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Article

Controlling the Formation of Foams in Broth to Promote the Co-Production of Microbial Oil and Exopolysaccharide in Fed-Batch Fermentation

1
College of Agriculture and Bioengineering, Heze University, 2269 University Road, Heze 274015, China
2
The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, 1800# Lihu Road, Wuxi 214122, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Fermentation 2022, 8(2), 68; https://doi.org/10.3390/fermentation8020068
Submission received: 5 January 2022 / Revised: 29 January 2022 / Accepted: 30 January 2022 / Published: 7 February 2022
(This article belongs to the Special Issue Applied Microorganisms and Industrial/Food Enzymes)

Abstract

:
A large amount of foam is generated in the production of microbial oil and exopolysaccharide (EPS) by Sporidiobolus pararoseus JD-2, which causes low efficiency in fermentation. In this study, we aimed to reduce the negative effects of foams on the co-production of oil and EPS by controlling the formation of foams in broth. As we have found, the formation of foams is positively associated with cell growth state, air entrapment, and properties of broth. The efficient foam-control method of adding 0.03% (v/v) of the emulsified polyoxyethylene polyoxypropylene pentaerythritol ether (PPE) and feeding corn steep liquor (CSL) at 8–24 h with speed of 0.02 L/h considerably improved the fermentation performance of S. pararoseus JD-2, and significantly increased the oil and EPS concentrations by 8.7% and 12.9%, respectively. The biomass, oil, and EPS concentrations were further increased using a foam backflow device combined with adding 0.03% (v/v) of the emulsified PPE and feeding CSL at 8–24 h, which reached to 62.3 ± 1.8 g/L, 31.2 ± 0.8 g/L, and 10.9 ± 0.4 g/L, respectively. The effective strategy for controlling the formation of foams in fermentation broth reported here could be used as a technical reference for producing frothing products in fed-batch fermentation.

1. Introduction

Microbial oil, a type of biodiesel, can be obtained from renewable raw materials, by oleaginous microorganisms, with many advantages, e.g., short production time and low pollution of the environment [1,2,3]. However, high production cost limits the broader application of microbial oils [4]. In order to decrease the production cost of microbial oil, many strategies have been applied: (1) genetic modification of the biosynthetic pathway of microbial oil in oleaginous microorganism [5,6]; (2) use of the cheaper raw materials as feedstock [7,8]; (3) optimization of the medium components and culture methods [9,10,11]; (4) mixed culture of oleaginous yeast and oleaginous microalgae [12,13]; (5) co-production of microbial oil and high value-added products, e.g., exopolysaccharide (EPS) [14]. In 2010, we obtained an oleaginous yeast (i.e., Sporidiobolus pararoseus JD-02, CCTCC M2010326), which could be used to co-produce microbial oil, carotenoid, and EPS [4,15,16]. Carotenoid and EPS, as high value-added products, have been widely used in the food industry, pharmaceutical industry, and chemical industry [17,18]. In previous studies, we tried to increase the production of microbial oil, carotenoid, and EPS by optimization of media components and culture conditions [4,15,16], and by limitation of ammonia-nitrogen supply [11]. Although these methods were used to increase the production of these value-added products with a satisfactory result, large amounts of foams led to an increase in the escape of fermentation broth and a decrease in the utilization rate of equipment. Therefore, how to control the formation of foams in fermentation broth has become the key problem, which when solved will be beneficial to increase the utilization rate of feedstock and equipment, as well as to cut production cost.
Foams are comprised of thousands of bubbles in liquid caused by mechanical or chemical factors [19]. Foaming is considered a “general nuisance” in industrial fermentation because the fermentation process provides the essential conditions for foam formation [20]. There are two essential conditions for foam formation and stability: the external force and the property of solution [21]. Many factors affect the stability and formation of foams: the air entrapment in solution (e.g., gas flow rate and stirring frequency), the compositions and viscosity of media (e.g., pH, concentration of proteins and sugars, as well as presence of surfactant), the growth state of microbial cells (e.g., logarithmic phase, stable phase, and death phase), and the concentration of metabolites and surface-active substances (e.g., cresotic acid, rhamnolipid, and saponin) [19,22,23,24]. The final foam volume depends on the complex interplay of four processes: bubble formation, bubble–atmosphere coalescence, bubble breakup into tiny bubbles, and bubble–bubble coalescence to increase bubble size [21]. A small amount of bubbles helps to increase media oxygen transfer, but excessive foam leads to a decrease in the utilization rate of equipment and to an increase in the escape of fermentation broth [19]. In order to relieve the negative effects of foams, foam control systems are widely used in industrial fermentation. For example, reasonably adjusting the media components and the culture conditions can be used to prevent the formation of foams [11,19,25]. The most common strategy is to use antifoaming equipment or antifoaming agents to crush the pre-existing foams, and thus avoid the abundant accumulation of foams [26,27]. In addition, Zaky et al. has reported that seawater can also be used to control the formation of foams in the production of biofuel [28,29]. Although these methods on controlling foams have achieved positive results, foaming results from complex interactions among the aforementioned factors. Therefore, the best foam control method is still needed to optimize and achieve the best efficiency of an industrial fermentation process (i.e., high carbon yield, final titer, and productivity).
The aim of the work presented here was to control the formation of foams in a medium, and thus promote the co-production of microbial oil and EPS by S. pararoseus JD-2 in fed-batch fermentation. To do this, the relationships between foams and the key factors involved in foaming were first discussed. Subsequently, different strategies were used to control the formation of foams in fed-batch fermentation, including screening of defoamers, optimization of adding ways of CSL, as well as use of foam backflow devices. After controlling the formation of foams according to the strategies reported in this study, S. pararoseus JD-2 produced 31.2 ± 0.8 g/L of oil and 10.9 ± 0.4 g/L of EPS in fed-batch fermentation. The effective strategy for controlling the formation of foams in fermentation broth reported here could be used as a technical reference for producing frothing products in fed-batch fermentation.

