Isolated Microorganisms for Bioconversion of Biodiesel-Derived

REVIEW ARTICLES

Isolated Microorganisms for Bioconversion of Biodiesel-Derived Glycerol Into 1,3-Propanediol Laura MITREA1, Lavinia-Florina CĂLINOIU1, Gabriela PRECUP1, Maria BINDEA1, Bogdan RUSU1, Monica TRIF1, Bianca-Eugenia ŞTEFĂNESCU1,2, Ioana-Delia POP1,3 , Dan-Cristian VODNAR1*

Department of Food Science, Life Science Institute, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, 3-5 Calea Mănăştur Street, Cluj-Napoca 400372, Romania. 2 Department of Pharmaceutical Botany, Iuliu Hațieganu University of Medicine and Pharmacy, 12 I. Creangă Street, Cluj-Napoca 400010, Romania. 3 Department of Exact Sciences, Horticulture Faculty, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, 3-5 Calea Mănăştur Street, Cluj-Napoca 400372, Romania. * Corresponding author, e-mail: [email protected] 1

Bulletin UASVM Food Science and Technology 74(2)/2017 ISSN-L 2344-2344; Print ISSN 2344-2344; Electronic ISSN 2344-5300 DOI: 10.15835/buasvmcn-fst: 0014

ABSTRACT

During biodiesel production, massive amounts of raw glycerol are created generating an environmental issue and the same time an increase of biodiesel production cost at the same time. This raw glycerol could be converted by specific strains into value-added products, like 1,3-propanediol (1,3-PD), an important monomer used in the synthesis of biodegradable polyesters. The present work is based on recent scientific articles and experimental studies on the targeted topic, namely on the use of bacterial strains for bioconversion of biodiesel-derived glycerol into valuable products, like 1,3-PD. Concentrations, yields and productivity of 1,3-PD are presented for various bacterial strains. Important results as respects the microbial bioconversion of biodiesel-derived glycerol into 1,3-PD were registered for strains like Klebsiella pneumoniae, Citrobacter freundii, Escherichia coli and Lactobacillus diolivorans. From this study can be concluded that waste glycerol may be used as a nutrient source for microbial development and the production of 1,3-propanediol with high concentrations and yields. Keywords: 1,3-propanediol, bioconversion, biodiesel, microorganisms, raw glycerol

INTRODUCTION

Nowadays, the biofuels requirement has been increased mainly because of the crude oil reserves deficiency. Biodiesel, which is a wellknown biofuel, is produced from vegetable oils, animal fats, or recycled greases (Drożdżyńska et al., 2011; Kong et al., 2016). Biodiesel is presented as alkyl esters long chains, formed during the transesterification reaction of triglycerides with an alcohol, resulting in crude glycerol as the principle by-product (Chen et al., 2017; Garlapati et al., 2016). According to the literature, a general ratio between the biodiesel production and the generated residual glycerol underlines that one part of raw glycerol is produced for every 10 parts

of biodiesel (Drożdżyńska et al., 2011; Galea et al., 2016). With other words, the biodiesel synthesis generates about 10% (w/w) of crude glycerol from the total biodiesel production (Leoneti et al., 2012; Mu et al., 2008). Both biodiesel and crude glycerol can be produced by two ways: (1) hydrolytically from oils and fats by soaps and fatty acids production, and by (2) transesterification of fats or oils with alcohol in the presence of a catalyst. The catalyst could be acid, base, or enzyme. Mostly used catalyst is NaOH or KOH (Mu et al., 2008; Pagliaro and Rossi, 2008). After a proper purification, biodiesel derived glycerol can be used in various applications (Konstantinović et al., 2016). From

44

MITREA et al.

