Homogeneous catalytic hydrogenation of lipids in aqueous dispersions and bacterial cell membranes with an efficient water-soluble Pd(II)-sulfosalan catalyst, Na2[Pd(HSS)]

Article abstract of DOI:10.1016/j.catcom.2020.106153

The recently synthesized water-soluble Na₂[Pd(HSS)] (Na₂HSS = hydrogenated sulfonated salen) was shown to be a non-toxic, active catalyst for modification of model and biomembranes by homogeneous catalytic hydrogenation. Hydrogenation of the unsaturated fatty acyl residues in soy-bean lecithin liposomes and in biomembranes of intact Pseudomonas putida F1 cells was accompanied by substantial cis-trans isomerization around the C[dbnd]C double bonds. The hydrogenations could be run in aqueous media under mild conditions (25 °C, 1 bar H₂). Partial saturation (up to 10% conversion) of the membrane lipids of P. putida F1 did not damage the cells.

Full text of DOI:10.1016/j.catcom.2020.106153

CatalysisCommunications147(2020)106153
Contents lists available at ScienceDirect
Catalysis Communications
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Short communication
Homogeneous catalytic hydrogenation of lipids in aqueous dispersions and
bacterial cell membranes with an efficient water-soluble Pd(II)-sulfosalan
catalyst, Na2[Pd(HSS)]
⁎
⁎
Réka Gombosa, , Szilvia Bundaa,b, Brigitta Nagyházia, Ferenc Joóa,c,
a University of Debrecen, Department of Physical Chemistry, P.O.Box 400, Debrecen H-4002, Hungary
b University of Debrecen, Doctoral School of Chemistry, P.O.Box 400, Debrecen H-4002, Hungary
c MTA-DE Redox and Homogeneous Catalytic Reaction Mechanisms Research Group, P.O.Box 400, Debrecen H-4002, Hungary
A R T I C L E I N F O
A B S T R A C T
Keywords:
The recently synthesized water-soluble Na2[Pd(HSS)] (Na2HSS = hydrogenated sulfonated salen) was shown to
be a non-toxic, active catalyst for modification of model and biomembranes by homogeneous catalytic hydro-
genation. Hydrogenation of the unsaturated fatty acyl residues in soy-bean lecithin liposomes and in biomem-
branes of intact Pseudomonas putida F1 cells was accompanied by substantial cis-trans isomerization around the
C]C double bonds. The hydrogenations could be run in aqueous media under mild conditions (25 °C, 1 bar H2).
Partial saturation (up to 10% conversion) of the membrane lipids of P. putida F1 did not damage the cells.
Aqueous
Bacterial cells
Hydrogenation
Isomerization
Polar lipids
Pd(II)-sulfosalan catalyst
1. Introduction
complexes of sulfonated triphenylphosphines were applied [4–7] but
later Vígh and Joó introduced the use of the Pd(II)-complex of Alizarin
Polar lipids are essential components of biological membranes since
they form the basic structure of cell boundaries, the polar lipid bilayer
[1,2]. Many of such polar lipids contain unsaturated or multiply un-
saturated fatty acyl chains esterified in glycerol. Among other factors,
the space requirement of a lipid molecule is largely determined by the
number and configuration of its unsaturated aliphatic chains. A lipid
bilayer containing a large proportion of polar lipids with cis-un-
saturated acyl chains, will provide a more fluid (less rigid) environment
for the myriads of molecules built into or associated with the mem-
brane. In such a way, the general degree of unsaturation of the mem-
brane-building lipids has direct relevance to the properties and phy-
siological functions of the cells.
Red S, [Pd(QS)2] [8]. Isolated biomembranes [9], protoplasts [6] and
whole live cells [10–12] were subjected to such modification and the
results allowed important conclusions on temperature stress tolerance
of the cells [10,11,13].
[Pd(QS)2] proved highly active for hydrogenation of biomembranes,
showed no toxicity and had no self-effect on the membrane properties.
However, drawbacks of its use include the need of activation under H2,
and the very high oxygen sensitivity of its hydrogenated intermediates,
which make obtaining consistent hydrogenation results much depen-
dent on the experimenter's experience and skill.
