Lipid Degrading Bacteria and Their Biotechnology Application:
Review of Present Scenario
http://www.journals.elsevier.com/journal-of-bioscience-and-bioengineering/
Aqsad Rashda*, Tahir Iqbal, Muhammad Kaleem Sarwar, Muhammad Nadeem
Abbas, Fareeha Azam, Iqra Azam and Waheed Iqbal.
*Aqsad Rashda (Corresponding author)
Department of Zoology, University of Gujrat
Department of Zoology, University of Gujrat, Punjab, Pakistan
Tel: 03068723540 E-mail: aqsadrashda@gmail.com
Abstract
Lipids are long chain fatty acids that offer wide applications for mankind.
When released in environment, most of the forms of lipids undergo degradation. This
review paper is intended to provide an overview about the microbial lipid
degradation. Lipolytic enzymes mainly lipases have been explained here. Many
microbial lipase-producing strains are reviewed along with the main substrates and
factors affecting lipid biodegradation. Finally, some important applications of
lipolytic bacteria and lipases have been discussed.
Key words: Lipolytic Bacteria, Bacterial lipases, conditions for lipid biodegradation,
lipase applications.
1. Introduction
Lipids are long chain fatty acids that are bonded to glycerol, alcohols or other
groups by an ester or ether linkage. These are classified into two main groups, Fats
and oils that have the alcohol groups esterified with fatty acids, mostly in the form of
triglycerides (Alves et al., 2009). Due to unique physiochemical properties, specific
chemical composition and properties, lipids have been utilized as foods, fuels and
lubricants. There are various sources of lipids such as vegetable, animal, and marine
sources (Aluyor et al., 2009). But on the other hand lipids like fats, greases and oils
are dominant organic matters present in municipal and some industrial wastewater,
causing severe environmental pollution (Prasad and Manjunath, 2011). However,
when discharged in the environment, lipids undergo degradation. One of the
promising degradation methods - Microbial degradation - of oil wastewater is a major
interest in recent years (WU Lanet al., 2009). Various microorganisms such as
bacteria, yeasts and molds have been observed capable of degrading oil waste water
completely (Ammar et al., 2005; Dhouib et al., 2006; Erguder et al., 2000; Ettayebi et
al., 2003; Kissi et al., 2001).
Microbial degradation and hydrolysis of lipids requires specific lipolytic
enzymes which are called Lipases. Lipases are serine hydrolases of appreciable
physiological significance and industrial potential to catalyze various reactions such
as hydrolysis, esterification, interesterification, aminolysis and alcoholysis (Jaeger
and Eggert, 2002). Microbial lipases have been produced by fungi, yeasts and bacteria
as intracellular, extracellular and cell-bound enzyme (Bhumibhamon et al., 2002).
The yeast, Candida deformans produces extracellular lipase of great biotechnological
importance (Muderwa and Ratamahenina, 1985).
microorganisms
are
inhabitants
of
different
These lipase producing
environmental
niches.
These
microorganisms have been isolated from a variety of sources and degrading efficiency
has been studied both as single culture and mixed culture formula (Bhumibhamon et
al., 2002)
This paper examines the biodegradation of lipids specifically by using
bacterial lipase and the applications of these lipase-producing bacteria in environment
as well as in industry processes.
2. General properties of lipids
Lipids are essential to all living organisms, like other organic compounds they
have specific properties due to their chemical composition. Fats and oils consist of
mixtures of fatty acid esters of the trihydroxy alcohol or glycerol (Nwobiet al., 2006).
Thus the physical properties of fats and oils depend on the nature of fatty acids
involved in the ester formation (Aluyor et al., 2009). Triglyceride is an important
component of natural oil or fat which can be hydrolyzed into diacylglycerol,
monoacylglycerol, glycerol, and fatty acids. Glycerol and fatty acids are largely used
as raw materials, for instance, monoacylglycerol is employed as an emulsifying agent
in the cosmetics, food and pharmaceutical industries (Karigar and Rao, 2011).
.
3. Lipases
Enzymes are biological catalysts that are involved in the conversion of
substrates into products by lowering the activation energy of the reaction (Karigar and
Rao, 2011). Microbial enzymes are generally considered more useful than the
enzymes derived from animals or plants due to the great variety of catalytic activities
available, ease of genetic manipulation, high yields possibility, regular supply due to
absence of seasonal fluctuations and rapid growth of microorganisms on inexpensive
media (Iftikhar & Hussain, 2002; Iftikhar et al., 2003; Iftikhar et al., 2010b). Lipids
are hydrolyzed or degraded by specific lipolytic enzymes. Lipases are the major
lipolytic enzymes found in bacteria and offer wide range of applications. They
catalyze both the hydrolysis and the production of poorly soluble or insoluble longchain triacylglycerols having an acyl chain length of ≥ 10 carbon atoms depending
upon the availibility of water (Gupta et al., 2004). Thus generating free fatty acids,
mono and diacylglycerols and glycerol (Lutz, 2004; Kempka et al., 2008) (Fig. 1).