the chemical point of view, glycerol molecules are small, uncharged and can pass easily through the cytoplasmic membrane in different microbial cells. On this way, multiple microorganisms can use glycerol as carbon source, because of the fact that glycerol can be metabolized both oxidatively and reductively inside the microbial cell. In conclusion, numerous chemical compounds could be obtained through microbial glycerol fermentation process (e.g. propionic acid, succinic acid, butanol, 1,3-propanediol (1,3-PD), dihydroxyacetone etc.) (Cătoi et al., 2006; Cătoi et al., 2013; Hejna et al., 2016; Vodnar et al., 2013). 1,3-Propanediol represents an important pro duct that can be obtained through waste glycerol fermentation. 1,3-PD is a chemical compound especially used in the synthesis of biodegradable plastic materials, as polytrimethylene terephtha late (PTT) which holds better environmental qualities than many other plastic materials, like polyethylene terephthalate (PET) or polybutylene terephthalate (PBS) (Biebl et al., 1999; Mu et al., 2008; Zheng et al., 2017). Recent studies reveal that 1,3-PD can be used in food and beverage industries also for its capacity to modify the flavor and tastes profiles (Dierbach et al., 2013). New concepts are intensely studied for 1,3-pro panediol natural production. The utilization of microorganisms to produce 1,3-PD from crude glycerol represents a hot topic in terms of research work. A various number of microorganisms can grow anaerobically on glycerol, as energy and nutrient source. By now, a couple of bacterial strains acting as biocatalysts are used and well investigated for the production of 1,3-propanediol (e.g. K. pneumoniae, K. oxytoca, K. planticola, C. freundii, E. coli, L. diolivorans etc. (Mu et al., 2008; Pflügl et al., 2012).

ISOLATED STRAINS USED FOR THE PRODUCTION OF 1,3-PROPANEDIOL

Recent scientific articles and experimental studies on the targeted topic were investigated for this work. Several strains from different genres (e.g. Klebsiella, Citrobacter, Clostridium, E. coli, Lactobacillus) were evaluated for their potential to metabolize the biodiesel waste glycerol and to produce 1,3-propanediol. 1,3-PD PRODUCTION BY KLEBSIELLA STRAINS K. pneumoniae a strain from Enterobacteriaceae family, gives good results in 1,3-PD production. A Bulletin UASVM Food Science and Technology 74(2) / 2017

study presented by Rossi et al. (2012) shows that Klebsiella pneumoniae BLh-1 gives fine outcomes regarding the degradation of raw glycerol. The fermentation from this study was performed during 32h of cultivation in anaerobic conditions in a controlled bioreactor. The production of 1,3-propanediol registered a concentration of 19.9 g/L, and a theoretical yield of 0.72 mol 1,3-PD/mol glycerol. Same authors point that K. pneumoniae BLh-1 strain produces similar results when pure glycerol is used as a nutrient substrate. The production of 1,3-PD in this case was about 22.8 g/L, and a yield of 0.68 mol product/mol glycerol (Rossi et al., 2012). The metabolic network of 1,3-propanediol production in Klebsiella pneumoniae was analyzed by Zhang and Xiu (Zhang and Xiu, 2009). From the metabolic point of view, K. pneumoniae is a versatile strain which is able to develop in both the absence and the presence of oxygen. From previous reports it can be observed that microbial production of 1,3-propanediol is always ran under anaerobic conditions (Menzel et al., 1997; Mu et al., 2008). Zhang and Xiu noticed that a great yield (theoretical optimal yield: 0.844 mol/mol) could be obtained if the PPP (pentose phosphate pathway) is exploited and the transhydrogenase has an elevated stream under anaerobic condition (Zhang and Xiu, 2009). Da Silva et al. (2015) investigated another Klebsiella strain for its capacity to use raw or pure glycerol as carbon source. They tested the effects of some parameters like pH, temperature and stirrer speed on the conversion of glycerol into 1,3-propanediol by K. pneumoniae strain GLC29. Regarding both production and productivity of 1,3-propanediol, the best conditions for the bioconversion of glycerol were as follows: pH 6.9–7.1, temperature 33°C to 38.5°C, stirrer speed 110 to 180 rpm, glycerol concentration between 39–49 g/L. Batch fermentation was conducted at pH of 7.0, temperature of 35°C, stirrer speed of 150 rpm, and glycerol concentration of 40 g/L. Under these conditions were produced 20.4 g/L of 1,3-PD, with a maximal volumetric productivity of 2.92 g/L/h and a yield of 0.51 g/g. During the process were obtained some byproducts, like acetic acid (about 7.0 g/L) and formate (about 3.7 g/L). From this study can be concluded that K. pneumoniae strain GLC29 showed a good potential for the bioconversion of glycerol into 1,3-PD, with