2. Materials and Methods

2.1. Strain and Culture Conditions

Strain S. pararoseus JD-2 (CCTCC M2010326) was used as a fermentation strain for co-producing microbial oil and EPS, which was isolated from bean-based sauce [15]. The YPD medium (Yeast extract 10 g/L, Peptone 20 g/L, Dextrose 20 g/L) was used for activating S. pararoseus JD-2. Unless stated otherwise, S. pararoseus JD-2 was cultivated at 28 °C and pH 6.0 for 72 h.
The fed-batch fermentation was performed in a 7-L fermenter (KF-7 l, Korea Fermenter Co., Inchon, Korea) containing 3 L of the medium with an inoculum size of 10% (v/v), and the inoculum was obtained from a seed culture grown to logarithmic phase (about 10 h). The seed medium was prepared according to the description reported by Wang et al. [11]. The initial culture medium used for fermentation consisted of (per liter): 120 g glucose, 20 g corn steep liquor (CSL; purchased from Shandong Shouguang Juneng Golden Corn Co., Ltd., Shouguang, China), 1.2 g (NH4)2SO4, 1 g K2HPO4, and 0.1 g Na2SO4. The dissolved oxygen level and temperature were set at 20% and 28 °C, respectively. The 800 g/L sterile glucose solution was used to maintain the glucose concentration at ~15 g/L by adjusting the feeding rate. Additionally, the medium was adjusted to pH 6.0 with 20% (m/v) NaOH.

2.2. Extraction of Microbial Oil and EPS

A sample was taken from the fermenter and then centrifuged at 10,000 rpm for 20 min (Sorvall LYNX4000, ThermoFisher Scientific, Waltham, MA, USA). The cell pellets were used to extract microbial oil and the culture supernatants were used to extract EPS. The entire processes of extracting oil and EPS were referred to in previous reports [11,16].

2.3. Analyzing the Performance of Defoamer

Analyzing the performance of defoamer was based on the principle of the previous methods reported by Tamura et al. [30]. Then, 300 mL of fermentation broth was added into a graduated cylinder (range 1000 mL) and then blew air with a speed of 1 L/min. The schematic diagram of the foam forming device is presented in Figure 1a. The time it took foams to reach 700 mL was used to reflect the foaming ability of broth. Subsequently, 300 μL of defoamer with 10 times more dilution was added into the foam forming device, and the time of foam fading away was used to reflect the defoaming ability of the defoamer.
In order to analyze the antifoaming ability of defoamer, 300 mL of fermentation broth and 300 μL of defoamer with 10 times more dilution were added into a graduated cylinder (range 1000 mL) and then blew air with speed of 1 L/min. The time that that foams reached 400 mL was used to reflect the antifoaming ability of defoamer. In addition, different strategies were used to enhance defoaming ability of defoamer, e.g., defoamer plus soybean oil with 1:1.5, defoamer plus Tween 80 with 100:1, and mixed defoamer with 1:1.

2.4. The Mode of Corn Steep Liquor (CSL) Feeding

Four modes of CSL feeding were performed in fed-batch fermentation by S. pararoseus JD-2 (Table 1). The total CSL in the medium at different modes of CSL feeding was identical, and the total CSL was added into the fermentation medium at different incubation times and with different concentrations and feeding rates. It should be noted that the initial concentration of CLS in the media is inconsistent at different modes of CLS feeding, from 5 g/L to 20 g/L.

2.5. Analytical Methods

Then, 200 μL of samples were taken from the shake flasks or fermenter every 4 hours. These samples were used to measure the biomass using a spectrophotometer at 600 nm after 25 times more dilution, and to analyze the concentration of microbial oil and EPS. According to our previous description [11,16], the concentration of microbial oil and EPS was detected by weight after extraction. The analyses of biomass and concentration of microbial oil and EPS were performed in triplicate.

2.6. Statistical Analysis

The experiments in this study were independently carried out at least three times, and data are expressed as mean and standard deviation (±SD). Student’s t test was used to compare statistical difference among the groups of experiment data.