Lipases are produced by both prokaryotes such as bacteria and archaea and
eukaryotes, including animals, plants and fungi (Wang et al., 2008).
Among microbial lipases, bacterial lipases are most important. These are
normally produced in the presence of oil or any other lipidic substrate, like fatty acids,
fatty acid esters and glycerol, as carbon source along with the presence of any
complex nitrogen source (Gupta et al., 2004). These are generally extracellular and
are greatly affected by physicochemical and nutritional factors, such as temperature,
pH, carbon and nitrogen sources, inorganic salts, dissolved oxygen concentration and
agitation (Gupta et al., 2004).
Filamentous fungi, especially Rhizopus, Aspergillus, Mucor, Fusarium
,Penicillium and Humicola, produce lipases with good lipolytic activities, besides
bacterial sources ( Alves, 2002; Fuglsang, 2007).
Lipase producing microorganisms have been isolated from various habitats
and sources such as industrial wastes, dairy plants, vegetable oil processing factories
and soil contaminated with oil (Sharma et al., 2001).
4. Lipases Producing Microorganisms
Bacteria - Various species of bacteria showing lipolytic activity have been isolated
and characterized. Table 1 shows source and lipid biodegradation activities of some
recently identified bacterial strains. Matsumiya et al., (2007) reported the isolation of
microorganisms that degrade lipids from a variety of environmental sources for the
construction of waste water treatment system containing lipids. Among the isolated
strains, Burkholderia sp. DW2-1 showed maximum rate of degradation of 1% (w/v)
salad oils.
Płaza et al., (2008) investigated biodegradation of crude oil and 7 diverse
distillation products by Alcaligene spiechaudii SRS and Ralstonia picketti SRS.
Crude oil degradation was above 80% after incubation of 20 days for both strains and
their mixture.
Čipinytė et al. (2009) screened grease wastes utilization microorganisms. Five
strains (UP2, F2, E13, Kl1 and N3) showed lipolytic activity and rapidly degraded
olive oil and sunflower oil, tallow and lard. Two of these strains identified as
Enterobacter aerogenes E13 and Arthrobacter sp. N3 were found to have the highest
lipase activity and the more intensive rates of the degradation of saturated (stearic and
palmitic) and unsaturated (linoleic and oleic) fatty acids and triglycerides containing
these fatty acids. Mixed culture of these strains E. aerogenes E13 and Arthrobacter
sp. N3 grown on mineral medium containing 0.5% of sunflower oil produced
monoglycerides, diglycerides and free fatty acids. According to this research, the
mixed culture of strains E. aerogenes E13 and Arthrobacte rsp. N3 may be applicable
for an effective grease waste reduction.
Prasad and Manjunath (2011) carried out studies on biodegradation of high fat
and oil wastewater by lipase producing bacteria such as Bacillus subtilis, B.
licheniformis, B. amylo liquefaciens, Serratia marsescens, Pseudomonas aeruginosa
and Staphylococcus aureus in wastewater released from palm oil mill, slaughter
house, dairy, soap industry and domestic wastewater with both individual and mixed
culture (consortia). After 12 d of BOD and lipid content was observed to be decreased
in consortia (Table 1).
Fungi - Most commercially valuable lipase-producing fungi belong to the genera
Rhizopus sp., Penicillium sp., Aspergillus sp., Mucor sp., Geotrichum sp., and
Rhizomucor sp. (Thakur, 2012). Vishnupriya et al. studied the lipase production by
Sterptomyces grisesus and obtained maximum enzyme activity of 51.9U/ml. Fungal
lipase production varies according to the strain, cultivation conditions, composition of
the growth medium, temperature, pH, and the kind of carbon and nitrogen sources
(Cihangir and Sarikaya, 2004).
Due to increasing industrial demands of new lipases, isolation and
identification of lipase producing fungi has also been reported in many studies.
