Appl Microbiol Biotechnol

DOI 10.1007/s00253-017-8149-0

MINI-REVIEW

Lipid accumulation in prokaryotic microorganisms

from arid habitats
Philippa Hauschild 1 & Annika Rttig 1 & Mohamed H. Madkour 2 &
Ahmed M. Al-Ansari 2 & Naief H. Almakishah 2 & Alexander Steinbchel 1,2

Received: 14 November 2016 / Revised: 23 January 2017 / Accepted: 25 January 2017

# Springer-Verlag Berlin Heidelberg 2017

Abstract This review shall provide support for the suitability
of arid environments as preferred location to search for un-
known lipid-accumulative bacteria. Bacterial lipids are
attracting more and more attention as sustainable replacement
for mineral oil in fuel and plastic production. The develop-
ment of prokaryotic microorganisms in arid desert habitats is
affected by its harsh living conditions. Drought, nutrient lim-
itation, strong radiation, and extreme temperatures necessitate
effective adaption mechanisms. Accumulation of storage
lipids as energy reserve and source of metabolic water repre-
sents a common adaption in desert animals and presumably in
desert bacteria and archaea as well. Comparison of corre-
sponding literature resulted in several bacterial species from
desert habitats, which had already been described as lipid-
accumulative elsewhere. Based on the gathered information,
literature on microbial communities in hot desert, cold desert,
and humid soil were analyzed on its content of lipid-
accumulative bacteria. With more than 50% of the total com-
munity size in single studies, hot deserts appear to be more
favorable for lipid-accumulative species then humid soil
(20%) and cold deserts (17%). Low bacterial lipid accumu-
lation in cold deserts is assumed to result from the influence of
Electronic supplementary material The online version of this article
(doi:10.1007/s00253-017-8149-0) contains supplementary material,
which is available to authorized users.
* Alexander Steinbchel
steinbu@uni-muenster.de
1
Institut fr Molekulare Mikrobiologie und Biotechnologie,
Westflische Wilhelms-Universitt Mnster, Corrensstrae 3,
D-48149 Mnster, Germany
2
Environmental Sciences Department, Faculty of Meteorology,
Environment and Arid Land Agriculture, King Abdulaziz University,
Jeddah 21589, Saudi Arabia
low temperatures on fatty acids and the increased necessity of
permanent adaption methods.
Keywords Arid habitats . Lipid accumulation . Lipids .
Storage compounds . Metabolic water
Introduction
In times of a growing human population accompanied by
shrinking availability of resources and climatic changes,
sustainable-orientated industry becomes more and more im-
portant. Especially the oil industry as basis for petrochemistry,
motor fuel and plastic production is often recommended for
improvement (Klinger 2015; Reuning 2015; Opatz and
Arduengo 2016). In this context, bacteria and other microor-
ganisms provide multiple approaches for alternative produc-
tion methods. Several bacterial strains are for example known
to accumulate lipids, which can be processed similarly to min-
eral oil. Their chemical structure enables classification into
three sub-groups with different applicability.
The most common sub-group of these compounds are
polyhydroxyalkanoates (PHAs), esterified polymers of
3-hydroxyfatty acids (Fig. 1; Steinbchel 2001; Alvarez and
Steinbchel 2002). Their synthesis is described in detail else-
where (Anderson and Dawes 1990; Steinbchel and Valentin
1995). PHAs are highly hydrophobic polymeric lipids and are
therefore investigated for sustainable plastic production. By
modifying the composition of their sub-units, the properties
of the final polymer material can be adjusted (Anderson and
Dawes 1990). Bacterial Bbioplastic^ is as modificable as con-
ventional plastics but is in addition biodegradable. This may
also establish new fields of medical and pharmaceutical appli-
cations, e.g., for degradable implants and retard materials