3. Results and Discussion

3.1. The Relationships between Foams and the Key Factors Involved in Foaming in Fed-Batch Ferementation by S. pararoseus JD-2

As mentioned earlier, many factors affect the stability and formation of foam, e.g., the air entrapment in solution, the compositions and viscosity of the media, and the growth state of microbial cells [19,22,23,24]. In order to discuss the relationships between foams and the key factors involved in foaming, the cell growth state, the air entrapment, and the properties of broth were investigated. The foam formation occurred before 36 h of the whole fermentation period in fed-batch fermentation, especially before 24 h (Figure 2). As shown in Figure 2a, S. pararoseus JD-2 was at the early stable growth phase before 36 h, indicating that cell growth state is positively associated with foam formation. Similar results were also found in previous studies, in which the foam volume increased with the increase in cell growth rate [31,32]. Since S. pararoseus JD-2 is an aerobe [15], more oxygen was needed to maintain the cell growth with high rate. Therefore, the fast agitation speed and the high ventilatory capacity were needed to meet the oxygen supply at the early stable growth phase (Figure 2b). Based on the previous results reported by Conceicao et al. [33], static submerged cultivation was beneficial to surfactant production because of the decrease in foam formation. Therefore, air entrapment is also positively associated with foam formation (Figure 2b). Vardar-Sukan pointed out that the concentration of salts, proteins, and sugars in media affects foam formation [19], and this may be why foams were observed to have rapidly formed at a high concentration of protein (Figure 2c). In addition, the foam volume increased with the increase in EPS concentration and apparent viscosity of broth (Figure 2c). The results reported by Dai et al. indicated that the high viscosity of pre-hydrolysate causes the serious foam formation during air-aerated and agitated processes [34]. It should be noted that foams gradually faded away despite the high apparent viscosity after 40 h (Figure 2c). This is possibly because of the reduced agitation speed and ventilatory capacity. This theory is supported by previous results reported by Gong et al. [35], in which reducing aeration eases foaming at the later stages of fermentation.

3.2. Optimization of Defoamer to Enhance Defoaming Ability and to Improve Efficiency of Fermentation Process

As mentioned above, foam formation is positively associated with the cell growth state, the air entrapment, and the properties of broth (Figure 2). Foam formation seems inevitable in agitated submerge fermentation, especially for producing biosurfactant, e.g., rhamnolipids [20,36]. However, excessive foams can do great harm to the normal fermentation process and to the best fermentation efficiency [19]. Therefore, natural or synthetic defoamers were usually used to prevent the formation of foam and/or to crush the pre-existing foams [19,20]. In order to obtain the best defoamer used to avoid the abundant accumulation of foams in fermentation by S. pararoseus JD-2, we investigated the defoaming and antifoaming abilities of one natural defoamer and three synthetic defoamers. As is expected, different defoamers showed the different defoaming abilities and antifoaming abilities (Figure 1b). Among these test defoamers, polyoxyethylene polyoxypropylene pentaerythritol ether (PPE) showed the greatest defoaming capacity and the longest foam-inhibiting time, and the natural defoamer (i.e., soybean oil) showed the worst defoaming abilities and antifoaming abilities (Figure 1b). PPE, as a safe food additive, has been widely used in industrial fermentation because of the high thermal stability, the chemical stability, and the best defoaming capacity [37]. It should be noted that the defoaming abilities and antifoaming abilities could be enhanced using three synergistic methods, i.e., carrier addition method (i.e., PPE plus soybean oil with 1:1.5), emulsifying method (i.e., PPE plus Tween 80 with 100:1), and combination method (PPE plus Polyoxypropylene oxyethylene glycol ether (GPE) with 1:1) (Figure 1c). As shown in Figure 1c, the emulsified PPE using Tween 80 showed the shortest time of defoaming and the longest time of foam-inhibiting. Emulsification promotes the substance into the other incompatible substance in liquid [38], and this may be why the emulsified PPE showed the best defoaming abilities and antifoaming abilities. Therefore, the emulsified PPE was used as the preferred defoamer for defoaming and antifoaming during fermentation by S. pararoseus JD-2 in the next study.
Although addition of defoamer can avoid the abundant accumulation of foams, defoamer negatively affects dissolved oxygen level in fermentation broth, thus restricting the fermentation performance of production strains [39]. Furthermore, the addition of the defoamer will be detrimental to the extraction and purification of target products [40]. These findings are confirmed once again in our results. As can be seen from Figure 1d, the biomass, microbial oil, and EPS concentrations obviously decreased during the addition of more than 0.3% (v/v) of the emulsified PPE. The addition of 0.03% (v/v) of the emulsified PPE in fermentation broth resulted in 51.5 ± 1.7 g/L of biomass, 25.6 ± 1.2 g/L of oil, and 9.5 ± 0.6 g/L of EPS, which is the best condition for cultivation of S. pararoseus JD-2 (Figure 1d). Thus, 0.03% (v/v) of the emulsified PPE was used to control foam formation in fed-batch fermentation by S. pararoseus JD-2 in the next study.