In the course of our long-time research into aqueous organometallic
catalysis [14], we have recently launched a study of the catalytic
properties of transition metal salan complexes [15]. Salans are tetra-
hydrogenated derivatives of salen (1,2-bis(salicylaldiminato)ethane)
and its analogues. Among other means, salans can be made water-so-
luble by sulfonation, and in contrast to sulfonated salens [16–18], they
show resistance to hydrolysis in aqueous solutions even at high tem-
peratures and in the presence of metal ions. The Pd(II)-complex of the
simplest salan (HSS = hydrogenated and sulfonated salen), as a
The idea of changing the degree of C]C unsaturation of a biological
membrane by catalytic hydrogenation can be traced back to the pio-
neering work of Chapman and Quinn [3]. During the early studies in
which heterogeneous catalysts (such as PtO2) [3], or water-insoluble
metal complexes (e.g. [RhCl(PPh3)3]) were applied, it was realized that
biocompatible and water-soluble homogeneous hydrogenation catalysts
were needed for optimal results [4]. At first, Rh(I)- and Ru(II)-
Abbreviations: salen, N,N′-bis(salicylaldiminato)-1,2-diaminoethane; sulfosalan, Na2HSS = hydrogenated and sulfonated salen = N,N′-bis(2-hydroxy-5-sulfonato-
benzyl)-1,2-diaminoethane, diNa-salt; QS, 1,2-dihydroxy-9,10-anthraqinone-3-sulfonate, Na-salt; OD, optical density; CMC, critical micelle-forming concentration;
16:0, palmitic acid; 16:1, palmitoleic acid; 18:0, stearic acid; cis-18:1, oleic acid; trans-18:1, elaidic acid; 18:2, linoleic acid; 18:3, linolenic acid
⁎ Corresponding authors at: University of Debrecen, Department of Physical Chemistry, P.O.Box 400, Debrecen H-4002, Hungary.
E-mail addresses: gombos.reka@science.unideb.hu (R. Gombos), bunda.szilvia@science.unideb.hu (S. Bunda), nagyhazi.brigitta@gmail.com (B. Nagyházi),
joo.ferenc@science.unideb.hu (F. Joó).
https://doi.org/10.1016/j.catcom.2020.106153
Received 6 August 2020; Received in revised form 27 August 2020; Accepted 28 August 2020
Availableonline10September2020
1566-7367/©2020ElsevierB.V.Allrightsreserved.

R. Gombos, et al.
CatalysisCommunications147(2020)106153
3. Results and discussion
The main purpose of the research was to explore the scope of the use
of Na2[Pd(HSS)] as catalysts for hydrogenation of biomembranes. This
study included first the hydrogenation of soy-bean lecithin liposomes
(model-membranes) followed by hydrogenation of Pseudomonas putida
F1 bacteria as intact cells. For comparison, aqueous micellar solutions
of oleic and linoleic acids were also hydrogenated.
Fig. 1. Na2[Pd(HSS)].
disodium salt, Na2[Pd(HSS)], is shown on Fig. 1.
3.1. Hydrogenation of soy-bean lecithin liposomes and oleic and linoleic
acids with the water-soluble Na2[Pd(HSS)] catalyst
Complexes with salan-type ligands have been already studied in
aqueous systems as catalysts [18–20] or as bioactive agents [21,22]. We
have successfully applied Pd(II)-complexes of HSS and analogous li-
gands (such as BuHSS with a 1,4-butylene bridge between the N-atoms)
for Sonogashira [23] and Suzuki [24] CeC coupling reactions in aqu-
eous systems. The selectivity of the Na2[Pd(HSS)] catalyst in hydro-
genation of C]C vs C]O bonds was studied in detail in the biphasic
hydrogenation of cinnamaldehyde, and –in addition to the outstanding
catalytic activity– a high preference for hydrogenation of the olefinic
bond over the carbonyl was established [25]. Similarly, Na2[Pd(HSS)]
actively catalyzed the simultaneous redox isomerization and C]C re-
duction of allylic alcohols [15], but was inactive in the hydrogenation
of ketones.
The main fatty acyl components of soy-bean lecithin are the satu-
rated palmitic (16:0) and stearic (18:0) acids, and the unsaturated oleic
(cis-18:1), linoleic (18:2) and linolenic (18:3) acids. In aqueous lipo-
somes this lecithin forms vesicles with lipid bilayer boundaries. For
comparison, free oleic and linoleic acids were also hydrogenated in
aqueous solutions containing amounts of these substrates
(7.8 × 10−6 mol) commensurable to those present in the liposomes
(1 mg lipid/mL). The concentrations of the free acids in such samples
were higher than their respective critical micelle-forming concentra-
tions (CMC) [28,29] which ensured that oleic and linoleic acid were
present in form of micelles.
