Skip to main content
Log in

Design of nutrient gas-phase bioreactors: a critical comprehensive review

  • Critical Review
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

To reach an efficient and economical gas-phase bioreactor is still one of the most critical challenges in biotechnology engineering. The numerous advantages of gas-phase bioreactors (GPBs) as well as disadvantages of these bioreactors should be exactly recognized, and efforts should be made to eliminate these defects. The first step in upgrading these bioreactors is to identify their types and the results of previous research. In the present work, a summary of the studies carried out in the field of cultivation in these bioreactors, their classification, their components, their principles and relations governing elements, modeling them, and some of their inherent engineering aspects are presented. Literature review showed that inoculation of shoots, roots, adventurous roots, callus, nodal explants, anther, nodal segment, somatic embryo, hairy roots, and fungus is reported in 15, 2, 2, 2, 3, 2, 1, 1, 37, and 5 cases, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

A m :

Amplitude of sound wave (m)

C :

Speed of sound (m s1)

C C :

Cunningham slip correction factor (-)

C c :

Critical concentration of the nutrient (mL mg1)

C E :

Concentration of the nutrient at equilibrium (mL mg1)

C s :

Concentration of the limiting nutrient in the medium (g L1)

D :

Sauter mean diameter (m)

d :

Disc diameter (m)

d 0 :

The initial diameter of the jet or nozzle outlet diameter (m)

D f :

Diameter of the fiber (hairy root) (m)

d m :

Mean diameter (m)

D p :

Diameter of the mist particle (m)

DW f :

Final dry weight of the hairy roots (g)

DW i :

Initial dry weight of the hairy roots (g)

f :

Frequency (H)

F 0 :

Initial feed flow rate per unit mass, felt by the bed (mL day1 mg1)

FW :

Fresh weight of hairy roots (g)

G L :

Mass flow rate of fluid entering the disc (kg h1)

h :

Diameter of the holes or the height of the blades on the disc (m)

H c :

Critical specific liquid hold up (mL mg1)

H s :

Specific liquid hold up at saturation (mL mg1)

I :

Power surface intensity (ratio of power delivered at the surface) (kg s3)

k :

Boltzmann constant (-)

k 1 :

Growth rate constant of primary root after branching starts (mg day1 mg1)

k 2 :

Growth rate constant of branches during branching period (mg day1 mg1)

k 3 :

Growth rate constant of branches after maturity time (mg day1 mg1)

k cm :

Rate of nutrient consumption by roots per unit mass of the roots (Day1)

k d :

Proportionality constant for drainage equation (Day1)

k f :

Biomass per unit mass of nutrient uptake (mg mg1)

k g :

Fraction of nutrient utilized for growth (-)

k m :

Growth rate constant of primary hairy root after maturity time (mg day1 mg1)

k n :

Knult number (-)

k tot :

Growth rate constant of root (mg day1 mg1)

k u :

Kuwabara number (-)

L :

Length of the bed (m)

l :

Length of hairy root (m)

l 0 :

Initial length of hairy root (cm)

l 1 :

Length of hairy root before branching starts (cm)

l 2 :

Length of hairy root after branching and before maturity (cm)

l 3 :

Length of hairy root after maturity and before harvesting (cm)

M :

Mass of hairy root (kg)

m :

Mass fraction of the droplets with diameter Dp (kg)

a :

Mass flow rate of air (kg s1)

m f :

Mass of fructose (g)

m g :

Mass of glucose (g)

L :

Mass flow rate of liquid (kg s1)

m p :

Mass of a mist particle (kg)

m s :

Mass of sucrose (g)

N :

Rotational velocity of disc (rev min1)

n :

Number of holes or blades on the disc (-)

Oh :

Ohnesorge number (-)

Q :

Volumetric flow rate (m3 s1)

Q m :

Volumetric flow rate of mist during the mist-On cycle (m3 min1)

R :

Radius of culture chamber (m)

r :

Radius of hairy root (m)

R aL :

Mass ratio of air to liquid (-)

t :