(Holmes 2002; Hazer and Steinbchel 2007), once the mate-
rials have been studied in more detail.
Less species are known to accumulate triacylglycerols
(Steinbchel 2001; Alvarez and Steinbchel 2002). They are
defined as esters of fatty acids and glycerol (Fig. 1; Stveken
et al. 2005; Alvarez 2006). Due to their ester bond, it is pos-
sible to transesterify bacterial triacylglycerol (TAG) with
short-chain-length alcohols. This process is currently used to
convert vegetable TAG into biodiesel and biodiesel-like com-
pounds (Alvarez 2006; Kalscheuer et al. 2006a). Production
of vegetable oil is highly dependent on the production of soy-
beans, rapeseed, or oil palms. Their cultivation occupies a
great part of cropland, which is in effect primarily needed
for food productionespecially on account of the growing
world population. Alternative production methods are urgent-
ly required. Transesterification in particular of bacterial TAG
offers numerous advancements when compared to the
established method. Cultivation of bacteria occupies less
space but yields a better return than cultivation of plants.
Due to its flexibility regarding the carbon source, an optimized
bacterial strain is able to convert nearly the whole vegetable
biomass into TAG, whereas vegetable-based methods are ex-
clusively using the oleaginous seeds (Kalscheuer et al. 2006a).
Bacterial wax esters (WEs) are oxoesters of long-chain fatty
acids and long-chain alcohols (Fig. 1; Stveken et al. 2005;
Alvarez 2006). Synthesis of WE (and TAG) has been inten-
sively investigated (Murphy 1993; Alvarez et al. 1997; Reiser
and Somerville 1997; Alvarez and Steinbchel 2002; Ishige
et al. 2003; Kalscheuer and Steinbchel 2003). WE appear to
be capable of replacing several petrochemically synthesized
waxes. Synthetic waxes are important additives in numerous
industry sectors. Application includes for example food
(additive E910 in European countries; Ahlers 2015), cosmetics,
or additives in lubricant and varnish (Yermanos 1975;
Kalscheuer et al. 2006b; Alvarez 2010; Lautenschlger 2014).
Production with bacterial PHA, TAG, and WE represents a
sustainable and forward-looking technology. Nevertheless,
enhancement of its productivity is urgently required to be-
come competitive with current methods. The selective search
for new promising species aims at highly effective bacterial
strains, which are essential in this context.
This review shall provide support for the suitability of arid
environments as convenient location of undiscovered lipid-
accumulative bacteria. It considers the appearance of lipid ac-
cumulating strains dependent on the humidity of their habitat.
Special attention is thereby paid to deserts as the most extreme
form of arid environments. It should not be ignored that beside
prokaryotes, eukaryotic microorganisms like microalgae are
also capable of accumulating lipids (see for example Hu et al.
2008). However, these microalgae are preferentially suitable
for the production of specialty lipids and carotenoids which
are not required in bulk amounts. Due to the slow growth and
their growth to only low cell densities, it will be difficult to
Appl Microbiol Biotechnol
establish economic feasible lipid production processes
employing microalgae for bulk lipids as it is required for bio-
fuel formation. Therefore, this short review will focus on pro-
karyotes and in particular bacteria as lipid producers.
Arid environments and their qualities as bacterial
habitats
Arid climate is characterizing a great fraction of the terrestrial
habitats; one third of the emerged land is covered with deserts
(Pott 2005). Dependent on their mean annual temperature, a
distinction is drawn between hot and cold desert types. Low
water availability dominates both of them but evolves from
different mechanisms.
In hot deserts, drought is caused by low rainfall per year in
combination with high evaporation. Dry winds usually inten-
sify the substrates water loss and shape the deserts relief by
transporting sand particles (Jckli 1985). Long periods with-
out rainfall are interrupted by rain events at irregular intervals.
During this time, the rain of the whole year can fall within a
few hours or days (Pott 2005).
Cold desertslike the dry valleys in the Antarcticaare
typically found at the polar caps of our planet. Drought in cold
deserts results from low precipitation and low air humidity as
well, but additionally from the sub-zero temperatures (Pott
2005; Pearce 2012). Rainfall and groundwater are fixed in
form of ice and snow nearly throughout the whole year
(Miotke 1985; Pott 2005). This keeps humidity unreachable
for organisms, which are dependent on liquid water.
Nevertheless, habitats with milder microclimate exist and en-
able microorganisms to survive. Strong winds are responsible
for periodic movement and alteration of the immature soil.
Dependent on its location, the arising soil composition may
offer small areas with less hostile temperature (Miotke 1985).
Beside its effect on water availability, the extreme temper-
ature of desert habitats influences the fluidity of the bacterial
biomembrane. At moderate temperatures, its phospholipids
remain in a steady state equilibrium and the biomembrane is
semifluid. High temperature, as found in hot deserts, increases
the mobility of membrane lipids and thereby its fluidity. Low
temperature, as found in cold deserts, reduces lipid mobility
and results in lipid interlinkages and jellylike membrane struc-
ture (Nelson and Cox 2008a). Thermal fluctuation represents
an additional challenge in hot deserts. Local temperature
changes of up to 50 C between night and day are character-
istic for these habitats (Pott 2005).
Desert organisms are often exposed to a considerable ex-
tent to solar radiation. Frequency and intensity are thereby
influenced by the desert type and its global location. Many
hot deserts are located close to the equator. Desert organisms