3.3. The Effects of the Mode of Corn Steep Liquor Feeding on Fermentation Performance of S. pararoseus JD-2

The concentration of proteins in media is one of the key factors in foam formation [19]. Corn steep liquors (CSL), one of the most commonly used complex organic nitrogen sources, are rich in proteins, sugars, inorganic salts, and vitamins [41]. Therefore, we investigated the effects of CSL on fermentation performance of S. pararoseus JD-2. The effect of the pH of CSL on foam formation was first investigated. The foaming time increased with the increase in pH, whereas the time of the disappearance of foams decreased with the increase in pH (Table 2). As far as we know, protein solubility is closely associated with the pH in solution [42]. We speculated that the proteins in CSL decreased with the increase in pH because of the protein deposition, thus limiting the formation of foams. Given the importance of protein and the optimized pH for cell growth, the best pH in CSL was set at 6.
Next, four modes of CSL feeding were investigated to further improve the fermentation performance of S. pararoseus JD-2 (Table 1). The modes of CSL feeding significantly affected the fermentation performance of S. pararoseus JD-2, including escape volume, biomass, microbial oil, and EPS concentrations (Figure 3). The highest escape volumes (i.e., 1.3 L) were found during one-time addition of the overall CSL (i.e., Mode I). By contrast, only 0.3 L broth escaped from the fermenter during feeding CSL at 8–24 h with speed of 0.02 L/h (i.e., Mode IV), which was down by 76.9% as compared with one-time addition (Figure 3a). In addition, the biomass (i.e., 58.0 ± 1.1 g/L vs. 52.4 ± 1.2 g/L), microbial oil concentration (i.e., 27.5 ± 1.2 g/L vs. 25.3 ± 1.0 g/L), and EPS concentration (i.e., 10.5 ± 0.8 g/L vs. 9.3 ± 0.7 g/L) in Mode IV were increased by 10.7%, 8.7%, and 12.9% as compared with in Mode I, respectively (Figure 3b–d). Similar results were also found in Liu’s reports, in which feeding trypsin resulted in lower formation of foams and higher L-glutamic acid production [43]. Interestingly, although there were no escape volumes during feeding CSL at 24–36 h with a speed of 0.03 L/h (i.e., Mode II), the biomass, microbial oil, and EPS concentrations were obviously inferior to the other three modes (Figure 3b–d). This is probably due to the nutrient deficiencies for cell growth in the early fermentation stage.

3.4. Using the Foams Backflow Device to Increase the Utility Ratio of Feedstock in Fed-Batch Fermentation by S. pararoseus JD-2

As mentioned above (Figure 3a), there is still fermented liquid leakage in Mode IV. In order to increase the utility ratio of feedstock in fed-batch fermentation by S. pararoseus JD-2, a foam backflow device was used to recycle the foams during fed-batch fermentation at the condition of feeding CSL at 8–24 h with speed of 0.02 L/h. The schematic diagram of the foam backflow device is shown in Figure 4a. The excess foams were entered into the collection bottle of the device and crushed, and then the liquor in the collection bottle was pumped into the fermenter by a peristaltic pump. As a control, the fermentation progress at the condition of the one-time addition of the overall CSL combined with the foam backflow device was also investigated. As can be seen from Table 3, using the foam backflow device was beneficial to increase biomass, microbial oil, and EPS concentrations. As compared with only feeding CSL at 8–24 h with speed of 0.02 L/h, the biomass, microbial oil, and EPS concentrations were increased by 7.4%, 13.5%, and 3.8% at the condition of feeding CSL at 8–24 h with speed of 0.02 L/h combined with foams backflow device, respectively. Our results are consistent with the previous results [36,44,45]. In addition, Anic et al. pointed out that application of foam adsorption increased the rhamnolipid yield from glucose feed [36]. It is worth noting that using the foam backflow device has no significant effect on the increase in biomass and products yielded during excess foams formation. As can be seen from Figure 4b, the cell growth was obviously inhibited at the condition of one-time addition of the overall CSL combined with the foam backflow device. One of the main reasons may be nutrient deficiencies because of the large amounts of fermented liquid leakage. Therefore, how to improve the efficiency of foam breakers is also important for controlling the formation of foams in fed-batch fermentation [45].

4. Conclusions

Foaming is considered a “general nuisance” in industrial fermentation because excessive foaming can lead to a decrease in the utilization rate of equipment and to an increase in the escape of fermentation broth. In this study, we pointed out that foam formation in fed-batch fermentation by S. pararoseus JD-2 is positively associated with the cell growth state, the air entrapment, and the properties of broth. We found that different defoamers and modes of CSL feeding show the different effects on the formation of foams. The addition of 0.03% (v/v) of the emulsified PPE using Tween 80 in fermentation broth showed the best defoaming abilities and antifoaming abilities. In addition, feeding CSL at 8–24 h with speed of 0.02 L/h resulted in only 0.3 L of fermented liquid leakage, and increased biomass, microbial oil and EPS concentrations. The foam backflow device once again proved beneficial for fed-batch fermentation. Under such efficient foam-control, S. pararoseus JD-2 produced 31.2 ± 0.8 g/L of microbial oil and 10.9 ± 0.4 g/L of EPS, which increased by 23.3% and 17.2%, respectively, in comparison to uncontrolled foaming.