Isolated Microorganisms for Bioconversion of Biodiesel-Derived Glycerol Into 1,3-Propanediol

an increased production and productivity (Da Silva et al., 2015). In a study performed by Garlapati et al. (2016) was reported that Klebsiella oxytoca has the ability to transform crude-glycerol into 1,3-PD under fed-batch and batch fermentation conditions, registering a yield and a productivity from 0.41 to 0.53 g/mol, respectively from 0.63 to 0.83 g/L/h (Garlapati et al., 2016). In a recent paper (Yang et al., 2017) Klebsiella pneumoniae ATCC 8724 has been thoroughly investigated under both batch and repeated experimental trials, for its potential to use the waste glycerol for 1,3-propanediol production. This strain was tested under both batch and repeated batch fermentation, under aerobic and anaerobic conditions. The cultivation outcome points that aerobic regimes gave lower results than the anaerobic one. The waste glycerol used in a concentration of 60 g/L consisting in 2% (w/v) impurities (salts: NaCl, KCl) at a pH of 8, exerted important inhibitory effects during batch fermentation. Good results were registered for the final 1,3-PD yield (up to 0.65 mol/mol), when the content of salts from the medium was below 1% (w/v) during batch cultivation. More than that, repeated fermentation trial was demonstrated with immobilized cells, by using biodiesel-derived glycerol as substrate. After five cycles of batch cultivation, 83% of 1,3-PD was reached, comparing with the first cycle of fermentation. The highest value for the concentration and the yield of 1,3-propanediol were achieved at the second cycle cultivation, respectively 20 g/L and 0.64 mol/mol (Yang et al., 2017). 1,3-PD PRODUCTION BY CLOSTRIDIUM STRAINS Clostridium species were identified as potential producers of 1,3-propanediol. For example, Clostridium butyricum strain F2b was tested by different research groups (Papanikolaou and Aggelis, 2003; Papanikolaou et al., 2004; Papanikolaou et al., 2008) for its ability to use crude glycerol as a nutrient substrate. This particular strain was cultivated on raw glycerol in batch and single-stage continuous cultures, and it was noticed that the intake of an increased level of the substrate significantly influence the final concentration of 1,3-PD, by favoring the production of acetic and butyric acids (Papanikolaou et al., 2004).

