World J Microbiol Biotechnol (2016) 32:178
DOI 10.1007/s11274-016-2136-y
REVIEW
Microbial production of metabolites and associated enzymatic
reactions under high pressure
Yongsheng Dong1 • Hua Jiang2
Received: 17 June 2016 / Accepted: 8 September 2016 / Published online: 15 September 2016
Ó Springer Science+Business Media Dordrecht 2016
Abstract High environmental pressure exerts an external
stress on the survival of microorganisms that are com-
monly found under normal pressure. In response, many
growth traits alter, including cell morphology and physi-
ology, cellular structure, metabolism, physical and chemi-
cal properties, the reproductive process, and defense
mechanisms. The high-pressure technology (HP) has been
industrially utilized in pressurized sterilization, synthesis of
stress-induced products, and microbial/enzymatic trans-
formation of chemicals. This article reviews current
research on pressure-induced production of metabolites in
normal-pressure microbes and their enzymatic reactions.
Factors that affect the production of such metabolites are
summarized, as well as the effect of pressure on the per-
formance of microbial fermentation and the yield of fla-
voring compounds, different categories of induced
enzymatic reactions and their characteristics in the super-
critical carbon dioxide fluid, effects on enzyme activity,
and the selection of desirable bacterial strains. Techno-
logical challenges are discussed, and future research
directions are proposed. Information presented here will
benefit the research, development, and application of the
HP technology to improve microbial fermentation and
enzymatic production of biologically active substances,
& Hua Jiang
jhmengyou@163.com
1
School of Bioengineering, Shandong Provincial Key
Laboratory of Microbial Engineering, Qilu University of
Technology, Jinan 250353, Shandong, People’s Republic of
China
2 mation and enzymatic transformation of chemicals through
College of Food Science and Engineering, Qilu University of
Technology, Jinan 250353, Shandong, People’s Republic of
China
thereby help to meet their increasing demand from the
ever-expanding market.
Keywords High-pressure technology
Microbes
Stress-
induced metabolites
Fermentation
Enzymatic reactions

Enzyme activity
Introduction
The effect of pressure on cell metabolism is not generally
considered when normal-pressure microbes are cultured
under the atmospheric pressure. However, if these organ-
isms are exposed to a high-pressure environment, their
growth and metabolism alter correspondingly.
The high-pressure (HP) technology has been applied
industrially to culture microbes for the production of cer-
tain biological compounds. Under high pressure cell
structure, physiology, physical and chemical properties,
cell metabolism, hereditary materials, and the defense
mechanism all go through various changes. Research in
this promising new field aims to identify beneficial stress-
induced metabolites and improve their yield through the
manipulation of pressure.
The technology gradually matured since the early 1990s,
and the applications have expanded. The HP technology is
now mainly used in the following fields: elimination of
harmful microorganisms (e.g. the processing and storage of
food in industries); cultivation of deep sea microbes that
are un-cultivatable under normal pressure conditions (to
identify new resources in marine microbes); Production of
certain stress-induced metabolites; and microbial transfor-
the special properties of moderately high pressure (e.g. the
supercritical state).
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Within the biologically tolerable pressure range, pres-

sure usually does not affect the strength of covalent bonds
of a chemical compound, but it damages the non-covalent
bonds and weakens the hydrophobic interactions (Con-
sidine et al. 2008; Marina et al. 2016). Under pressure, the
strength of hydrogen bonds and the ionization of acids,
bases and salts are enhanced, while the ionic bonds fall
apart (Silva et al. 2001). High pressure can also cause
microbial death through changing the permeability of cell
membranes (Klotz et al. 2010; Marta et al. 2016) and
subsequent loss of cellular components (Pierre et al. 2016),
as well as through damaging the nucleic acids, and irre- Fig. 1 The effect of high pressure on microbes and enzymes.