Author Contributions

Methodology, Y.-F.G., H.-T.W. and M.-Q.W.; investigation, Y.-F.G., H.-T.W. and M.-Q.W.; data curation, Y.-F.G. and M.-Q.W.; writing—original draft preparation, Y.-F.G.; writing—review and editing, J.-Z.X.; supervision, J.-Z.X. and Y.-L.W.; project administration, J.-Z.X. and Y.-L.W.; funding acquisition, J.-Z.X. and Y.-L.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Laboratory of Industrial Biotechnology, Ministry of Education, Jiangnan University, grant number KLIB-KF 201706 and KLIB-KF 202004, the Project of Shandong Province Higher Educational Science and Technology Program, grant number J17KA125. The APC was funded by Qingchuang Science and Technology Support Program of Shandong Provincial College.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to acknowledge Wei-Guo Zhang from School of Biotechnology, Jiangnan University for data analysis.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Caporusso, A.; Capece, A.; De Bari, I. Oleaginous Yeasts as Cell Factories for the Sustainable Production of Microbial Lipids by the Valorization of Agri-Food Wastes. Fermentation 2021, 7, 50. [Google Scholar] [CrossRef]
  2. Shaigani, P.; Awad, D.; Redai, V.; Fuchs, M.; Haack, M.; Mehlmer, N.; Brueck, T. Oleaginous yeasts- substrate preference and lipid productivity: A view on the performance of microbial lipid producers. Microb. Cell Factories 2021, 20, 220–237. [Google Scholar] [CrossRef]
  3. Zhang, L.; Song, Y.; Wang, Q.; Zhang, X. Culturing rhodotorula glutinis in fermentation-friendly deep eutectic solvent extraction liquor of lignin for producing microbial lipid. Bioresour. Technol. 2021, 337, 125475. [Google Scholar] [CrossRef]
  4. Han, M.; Xu, J.Z.; Liu, Z.M.; Qian, H.; Zhang, W.G. Co-production of microbial oil and exopolysaccharide by the oleaginous yeast Sporidiobolus pararoseus grown in fed-batch culture. RSC Adv. 2018, 8, 3348–3356. [Google Scholar] [CrossRef] [Green Version]
  5. Ledesma-Amaro, R. Microbial oils: A customizable feedstock through metabolic engineering. Eur. J. Lipid Sci. Technol. 2014, 117, 141–144. [Google Scholar] [CrossRef]
  6. Qiao, K.; Wasylenko, T.M.; Zhou, K.; Xu, P.; Stephanopoulos, G. Lipid production in Yarrowia lipolytica is maximized by engineering cytosolic redox metabolism. Nat. Biotechnol. 2017, 35, 173–177. [Google Scholar] [CrossRef]
  7. Manowattana, A.; Techapun, C.; Watanabe, M.; Chaiyaso, T. Bioconversion of biodiesel-derived crude glycerol into lipids and carotenoids by an oleaginous red yeast Sporidiobolus pararoseus KM281507 in an airlift bioreactor. J. Biosci. Bioeng. 2018, 125, 59–66. [Google Scholar] [CrossRef]
  8. Sathiyamoorthi, E.; Kumar, P.; Kim, B.S. Lipid production by Cryptococcus albidus using biowastes hydrolysed by indigenous microbes. Bioprocess Biosyst. Eng. 2019, 42, 687–696. [Google Scholar] [CrossRef]
  9. Pawar, P.; Odaneth, A.A.; Vadgama, R.; Lali, A.M. Simultaneous lipid biosynthesis and recovery for oleaginous yeast Yarrowia lipolytica. Biotechnol. Biofuels 2019, 12, 237–254. [Google Scholar] [CrossRef] [Green Version]
  10. Sakarika, M.; Kornaros, M. Kinetics of growth and lipids accumulation in Chlorella vulgaris during batch heterotrophic cultivation: Effect of different nutrient limitation strategies. Bioresour. Technol. 2017, 243, 356–365. [Google Scholar] [CrossRef]
  11. Wang, H.; Hu, B.; Liu, J.; Qian, H.; Xu, J.; Zhang, W. Co-production of lipid, exopolysaccharide and single-cell protein by Sporidiobolus pararoseus under ammonia nitrogen-limited conditions. Bioprocess Biosyst. Eng. 2020, 43, 1403–1414. [Google Scholar] [CrossRef]
  12. Zeng, Y.; Xie, T.; Li, P.; Jian, B.; Li, X.; Xie, Y.; Zhang, Y. Enhanced lipid production and nutrient utilization of food waste hydrolysate by mixed culture of oleaginous yeast Rhodosporidium toruloides and oleaginous microalgae Chlorella vulgaris. Renew. Energy 2018, 126, 915–923. [Google Scholar] [CrossRef]
  13. Arora, N.; Patel, A.; Mehtani, J.; Pruthi, P.A.; Pruthi, V.; Poluri, K.M. Co-culturing of oleaginous microalgae and yeast: Paradigm shift towards enhanced lipid productivity. Environ. Sci. Pollut. Res. 2019, 26, 16952–16973. [Google Scholar] [CrossRef]
  14. Liu, G.; Miao, X. Switching cultivation for enhancing biomass and lipid production with extracellular polymeric substance as co-products in Heynigia riparia SX01. Bioresour. Technol. 2017, 227, 214–220. [Google Scholar] [CrossRef] [PubMed]