Film thickness at the nozzle outlet (m)

T :

Temperature (℃)

T c :

Maximum duration of the mist-On cycle (min)

T i :

Time (Day)

T M :

Maximum duration of the mist-Off cycle (min)

V :

Volume of the Cultivation Chamber (L)

V 0 :

Velocity of the droplets through the root bed (m s1)

V dep-med :

The volume of culture medium that is absorbed during a day (m3)

v g :

Velocity of the gas (air) (m s1)

v p :

Velocity of the mist particles (m s1)

V req :

Required volume of the culture medium (mL)

Wn :

Weber number (-)

Wn a :

Weber number of air (-)

y 1 :

Distance the particle’s streamline (m)

Y s :

Apparent biomass yield based on sucrose (g g1)

Z :

Height of nozzle above culture bed (m)

α :

Fraction of the bed volume filled with fiber fibers (roots) (-)

β :

Packing fraction (-)

ΔDW :

Dry weight changes (g)

ΔGE :

Glucose equivalent changes (g)

ΔP L :

Injection pressure differential across nozzle (Pa)

Δt :

Period (Day)

Δt 1 :

The period before branching starts (Day)

Δt 2 :

The period after rooting and before maturity (Day)

Δt 3 :

The period after maturity and before harvesting (Day)

η :

Overall capture efficiency (-)

η B :

Percent of droplets that remain in the bed (-)

η c :

Combined capture efficiency of all mechanisms involved (-)

η Diff :

Diffusion efficiency (-)

η i :

Efficiency for each individual mechanism (-)

η Int + Imp :

Efficiency of both interception and impaction (-)

θ :

Jet cone angle (Degree)

µ :

Fluid dynamic viscosity (kg m1 s)

µ a :

Viscosity of the air (kg m1 s)

µ L :

Liquid dynamic viscosity (kg m1 s)

µ m :

Mist dynamic viscosity (kg m1 s)

ξ :

Average specific growth rate (g day1)

ρ :

Density of hairy root (kg m3)

ρ a :

Density of air (kg m3)

ρ FW :

Density of fresh weight of hairy roots (g mL1)

ρ L :

Density of liquid (kg m3)

σ :

Surface tension (N m1)

ω :

The time mist generator system is on (min h1)

B5 :

Gamborg’s medium [168] (-)

BA :

6-Benzyladenine (-)

BAP :

6-Benzylamino-purine (-)

BM :

Basal nutrient medium [72] (-)

CCCM :

Chemical composition of culture medium (-)

CFD :

Computational fluid dynamics (-)

GPB :

Gas-phase bioreactor (-)

GPBs :

Gas-phase bioreactors (-)

IAA :

Indole acetic acid (-)

IBA :

Indole-3-butyric acid (-)

ITB :

Inoculate tissue in bioreactor (-)

MS :

Murashige and Skoog’s medium [169] (-)

NAA :

α-Naphthaleneacetic acid (-)

OCN :

Off/on cycle of nourishment (mist-on: whole cycle) (-)

PNSS :

Pump-nozzle spraying system (-)

PSCB :

Plant species cultivated in bioreactor (-)

SH :

Schenk and Hildebrandt’s medium [170] (-)

SSC :

Semi-solid culture (-)

SSEPP :

Spray system equipped with a peristaltic pump (-)

SSS :

Semi-solid System (-)

TAS :

Type of atomizer system (-)

TCC :

Temperature of cultivation chamber during the growth period (℃)

TNS :

Trickling nozzle system (-)

UAN :

Ultrasonic atomizer nozzle (-)

UTEAW :

Ultrasonic transducer equipped with acoustic window (-)

UTOW :

Ultrasonic transducer with open window (-)

VCC :

Volume of the culture chamber (L)

VCM :

Volume of the culture medium (L)

WPM :

McCown’s woody plant [171] (-)

References

  1. Gaosheng H, Jingming J (2012) Production of useful secondary metabolites through regulation of biosynthetic pathway in cell and tissue suspension culture of medicinal plants. In: Leva A (ed) Recent advances in plant in vitro culture. IntechOpen, London