(a) Synthesis of stress-induced metabolites in microbial cells under
versibly deactivating the enzymes (Bang and Chung 2010; pressure, (b) effects of pressure on microbial fermentation, (c) bio-
Inácio et al. 2014). transformation reactions of microorganisms under pressure, (d) effect
Baro-adapted microbes are naturally found in high of pressure on enzyme activity, (e) effect of pressure on enzymatic
pressure environments. Their pressure tolerance is due to a reactions
set of pressure regulating genes in their genomes. These
genes start to express when the pressure reaches 0.3 MPa, is the self-protection mechanism preserved through the
while at the same time the expression of certain other course of microbial evolution (Li et al. 2013). The com-
proteins decrease, leading to fewer channels in the cell pounds produced are called stress-induced metabolites.
membrane and correspondingly less diffusion leakage of Pressure of the culture environment can significantly
carbohydrates and other nutrients to the external environ- affect microbial metabolism. Trehalose and glutathione are
ment (Wei 2013). two major stress-induced metabolites with industrial value
Normal-pressure microorganisms however go through that are produced by microbes under pressure (Fig. 2).
morphological changes under high pressure. The structures When Qiao et al. used high purity air (O2:N2 = 21:79) as
and functions of cell wall and cell membrane, biochemical the pressure medium to culture S. cerevisiae CICC1339
reactions, and gene expression all alter (Coelho et al.
2004), and subsequently leading to a remodeled cell
metabolism through either directly targeting the chemical
reactions or changing the expression of relevant genes
involved in these reactions (Lee et al. 2006).
Pressure, as a physical factor of enzymology, can affect
the catalytic activity of enzymes by modifying the
enzyme’s structure (Jiang et al. 2015) and thereby its
activity (Krystyna et al. 2014). High pressure may also lead
to the denaturation of proteins and the loss of enzyme
functions (Tran and Chang 2014).
In this article, we summarized and discussed the current
studies on pressure induced production of metabolites in
normal-pressure microbes, and the effects of pressure on
enzymatic reactions (Fig. 1). We hope this review will
facilitate the research and application of the HP technology
in industries involving microbial fermentation and enzyme
catalysis.

Synthesis of stress-induced metabolites

Under normal pressure, the anabolic and catabolic reac-

tions in a microorganism remain balanced. This balance is
disturbed when a microbe faces pressure. A suite of genes
are instinctively turned on to synthesize compounds that
prevent pressure damage. This stress response of microbes
Fig. 2 The production of stress-induced metabolites in yeast cells
under pressure. a SEM photographs of S. cerevisiae cells under
0.1 MPa, b SEM photographs of S. cerevisiae cells under 1.0 MPa

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World J Microbiol Biotechnol (2016) 32:178
under 0.5 MPa pressure and after 6 h of cultivation the
glutathione concentration increased by 58.7 % in compar-
ison with the control cells grown at normal pressure (Qiao
et al. 2006). Similarly, when Dong et al. grew S. cerevisiae
under 1.0 MPa pressure for 3 h they noticed an increased
yield of trehalose by 82.9 % (Dong et al. 2007b). Trehalose
non-specifically protects cells under adverse conditions
(Liang et al. 2013), while glutathione is involved in
apoptosis (Kiriyama et al. 2012). These two products are
normally present at very low concentrations in microor-
ganisms (Bachhawat et al. 2012), but their production
increases when cells undergo stress, presumably for self
protection (Zheng et al. 2014).
The metabolism of microbes under pressure is influ-
enced by a number of factors, including the intensity of
pressure, the length of treatment, how fast the pressure is
applied, temperature, and pH (Zhou et al. 2014). Microbes
normally grow slower when pressure increases and the
treatment time prolongs, and in some cases they may even
get killed (Qamar et al. 2014). Short treatment with mild
pressure, however, improves the yield of stress-induced
products (Fan et al. 2004). Future studies should devote
efforts to better understand the interactions of the above
mentioned factors and identify optimal culturing condi-
tions, so as to increase the yield of stress-induced products.
Effects of pressure on fermentation
High pressure can alter the fermentation process and affect
the yield of flavoring compounds. Dong et al. cultured S.
cerevisiae B9 under 0.5 MPa and noticed a slower pro-
duction and reduction of diacetyl compounds as the pres-
sure increased, and the yield of alcohols and esters also
decreased, there was however an increase in the yield of
acetaldehyde as the pressure increased (Dong et al. 2007a).
Pressure can also slow down fermentation reactions by
decelerating sugar consumption and ethanol production
(Dong and Li 2009).