must therefore arrange with daily exposure to energy-rich ra-
diation. Typically, the high daily dosages are only diminished
Appl Microbiol Biotechnol
at rare intervals by an overcast sky (Lubin 1998; Pott 2005). In
polar cold deserts, daily exposure to the solar radiation chang-
es with the length of the day. During the time of polar day, the
soil or ice surface is exposed for 24 h to sunlight with a max-
imum dosage of UV radiation. In contrast, the polar night is
characterized by 24 h of darkness and therefore by a minimal
radiation exposure (Miotke 1985). Solar radiation at the polar
caps arrives flat angled and at low energy. However, these
regions are covered by conspicuously thin ozone layers,
which results in a high penetration of UV radiation. Total
UV-radiation dosage at the soil surface is consequently
highin particular during the polar day (Mallwitz and
Zieger 1993; Pearce 2012).
Both desert types produce little biomass, with cold deserts
to a greater extent than hot deserts (Miotke 1985). In barren
desert habitats, the nutrient base of food chains is restricted
and consequently that of bacterial metabolism as well
(Newsham et al. 2010). Metabolic processes are additionally
limited by water shortage. For many bacteria, drought sig-
nifies therefore dormancy and gradually desiccation. Loss of
water molecules in combination with high UV-radiation dos-
age can thereby result in cell damage, e.g., protein oxidation
and DNA strand breaks. The arising reactive oxygen species
(ROS) enhance oxidation reactions and may induce a vicious
circle of cell destruction (Dose et al. 1992; Halliwell 1995;
Nauser et al. 2005; Fredrickson et al. 2008). Desiccation rep-
resents a great challenge for bacterial cells but unprepared
exposure of desiccated cells to water likewise. As it was men-
tioned above, sudden rainfalls can interrupt the drought pe-
riods of hot deserts. In dried bacterial cells, the abundant avail-
ability of water may result in cell lysis, protein, and DNA
damages (Potts 1994).
Hence, hot and cold deserts as the most extreme form of
arid environments are challenging habitatseven for bacteria.
They are characterized by alternating weather and rough cli-
matic conditions. Simultaneously, desert bacteria have to ar-
range with long-lasting water shortage and low food supply.
The role of lipids in the adaptation to drought
Accumulation of lipids represents a possible adaptation of
bacteria and other desert organisms to the harsh living con-
ditions in arid environments. Lipids can play an important
role in water procurement, even in times of drought. Via
aerobic degradation of lipids by -oxidation, citric acid
cycle, and oxidation of the generated reducing equivalents
by the respiratory chain, the organism can gain 107.1 g
metabolic water per 100 g fat (Young 1976), whereas car-
bohydrate and protein oxidation provide less metabolic
water (Schmidt-Nielsen and Schmidt-Nielsen 1952).
Degradation of 100 g carbohydrates was found to produce
55.5 g water, and degradation of 100 g protein resulted
even in only 41.3 g water (Baldwin 1964). Some desert
animals like the kangaroo rat (Dipodomys ssp.) are able
to cover nearly their whole water demand by these oxida-
tion processes (Schmidt-Nielsen 1972; Schmidt-Nielsen
and Schmidt-Nielsen 1952; Lohmann 2013). Hence, lipid
metabolism is also considered to act as water reserve in
adapted desert bacteria (Alvarez et al. 2004; Hernndez
et al. 2008; Bequer Urbano et al. 2013, 2014).
In addition, storage lipids represent an important energy
reserve, which may enable bacteria to survive the deserts long
periods of nutrient lack. Their energy density is twice as high
as that of carbohydrates and proteins. Degradation of lipids
provides 9.3 kcal/g, whereas degradation of carbohydrates
and proteins gives only 4.1 kcal/g (Mller and Raschke
2004). Among the bacterial storage lipids, TAGs are assumed
to be the preferred energy reserve. Their acyl compounds are
maximally reduced and offer therefore the highest amount of
energy during oxidation (Alvarez and Steinbchel 2002).
Lipid metabolism can be used to balance unsteady nutrient
supply and to reduce cell damage due to unintended metabolic
reactions. In times of nutrient lack, e.g., during dry periods in
deserts, lipid degradation provides reducing equivalents and
keeps the bacterial metabolism running. During nutrient abun-
dance, e.g., after rainfall events in hot deserts, lipid accumu-
lation catches critical amounts of reducing equivalents.
Redundant reducing equivalents would otherwise react else-
where randomly (Alvarez and Steinbchel 2002; Senior and
Dawes 1971). This system of lipid transformation may enable
a smooth metabolism in adapted desert bacteria.
Finally, accumulated lipids are considered to contribute to
an increased stability of rehydrated bacterial cells. They seem
to be involved in protecting cells from cell lysis and deficient
membrane integrity during sudden water availability (Singh
et al. 2002; Alvarez et al. 2004). Accumulated lipids may
counteract unfavorable membrane states not only after rain
events but also in adaption to the extreme temperature of de-
sert biotopes. By influencing its phospholipid composition,
they regulate the fluidity of membranes (Singh et al. 2002).
Increased utilization of unsaturated fatty acids in cold environ-
ments improves the membrane fluidity. In hot environments,
integration of saturated fatty acids improves the membrane
stability (Nelson and Cox 2008a).
All mentioned tasks of accumulated lipids are resulting in
reduced sensibility of bacteria to the characteristic living con-
ditions in deserts. Consequently, lipid accumulation is assumed
to occur frequently in bacterial strains from desert habitats.
Other well-known adaptations of bacteria to desert
environment
Cellular lipids, accumulated as storage compounds,
may provide metabolic water to desiccated bacteria.

