurately compare the selectivity of hydrogel PPH-OP for uranium against
the other metals, the uranyl ion with a concentration of 500 nM was mixed with
related metal ions of different concentrations. The adsorbent with a dry weight
of 2 mg was added to 100 ml of the described mixture and the concentration of
uranium after being adsorbed for 2 h was determined by ICP-MS. If uranium
was detected, the concentration of the metal ions was diluted by 10 times and the
process was repeated until uranium was not detected29.
Carbonate competition assay. The carbonate competition assay was performed
by using a freshly prepared carbonate solution. All the used deionized water was
freshly prepared and degassed before use. The further sorption of atmospheric
(1)
CO2 was also avoided. The final concentration of 10 μM peptide omiganan was
added to a carbonate solution containing 10 μM uranyl and carbonate of different
concentrations (ranging from 10−5 M to 10−1 M) and the pH of the solution
maintained at 8.9. The adsorption of uranium was determined by using ICP-OES.
Uranium extraction capacity assay in natural seawater. The natural seawater
collected from the west coast of Haikou City, Hainan Province, China, was used
for the uranium extraction capacity assay. The dry weight of 10 mg adsorbent was
soaked in 100 l natural seawater. The seawater flowed through the adsorbent at
a speed of 5 l h−1 by using the previously described equipment at 25 °C without
protection from sunlight41. The capacities to adsorb uranium and other metals
were determined by testing the concentration of uranium in the seawater and the
contents of uranium in the adsorbent after the adsorption. To analyse the influence
of marine microorganisms on uranium adsorption capacity, the natural seawater
was filtered through a 0.22 µm filter to remove the microorganisms. The uranium
extraction capacity in the non-filtered natural seawater was also determined.
Data availability
The data supporting the findings of this study are available in the paper and its
Supplementary Information.
Received: 25 November 2020; Accepted: 7 March 2021;
Published: xx xx xxxx
(2)
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Acknowledgements
This work was supported by the Hainan Science and Technology Major Project
(ZDKJ2019013 and ZDKJ2020011), the National Natural Science Foundation of China
(41966009, U1967213, 51775152 and 61761016), the Hainan Provincial Natural Science
Foundation of China (2019CXTD401) and the National Key R&D programme of China
(2018YFE0103500).
Author contributions
Y.Y., Q.Y. and N.W. conceived the research and designed the experiments. Q.Y., M.C., L.F.,
S.F., T.L., T.F. and B.Y. carried out the experiment. All authors analysed the data. Y.Y., N.W.
and Z.G. contributed to the project discussions. Y.Y., Q.Y. and N.W. wrote the paper.
Competing interests
The authors declare no competing interests.
Additional information
Supplementary information The online version contains supplementary material
available at https://doi.org/10.1038/s41893-021-00709-3.
Correspondence and requests for materials should be addressed to N.W.
Peer review information Nature Sustainability thanks Shengqian Ma, Shuao Wang and
the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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