    Google Scholar 

  2. Takayama S, Akita M (1994) The types of bioreactors used for shoots and embryos. Plant Cell Tissue Organ Cult 39:147–156

    Article  Google Scholar 

  3. Elateeq AA, Sun Y, Nxumalo W, Gabr AMM (2020) Biotechnological production of silymarin in Silybum marianum L.: a review. Biocatal Agric Biotechnol 29:101775

    Article  Google Scholar 

  4. Eibl D, Eibl R (2002) Bioreactors for plant cell and tissue cultures. In: Oksman-Caldentey KM, Barz W (eds) Plant biotechnology and transgenic plants. CRC Press, Boca Raton, pp 152–183

    Google Scholar 

  5. Nguyen LN, Truong MV, Nguyen AQ et al (2020) A sequential membrane bioreactor followed by a membrane microalgal reactor for nutrient removal and algal biomass production. Environ Sci Water Res Technol 6:189–196

    Article  CAS  Google Scholar 

  6. Sim Y-B, Jung J-H, Baik J-H et al (2021) Dynamic membrane bioreactor for high rate continuous biohydrogen production from algal biomass. Bioresour Technol 340:125562

    Article  CAS  PubMed  Google Scholar 

  7. Liang W, Zhuang Z, Lei Y et al (2020) Proliferation of biomass and its impact on the operation of a submerged membrane bioreactor. E3S Web Conf 145:2076

    Article  CAS  Google Scholar 

  8. Miao GP, Zhu CS, Yang YQ et al (2014) Elicitation and in situ adsorption enhanced secondary metabolites production of Tripterygium wilfordii Hook. f. adventitious root fragment liquid cultures in shake flask and a modified bubble column bioreactor. Bioprocess Biosyst Eng 37:641–650

    Article  CAS  PubMed  Google Scholar 

  9. Käß F, Hariskos I, Michel A et al (2014) Assessment of robustness against dissolved oxygen/substrate oscillations for C. glutamicum DM1933 in two-compartment bioreactor. Bioprocess Biosyst Eng 37:1151–1162

    Article  PubMed  CAS  Google Scholar 

  10. Kurt T, Marbà-Ardébol A-M, Turan Z et al (2018) Rocking Aspergillus: morphology-controlled cultivation of Aspergillus niger in a wave-mixed bioreactor for the production of secondary metabolites. Microb Cell Fact 17:1–9

    Article  CAS  Google Scholar 

  11. Shohael AM, Yeoup P-K (2018) Commercial production of plant cells in large scale bioreactor for the production of secondary metabolites. In: In vitro cellular & developmental biology-plant. Springer, New York, NY, USA, pp S42–S43

  12. Vazquez-Marquez AM, Zepeda-Gómez C, Burrola-Aguilar C et al (2019) Effect of stirring speed on the production of phenolic secondary metabolites and growth of Buddleja cordata cells cultured in mechanically agitated bioreactor. Plant Cell Tissue Organ Cult 139:155–166

    Article  CAS  Google Scholar 

  13. Costa PC, Echer dos Reis E, Salgueiro de Carvalho L et al (2021) Making the process of enzyme production in solid-state cultivation cleaner and more sustainable—reuse of raw materials and a syringe-type bioreactor enter in the scene. ACS Sustain Chem Eng 9:14134–14142

    Article  CAS  Google Scholar 

  14. Prell C, Vonderbank S-A, Meyer F et al (2021) Metabolic engineering of Corynebacterium glutamicum for de novo production of 3-hydroxycadaverine. Curr Res Biotechnol. https://doi.org/10.1016/j.crbiot.2021.12.004

    Article  Google Scholar 

  15. Li X, Zhang M, Luo J et al (2019) Efficient succinic acid production using a biochar-treated textile waste hydrolysate in an in situ fibrous bed bioreactor. Biochem Eng J 149:107249