Nevertheless, bacteria from desert habitats must always
arrange with water loss. Water molecules are involved in
many cellular components, e.g., the hydrate envelope of
proteins. At least 0.05 g water per gram protein is essential
to generate a functional hydrate envelope (Potts 1994). To
protect cellular components in case of lost interacting
water molecules, desert bacteria often accumulate
polyhydroxylated compoundslike trehalose. These com-
pounds are assumed to take the position of missing water
molecules by forming hydrogen bonds (water-replacement
hypothesis; Crowe et al. 1988). Additionally, accumulated
trehalose can evolve into a preserving and chemical inert
substance, which fills the whole bacterial cell and slows
down chemical reactions. In this so-called Bglassy state,^
bacteria are able to resist a drought for a long time
(Bglassy-state theory^; Green and Angell 1988).
To minimize water loss, some bacterial species produce
extracellular polysaccharides. These polymers form a
highly viscous and mostly hygroscopic envelope around
the bacterial cells and keep intracellular water molecules
inside during drought (Billi and Potts 2000). A thickened
cell wall, as it was found in species of -proteobacteria,
fulfills the same function (Houang et al. 1998). The ex-
tracellular polymer matrix can be enriched with radiation-
protecting pigments. They reduce the appearance of cell
damages as described above by absorbing UV radiation
(Billi and Potts 2000).
Aside from that, many desert bacteria show behavioral
adaptation to their environment. Especially endolithical
life and the formation of biological soil crusts are to be
mentioned. Endolithic bacteria settle micropores of rocks,
which protect them from radiation, strong wind, and un-
steady temperatures. Beside of this, air moisture precipi-
tates at the rocks surface and supply endolithic species
with liquid watereven at extreme hot and dry places
(Nienow 2009; Wierzchos et al. 2012). Biological soil
crusts are natural communities of microorganisms, which
cover the surface of stones or soil (Nienow 2009; Rajeev
et al. 2013). They enable prokaryotic desert microorgan-
isms to change their location in adaption to current weather
conditions. During long periods of drought, cyanobacteria
were found to move to the crusts protective bottom side.
During rain events, the investigated species Microcoleus
vaginatus showed hydrotaxis to the crusts surface and its
increased water availability (Garcia-Pichel and Pringault
2001).
Several microbial strategies for optimized water
utilization in dry environments are known today.
Nevertheless, desert bacteria and their behavior are diffi-
cult to investigate, and many adaptation mechanisms were
only proposed. Further research is required to confirm
current assumptions and to estimate their potential for
the future.
Appl Microbiol Biotechnol
The occurrence of (storage) compound accumulation
in bacteria
With the properties of accumulated lipids on the one hand and
the living conditions in arid environments on the other hand, a
link between the ability to store lipids and the appearance of
bacterial strains in desert habitats is considered. This review
intents to compare documented bacterial lipid accumulation
and the detection of respective bacterial strains in desert soils
by means of literature research. For that purpose, several bac-
terial strains, which were described as lipid accumulative in
literature, were scanned for detection in desert soil. Only very
few studies in literature have analyzed bacterial desert isolates
and lipid accumulation simultaneously so far. Thus, the liter-
ature describing isolation of bacteria from desert soil was
compared with the literature describing detection of lipid ac-
cumulation in single species. As shown in Table 1, the litera-
ture search revealed 35 bacterial desert species, which were
proven to be lipid accumulative. Interestingly, most of them
belong to the phylum Actinobacteria (17 species), followed
by -Proteobacteria (9 species) and Firmicutes (5 species).
Single findings represent strains from cyanobacteria,
-Proteobacteria, and -Proteobacteria. Only six isolates
from desert soil samples were already classified as lipid accu-
mulative by the scientists who isolated them (Ramlibacter
henchirensis sp. nov. TMB834, Ramlibacter tataouinensis
sp. nov. TTB310 (Heulin et al. 2003), Rhodococcus jostii
RHA1 (Hernndez et al. 2008), Streptomyces sp. G25,
Streptomyces sp. G49, and Rhodococcus sp. A27 (Rttig
et al. 2016). One of themR. jostii RHA1is already in
the focus of current lipid research (Hernndez et al. 2008).
In comparison with the occurrence of lipid accumulation,
Table S1 summarizes the accumulation of other intracellular
compounds in a selection of the most interesting bacterial
strains. Most of the known bacteria are able to produce storage
compounds under particular circumstances. Hence, Table S1
does not claim to be complete. It rather represents a standard
and working tool to establish the dimension of bacterial lipid
accumulation. All species mentioned in Table S1 originate
from places with low water availability. Salt-rich environ-
ments are included due to the similar effect of osmotic stress
and drought stress on bacterial cells (Alvarez et al. 2004).
The ability to accumulate trehalose or sucrose is widely dis-
tributedespecially in Actinobacteria (McBride and Ensign
1987). Additionally, Actinobacteria are characteristic inhabitants
of arid soil (Skujin 1984) and provide therefore a large fraction
of the species listed in Table S1. Compared with Table 1, the
fraction of cyanobacteria is distinctly larger in Table S1. Lipid
accumulation seems to be consequently uncommon in this tax-
on. Furthermore, several species appear to be unknown for lipid
accumulation but are able to accumulate other compounds as has
been shown. They belong in particular to the taxa Bacteroidetes
and Deinococcus-Thermus as well as to the Archaea.
Table 1 Bacterial strains from arid soil habitats with the ability to accumulate lipids