When yeast is brewed in large tanks, the hydrostatic
pressure from the fermenting mash and the pressure caused
by the metabolic waste (CO2) both affect the metabolism of
yeast cells (Yang et al. 2013; Schievano et al. 2016)
(Fig. 3). The pressure exerted onto the yeast cells increases
as the height of the tank increases, causing a decreased
production of higher alcohols in the beer (Aguilera et al.
2005a, b). Pressure from CO2 alters the fermentation
pathway, reduces the production of esters, which ultimately
changes the taste and flavor of the beer (Landaud et al.
2001). Pressure was also noticed to affect gene expression
of certain enzymes, causing decreased production of acetyl
Co-A and ethyl acetate, and increased production of fatty
esters (Aguilera et al. 2005a, b). Additionally, increased
Page 3 of 7 178
partial pressure of CO2 promotes the pyruvate dehydro-
genase catalyzed reaction to shift towards the formation of
pyruvate, making it possible to synthesize more acetalde-
hyde (Keisuke et al. 2005).
Therefore one of easiest methods to ensure consistency
of desired flavor in beers is to adjust the concentration of
CO2 in the fermenting tanks, as fermentation pressure plays
an important role in the content of produced esters.
Effect of pressure on enzymatic reactions
Most enzymatic reactions take place within in a narrow
pressure range. Change to the pressure can affect the
chemical bonds that hold the enzyme together, alter the
enzyme volume, and shift the chemical equilibrium regu-
lated by the enzyme. Elevated pressure promotes chemical
reactions that decrease the activation volume while inhibits
reactions that increase the activation volume (Bruins et al.
2006).
Since pressure affects the enzyme volume without
altering its binding property or the activation energy, it is
often used to study the mechanism of enzymatic reactions
(Željko et al. 2012; Kirsch et al. 2013; Sandipam et al.
2014). To maintain the stability and function of enzymes,
the pressure applied is normally under 200 MPa.
The supercritical carbon dioxide (SC-CO2) fluid is
commonly used in food industry as a non-aqueous phase
solvent to promote enzymatic reactions (Glaucia and
Marleny 2013; Myunggu et al. 2013; Naya and Imai 2016).
Supercritical condition has also been used to facilitate
enzymatic reactions involving the synthesis and separation
of chiral compounds (Tomoko 2013). SC-CO2 is created at
a pressure of above 7.38 MPa. This pressure affects the
3-D configuration of the enzyme (Rodrigo et al. 2015). The
typical enzyme catalyzed reactions under SC-CO2 are
shown in Table 1 below.
Suitable pressure can also improve the biotransforma-
tion reactions in microorganism cells (Qiao et al. 2005).
Pressure improved the solubility of steroid in the reaction
medium, and promoted the interactions between the sub-
strates and the enzyme (Xu et al. 2004).
These examples illustrate that difficult enzymatic reac-
tions and biotransformations under normal pressure can be
achieved with a high pressure treatment.
Effect of pressure on enzyme activity
High pressure slows down the growth of microorganisms if
they do not get killed. As a result, mild pressure is often
used to treat microbes for various purposes. Isolated
enzymes are more resistant to high pressure treatment (Li
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178 Page 4 of 7
Fig. 3 The fermentation
production of yeast under
pressure. a Large fermenter,
b SEM photographs of S.
cerevisiae cells under 0.3 MPa
Table 1 Summary of enzyme catalyzed reactions under SC-CO2
The name of reaction Enzymes
The esterification of oleic acid and methanol Lipase
The biodiesel production of Lipids and methanol Lipase
The conversion of corn oil and methanol Lipase
The hydrolysis of fat Lipase
The ethanolysis of oil 1,3-regiospecific lipase
The isomerization of linoleic acid and conjugated linoleic acid Linoleic acid isomerase
et al. 2012), although high pressure can deactivate an
enzyme by changing its spatial structure or rearranging its
subunits (Lakshmi et al. 2016).