  15. Han, M.; He, Q.; Zhang, W.G. Carotenoids production in different culture conditions by Sporidiobolus pararoseus. Prep. Biochem. Biotech. 2012, 42, 293–303. [Google Scholar] [CrossRef] [PubMed]
  16. Han, M.; Xu, Z.-Y.; Du, C.; Qian, H.; Zhang, W.-G. Effects of nitrogen on the lipid and carotenoid accumulation of oleaginous yeast Sporidiobolus pararoseus. Bioprocess Biosyst. Eng. 2016, 39, 1425–1433. [Google Scholar] [CrossRef] [PubMed]
  17. Gupta, A.K.; Seth, K.; Maheshwari, K.; Baroliya, P.K.; Meena, M.; Kumar, A.; Vinayak, V. Harish Biosynthesis and extraction of high-value carotenoid from algae. Front. Biosci. 2021, 26, 171–190. [Google Scholar] [CrossRef]
  18. Rehm, B.H.A. Bacterial polymers: Biosynthesis, modifications and applications. Nat. Rev. Microbiol. 2010, 8, 578–592. [Google Scholar] [CrossRef]
  19. Vardar-Sukan, F. Foaming: Consequences, prevention and destruction. Biotechnol. Adv. 1998, 16, 913–948. [Google Scholar] [CrossRef]
  20. Junker, B. Foam and its mitigation in fermentation systems. Biotechnol. Progr. 2007, 23, 767–784. [Google Scholar] [CrossRef]
  21. Denkov, N.; Tcholakova, S.; Politova-Brinkova, N. Physicochemical control of foam properties. Curr. Opin. Colloid Interface Sci. 2020, 50, 101376. [Google Scholar] [CrossRef]
  22. Lesov, I.; Tcholakova, S.; Kovadjieva, M.; Saison, T.; Lamblet, M.; Denkov, N. Role of Pickering stabilization and bulk gelation for the preparation and properties of solid silica foams. J. Colloid Interface Sci. 2017, 504, 48–57. [Google Scholar] [CrossRef]
  23. Liao, S.; Ghosh, A.; Becker, M.D.; Abriola, L.M.; Cápiro, N.L.; Fortner, J.D.; Pennell, K.D. Effect of rhamnolipid biosurfactant on transport and retention of iron oxide nanoparticles in water-saturated quartz sand. Environ. Sci. Nano 2020, 8, 311–327. [Google Scholar] [CrossRef]
  24. Politova, N.; Tcholakova, S.; Valkova, Z.; Golemanov, K.; Denkov, N.D. Self-regulation of foam volume and bubble size during foaming via shear mixing. Colloids Surf. A Physicochem. Eng. Asp. 2018, 539, 18–28. [Google Scholar] [CrossRef]
  25. Cheng, X.-H.; Wang, K.; Cheng, N.-Q.; Mi, S.-Y.; Sun, L.-S.; Yeh, J.-T. The control of expansion ratios and cellular structure of supercritical CO2-aid thermoplastic starch foams using crosslinking agents and nano-silica particles. J. Polym. Res. 2021, 28, 35–43. [Google Scholar] [CrossRef]
  26. Akter, M.M.; Theary, K.; Kalkornsurapranee, E.; Prabhakar, C.S.; Thaochan, N. The effects of methyl eugenol, cue lure and plant essential oils in rubber foam dispenser for controlling Bactrocera dorsalis and Zeugodacus cucurbitae. Asian J. Agric. Biol. 2021, 9, 356–367. [Google Scholar] [CrossRef]
  27. Jin, Y.; Li, J.; Wu, S.; Zhou, F. Comparison of polyurethane foam dressing and hydrocolloid dressing in patients with pressure ulcers A randomized controlled trial protocol. Medicine 2021, 100, e24165. [Google Scholar] [CrossRef]
  28. Zaky, A.S. Introducing a Marine Biorefinery System for the Integrated Production of Biofuels, High-Value-Chemicals, and Co-Products: A Path Forward to a Sustainable Future. Processes 2021, 9, 1841. [Google Scholar] [CrossRef]
  29. Zaky, A.S.; Carter, C.E.; Meng, F.; French, C.E. A preliminary life cycle analysis of bioethanol production using seawater in a coastal biorefinery setting. Processes 2021, 9, 1399. [Google Scholar] [CrossRef]
  30. Tamura, T.; Kageyama, M.; Kaneko, Y.; Kishino, T.; Nikaido, M. Direct Observation of Foam Film Rupture by Several Types of Antifoams Using a Scanning Laser Microscope. J. Colloid Interface Sci. 1999, 213, 179–186. [Google Scholar] [CrossRef]
  31. Valdés-Velasco, L.M.; Favela-Torres, E.; Théatre, A.; Arguelles-Arias, A.; Saucedo-Castañeda, J.G.; Jacques, P. Relationship between lipopeptide biosurfactant and primary metabolite production by Bacillus strains in solid-state and submerged fermentation. Bioresour. Technol. 2021, 345, 126556. [Google Scholar] [CrossRef]
  32. Xu, N.; Liu, S.; Xu, L.; Zhou, J.; Xin, F.; Zhang, W.; Qian, X.; Li, M.; Dong, W.; Jiang, M. Enhanced rhamnolipids production using a novel bioreactor system based on integrated foam-control and repeated fed-batch fermentation strategy. Biotechnol. Biofuels 2020, 13, 80–89. [Google Scholar] [CrossRef] [PubMed]
  33. Conceição, K.S.; Almeida, M.D.A.; Sawoniuk, I.C.; Marques, G.D.; Faria-Tischer, P.C.D.S.; Tischer, C.A.; Vignoli, J.A.; Camilios-Neto, D. Rhamnolipid production by Pseudomonas aeruginosa grown on membranes of bacterial cellulose supplemented with corn bran water extract. Environ. Sci. Pollut. Res. 2020, 27, 30222–30231. [Google Scholar] [CrossRef] [PubMed]
