The co-involvement of biological molecules and nanomaterials has increasingly come to the fore in modern-day applications. While the “bio–nano” (BN) interface presents physico-chemical characteristics that are manifestly different from those observed in isotropic bulk conditions, the underlying molecular reasons remain little understood; this is especially true of anomalies in interfacial hydration. In this paper, we leverage atomistic simulations to study differential adsorption characteristics of a small protein on the inner (concave) surface of a single-walled carbon nanotube whose diameter exceeds dimensions conducive to single-file water movement. Our findings indicate that the extent of adsorption is decided by the degree of foldedness of the protein conformational substate. Importantly, we find that partially folded substates, but not the natively folded one, induce reorganization of the protein hydration layer into an inner layer water closer to the nanotube axis and an outer layer water in the interstitial space near the nanotube walls. Further analyses reveal sharp dynamical differences between water molecules in the two layers as observed in the onset of increased heterogeneity in rotational relaxation and the enhanced deviation from Fickian behavior. The vibrational density of states reveals that the dynamical distinctions are correlated with differences in crucial bands in the power spectra. The current results set the stage for further systematic studies of various BN interfaces vis-à-vis control of hydration properties.

1.
A. W.
Harris
and
J. N.
Cha
,
Mol. Syst. Des. Eng.
5
,
1088
(
2020
).
2.
A.
Precupas
,
D.
Gheorghe
,
A.
Botea-Petcu
,
A. R.
Leonties
,
R.
Sandu
,
V. T.
Popa
,
E.
Mariussen
,
E. Y.
Naouale
,
E.
Rundén-Pran
,
V.
Dumit
,
Y.
Xue
,
M. R.
Cimpan
,
M.
Dusinska
,
A.
Haase
, and
S.
Tanasescu
,
Chem. Res. Toxicol.
33
,
2054
(
2020
).
3.
B.
Liu
and
J.
Liu
,
J. Am. Chem. Soc.
139
,
9471
(
2017
).
4.
L.
Fu
,
M.
Morsch
,
B.
Shi
,
G.
Wang
,
A.
Lee
,
R.
Radford
,
Y.
Lu
,
D.
Jin
, and
R.
Chung
,
Nanoscale
9
,
13683
(
2017
).
5.
A. S.
Campbell
,
C.
Dong
,
F.
Meng
,
J.
Hardinger
,
G.
Perhinschi
,
N.
Wu
, and
C. Z.
Dinu
,
ACS Appl. Mater. Interfaces
6
,
5393
(
2014
).
6.
J.
Tian
and
A. E.
Garca
,
J. Chem. Phys.
134
,
225101
(
2011
).
7.
M.
Penna
and
I.
Yarovsky
,
Nanoscale
12
,
7240
(
2020
).
8.
D.
Lucent
,
V.
Vishal
, and
V. S.
Pande
,
Proc. Natl. Acad. Sci. U. S. A.
104
,
10430
(
2007
).
9.
E. J.
Sorin
and
V. S.
Pande
,
J. Am. Chem. Soc.
128
,
6316
(
2006
).
10.
Y.
Kang
,
Q.
Wang
,
Y.-C.
Liu
,
J.-W.
Shen
, and
T.
Wu
,
J. Phys. Chem. B
114
,
2869
(
2010
).
11.
J.
Tian
and
A. E.
Garcia
,
J. Am. Chem. Soc.
133
,
15157
(
2011
).
12.
M. V.
Athawale
,
S. N.
Jamadagni
, and
S.
Garde
,
J. Chem. Phys.
131
,
115102
(
2009
).
13.
H. K.
Baca
,
E.
Carnes
,
S.
Singh
,
C.
Ashley
,
D.
Lopez
, and
C. J.
Brinker
,
Acc. Chem. Res.
40
,
836
(
2007
).
14.
J.
Schneider
and
L.
Colombi Ciacchi
,
J. Am. Chem. Soc.
134
,
2407
(
2012
).
15.
Y.
Wang
,
Z.
Qin
,
M. J.
Buehler
, and
Z.
Xu
,
Nat. Commun.
7
,
12854
(
2016
).