Taxonomic classification Strain known for lipid accumulation Strain found in desert sample Site of isolation Fatty acid References

Actinobacteria Arthrobacter AK19 Arthrobacter ssp. Sahara desert, Antarctic TAG Essoussi et al. (2012)
Dry Valleys Johnson et al. (1978)
Ratledge (1984)
Corynebacterium ssp. 7E1C Corynebacterium ssp. Antarctic Dry Valleys WE Johnson et al. (1978)
Bacchin et al. (1974)
Appl Microbiol Biotechnol

Dietzia maris 53 Dietzia maris Desert in Al Abdali PHA, TAG, WE Al-Awadhi et al. (2012)
(Kuwait) Alvarez (2003)
Gordonia sp. KTR9 Gordonia sp. KTR9 Mojave desert TAG Eberly et al. (2013)
Thompson et al. (2005)
Micromonospora echinospora Micromonospora echinospora Sandstone desert, Tunisia TAG Essoussi et al. (2012)
Nocardia ssp. Nocardia ssp. Sahara desert, Antarctic TAG Essoussi et al. (2012)
Dry Valleys Murphy (2001)
Cary et al. (2010)
Nocardia asteroides 419 Nocarida asteroides Desert in Tucson, AZ PHA, TAG, WE McClung (1960)
Alvarez (2003)
Psychrobacter urativorans Psychrobacter urativorans Antarctic Dry Valleys WE Shravage et al. (2007)
Russell (1974)
Rhodococcus ssp. Rhodococcus ssp. Arid habitats PHA, TAG Hernndez et al. (2008)
LeBlanc et al. (2008)
Alvarez (2003)
Rhodococcus sp. A27 Rhodococcus sp. A27 Desert sand from Saudi Arabia TAG Rttig et al. (2016)
Rhodococcus erythropolis Rhodococcus erythropolis Desert sand PHA, WE, TAG Radwan and Al-Muteirie (2001)
Alvarez (2003)
Alvarez et al. (1997)
Rhodococcus jostii RHA1 Rhodococcus jostii RHA1 High-altitude desert in Arizona TAG, WE, PHA Hernndez et al. (2008)
Woods et al. (2011)
Rhodococcus opacus Rhodococcus opacus Kizil-Kum desert TAG, WE, PHA Alvarez et al. (1997)
Jadan et al. (2001)
Olukoshi and Packter (1994)
Rhodococcus ruber Rhodococcus ruber Desert dust in Mali, PHA, TAG, WE Kellogg et al. (2004)
desert in Kuwait Al-Awadhi et al. (2012)
Alvarez et al. (1997)
Streptomyces ssp. Streptomyces ssp. Mongolian semidesert TAG Olukoshi and Packter (1994)
Kurapova et al. (2012)
Streptomyces sp. G25 Streptomyces sp. G25 Desert sand from Saud Arabia TAG Rttig et al. (2016)
Streptomyces sp. G49 Streptomyces sp. G49 Desert sand from Saudi Arabia TAG Rttig et al. (2016)
Streptomyces albus Streptomyces albus Desert in Al Abdali (Kuwait), TAG Al-Awadhi et al. (2012)
Antarctic Dry Valleys Cary et al. (2010)
Olukoshi and Packter (1994)
Streptomyces coelicolor J802 Streptomyces coelicolor Mongolian semidesert TAG, PHA Kurapova et al. (2012)
Olukoshi and Packter (1994)
Streptomyces griseus Streptomyces griseus Mongolian semidesert TAG Kurapova et al. (2012)
Olukoshi and Packter (1994)
Cyanobacteria Microcoleus vaginatus Microcoleus vaginatus Cold desert, Colorado plateau PHA Rajeev et al. (2013)
Firmicutes Bacillus sp. JMa5 Bacillus ssp. Antarctic Dry Valleys PHA Cary et al. (2010)
Wu et al. (2001)
Bacillus cereus Bacillus cereus Californian desert PHA Mizuno et al. (2010)
Hagen et al. (1968)
Table 1 (continued)

Taxonomic classification Strain known for lipid accumulation Strain found in desert sample Site of isolation Fatty acid References

Singh et al. (2009)