The above observations encouraged us to apply Na2[Pd(HSS)] for
the catalytic hydrogenation of phospholipids (in aqueous dispersions,
i.e. liposomes). Hydrogenation of the unsaturated fatty acyl con-
stituents of lipids in the membranes of the bacterium Pseudomonas pu-
tida F1 was also attempted. The results of this investigation are de-
scribed below.
The time course of the hydrogenation of soy-bean lecithin, oleic acid
and linoleic acid is depicted on Fig. 2. It can be seen that all three
substrates were hydrogenated effectively under very mild conditions:
T = 37 °C, P(H2) = 3 bar, c(cat) = 2.5 × 10−4 M.. However, due to
the different concentration of reducible olefinic units in the three ex-
periments, and to the different physical state of the substrates in the
reaction mixtures (lipid vesicles vs fatty acid micelles) the measured
conversions do not directly reflect the individual reactivity of the sub-
strates (see also Table 1 and subsequent discussion).
2. Experimental
The reaction proceeds fast even at atmospheric hydrogen pressure
(Fig. 3). As expected, the conversion of linoleic and oleic acids in-
creased steadily with increasing P(H2). Conversely, the rate of hydro-
genation of soy-bean lecithin was only slightly effected by the H2
pressures above 1 bar. A similar phenomenon was already observed
with the [Pd(QS)2] catalysts [30], and was shown to be the con-
sequence of the increased rigidity of the lipid bilayer upon extensive
hydrogenation which prevented further interaction of the catalyst with
the unreacted substrates buried into the inner region of the bilayer.
We assume that increasing rigidity of the lipid bilayer is responsible
for the small H2 pressure effect on liposome hydrogenation determined
in the present study, too. This suggestion is corroborated by hydro-
genation of soy-bean lecithin – cholesterol mixtures. When sonicated
together, cholesterol is built into the lipid bilayer and increases its
stiffness. The data in Table 1 show, that large amounts of cholesterol
Na2[Pd(HSS)] was synthesized as described in the literature [15].
Soy-bean lecithin was a product of BiYo Product Kft (Komárom, Hun-
gary). Oleic and linoleic acids were supplied by Sigma-Aldrich. All
other chemicals were commercial products of highest available purity
obtained from Sigma-Aldrich and Merck. Organic solvents were pur-
chased from Molar Chemicals. Ion-exchanged water (S ≤ 1 μS) was
used. Gases were supplied by Linde Gas Hungary.
Liposomes were prepared by sonication of soy-bean lecithin in
water (typically 1.0 mg/mL) with the use of a Branson Sonifier 250
ultrasound desintegrator. The Pseudomonas putida F1 bacteria strain
was kindly provided by Prof. David Gibson, University of Iowa, Iowa
City, USA) to the Department of Biochemical Engineering, University of
Debrecen and was maintained and grown in BSM culture medium [26].
The toxicity of Na2[Pd(HSS)] was assessed by comparison of the growth
curves of the bacteria both in the absence and in the presence of the
catalyst (8.3 × 10−6 mol/100 mL). Cell concentrations were de-
termined from optical density (OD) of the cell cultures, based upon
calibration against cell numbers counted with the use of a Bürker
chamber.
Hydrogenations of liposomes and Pseudomonas putida F1 cells were
carried out in water with magnetic stirring with Na2[Pd(HSS)] as cat-
alyst both at atmospheric H2 pressure in Schlenk tubes or at elevated
pressures (up to 7 bar H2) with the use of glass pressure tubes. For
hydrogenation (and for control samples), the bacteria were washed off
the surface of the culture gel in the Petri dishes with water.
Lipid samples were analysed by gas chromatography after trans-
methylation in HCl/MeOH at 80 °C for 2 h under Ar [27] with the use of
a Hewlett Packard 5890 Series II equipment and a HP-ULTRA-2
(25 m × 0.2 mm × 0.33 μm) or a HP-88 (30 m × 0.25 mm × 0.20 μm)
column. Other details, including the temperature programs, and the
calculation of the changes in the unsaturation of hydrogenated lipid
mixtures (conversion) from the chromatographic peak areas can be
found in Appendix A.