16.
Y.
Kang
,
Q.
Wang
,
Y.-C.
Liu
,
T.
Wu
,
Q.
Chen
, and
W.-J.
Guan
,
J. Phys. Chem. B
112
,
4801
(
2008
).
17.
Q.
Chen
,
Q.
Wang
,
Y. C.
Liu
,
T.
Wu
,
Y.
Kang
,
J. D.
Moore
, and
K. E.
Gubbins
,
J. Chem. Phys.
131
,
015101
(
2009
).
18.
Y.
Kang
,
Y.-C.
Liu
,
Q.
Wang
,
J.-W.
Shen
,
T.
Wu
, and
W.-J.
Guan
,
Biomaterials
30
,
2807
(
2009
).
19.
H.
Kumar
,
B.
Mukherjee
,
S. T.
Lin
,
C.
Dasgupta
,
A. K.
Sood
, and
P. K.
Maiti
,
J. Chem. Phys.
134
,
124105
(
2011
).
20.
S.
Dalla Bernardina
,
E.
Paineau
,
J.-B.
Brubach
,
P.
Judeinstein
,
S.
Rouzière
,
P.
Launois
, and
P.
Roy
,
J. Am. Chem. Soc.
138
,
10437
(
2016
).
21.
T. A.
Pascal
,
W. A.
Goddard
, and
Y.
Jung
,
Proc. Natl. Acad. Sci. U. S. A.
108
,
11794
(
2011
).
22.
K. V.
Agrawal
,
S.
Shimizu
,
L. W.
Drahushuk
,
D.
Kilcoyne
, and
M. S.
Strano
,
Nat. Nanotechnol.
12
,
267
(
2017
).
23.
S. B.
Ahmed
,
Y.
Zhao
,
C.
Fang
, and
J.
Su
,
Phys. Lett. A
381
,
3487
(
2017
).
24.
K.
Ritos
,
D.
Mattia
,
F.
Calabrò
, and
J. M.
Reese
,
J. Chem. Phys.
140
,
014702
(
2014
).
25.
P.
Roy
,
B.
Ghosh
,
P.
Chatterjee
, and
N.
Sengupta
,
J. Chem. Inf. Model.
59
,
2026
(
2019
).
26.
S.
Park
,
D. E.
Moilanen
, and
M. D.
Fayer
,
J. Phys. Chem. B
112
,
5279
(
2008
).
27.
N. V.
Nucci
,
M. S.
Pometun
, and
A. J.
Wand
,
Nat. Struct. Mol. Biol.
18
,
245
(
2011
).
28.
T.
Wohlfromm
and
M.
Vogel
,
J. Chem. Phys.
150
,
245101
(
2019
).
29.
N.
Sengupta
,
S.
Jaud
, and
D. J.
Tobias
,
Biophys. J.
95
,
5257
(
2008
).
30.
T. Q.
Luong
,
P. K.
Verma
,
R. K.
Mitra
, and
M.
Havenith
,
Biophys. J.
101
,
925
(
2011
).
31.
M.
Gupta
,
P.
Khatua
,
C.
Chakravarty
, and
S.
Bandyopadhyay
,
J. Phys. Chem. B
122
,
1560
(
2018
).
32.
T.
Wang
,
Y.
Zhu
, and
F.
Gai
,
J. Phys. Chem. B
108
,
3694
(
2004
).
33.
M. U.
Johansson
,
M.
de Château
,
M.
Wikström
,
S.
Forsén
,
T.
Drakenberg
, and
L.
Björck
,
J. Mol. Biol.
266
,
859
(
1997
).
34.
W.
Jin
,
O.
Kambara
,
H.
Sasakawa
,
A.
Tamura
, and
S.
Takada
,
Structure
11
,
581
(
2003
).
35.
W. L.
Jorgensen
,
J.
Chandrasekhar
,
J. D.
Madura
,
R. W.
Impey
, and
M. L.
Klein
,
J. Chem. Phys.
79
,
926
(
1983
).
36.
W.
Humphrey
,
A.
Dalke
, and
K.
Schulten
,
J. Mol. Graphics
14
,
33
(
1996
).