Bacillus licheniformis Bacillus licheniformis Sonora desert PHA Benardini et al. (2003)
Singh et al. (2009)
Bacillus megaterium Bacillus megaterium African desert (Mali) PHA Mizuno et al. (2010)
Lpez et al. (2012)
Kellogg et al. (2004)
Bacillus subtilis K8 Bacillus subtilis Sonora desert, desert dust in Mali PHA Benardini et al. (2003)
Singh et al. (2009)
Kellogg et al. (2004)
-Proteobacteria Azospirillum lipoferum sp. 59b Azospirillum lipoferum Symbiotic in Indian desert PHA Sadasivan and Neyra (1985)
Rao and Venkateswarlu (1982)
-Proteobacteria Ramlibacter henchirensis sp. nov., TMB834 Ramlibacter henchirensis sp. nov., TMB834 Semidesert in Tunisia PHA Heulin et al. (2003)
Ramlibacter tataouinensis sp. nov., TTB310 Ramlibacter tataouinensis sp. nov., TTB310 Semidesert in Tunisia PHA Heulin et al. (2003)
-Proteobacteria Acinetobacter calcoaceticus Acinetobacter sp. Desert soil in Kuwait WE, TAG Reiser and Somerville (1997)
Obuekwe et al. (2009)
Acinetobacter lwoffi Acinetobacter lwoffi Vulcanic rock from Atacama desert TAG Vachon et al. (1982)
Campos et al. (2009)
Acinetobacter sp. HO1-N Acinetobacter sp. Antarctic Dry Valleys WE, TAG Cary et al. (2010)
Singer et al. (1985)
Azotobacter chroococcum MAL-201 Azotobacter chroococcum Desert soil PHA Pal et al. (1997)
Abdel-Ghaffar (1989)
Azotobacter vinelandii Azotobacter sp. Sonora desert PHA Nijhoff and Publishers (1982)
Stevenson and Socolofsky (1966)
Pseudomonas ssp. Pseudomonas ssp. Desert PHA Philip et al. (2007)
Radwan and Al-Muteirie (2001)
Pseudomonas aeruginosa Pseudomonas aeruginosa Oil field in desert (Kuwait) PHA Taylor et al. (2002)
Timm and Steinbchel (1990)
Philip et al. (2007)
Pseudomonas oleovorans Pseudomonas oleovorans Desert dust from Africa PHA Griffin et al. (2001)
Anderson and Dawes (1990)
Pseudomonas putida Pseudomonas putida Oil field in desert (Kuwait) PHA Agrawal et al. (2014)
Sorkhoh et al. (2010)

Lipid-accumulative strains were assembled from corresponding literature and compared with reported bacterial communities from arid habitats. Lipid accumulation was defined as the ability to store
intracellular PHA, TAG, or WE granules
Appl Microbiol Biotechnol
Appl Microbiol Biotechnol
The coherence of (storage) compound accumulation
in bacteria and their occurrence in arid environment
As described above, drought-induced cell stress appears to
stimulate bacterial lipid accumulation. Hence, the content of
lipid-accumulative bacteria is supposed to be remarkably high
in arid environments. Analysis of the bacterial composition in
ten published studies on hot and cold deserts shall provide
support for this assumption. Studies were analyzed on their
content of accumulative bacteria by using the presented col-
lection of species (Table 1 and Table S1).
As it can be seen in Figs. 1 and 2, all analyzed studies
contain accumulative species. However, the fraction of ac-
cumulative species is higher in samples from hot deserts
then in samples from cold deserts. Between 25 and 50% of
the hot desert bacteria are presumably able to accumulate
storage compounds (Fig. 1), whereas only half of the cold
desert community studies indicate similar values (Fig. 2).
The cold desert community studies show additionally
stronger variations in their content of accumulative spe-
cies. Consequently, the ability to accumulate storage com-
pounds seems to occur more frequently in hot desert bac-
teria then in cold desert bacteria. Different duration of nu-
trient lack and drought in hot and cold desert habitats is
considered to result in adaption mechanisms with different
permanency. In hot deserts, periods of shortage are
interrupted by abundant nutrient and water supply after
rainfall events, whereas water in cold deserts is hardly ever
unfreezed (see above). Consequently, cold desert bacteria
cannot rely on continuous regeneration of their storage
compounds and are dependent on long-lasting adaption
mechanisms. Accumulation of storage compounds is as-
sumed to be replaced by more permanent methods, like
using locally melted water of microhabitats or benefiting
from air humidity (Palmer and Friedmann 1990).
Fig. 1 Chemical structures of the different lipids, which are known to be
accumulated in bacteria. a Structure of the common PHA sub-unit poly
(-hydroxybutyrate), which is characterized by a methyl group. Other PHA
sub-units have different side groups. b Structure of TAG. Side groups are
Consistent with this assumption, the number of lipid-
accumulative species is clearly larger in the hot desert studies
then in the cold desert studies. This correlation is not influ-
enced by the inclusion of species with the accumulation of
additional compounds besides lipids (medium gray fractions;
Figs. 1 and 2). Lipid-accumulative species and species with
additional compound accumulation together constitute be-
tween 8% (Fig. 1a) and 51% (Fig. 1f) of the total community
size in the hot desert studies. In five of six studies, its fractions
exceed thereby 20% and in three of six studies even 40% of
the total community size. The fraction of lipid-accumulative
species in the cold desert studies range between 2% (Fig. 2a)
and 17% (Fig. 2b). Only one of them exceeds 10% of the total
community size (Fig. 2b).
The different occurrence of lipid accumulation in bacte-
ria from hot and cold deserts may arise due to the deserts
temperatures. Its influence on the consistency of cellular
lipids (see above) is assumed to promote lipid accumula-
tion in hot environments but restrict it in cold environ-
ments (Annous et al. 1997; Nelson and Cox 2008b).
In summary, all analyzed studies with different bacterial de-
sert communities contain lipid-accumulative species.
Nonetheless, the majority of cultivated bacteria in all studies
do not accumulate lipids from the current state of knowledge.
Further research on the distribution of lipid accumulation in
desert bacteria is required to determine its dimension accurately.
To generate a comparable norm, bacterial lipid accumula-
tion in nutrient rich and humid environment was evaluated.
Five different studies of humid soil samples were therefore
analyzed for their bacterial compositions, based on the pre-
sented species collections (Table 1 and Table S1). The analysis
gave a smaller content of accumulative species in humid soil
samples then in hot desert soil samples (Fig. 3). Two of the
five humid soil studies contain at least 25% accumulative
species (Fig. 3b, d), whereas compound accumulation arises
normally made of long hydrocarbon chains (R, R, R). c Structure of WE.
Side groups result from the condensation of an acyl CoA (R) with a fatty
alcohol (R) and are therefore hydrophobic hydrocarbon chains as well