Fig. 2. Time course of the hydrogenation of soy-bean lecithin ( ), linoleic acid (
) and oleic acid ( ) with Na2[Pd(HSS)] catalyst in water. Conditions: cliposome
=
1.0 mg/mL, noleic
=
nlinoleic
=
2.33
×
10−5 mol, ncatalyst
acid
= 7.5 × 10−7 mol, V = 3 mL, T = 37 a°cCid, P(H2) = 3 bar.
2

R. Gombos, et al.
CatalysisCommunications147(2020)106153
Table 1
is an advantageous feature of the Na2[Pd(HSS)] catalyst, allowing hy-
drogenation of temperature-sensitive cells or isolated organelles. Note,
that such an extent of hydrogenation is already sufficient to trigger
physiological changes in the cells, and extensive saturation of their lipid
membranes may even be fatal [31].
Fatty acid composition (%) of non‑hydrogenated (control) soy-bean lecithin and
that of lecithin samples hydrogenated with Na2[Pd(HSS)] catalyst in the pre-
sence of various amounts of cholesterol.
Control⁎ Hydrogenated together with added Cholesterol
(m/m %)
3.2. Catalytic hydrogenation of membrane lipids in Pseudomonas putida F1
bacteria
0
15
60
Stearic a. (18:0)
Elaidic a. (trans-18:1)
Oleic a. (cis-18:1)
Linoleic a. (18:2)
Linolenic a. (18:3)
Conversion (%)
8
13
0
12
2
13
2
0
Pseudomonas putida F1 is
a rod-like Gram-negative γ-proteo-
19
66
7
40
47
0
38
43
5
24
54
7
bacterium found in soils and natural waters. It tolerates heavy metals
and is capable for degradation of various aromatic hydrocarbons which
makes the bacteria useful for decontamination of soils and polluted
waters [26,32]. Furthermore, its durability and relatively simple
membrane fatty acid composition makes it an attractive bacterial
system for studying the effect of hydrogenation on the cells with the
new Na2[Pd(HSS)] catalyst.
–
22
18
10
Conditions: cliposome = 1.0 mg/mL, ncatalyst = 7.5 × 10−7 mol, V = 3 mL,
T = 37 °C, P(H2) = 3 bar, t = 2 h.
⁎
Control samples were prepared directly from commercial lecithin with no
addition of cholesterol and no hydrogenation.
The lipid and fatty acid compositions of the Pseudomonas putida F1
subspecies are not available in the literature, however, they were es-
tablished for several Pseudomonas putida species; the main components
were 16:0 (20%), 16:1 (18%) and 18:1 (25%) and the fatty acid com-
position did not significantly depend on the various additives in the
culture medium [33–35].
The toxicity of Na2[Pd(HSS)] on Pseudomonas putida F1 was de-
termined by growing the cells in BSM culture medium both in the ab-
sence and in the presence of the Pd(II)-salan catalyst. The growth
curves were very similar and the growth rate in the exponential phase
was almost identical for both cultures (Fig. S7). It could be concluded
therefore, that in the applied concentration (8.3 × 10−5 M), Na2[Pd
(HSS)] did not show any toxicity for the studied Pseudomonas putida F1
subspecies.
Table 2 shows the fatty acid composition of the bacteria before and
after hydrogenation. The reactions were run at T = 37 °C and P
(H2) = 3 bar for 4 h, therefore the control sample of the cells was also
kept under the same conditions but in the absence of H2. The data for
the control (c) and hydrogenated (h) cells show that the relative amount
of all C16 and all C18 acids did not change significantly during hy-
drogenation (C16: 65% c vs 64% h; C18: 31% c vs 34% h) what also
confirms the reliability of lipid analysis. Conversely, within the C16 and
C18 subgroups, substantial hydrogenation and isomerization could be
detected. Cis-trans isomerization was very conspicuous in the case of
palmitoleic acid (cis-16:1), but could be observed among the 18:1 fatty
acid species, too. Altogether a 10% overall hydrogenation conversion
was achieved. Gas chromatograms of the fatty acid methyl esters ob-
tained by transmethylation of the lipids in hydrogenated and control P.
putida F1 cells are shown on Fig. 4.
Fig. 3. Conversions of soy-bean lecithin ( ), linoleic acid ( ) and oleic acid ( ) in
hydrogenation with Na2[Pd(HSS)] catalyst in water as functions of the hy-
drogen pressure. Conditions: cliposome = 1.0 mg/mL, noleic
= nlinoleic
acid
acid
= 2.33×10−5 mol, ncatalyst = 7.5 × 10−7 mol, V = 3 mL, T = 37 °C, t = 2 h.
substantially decreased the rate of lecithin hydrogenation: the conver-
sion fell from 22% to 10% in presence of 60 m/m % cholesterol.