    Article  CAS  Google Scholar 

  16. Khan MA, Ngo HH, Guo W et al (2019) Optimization of hydraulic retention time and organic loading rate for volatile fatty acid production from low strength wastewater in an anaerobic membrane bioreactor. Bioresour Technol 271:100–108

    Article  CAS  PubMed  Google Scholar 

  17. Li C, Gao S, Yang X, Lin CSK (2018) Green and sustainable succinic acid production from crude glycerol by engineered Yarrowia lipolytica via agricultural residue based in situ fibrous bed bioreactor. Bioresour Technol 249:612–619

    Article  CAS  PubMed  Google Scholar 

  18. Raza ZA, Tariq MR, Majeed MI, Banat IM (2019) Recent developments in bioreactor scale production of bacterial polyhydroxyalkanoates. Bioprocess Biosyst Eng 42:901–919

    Article  CAS  PubMed  Google Scholar 

  19. Poleto L, da Rosa LO, Fontana RC et al (2021) Production of antimicrobial metabolites against pathogenic bacteria and yeasts by Fusarium oxysporum in submerged culture processes. Bioprocess Biosyst Eng 44:1321–1332

    Article  CAS  PubMed  Google Scholar 

  20. Brauer H (1990) Growth of fungi and bacteria in the reciprocating jet bioreactor. Bioprocess Eng 6:1–15

    Article  Google Scholar 

  21. Liu C, Sun Y, Li N et al (2019) Impact of temperature fluctuation on anaerobic fermentation process of upgrading bioreactor under solar radiant heating. Appl Therm Eng 156:382–391

    Article  CAS  Google Scholar 

  22. Rayhane H, Josiane M, Gregoria M et al (2019) From flasks to single used bioreactor: scale-up of solid state fermentation process for metabolites and conidia production by Trichoderma asperellum. J Environ Manage 252:109496

    Article  CAS  PubMed  Google Scholar 

  23. Wang W, Knoshaug EP, Wei H et al (2020) High titer fatty alcohol production in Lipomyces starkeyi by fed-batch fermentation. Curr Res Biotechnol 2:83–87

    Article  Google Scholar 

  24. Sharma S, Verma R, Dhull S et al (2021) Biodegradation of waste cooking oil and simultaneous production of rhamnolipid biosurfactant by Pseudomonas aeruginosa P7815 in batch and fed-batch bioreactor. Bioprocess Biosyst Eng 45:309–319. https://doi.org/10.1007/s00449-021-02661-0

    Article  CAS  PubMed  Google Scholar 

  25. Menshutina NV, Guseva EV, Safarov RR, Boudrant J (2020) Modelling of hollow fiber membrane bioreactor for mammalian cell cultivation using computational hydrodynamics. Bioprocess Biosyst Eng 43:549–567

    Article  CAS  PubMed  Google Scholar 

  26. Luo C, Guo L, Zeng S, Long T (2021) Effects of turbulence fluctuation intensity in bioreactor of sewage treatment on physical and chemical properties of biofilms. Bioprocess Biosyst Eng 44:1865–1874. https://doi.org/10.1007/s00449-021-02566-y

    Article  CAS  PubMed  Google Scholar 

  27. Chopra J, Sen R (2018) Process optimization involving critical evaluation of oxygen transfer, oxygen uptake and nitrogen limitation for enhanced biomass and lipid production by oleaginous yeast for biofuel application. Bioprocess Biosyst Eng 41:1103–1113

    Article  CAS  PubMed  Google Scholar 

  28. Chen D-Z, Liu H-Y, Yu Y et al (2021) Enhanced biodegradation of n-Hexane in a two-phase partitioning bioreactor inoculated with Pseudomonas mendocina NX-1 under chitosan stimulation. J Hazard Mater 419:126330

    Article  CAS  PubMed  Google Scholar 

  29. Lu L, Baig ZT, Dong D, Xi J (2021) Preparation and characterization of a novel packing material for the gas-phase fluidized-bed bioreactor. Process Saf Environ Prot 150:433–439