Kaushik et al. (2006) documented the production of an extracellular lipase from
Aspergillus carneus. In another study WU Lanet al. (2008) checked the capability of
Yarrowia lipolyticaW29 immobilized by calcium alginate to degrade oil, this species
might be employed to a wastewater treatment system for the removal of oil. Further
studies have reported other lipase producing fungal species such as Aspergillus niger
(Ellaiah et al., 2004) Rhizopus arrhizus (Yang et al. 2005), Rhizopus sp. (Bapiraju et
al., 2005), Penicillium restrictum (Azeredo et al., 2007), Penicillium simplicissimum
(Vargas et al., 2008) and Sterptomyces grisesus (Vishnupriya et al., 2010) (Table 2).
5. Genes Encoding Lipases
With the advancements of modern technologies, genes encoding lipases in
various microorganisms have been identified. As lipase is considered as the key
enzyme to degrade lipids, it is encoded by lipA gene. LipA gene has been reported in
many studies. Long et al. (2007) detected lipA gene in Serratia marcescens
ECUCU1010. Moreover, Sl LipA was isolated from Serratia liquefaciens S33 DB-1
which can degrade C18 of fatty acid (Yao et al., 2007).The lipase gene (LipA) and
lipase chaperone-encoding genes (LipB) of strain Acinetobacter calcoaceticus RAG1has been cloned and sequenced (Sullivan et al., 1999). The gene coding for an
extracellular lipase of genus Bacillus has been cloned using PCR techniques. The
length of gene has been found to be 639 bp, encoding a peptide of 212 amino acids of
molecular mass of 19353 Da, and pI 9.28 (Rabbani et al., 2009).
The yeast Yarrowia lipolytica assimilates hydrophobic substrates, such as
alkanes, fats, oils and fatty acids, by the activation of different enzymes such as
lipases/esterases (LIP genes),
peroxisomal acyl-CoA oxidases (POX genes) and
cytochromes P450 (ALK genes) (Darvishi, 2012) . In this species, LIP2 gene
(GenBank AJ012632) encodes extracellular lipase.
Conditions for Lipid Degradation
Various factors may tend to increase or the decrease the rate of lipid
biodegradation. Most important factors are temperature and pH. Temperature has a
significant role in controlling the nature and efficiency of microbial degradation of
hydrocarbons (Leahy and Colwell, 1990). Degradation of long chain alkanes by
mesophiles at temperatures between 25 and 28 °C has been extensively studied
(Mishra et al. 2001). Bacillus cereus N-09 strain shows maximum degradation of
lipids and detergents at temperature of 30 °C, pH 6.00, and agitation speed of 130rpm
(Hidayat, 2011). Table 2 shows the optimized conditions for some lipolytic bacterial
strains. Sugimori et al., (2013) investigated capability of soil bacterium, Raoultella
planticola strain 232-2 for vegetable oil, lard, and beef tallow degradation under in
acidic environment. Highly effective degradation rate was observed at 35 °C and pH
4.0, and the 24-h degradation rate was 62.5 ± 10.5 % for 3,000 ppm mixed lipids.
Lipolytic activity of bacteria can be enhanced in the presence of exogenous
surfactants. Karpenko et al. (2006) reported the acceleration of oil degradation by
genus Rhodococcus in the presence of exogenous surfactants that has been produced
by Pseudomonas sp.
Various bacterial species capable of growing at high temperatures have also
shown lipolytic activities such as a novel oil degrading bacteria identified as
Pseudomonas aeruginosa has been isolated from hot spring, inhabiting at temperature
ranges between 15°C and 55°C (Hasanuzzaman et al., 2004).
At present, microorganisms such as Bacillus sp. strain 398 (Kim et al., 1994),
Bacillus thermocatenulatus (Schmidt-Dannert et al., 1994), Bacillus sp. strain A30-1
(Wang et al., 1995), Bacillus thermoleovorans ID-1 (Lee et al., 1999), Bacillus sp.
THL027 (Dharmsthiti and Luchai, 1999), Bacillus spp. (Handelsman et al., 1994;
Llarch et al., 1997; Becker et al., 1997; Nawani et al., 1998), Bacillus sp. RSJ-1
(Sharma et al., 2001) have been reported as thermostable lipase producers. As
thermophilic bacterial strains have an optimum growth temperature of 65–70°C,
lipases isolated from such strains are good candidates for lipid modifications
(Sigurgísladóttir et al., 1993) (Table 3).
6. Applications of lipids degrading bacteria
Lipases are widely present in nature, but only microbial lipases are
commercial significance (Kasra-Kermanshahiet al., 2011).
Bacterial lipases are greatly utilized in food and dairy industry for milk fat
hydrolysis, flavor enhancement, cheese ripening, and lipolysis of cream and butter fat
(Falch, 1999). Lipases are also used in textile industry to enhance fabric absorbency
(Sharma et al., 2001),in detergent industry as additive or supplement in washing
powder (Fuji et al., 1986) , for various transesterification reactions ( Fariha et al.,
2006) and for synthesis of biodegradable
compounds or polymers ( Linko et
al.,1998).