45

Chatzifragkou and colab. (Chatzifragkou et al., 2010) investigated the adaptation level of Cl. butyricum strain VPI 1718 to the culture media containing raw glycerol. The strain VPI 1718 appeared to be sensitive to a particular type of impurities existing in crude glycerol, like salts (NaCl), when flask fermentation under anaerobic conditions was imposed. It was noticed that NaCl exert inhibitory effect over the cell growth, but did not influence the 1,3-PD production when batch bioreactors trials are performed. Moreover, it was shown that the presence of methanol in the culture broth did not affect the microbial conversion of 1,3-propanediol from raw glycerol (Chatzifragkou et al., 2010). The biochemical behavior of the Clostridium butyricum VPI 1718 was explored by Chatzifragkou and colleagues (Chatzifragkou et al., 2011) in different fermentation regimes. Under non-aseptic fermentation conditions, VPI 1718 strain successfully convert the crude glycerol to 1,3-propanediol (up to 69.7 g/L of the final product). During the same trial, it was observed that VPI 1718 activity is not influenced by the size and the geometry of the bioreactor, and the production of 1,3-PD is not altered by the anaerobic regimes, when N2 in infused in the fermentation vessel. Cl. butyricum VPI 1718 is a very adaptable strain to the various fermentation regimes, and it can produce 1,3-propanediol at significant concentrations by using raw glycerol as a carbon source (Chatzifragkou et al., 2011). There are several strains of Clostridium genre which are not able to metabolize the glycerol as a sole carbon source. In this regard, González-Pajuelo et al. (2006) genetically engineered a particular strain of Clostridium, namely Cl. acetobutylicum DG1 (pSPD5), to induce the ability of converting the glycerol substrate to 1,3-PD. They introduced a specific plasmid (pSPD5) which is responsible for the 1,3-PD metabolic pathway, from a good 1,3-PD producing strain like Cl. butyricum VPI 3266. The mutant Cl. acetobutylicum registered similar values to those obtained in the case of Cl. butyricum VPI 3266, for the final product, 1,3-PD (concentration: 412 mM, molar yield: 0.64) (González-Pajuelo et al., 2006). 1,3-PD PRODUCTION BY CITROBACTER STRAINS Citrobacter freundii is another promising microorganism able to produce 1,3-propanediol among strains from Enterobacteriaceae family. In a research attained by Casali et al. (2012) two Bulletin UASVM Food Science and Technology 74(2) / 2017

46

strains were compared under the potential of 1,3-PD production, namely Citrobacter freundii strain DSM 15979 and Pantoea agglomerans DSM 30077, using crude glycerol as nutrient source. The optimal concentration of raw glycerol which provided the highest 1,3-propanediol productivity, was about 40 g/L as an average concentration of 20-60 g/L used in preliminary studies. The final quantity of 1,3-PD obtained using C. freundii strain was 12.92 g/L, while 6.14 g/L was obtained for P. agglomerans strain. Both nominated bacterial strains were able to grow on raw glycerol resulting an impressive accumulation of 1,3-PD in the fermentation broths. From this report can be observed that both C. freundii and P. agglomerans are novel strains able to convert raw glycerol into 1,3-propanediol recording good concentrations and conversion yields (Casali et al., 2012). The capacity of glycerol conversion to 1,3-propanediol by Citrobacter freundii strain DSM 30040 were investigated by Boenigk et al. (1993). In their work the process was optimized in single- and two-stage continuous cultures. The productivity of 1,3-PD was raised under the limitation of glycerol and elevated with the dilution rate (D) of 3.7 g/L/h. At the end of the procedure, the optimal conditions for the twostage fermentation process were as follows: a. first stage - glycerol limitation at 250 mM, pH 7.2, D=0.1 h-1, 31°C; b. second stage - additional glycerol, pH 6.6, D = 0.05 h-1, 28 ° C. The final concentration of consumed glycerol were 875 mM, while the concentration of 1,3-propanediol was 545 mM. The moderate production of 1,3-propanediol registered 1.38 g L-1 h-1. In order to obtain a continuous production of 1,3-propanediol through the glycerol conversion, same authors pointed that it could be helpful a growth limitation by adding nitrogen or phosphate to the culture media. This fact might allow glycerol to be present excessively in the culture media leading to maximum values of 1,3-PD concentrations. Considering these growth limitations, 2.9 mM of ammonium or 0.75 mM of phosphate were added to the culture media supplemented with 0.02% yeast extract. Contrary to batch cultures, cells were extended and occurred in chains. By this time, the bacterial cells were not efficiently productive considering the 1,3-PD concentrations (Boenigk et al., 1993). The isolated strain named Citrobacter freundii FMCC-B 294 (VK-19) were studied by Metsoviti Bulletin UASVM Food Science and Technology 74(2) / 2017

MITREA et al.