37.
J. C.
Phillips
,
R.
Braun
,
W.
Wang
,
J.
Gumbart
,
E.
Tajkhorshid
,
E.
Villa
,
C.
Chipot
,
R. D.
Skeel
,
L.
Kalé
, and
K.
Schulten
,
J. Comput. Chem.
26
,
1781
(
2005
).
38.
A. D.
MacKerell
,
D.
Bashford
,
M.
Bellott
,
R. L.
Dunbrack
,
J. D.
Evanseck
,
M. J.
Field
,
S.
Fischer
,
J.
Gao
,
H.
Guo
,
S.
Ha
,
D.
Joseph-McCarthy
,
L.
Kuchnir
,
K.
Kuczera
,
F. T. K.
Lau
,
C.
Mattos
,
S.
Michnick
,
T.
Ngo
,
D. T.
Nguyen
,
B.
Prodhom
,
W. E.
Reiher
,
B.
Roux
,
M.
Schlenkrich
,
J. C.
Smith
,
R.
Stote
,
J.
Straub
,
M.
Watanabe
,
J.
Wiórkiewicz-Kuczera
,
D.
Yin
, and
M.
Karplus
,
J. Phys. Chem. B
102
,
3586
(
1998
).
39.
A. D.
Mackerell
,
M.
Feig
, and
C. L.
Brooks
,
J. Comput. Chem.
25
,
1400
(
2004
).
40.
U.
Essmann
,
L.
Perera
,
M. L.
Berkowitz
,
T.
Darden
,
H.
Lee
, and
L. G.
Pedersen
,
J. Chem. Phys.
103
,
8577
(
1995
).
41.
S. E.
Feller
,
Y.
Zhang
,
R. W.
Pastor
, and
B. R.
Brooks
,
J. Chem. Phys.
103
,
4613
(
1995
).
42.
J.-P.
Ryckaert
,
G.
Ciccotti
, and
H. J. C.
Berendsen
,
J. Comput. Phys.
23
,
327
(
1977
).
43.
L.
Kalé
,
R.
Skeel
,
M.
Bhandarkar
,
R.
Brunner
,
A.
Gursoy
,
N.
Krawetz
,
J.
Phillips
,
A.
Shinosaki
,
K.
Varadarajan
, and
K.
Schulten
,
J. Comp. Phys.
151
,
283
(
1999
).
44.
L.
Zådek
,
M. V.
Novotny
, and
M. J.
Stone
,
Nat. Struct. Biol.
6
,
1118
(
1999
).
45.
G.
Lipari
and
A.
Szabo
,
J. Am. Chem. Soc.
104
,
4559
(
1982
).
46.
P.
Roy
,
S.
Roy
, and
N.
Sengupta
,
Biophys. J.
119
,
1525
(
2020
).
47.
K.-B.
Wong
and
V.
Daggett
,
Biochemistry
37
,
11182
(
1998
).
48.
M. J.
Stone
,
Acc. Chem. Res.
34
,
379
(
2001
).
49.
V.
Kasinath
,
K. A.
Sharp
, and
A. J.
Wand
,
J. Am. Chem. Soc.
135
,
15092
(
2013
).
50.
P.
Chatterjee
,
S.
Bagchi
, and
N.
Sengupta
,
J. Chem. Phys.
141
,
205103
(
2014
).
51.
M. C.
Morón
,
D.
Prada-Gracia
, and
F.
Falo
,
Phys. Chem. Chem. Phys.
18
,
9377
(
2016
).
52.
A.
Oleinikova
,
N.
Smolin
, and
I.
Brovchenko
,
Biophys. J.
93
,
2986
(
2007
).
53.
S.-T.
Lin
,
M.
Blanco
, and
W. A.
Goddard
,
J. Chem. Phys.
119
,
11792
(
2003
).
54.
M.-C.
Bellissent-Funel
,
A.
Hassanali
,
M.
Havenith
,
R.
Henchman
,
P.
Pohl
,
F.
Sterpone
,
D.
Van Der Spoel
,
Y.