Fig. 2 Occurrence of compound-accumulative bacteria in hot desert soil
samples. Bacteria were classified into lipid-accumulative species (black),
other compound-accumulative species (dark gray), lipid- and other
compound-accumulative species (medium gray), and non-accumulative
species (light gray). a Sample with 127 cultivated species from the desert
of Tataouine (Chanal et al. 2006). b Sample with 27 cultivated species
only in 620% of the total bacterial community in the last
three studies (Fig. 3ae). The two studies with high content
of accumulative species depict the bacterial composition of
tropical soil (Fig. 3b) and a European wheat field (Fig. 3d).
However, soil in the first study was enriched with PHA
(Boyandin et al. 2013), which is expected to have an influence
on the bacterial community composition. Its content of
degrading as well as that of accumulative species may be
clearly increased and thus not comparable anymore.
Comparison of the cold desert studies and the humid soil
studies gives no strikingly different occurrence of bacterial
compound accumulation and similar fluctuation of its quanti-
ty. Nevertheless, the fraction of only lipid-accumulative spe-
cies is distinctly higher in the humid soil studies. Lipid-
accumulative species are present in four of five humid soil
studies and reach between 5% (Fig. 3a) and 20% (Fig. 3e) of
the whole community size. Thus, the fraction of lipid-
accumulative species is highest in the analyzed hot desert soil
samples, followed by the humid soil samples and finally by
the cold desert soil samples.
Appl Microbiol Biotechnol
from the African desert dust (Griffin et al. 2001). c Sample with 32
cultivated species from the Sahara desert (Essoussi et al. 2012). d
Sample with 26 cultivated species from a Mongolian dry steppe
(Kurapova et al. 2012). e Sample with 16 cultivated species from arid
habitats in the USA (Kuske et al. 1997). f Sample with 16 cultivated
species from the Atacama desert (Bursy et al. 2008)
On closer examination of the hot desert studies as the most
promising bacterial community, identified accumulative bac-
teria are mostly able to incorporate more than one compound
(Fig. 1, medium gray fraction). The majority of these bacteria
is able to store lipids as required. Lipid-accumulative species
represent between 30% (Fig. 1a) and 75% (Fig. 1bd, f) of the
accumulative species (Fig. 1e). Thus, storage lipids play ob-
viously an outstanding role in hot desert bacteria with the
ability to accumulate compounds. These lipids may be respon-
sible for energy and water storage in times of drought as de-
scribed above. Other storage compounds like polysaccharides
may additionally contribute to protective and preventive
mechanisms. Nevertheless, not every bacterial species from
the analyzed hot desert soil studies is able to accumulate stor-
age lipids. Therefore, alternative adaptation mechanisms may
exist, which fulfill the same role as storage lipids.
The hot and cold desert studies with the largest sample size
are simultaneously the studies with the least percentage of
accumulative species (Figs. 1a and 2a). Usually, the signifi-
cance of studies increases with its sample size. This indicates
Appl Microbiol Biotechnol

Fig. 3 Occurrence of compound-

accumulative bacteria in cold
desert soil samples. Bacteria were
classified into lipid-accumulative
species (black), other compound-
accumulative species (dark gray),
lipid- and other compound-
accumulative species (medium
gray), and non-accumulative
species (light gray). a Sample
with 65 cultivated species from
the McMurdo Dry Valley,
Antarctica (Shravage et al. 2007).
b Sample with 12 cultivated
species from Victoria Land,
Antarctica (Aislabie et al. 2006). c
Sample with 22 cultivated species
from Antarctica (Aislabie et al.
2008). d Sample with 26
cultivated species from the
McMurdo Dry Valley, Antarctica
(Brambilla et al. 2001)