et al. (2013) for its capacity of converting the biodiesel-waste glycerol into 1,3-propanediol. Their work demonstrated that crude glycerol used as a carbon source was very efficient for both C. freundii growth and 1,3-propanediol production. Their study also demonstrates that fermentation processes performed in non-sterile conditions does not influence notably the final concentration of 1,3-PD. In this respect, Metsoviti et al. (2013) obtained 68.1 g/L of 1,3-PD with an yield of consumed glycerol of 0.40 g/g and a volumetric productivity of 0.79 g/L/h during a sterile fed-batch process, and 66.3 g/L of 1,3PD were obtained from 176 g/L of raw glycerol performing non-sterilized fed-batch fermentation. From this work can be noticed that Citrobacter freundii strain FMCC-B 294 can develop and can transform efficiently biodiesel-waste glycerol into 1,3-PD under non-sterile conditions (Metsoviti et al., 2013). Several strains of Klebsiella, Clostridium and Citrobacter employed for 1,3-PD production are presented in the Table 1. 1,3-PD GENERATED BY MUTANT ESCHERICHIA COLI Mutant microbial strains for an increased production of 1,3-propanediol were investigated by Cervin et al. (2004). The authors described a genetically modified microorganism obtained by using enzymes from Klebsiella and Saccharomyces strains, combined in a single strain of Escherichia coli K12. The resulted bacterium was able to transform glucose molecules straight to 1,3propanediol registering a final concentration of 130 g/L, with a yield of 0.34 mol/mol (Cervin et al., 2004). 1,3-PD GENERATED BY LACTIC BACTERIAL STRAINS Lactobacillus strains have been found to generate important quantities of 1,3-PD. Pflügl et al. (2012) examined the capacity of Lactobacillus diolivorans DSM 14421 to consume glycerol as nutrient substrate in order to generate high amounts of 1,3-propanediol. The investigation resulted a final concentration for 1,3-propanediol of 41.7 g/L, obtained under batch fermentation conditions, while 73.7 g/L were obtained under fed-batch fermentation conditions when glycerol was co-fermented with glucose. Same authors point that the addition of a specific supplement (vitamin B12) to the fermentation media have

47


Tab. 1. Klebsiella, Clostridium and Citrobacter metabolizers of biodiesel-derived glycerol for 1,3-propanediol production (Metsoviti et al., 2013) Strain

Fermenta tion type

Klebsiella pneumoniae DSM 2026

Integrated bioproces

Klebsiella pneumoniae DSM 4799 Klebsiella pneumoniae BLh-1 Klebsiella pneumoniae SU6

Klebsiella pneumoniae GLC29 Clostridium butyricum F2b

Clostridium butyricum VPI 1718

Clostridium butyricum AKR102a

Clostridium butyricum DSM 5431 Clostridium butyricum VPI 3266

Clostridium sp. IK 124

Citrobacter freundii FMCC-B 294

Fed-batch

1,3-PD concentration (g/L)

1,3-PD yield (mol/mol)

61.1

19.9

0.51

25.0

no data

48.1

0.55

47.1

0.53

69.7

0.55

Batch

Shake flask Batch

Continuous one stage

Continuous two stages Batch Batch

Fed-batch

Fed-batch Batch

Continuous

20.4

43.5 14.1 93.7 25.0

31.5

0.45

0.72

0.51

Jun et al., 2010

Mu et al., 2008

Rossi et al., 2012

Sattayasamitsathit et al., 2011

Da Silva et al., 2015

Papanikolaou et al., 2000

0.49


1.08

Chatzifragkou et al., 2010

0.63

0.50

0.50


Chatzifragkou et al., 2011

Wilkens et al. (2012) Rehman et al., 2008

Gonzalez-Pajuelo et al., 2004

Fed-batch

80.1

0.56

Hirschmann et al., (2005)

Fed-batch

68.1

0.40

Metsoviti et al., 2013

Batch

increased the production of 1,3-propanediol to a final concentration of 84.5 g/L (Pflügl et al., 2012).