  34. Dai, L.; Jiang, W.; Zhou, X.; Xu, Y. Enhancement in xylonate production from hemicellulose pre-hydrolysate by powdered activated carbon treatment. Bioresour. Technol. 2020, 316, 123944. [Google Scholar] [CrossRef] [PubMed]
  35. Gong, Z.; Peng, Y.; Wang, Q. Rhamnolipid production, characterization and fermentation scale-up by Pseudomonas aeruginosa with plant oils. Biotechnol. Lett. 2015, 37, 2033–2038. [Google Scholar] [CrossRef]
  36. Anic, I.; Apolonia, I.; Franco, P.; Wichmann, R. Production of rhamnolipids by integrated foam adsorption in a bioreactor system. AMB Express 2018, 8, 122. [Google Scholar] [CrossRef] [PubMed]
  37. Sharma, S.C.; Tsuchiya, K.; Sakai, K.; Sakai, H.; Abe, M.; Komura, S.; Sakamoto, K.; Miyahara, R. Formation and Characterization of Microemulsions Containing Polymeric Silicone. Langmuir 2008, 24, 7658–7662. [Google Scholar] [CrossRef] [PubMed]
  38. Liu, L.; Xiang, N.; Ni, Z.; Huang, X.; Zheng, J.; Wang, Y.; Zhang, X. Step emulsification: High-throughput production of monodisperse droplets. Biotechniques 2020, 68, 114–116. [Google Scholar] [CrossRef] [Green Version]
  39. He, Y. High cell density production of Deinococcus radiodurans under optimized conditions. J. Ind. Microbiol. Biotechnol. 2009, 36, 539–546. [Google Scholar] [CrossRef]
  40. Routledge, S.J. Beyond de-foaming: The effects of antifoams on bioprocess productivity. Comput. Struct. Biotechnol. J. 2012, 3, e201210001. [Google Scholar] [CrossRef] [Green Version]
  41. Maleki-Kakelar, M.; Azarhoosh, M.J.; Senji, S.G.; Aghaeinejad-Meybodi, A. Urease production using corn steep liquor as a low-cost nutrient source by Sporosarcina pasteurii: Biocementation and process optimization via artificial intelligence approaches. Environ. Sci. Pollut. Res. 2021, 1–15. [Google Scholar] [CrossRef] [PubMed]
  42. Paker, I.; Jaczynski, J.; Matak, K.E. Calcium hydroxide as a processing base in alkali-aided pH-shift protein recovery process. J. Sci. Food Agric. 2017, 97, 811–817. [Google Scholar] [CrossRef] [PubMed]
  43. Liu, X. Effects of proteases on L-glutamic acid fermentation. Bioengineered 2019, 10, 646–658. [Google Scholar] [CrossRef] [Green Version]
  44. Anic, I.; Nath, A.; Franco, P.; Wichmann, R. Foam adsorption as an ex situ capture step for surfactants produced by fermentation. J. Biotechnol. 2017, 258, 181–189. [Google Scholar] [CrossRef] [PubMed]
  45. Long, X.; Shen, C.; He, N.; Zhang, G.; Meng, Q. Enhanced rhamnolipids production via efficient foam-control using stop valve as a foam breaker. Bioresour. Technol. 2017, 224, 536–543. [Google Scholar] [CrossRef]
Figure 1. The effects of defoamers on defoaming, antifoaming and fermentation performance of S. pararoseus JD-2. (a) Simple foam forming device. (b) The antifoaming abilities of different defoaming:the DSA-5 represents the defoamer for bean products. (c) Effects of different synergistic methods on PPE defoaming ability (d) Effect of defoamer on S. pararoseus JD-2 fermentation. The data represent mean values and standard deviations obtained from three independent cultivations.
Figure 1. The effects of defoamers on defoaming, antifoaming and fermentation performance of S. pararoseus JD-2. (a) Simple foam forming device. (b) The antifoaming abilities of different defoaming:the DSA-5 represents the defoamer for bean products. (c) Effects of different synergistic methods on PPE defoaming ability (d) Effect of defoamer on S. pararoseus JD-2 fermentation. The data represent mean values and standard deviations obtained from three independent cultivations.
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Figure 2. Causes of severe foaming in fed-batch fermentation by S. pararoseus JD-2. (a) The relationship between defoamer and frothing. (b) The relationship between ventilation and frothing. (c) The relationship between the properties of broth and frothing. The dark histograms represent the high of foams excess of fermenters. The data represent mean values and standard deviations obtained from three independent cultivations.
Figure 2. Causes of severe foaming in fed-batch fermentation by S. pararoseus JD-2. (a) The relationship between defoamer and frothing. (b) The relationship between ventilation and frothing. (c) The relationship between the properties of broth and frothing. The dark histograms represent the high of foams excess of fermenters. The data represent mean values and standard deviations obtained from three independent cultivations.