presumably lower percentages of accumulative bacteria in not
reviewed microbial desert communities. The humid soil stud-
ies are comparatively based on larger sample sizes, and their
data are consequently better confirmed.
The presented analysis is based on information, gathered
from Table 1 and Table S1, in which the species were evaluated
by means of notes in the corresponding literature. However,
most of the so-called non-accumulative species were never
analyzed for their ability to synthesize storage compounds so
far. Further studies have to be done in this field to fortify the
presented conclusions. Continuative research may focus on
database search and detection of genomic evidences for lipid
accumulation in desert bacteria. The occurrence of genomic
homologs of the wax ester synthase/acyl coenzyme A
(acyl-CoA):diacylglycerol acyltransferase (WS/DGAT; AtfA)
in so-called non-accumulative species for example provides
support for TAG/WE accumulation (Stveken et al. 2005).
Suitability of desert bacteria for industrial feedstock
production
Taken together, especially arid habitats with hot climate ap-
pear to offer convenient conditions for bacterial lipid accumu-
lation. Five of six studies comprising 20 to 50% lipid-
accumulative strains provide support for hot deserts as prom-
ising locations of new strains, which are able to accumulate
PHA, TAG, or WE (Fig. 2). Humid habitats and arid habitats
with cold climate seem to be less favorable for lipid-
accumulative bacteria. Only 520% lipid-accumulative strains
were found in four of five studies with bacterial communities
from humid soil (Fig. 4) and even less in studies with com-
munities from cold desert soil (<20%; Fig. 3).
Nevertheless, the differences between the occurrence of
lipid-accumulative species in hot arid habitats and humid hab-
itats are smaller than expected. Differences in the extent of
lipid accumulation may explain this observation. Hot desert
species are assumed to accumulate larger amounts of lipids
per gram cell dry weight than humid soil species. Only few
investigations were done on this aspect in the literature. Rttig
and coworkers analyzed some strains from hot desert habitats
and their ability to store PHA, TAG, and WE (Rttig et al.
2016). Furthermore, Bequer Urbano and coworkers found 12
strains with the distinct ability to store TAG or WE in period-
ically desiccated high-altitude lakes (Bequer Urbano et al.
2013). An explicit comparison of these species and their ex-
tent of lipid accumulation with non-extremophilic bacteria
may be helpful.
If especially hot desert species produce a high cellular lipid
content, focusing on these habitats will save time and money

Fig. 4 Occurrence of compound-accumulative bacteria in humid and
nutrient-rich soil samples. Bacteria were classified into lipid-
accumulative species (black), other compound-accumulative species
(dark gray), lipid- and other compound-accumulative species (medium
gray), and non-accumulative species (light gray). a Sample with 61
cultivated species from compost (Boulter et al. 2002). b Sample with
during the search for effective production strains. However,
(hot) desert bacteria are difficult to cultivate under laboratory
conditions. They are highly specialized on desert environment
and may be dependent of non-standard cultivation conditions.
Lacking knowledge of the bacterial metabolism and special-
ized genetic regulation might also contribute to it. Hence, their
suitability for cultivation with established methods will be a
limiting factor for industrial use. As it can be seen in the
evaluated studies from cold desert habitats, this problem al-
ready appears during the first cultivation. Many prokaryotic
microorganisms found there are referred to as Buncultivated^
species. It might result from too complex cultivation proce-
dures under laboratory conditions. On the other hand, a few
lipid-accumulative desert species are already playing a role in
the current research. R. jostii RHA 1 for example can be cul-
tivated under laboratory conditions and is able to produce
evident amounts of storage lipids (Hernndez et al. 2008).
Streptomyces sp. G25 was found to accumulate nearly 50%
(w/w) fatty acids of its cell dry weight and Streptomyces sp.
G49 and Rhodococcus sp. A27 nearly 30% (w/w) after culti-
vation with conventional methods (Rttig et al. 2016).
Nevertheless, salt-rich soils as habitats of lipid-accumulative
species are suggested for closer examinations. As mentioned
Appl Microbiol Biotechnol
21 cultivated species from tropical soil, Vietnam (Boyandin et al.
2013). c Sample with 18 cultivated species from compost (Fracchia
et al. 2006). d Sample with 37 cultivated species from an European wheat
field (Smit et al. 2001). e Sample with 20 cultivated species from the
rhizospere in Indonesian soil (Widawati 2005)
above, it may promote bacterial lipid accumulation similar to
arid environment (Alvarez et al. 2004). However, species from
salt-rich locations may possibly be much easier to cultivate than
species from desert locations.
In summary, new applicable strains must show not only
efficient lipid accumulation but also suitability for large-
scale cultivation. Comparison of hot deserts as the most prom-
ising habitats in the presented analysis and salt-rich habitats as
possible alternative is supposed to give a convenient environ-
ment for the search after lipid-accumulative bacteria. Highly
effective screening techniques are thereby required to facili-
tate fast selection of eligible strains.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval This article does not contain any studies with animals
or human participants performed by any of the authors.
Appl Microbiol Biotechnol
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