CONCLUSIONS

80.2

References

Raw glycerol can be considered a safe, costeffective, reusable and, most important, biodegradable source of carbon in the same time. These particularities make it an inherent material for the production of various value-added compounds. Lately, there is an impressive industrial interest in the production of 1,3-propanediol through microbial fermentations, moreover, this technique seems to be in competition with the traditional methods used to obtain such products. 1,3-PD represents a very important chemical product with great potential in the industry of biodegradable plastic material, and also in the industry of food. It can be concluded that raw glycerol could become an appreciated material for the production of vari-

25.6

0.51

Anand and Saxena (2012)

ous bio-chemical products, with an economic impact. The present study highlights that the microorganisms from Enterobacteriaceae family (e.g. Klebsiella, Citrobacter, Lactobacillus, E. coli) and Clostridiaceae family (e.g. Clostridium) can be nominated as significant producers of 1,3-propanediol by using raw glycerol as nutrient. Biodieselderived glycerol can be considered a valuable raw material for future applications, considering that it supplies the carbon source for bacterial development. By recovering the waste glycerol from biofuels production and valorizing it through microbial fermentation in order to gain value-added products, could lead to a positive economic and environmental impact. Acknowledgements. This work was supported by the Partnership in Priority Areas Programme-

Bulletin UASVM Food Science and Technology 74(2) / 2017

48

MITREA et al.

PNII, developed with the support of ANCSI (POC/ ID P_37_637, 2016-2020).

REFERENCES

1. Anand P, Saxena RK (2012). A comparative study of solvent-assisted pretreatment of biodiesel derived crude glycerol on growth and 1,3-propanediol production from Citrobacter freundii. N Biotechnol, 29:199–205.

2. Biebl H, Menzel K, Zeng AP, Deckwer WD (1999). Microbial production of 1,3-propanediol. Appl Microbiol Biotechnol, 52: 289-297. 3. Boenigk R, Bowien S, Gottschalk G (1993). Fermentation of glycerol to 1,3-propanediol in continuous cultures of Citrobacter freundii. Appl Microbiol Biotechnol, 38: 453– 457.

4. Casali S, Gungormusler M, Bertin L, Fava F, Azbar N (2012). Development of a biofilm technology for the production of 1,3-propanediol (1,3-PDO) from crude glycerol. Biochem Eng J, 64: 84– 90. 5. Cătoi AF, Parvu A, Muresan A, Galea RF, Cătoi C (2006). Evaluation of nitric oxide synthesis in morbid obesity. Free Radic Res. 40: S140-S140.

6. Cătoi AF, Pârvu A, Galea RF, Pop ID, Mureşan A, Cătoi C (2013). Nitric Oxide, Oxidant Status and Antioxidant Response in Morbidly Obese Patients: the Impact of 1-Year Surgical Weight Loss. Obes Surg, 23: 1858-1863. 7. Cervin MA, Soucaille P, Valle F. Process for the biological production of 1,3-propanediol with high yield. E I DuPont de Nemours & Co. Patent US 2004/0152174 A1. Available in: http://www.google.ch/patents/US20040152174.

8. Chatzifragkou A, Dietz D, Komaitis M, Zeng AP, Papanikolaou S (2010). Effect of biodiesel-derived waste glycerol impurities on biomass and 1,3-propanediol production of Clostridium butyricum VPI 1718. Biotechnol Bioeng, 107,1:75-84.

9. Chatzifragkou A, Papanikolaou S, Dietz D, Doulgeraki AI, Nychas GJE, Zeng AP (2011). Production of 1,3-propanediol by Clostridium butyricum growing on biodiesel-derived crude glycerol through a non-sterilized fermentation process. Appl Microbiol Biotechnol, 91:101–112. 10. Chen JX, Zhang XL, Yan S, Tyagi RD, Drogui P (2017). Lipid production from fed-batch fermentation of crude glycerol directed by the kinetic study of batch fermentations. Fuel, 209: 1-9.