Table 1 shows also the relative reactivities of the unsaturated fatty
acid residues in soy-bean lecithin. Of those, 18:3 proved the most re-
active, and was completely eliminated during hydrogenation for 2 h.
The doubly unsaturated linoleic acid (18:2) reacted faster than oleic
acid (cis-18:1) which was practically not hydrogenated to stearic acid.
However, in the presence of cholesterol, small amounts of elaidic acid
(trans-18:1) were also formed.
Following hydrogenation, the samples were checked by visual mi-
croscopy. The bacteria were alive and moving, no change of their shape
The relative hydrogenation rates of oleic and linoleic acids were
studied also in micellar solutions of the free acids. Fig. 2 shows that
18:2 reacted substantially faster than cis-18:1 (similar to the reactivity
of the lipid-bound acids). However, under such conditions, extensive
cis-trans isomerization was also observed (Figs. S2, S4), leading to the
formation of several positional and geometric isomers of both oleic and
linoleic acids. With an increased catalyst concentration
(12.3 × 10−4 M) and at T = 30 °C, P(H2) = 3 bar, hydrogenation of
oleic acid (cis-18:1) afforded 30% isomerized products in 1 h (in ad-
dition to 28% stearic acid), while in 2 h, the conversion to isomerized
18:1 species (mostly elaidic acid, trans-18:1) increased to 45% (ac-
companied by 35% stearic acid). Such a high catalytic activity for cis-
trans isomerization was not observed earlier with the Rh(I)- and Ru(II)-
tertiary phosphine, and the [Pd(QS)2] catalysts. Note, that cis-to-trans
isomerization of the unsaturated fatty acyl chains in the lipid species
also contributes to the increase of rigidity of a membrane by decreasing
the space requirement of the lipids in the bilayer [13].
Table 2
Fatty acid composition (%) of total lipids of control (non‑hydrogenated) and
hydrogenated Pseudomonas putida F1 bacteria.
Fatty acid
Control cells (Non‑hydrogenated)
Hydrogenated cells
16:0
31
9
36
14
14
3
trans-16:1
cis-16:1
17:0
25
5
18:0
5
10
2
18:1⁎
18:1⁎
18:1⁎
2
2
5
22
17
Conditions: ncatalyst = 7.5 × 10−7 mol, V = 3.04 mL, T = 37 °C, P(H2) = 3 bar,
t = 4 h.
Catalyst: Na2[Pd(HSS)], solvent: water, concentration of cells: 9.5 × 106 cells/
mL.
Hydrogenation of soy-bean lecithin could be carried out even at
25 °C (16% conversion in 1 h, 3 bar H2, c(cat) = 12.3 × 10−4 M). This
⁎
mixture of positional and geometric isomers.
3

R. Gombos, et al.
CatalysisCommunications147(2020)106153
Fig. 4. Gas chromatograms of the fatty acid methyl esters obtained from control and hydrogenated Pseudomonas putida F1 cells.
was seen, neither the presence of cell debris was detected (Fig. S8). It
could be concluded that the studied P. putida F1 cells survived the
hydrogenation process, both the partial saturation of their membranes
by catalytic hydrogenation, and also the accompanying physical im-
pacts and stress.
Professors Levente Karaffa and Erzsébet Fekete (Department of
Biochemical Engineering, University of Debrecen) for their generous
help in the investigations and the useful discussions.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.catcom.2020.106153.
4. Conclusions
The Pd(II)-salan-type catalyst, Na2[Pd(HSS)] was shown highly ac-
tive for hydrogenation of the C]C bonds in the fatty acyl chains of the
polar lipid species found in soy-bean lecithin vesicles and in the bio-
membranes of Pseudomonas putida F1 cells. Hydrogenations were ac-
companied by cis-trans isomerization of the unsaturated acyl residues,
especially in case of the monounsaturated substrates such as oleic and
palmitoleic acids. The reactions could be carried out in aqueous media
under mild conditions (25–37 °C, 1–7 bar H2). A 10% loss in un-
saturation of the lipids did not damage the P. putida F1 cells. No toxicity
of the catalyst was detected. On the basis of the above findings, Na2[Pd
(HSS)] can be considered and recommended as an effective new water-
soluble catalyst for biomembrane hydrogenations.
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