Xu
, and
A. E.
Garcia
,
Chem. Rev.
116
,
7673
(
2016
).
55.
J.
Guo
,
X.
Yao
,
L.
Ning
,
Q.
Wang
, and
H.
Liu
,
RSC Adv.
4
,
9953
(
2014
).
56.
A. K.
Jana
,
M. K.
Tiwari
,
K.
Vanka
, and
N.
Sengupta
,
Phys. Chem. Chem. Phys.
18
,
5910
(
2016
).
57.
M.
Heyden
,
J. Chem. Phys.
150
,
094701
(
2019
).
58.
B.
Bagchi
,
Chem. Rev.
105
,
3197
(
2005
).
59.
F.
Pizzitutti
,
M.
Marchi
,
F.
Sterpone
, and
P. J.
Rossky
,
J. Phys. Chem. B
111
,
7584
(
2007
).
60.
P. E.
Theodorakis
,
H. P.
Hsu
,
W.
Paul
, and
K.
Binder
,
J. Chem. Phys.
135
,
164903
(
2011
).
61.
A.
Fiege
,
T.
Aspelmeier
, and
A.
Zippelius
,
Phys. Rev. Lett.
102
,
098001
(
2009
).
62.
Y. L.
Sun
,
M. H.
Sun
,
J. Y.
Li
,
A. P.
Wang
,
C. X.
Ma
,
W. D.
Cheng
, and
F.
Liu
,
Chin. Phys. Lett.
23
,
2830
(
2006
).
63.
S. K.
Sinha
and
S.
Bandyopadhyay
,
J. Chem. Phys.
135
,
135101
(
2011
).
64.
P.
Mark
and
L.
Nilsson
,
J. Phys. Chem. A
105
,
9954
(
2001
).
65.
M.
Marchi
,
F.
Sterpone
, and
M.
Ceccarelli
,
J. Am. Chem. Soc.
124
,
6787
(
2002
).
66.
S.
Arya
,
A. K.
Singh
,
K.
Bhasne
,
P.
Dogra
,
A.
Datta
,
P.
Das
, and
S.
Mukhopadhyay
,
Biophys. J.
114
,
2540
(
2018
).
67.
G. E.
Walrafen
and
Y. C.
Chu
,
J. Phys. Chem.
99
,
11225
(
1995
).
68.
G. E.
Walrafen
,
Y. C.
Chu
, and
G. J.
Piermarini
,
J. Phys. Chem.
100
,
10363
(
1996
).
69.
J. B.
Brubach
,
A.
Mermet
,
A.
Filabozzi
,
A.
Gerschel
, and
P.
Roy
,
J. Chem. Phys.
122
,
184509
(
2005
).
70.
J.
Li
,
J. Chem. Phys.
105
,
6733
(
1996
).
71.
S.
Chakraborty
,
H.
Kumar
,
C.
Dasgupta
, and
P. K.
Maiti
,
Acc. Chem. Res.
50
,
2139
(
2017
).
72.
H.
Wirtz
,
S.
Schäfer
,
C.
Hoberg
,
K. M.
Reid
,
D. M.
Leitner
, and
M.
Havenith
,
Biochemistry
57
,
3650
(
2018
).
73.
K.
Meister
,
S.
Ebbinghaus
,
Y.
Xu
,
J. G.
Duman
,
A.
Devries
,
M.
Gruebele
,
D. M.
Leitner
, and
M.
Havenith
,
Proc. Natl. Acad. Sci. U. S. A.
110
,
1617
(
2013
).
74.
C.
Rocchi
,
A. R.
Bizzarri
, and
S.
Cannistraro
,
Phys. Rev. E
57
,
3315
(
1998
).
75.
O.
Byl
,
J.-C.
Liu
,
Y.
Wang
,
W.-L.
Yim
,
J. K.
Johnson
, and
J. T.
Yates
,
J. Am. Chem. Soc.
128
,
12090
(
2006
).
76.
J. S.
Rao
,
M. D.
Smith
, and
L.
Cruz
,
J. Phys. Chem. B
118
,
3517
(
2014
).

Supplementary Material

You do not currently have access to this content.