Simultaneously, the enzyme is being employed in paper and pulp industry
(Bajpai, 1999), as a catalyst for manufacturing various products used in cosmetic
industry (Eugene, 1974), in biodiesel synthesis (Noureddini et al., 2005), in
pharmaceutical industry (Higaki and Morohashi, 2003) and in degreasing of leather
(Nakamura and Nasu, 1990).
In recent years, microbial degradation of oil containing wastewater is an
important concern (Lan et al., 2009). The utilization of lipase producing
microorganisms into wastewater treatment system for the degradation of fat and oil is
an interesting strategy (Bhumibhamon, 2002). Various microorganisms such as
bacteria, yeasts and molds have been observed to be capable of completely degrading
oil wastewater (Ammar et al., 2005; Dhouib et al., 2006; Erguder et al., 2000;
Ettayebi et al., 2003; Kissi et al., 2001). These microorganisms can be applied on
industrial as well as domestic wastewater
lipids.
containing lipids, in order to remove
Mongkolthanaruk and Dharmsthiti (2002) formulated a mixed bacterial
culture comprising of Pseudomonas aeruginosa LP602 and Acinetobacter
calcoaceticus LP009, for use in treatment of lipid-rich wastewater.
Oil spills are causing major hazards to the environment. Petroleum fuel spills
from tank failure, pipeline ruptures, different production storage and transportation
accidents are speculated as the most frequent organic pollutant of soil and aquatic
environment and have been grouped as hazardous wastes due to their cytotoxic,
carcinogenic and mutagenic effects on human (Margesin et al., 2003; Rahman et al.,
2002). Oil degrading bacteria have been used to clear up oil spills.
According to Kasra-Kermanshahi et al. (2011) lipase of P. aeruginosa KM110
is possibly an alkaline lipase and a candidate for various industrial applications such
as leather, detergent and fine chemical industries.
Extracellular lipase of Pseudomonas fluorescens KE38, is a candidate for
industrial applications due to its high stability, wide substrate specificity and cold
temperatures activity in the presence of organic solvents, and metal ions (Adan
Gokbulut and Arslanoglu, 2013).
Lipases have also found versatile applications in pharmaceutical industry.
Specifically, preparation of homochiral compounds being used against HIV and
synthesis of alkaloids, anti-tumor agents, vitamins and antibiotics are fundamental
applications of lipases (Jaeger and Eggert, 2002).
Furthermore, bacterial lipase treatment has been found to intensify the
designing of cotton fabrics (Lange, 1997 and Buchert et al., 2000). Bacterial lipases
have been analyzed for the efficiency as a scouring agent for raw cotton fabrics in
order to eliminate the natural hydrophobic substances found in the fiber (Raja et al.,
2012).
Biodiesel has been considered the most effective energy alternative.
At
present biodiesel has been commercially carried out using alkaline catalyst. Lipases
have been found to be active in transesterification process leading to production of
biodiesel, which may be proved to be environmental friendly and economical. This
involves use of immobilized lipases through various techniques (Jegannathan et al.,
2008).
Limitations of the industrial usage of these enzymes have chiefly been owing
to their high production costs, which may be reduced by molecular technologies, thus
enabling the production of these enzymes at high levels and in a virtually purified
form (Houde et al., 2004) (Table 5).
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Tables:
Table 1. Sources and lipolytic activities of bacterial strains
Source of Bacteria
Bacterial Strain
Sources of Carbon
Bacillus stearothermophilus
SB-1
Neem oil
Bradoo et al. (1999)
Bacillus licheniformis SB-3
Neem oil
Bradoo et al.(1999)
Icelandic hot spring
Bacillus thermoleovorans
IHI-91
Olive oil (triolein)
Palm oil mill effluent
Geobacillus zalihae T1T
Olive oil
Oil polluted soil
Burkholderia sp. Y1
1%
AlcaligenespiechaudiiSRS
Salad oil
Degree of
degradation
93%
Reference
Markossian et al. (2000)
Rahman et al. (2007)
83.1%
Muraoka et al.(2008)
Crude oil
80%
Płaza et al. (2008)
RalstoniapickettiSRS
Crude oil
80%
Płaza et al. (2008)
Oil contaminated soil
Enterobacteraerogenes E13
0.5% of sunflower
oil
Soil
Burkholderia cepacia. S31
Oil contaminated soil
Staphylococussps
1% olive oil
Barbeque oilcontaminated soil
Burkholderia cepacia
Peanut oil
10.5 U mL−1
Ma et al. (2010)
Slaughter house
S. aureus
Slaughter house
320 mg/L
Prasad and Manjunath, (2011)
Olive oil
Čipinytė, (2009)
226.1 u/ml
Lu et al. (2009)
Sirishaet al. (2010)
wastewater
wastewater
Food wastewater
Bacillus sp N-09
Noodles soup+LAS
73.5%
Hidayat, (2011)
Palm oil effluent
P. aeruginosa
Palm oil effluent
325 mg/L
Prasad and Manjunath, (2011)
Dairy effluent
S. marsescens
Dairy effluent
280
Prasad and Manjunath, (2011)
Oil processing plant
Pseudomnasaeruginosa
KM110
2 % Olive oil
Kasra-Kermanshahi et al. (2011)
Oil mill effluent
Bacillus sp .