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Figure 3. Effects of CSL feeding method on the fermentation of S. pararoseus JD-2. (a) The volumes of broth leakage in different modes of CSL feeding. (b) The biomass in different modes of CSL feeding. (c) The microbial oil concentration in different modes of CSL feeding. (d) The EPS concentration in different modes of CSL feeding. The data represent mean values and standard deviations obtained from three independent cultivations.
Figure 3. Effects of CSL feeding method on the fermentation of S. pararoseus JD-2. (a) The volumes of broth leakage in different modes of CSL feeding. (b) The biomass in different modes of CSL feeding. (c) The microbial oil concentration in different modes of CSL feeding. (d) The EPS concentration in different modes of CSL feeding. The data represent mean values and standard deviations obtained from three independent cultivations.
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Figure 4. Effect of foam backflow device on the fermentation of S. pararoseus JD-2. (a) Foam backflow device. ① Fermenter, ② Antifoaming paddle, ③ Stirring paddle, ④ Exhaust pipe, ⑤ Collection bottle, ⑥ Solution without foams, ⑦ Off-gases, ⑧ Feeding pipe, ⑨ Peristaltic pump. (b) Effect of foam backflow device on cell growth of S. pararoseus JD-2. The data represent mean values and standard deviations obtained from three independent cultivations.
Figure 4. Effect of foam backflow device on the fermentation of S. pararoseus JD-2. (a) Foam backflow device. ① Fermenter, ② Antifoaming paddle, ③ Stirring paddle, ④ Exhaust pipe, ⑤ Collection bottle, ⑥ Solution without foams, ⑦ Off-gases, ⑧ Feeding pipe, ⑨ Peristaltic pump. (b) Effect of foam backflow device on cell growth of S. pararoseus JD-2. The data represent mean values and standard deviations obtained from three independent cultivations.
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Table 1. Methods of feeding organic nitrogen source in S. pararoseus fed-batch fermentation.
Table 1. Methods of feeding organic nitrogen source in S. pararoseus fed-batch fermentation.
ModeLoading Volume
(L)
Initial Defoamer Concentration
(%)
Initial CSL Concentration
(g/L)
Time of CSL Feeding
(h)
Speed of CSL Feeding 1
(L/h)
I3.0020
II2.70.11024–360.03
III2.70.158–240.02
IV2.70.1108–240.02
1 The concentration of CSL used feeding in Mode II, Mode III, and Mode IV is 110 g/L, 155 g/L, and 110 g/L, respectively.
Table 2. The foaming ability and bubble-holding ability of corn steep liquor with different pH.
Table 2. The foaming ability and bubble-holding ability of corn steep liquor with different pH.
pH of CSL 1Time of Foaming (s) 2Time of Defoaming (s)
423120
530100
65550
7*5
8*3
1 The concentration of CSL is 20 g/L. 2 “*” represents no foaming.
Table 3. Effect of foam return device on the fermentation of S. pararoseus JD-2.
Table 3. Effect of foam return device on the fermentation of S. pararoseus JD-2.
Feeding ModeBiomass
(g/L)
Microbial Oil (g/L)EPS
(g/L)
Mode I plus foam backflow device52.2 ± 1.625.6 ± 0.79.1 ± 0.3
Mode IV plus foam backflow device62.3 ± 1.831.2 ± 0.810.9 ± 0.4
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Guo, Y.-F.; Wang, M.-Q.; Wang, Y.-L.; Wang, H.-T.; Xu, J.-Z. Controlling the Formation of Foams in Broth to Promote the Co-Production of Microbial Oil and Exopolysaccharide in Fed-Batch Fermentation. Fermentation 2022, 8, 68. https://doi.org/10.3390/fermentation8020068

AMA Style

Guo Y-F, Wang M-Q, Wang Y-L, Wang H-T, Xu J-Z. Controlling the Formation of Foams in Broth to Promote the Co-Production of Microbial Oil and Exopolysaccharide in Fed-Batch Fermentation. Fermentation. 2022; 8(2):68. https://doi.org/10.3390/fermentation8020068

Chicago/Turabian Style

Guo, Yan-Feng, Meng-Qi Wang, Yi-Lei Wang, Hong-Tao Wang, and Jian-Zhong Xu. 2022. "Controlling the Formation of Foams in Broth to Promote the Co-Production of Microbial Oil and Exopolysaccharide in Fed-Batch Fermentation" Fermentation 8, no. 2: 68. https://doi.org/10.3390/fermentation8020068

APA Style

Guo, Y. -F., Wang, M. -Q., Wang, Y. -L., Wang, H. -T., & Xu, J. -Z. (2022). Controlling the Formation of Foams in Broth to Promote the Co-Production of Microbial Oil and Exopolysaccharide in Fed-Batch Fermentation. Fermentation, 8(2), 68. https://doi.org/10.3390/fermentation8020068

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