When enzymes are treated with an appropriate pressure,
its activity can moderately increase (Zhao et al. 2015). For
example, Liu et al. reported that tryptase had the highest
activity at 300 MPa, 1.386 times higher than the untreated
sample. Fourier Transform Infrared Spectroscopy (FTIR)
analysis revealed that the peak area ratio of a-helix to b-
turn reached the maximum (2.749) after tryptase was
treated at 300 MPa (Liu et al. 2015). Since peptide bonds
remain unbroken at high pressure, the primary structure of
the enzyme stays the same. The proportion of a-helix in the
secondary structure must have played an important role in
the activation of the enzyme through the modification of
tertiary and quaternary structures (Liu et al. 2013; Scirè
et al. 2010; Saba et al. 2015).
Besides affecting the enzyme structure, pressure can
also induce microorganisms to produce more active
enzyme variants or to increase the production of enzymes.
When routine biological operations of a cell are disturbed
due to pressure, it modifies its reproduction approach and
initiates genetic mutations. Table 2 summarizes the
research results of microorganism mutation breeding with
high pressure. It’s evident that pressure can elevate enzyme
activity either through structural modification or through
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World J Microbiol Biotechnol (2016) 32:178
Reaction conditions References
40 °C, 10 MPa Philipe et al. (2016)
50 °C, 20 MPa Hanifa et al. (2014)
60 °C, 10 MPa Ozan and Edmonton (2013)
55 °C, 30 MPa Glaucia et al. (2012)
60 °C, 10 MPa Shin et al. (2010)
40 °C, 10 MPa Jiao et al. (2012)
mutation, and in some cases it can increase the production
of enzymes in microbes. Pressure can be a valuable tool for
the selection of desirable microbial strains for the pro-
duction of certain enzymes.
Summary and future directions
As an external stress factor, pressure can induce the pro-
duction of certain desirable metabolites in microorganisms.
Therefore, the optimization of growth pressure should be
studied more closely for concerned industries. New
metabolites induced by pressure stress should be identified;
the effects of pressure on involved enzymes should be
examined; and the working mechanism of pressure on
microbial responses should be investigated.
In the fermentation industry, high pressure affects the
yield of flavoring compounds, but quantifiable evidences
are lacking for the understanding of its mechanism.
Metabolic flux analysis can be used to quantitatively
describe the flux distribution of metabolic pathways during
fermentation under normal and increased pressures. Key
players that inhibit the synthesis of flavoring compounds
under high pressure fermentation should be identified. As
the fermentation apparatus becomes bigger as in an
industry, the effect of pressure must be considered as it’s
World J Microbiol Biotechnol (2016) 32:178
Table 2 Summary of microorganism breeding under high pressure
Strains Mutagenesis conditions Results
Flavobacterium sp. YY25 SC-CO2; 35 °C, 8 MPa, 30 min The activity of lipase was increased by 44.2 %
Bacillus subtilis K2 SC-CO2; 37 °C, 8 MPa, 30 min The activity of amylase was increased by *33 %
Thermus aquaticus SQ-11 Air; 70 °C, 1.0 MPa, 2 h The activity of trehalose synthase was increased by 89.1 %
one of the most important factors that regulate the pro-
duction of flavoring compounds. A backup measure is to
select for microbial strains that tolerant high pressure.
Regulating enzymatic reactions through pressure is a
vibrant new area in enzyme engineering. The supercritical
fluid has numerous advantages in promoting such reac-
tions, and its value has become increasingly recognized. In
recent years, research on enzymatic reactions in a super-
critical fluid has been heavily focused on the basic theories,
such as the reaction kinetics, reaction selectivity, and
potential applications.
Genetic engineering can be used to introduce pressure-
tolerant genes from a baro-tolerant microbial species to the
cell of a normal-pressure microbe, or to transfer genes with
special properties from a normal-pressure microbe to a
pressure-tolerant microbe. These approaches can quickly
create desirable strains with modified physiological func-
tions in the recipient cell. Additionally, supercritical CO2 is
a ‘‘green’’ mutagen with immense potential for the muta-
tion and selection of microorganisms with desirable traits.
The field of pressure biology is just unfolding. Research
and application of the HP technology still need to be
explored in various aspects, especially in terms of
increasing the yield of metabolites, improving activities of
the enzymes, and understanding the relationship between
pressure-modified enzyme structures and their functions. In
the near future, as we delve deeper into the research, the
HP technology will undoubtedly showcase its bountiful
applications and immense value in the biology field.
Acknowledgments This study was supported by the grant from the
National Science Foundation of China (No. 20176041).
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