Oil mill effluent
Mukesh et al . (2012)
Oil mill waste
Bacillus tequilensisNRRL B- Oil mill waste
41771
Kalyana et al . (2013)
Soil samples
Pseudomonas fluorescens
KE38
Adan and Arskanoglu, 2013
1% olive oil
mg/L
Table 2: Characteristics of Lipid degrading Fungi:
Fungal species
Medium
Optimal Conditions
Reference
Penicillium citrinum
5% peptone, 2% starch and
22°C and pH 7.2
Sztajer and Maliszewska, (1989)
Rapeseed oil
Rhizopus delemar
-
30°C and pH 8-8.5
Haas et al. (1992)
Ophiostoma piceae
Plant oils (Olive oil)
37°C and pH 5.5
Gao and Breuil, (1995)
30°C and pH 9
Hoshino et al. (1997)
40–50 °C and 1 h
Pollero et al. (2001)
30°C and pH 5
Bancerz et al. (2005)
Typhula ishikariensis group III, p-nitrophenyl palmitate
strain 6-1-1
Phoma glomerata
Triacylglycerol,
Phosphoglyceride and
Cholesterol ester
Penicillium chrysogenum 9’
Natural oils
Colletotrichum gloesporioides
Natural oils
Aspergillus oryzae
Rice hulls,Tween 80 and
-
Colen et al. (2006)
Romano et al. (2007)
olive oil
Paecilomyces
nostocoides Monoacylglycerols
Huang et al. (2009)
NTU-FC-LP01
Penicillium simplicissimum
Castor bean seeds waste
45°C and pH 6.5
Godoy et al. (2011)
Table 3. Optimized conditions for some lipolytic bacterial strains:
Strain
Optimized Conditions
Temperature
pH
References
Bacillus stearothermophilus SB-1
50 °C
3
Bradoo et al., 1999
Bacillus licheniformis SB-3
50 °C
3
Bradoo et al., 1999
Bacillus thermoleovorans IHI-91
65°C
6
Markossian et al., 2000
Geobacillus zalihae T1T
70°C
-
Rahman et al. (2007)
Burkholderia cepacia. S31
70 °C
9
Lu et al. (2009)
Staphylococussps
36°C
7
Sirishaet al., 2010
Burkholderia cepacia
37°C
8
Ma et al. (2010)
Pseudomnasaeruginosa KM110
45°C
7-10
Bacillus sp N-09
30°C
6
Hidayat, 2011
Bacillus sp .
35°C
8
Mukesh et al ., 2012
Bacillus tequilensisNRRL B-41771
34°C
7
Kalyana et al ., 2013
Pseudomonas fluorescens KE38
45 °C
8
Adan and Arskanoglu, 2013
Kasra-Kermanshahi et al., 2011
Table 5. Applications of lipid degrading fungi and bacteria
Industry
Chemical (waste)
Leather industry
Lipidic
Fungal or bacterial strains
used
Saccharomyces cerevisiae
Degree of degradation
Reference
2749 U mg−1
Teles et al. (2001)
concentrate of
sheep fleshing
Food-processing
Rhizopus oryzae
Petrobras Research Center
Toxic and alkaline
using castor bean seeds
waste
Leather, detergent and
Penicillium simplicissimum
P. aeruginosa KM110
chemical industries
Oil mill wastewater
López et al. (2010)
155.0 U/g after 96 h
Godoy et al. (2011)
Kasra-Kermanshahi et al.
(2011)
Fatty acids and
Yarrowia lipolytica
Fickers and Nicaud, 2013
Yarrowia lipolytica
Fickers and Nicaud, 2013
triglycerides
Food industry
Grease
Figures:
Fig. 1. Hydrolytic and Synthetic Actions of Lipase (Source: Jaeger and Reetz 1998)