11. Da Silva GP, De Lima CJB, Contiero J (2015). Production and productivity of 1,3-propanediol from glycerol by Klebsiella pneumoniae GLC29. Catal Today, 257: 259–266.

12. Dierbach LA, Barber DD., Li H-C, Topinka JB, Zeller BL, High R (2013). Food and beverage products containing 1,3-propanediol and methods of modifying flavor release using 1,3-propanediol. Patent WO 2013134607 A1. Available in http://www.google.com/patents/ WO2013134607A1?cl=en. 13. Drożdżyńska A, Leja K, Czaczyk K (2011). Biotechnological production of 1,3-propanediol from crude glycerol. BioTechnologia. 92(1): 92-100. 14. Galea RF, Cătoi AF, Pop E, Mironiuc A, Chiorescu S, Mihăileanu F, Grad O, Mircioiu D (2016). The Importance Bulletin UASVM Food Science and Technology 74(2) / 2017

of Dynamic Upper Gastrointestinal Barium X-Ray Examination in Bariatric Surgery. 20TH WORLD CONGRESS. 97-103.

15. Garlapati VK, Shankar U, Budhiraja A (2016). Bioconversion technologies of crude glycerol to value added industrial products. Biotechnol Rep, 9: 9–14. 16. Gonzalez-Pajuelo M, Andrade JC, Vasconcelos I (2004). Production of 1,3-propanediol by Clostridium butyricum VPI 3266 using a synthetic medium and raw glycerol. J Ind Microbiol Biotechnol, 34:442–446. 17. González-Pajuelo M, Meynial-Salles I, Mendes F, Soucaille Ph, Vasconcelos I (2006). Microbial conversion of glycerol to 1,3-propanediol: physiological comparison of a natural producer, Clostridium butyricum VPI 3266, and an engineered strain, Clostridium acetobutylicum DG1(pSPD5). Appl Environ Microbiol, 72,1: 96–101. 18. Hejna A, Kosmela P, Formela K, Piszczyk Ł, Haponiuk JT (2016). Potential applications of crude glycerol in polymer technology – Current State and Perspectives. J Renew Sustain Ener, 66: 449–475.

19. Hirschmann S, Baganz K, Koschik I, Vorlop KD (2005). Development of an integrated bioconversion process for the production of 1,3-propanediol from raw glycerol waters. Landbauforschung Völkenrode, 55:261–267.

20. Jun SA, Moon C, Kang CH, Kong SW, Sang BI, Um Y (2010). Microbial fed-batch production of 1,3-propanediol using raw glycerol with suspended and immobilized Klebsiella pneumoniae. Appl Biochem Biotech, 161:491–501. 21. Kong PS, Aroua MK, Wan Daud WMA (2016). Conversion of crude and pure glycerol into derivatives: A feasibility evaluation. Renewable and Sustainable Energy Reviews, 63:33–555.

22. Konstantinović SS, Danilović BR, Ćirić JT, Ilić SB, Savić DS, Veljković VB (2016). Valorization of crude glycerol from biodiesel production. Chem Ind Chem Eng, 22 (4): 461−489. 23. Leoneti AB, Aragão-Leoneti V, De Oliveira SVWB (2012). Glycerol as a by-product of biodiesel production in Brazil: Alternatives for the use of unrefined glycerol. Renew Energ, 45: 138-145.

24. Menzel K, Zeng AP, Deckwer WD (1997). High concentration and productivity of 1,3-propanediol from continuous fermentation of glycerol by Klebsiella pneumoniae. Enz Microb Technol, 20:82-86.

25. Metsoviti M, Zeng A-P, Koutinas AA, Papanikolaou S (2013). Enhanced 1,3-propanediol production by a newly isolated Citrobacter freundii strain cultivated on biodieselderived waste glycerol through sterile and non-sterile bioprocesses. J Biotechnol, 163: 408– 418. 26. Mu Y, Xiu Z-L, Zhang D-J (2008). A combined bioprocess of biodiesel production by lipase with microbial production of 1,3-propanediol by Klebsiella pneumoniae. Biochem Eng J, 40: 537–541. 27. Pagliaro M, Rossi M (2008). The future of glycerol: new uses of a versatile raw material; chapter 1 glycerol: properties and production. RSC Green Chemistry Book Series, 10-14.


49

28. Papanikolaou S, Ruiz-Sanchez P, Pariset B, Blanchard F, Fick M (2000). High production of 1,3-propanediol from industrial glycerol by a newly isolated Clostridium butyricum strain. J Biotechnol, 77:191–208.

34. Rossi DM , Da Costa JB, De Souza EA, Peralba MCR, Ayub MAZ (2012). Bioconversion of residual glycerol from biodiesel synthesis into 1,3-propanediol and ethanol by isolated bacteria from environmental consortia. Renew Energy, 39: 223-227.

30. Papanikolaou S, Fick M, Aggelis G (2004). The effect of raw glycerol concentration on the production of 1,3-propanediol by Clostridium butyricum. J Chem Technol Biotechnol, 79:1189–1196.

36. Vodnar DC, Dulf FV, Pop OL, Socaciu C (2013). L (+)-lactic acid production by pellet-form Rhizopus oryzae NRRL 395 on biodiesel crude glycerol, Microb Cell Fact, 12: 92.

29. Papanikolaou S, Aggelis G (2003). Modelling aspects of the biotechnological valorization of raw glycerol: production of citric acid by Yarrowia lipolytica and 1,3-propanediol by Clostridium butyricum. J Chem Technol Biotechnol, 78:542–547.

31. Papanikolaou S, Fakas S, Fick M, Chevalot I, Panayotou MG, Komaitis M, Marc I, Aggelis G (2008). Biotechnological valorization of raw glycerol discharged after bio-diesel (fatty acid methyl esters) manufacturing process: Production of 1,3-propanediol, citric acid and single cell oil, Biomass Bioenergy, 32:60 – 71. 32. Pflügl S, Marx H, Mattanovich D, Sauer M (2012). 1,3-Propanediol production from glycerol with Lactobacillus diolivorans. Bioresource Technol, 119: 133– 140.

33. Rehman A, Matsumura M, Nomura N, Sato S (2008). Growth and 1,3-propanediol production on pre-treated sunflower oil bio-diesel raw glycerol using a strict anaerobe Clostridium butyricum. Curr Res Bacteriol, 1:7– 16.

35. Sattayasamitsathit S, Prasertsana P, Methacanonc P (2011). Statistical optimization for simultaneous production of 1,3-propanediol and 2,3-butanediol using crude glycerol by newly bacterial isolate. Process Biochem, 46:608–614. 37. Wilkens E, Ringel AK, Hortig D, Willke T, Vorlop KD (2012). High-level production of 1,3-propanediol from crude glycerol by Clostridium butyricum AKR102a. Appl Microbiol Biot, 93:1057–1063.

38. Yang X, Kim DS, Choi HS, Kim CK, Thapa LP, Park C, Kim SW (2017). Repeated batch production of 1,3-propanediol from biodiesel derived waste glycerol by Klebsiella pneumoniae. Chem Eng J, 314: 660-669.

39. Zhang Q, Xiu Z (2009). Metabolic pathway analysis of glycerol metabolism in Klebsiella pneumoniae incorporating oxygen regulatory system. AIChE J, 25:103115. 40. Zheng SN, Zhu KK, Li W, Ji Y (2017). Hydrogenation of dimethyl malonate to 1,3-propanediol catalyzed by a Cu/ SiO2 catalyst: the reaction network and the effect of Cu+/ Cu-0 on selectivity. New J Chem, 41: 5752-5763.

Bulletin UASVM Food Science and Technology 74(2) / 2017