    Article  CAS  Google Scholar 

  30. Baskaran D, Sinharoy A, Pakshirajan K, Rajamanickam R (2020) Gas-phase trichloroethylene removal by Rhodococcus opacus using an airlift bioreactor and its modeling by artificial neural network. Chemosphere 247:125806

    Article  CAS  PubMed  Google Scholar 

  31. Eknadiosyants OK (1970) Poluchenie aerozolei. Fizicheskie osnovy ul’trazvukovoi tekhnologii (Production of Aerosols. Physical Principles of Ultrasonic Technology), Rozenberg, LD, Ed

  32. Shiau YJ, Chu CY (2010) Comparative effects of ultrasonic transducers on medium chemical content in a nutrient mist plant bioreactor. Sci Hortic (Amsterdam) 123:514–520. https://doi.org/10.1016/J.SCIENTA.2009.10.012

    Article  CAS  Google Scholar 

  33. McDonell VG (2017) Atomization and sprays. CRC Press

    Google Scholar 

  34. Shafaei SM, Nourmohamadi-Moghadami A, Rahmanian-Koushkaki H, Kamgar S (2019) Neural computing efforts for integrated simulation of ultrasound-assisted hydration kinetics of wheat. Inf Process Agric 6:357–374

    Google Scholar 

  35. Putra BTW (2020) A new low-cost sensing system for rapid ring estimation of woody plants to support tree management. Inf Process Agric 7:369–374

    Google Scholar 

  36. Wang S, Li Y, Yuan J et al (2021) Recognition of cotton growth period for precise spraying based on convolution neural network. Inf Process Agric 8:219–231

    Google Scholar 

  37. Adeboye OB, Schultz B, Adeboye AP et al (2021) Application of the AquaCrop model in decision support for optimization of nitrogen fertilizer and water productivity of soybeans. Inf Process Agric 8:419–436

    Google Scholar 

  38. Mehdizadeh SA, Minaei S, Hancock NH, Torshizi MAK (2014) An intelligent system for egg quality classification based on visible-infrared transmittance spectroscopy. Inf Process Agric 1:105–114

    Google Scholar 

  39. Gongal A, Karkee M, Amatya S (2018) Apple fruit size estimation using a 3D machine vision system. Inf Process Agric 5:498–503

    Google Scholar 

  40. Fathizadeh Z, Aboonajmi M, Hassan-Beygi SR (2021) Nondestructive methods for determining the firmness of apple fruit flesh. Inf Process Agric 8:515–527. https://doi.org/10.1016/j.inpa.2020.12.002

    Article  Google Scholar 

  41. Shaik MI, Effendi NFA, Sarbon NM (2021) Functional properties of sharpnose stingray (Dasyatis zugei) skin collagen by ultrasonication extraction as influenced by organic and inorganic acids. Biocatal Agric Biotechnol 35:102103

    Article  CAS  Google Scholar 

  42. Ramos-De-La-Pena AM, Renard CMGC, Montañez JC et al (2015) Ultrafiltration for genipin recovery technologies after ultrasonic treatment of genipap fruit. Biocatal Agric Biotechnol 4:11–16

    Article  Google Scholar 

  43. Mirzabe AH, Hajiahmad A, Fadavi A, Rafiee S (2020) Ultrasonic production of plant nutrients mist to use in aeroponic systems: feasibility and investigation of some effective parameters. Iran J Biosyst Eng 51:585–598. https://doi.org/10.22059/IJBSE.2020.295739.665263

    Article  Google Scholar 

  44. Weathers P, Liu C, Towler M, Wyslouzil B (2008) Mist reactors: principles, comparison of various systems, and case studies. Electron J Integr Biosci 3:29–37

    Google Scholar 

  45. Topp MN, Eisenklam P (1972) Industrial and medical uses of ultrasonic atomizers. Ultrasonics 10:127–133

    Article  CAS  PubMed  Google Scholar 

  46. Rooney JA (1981) 6. Nonlinear Phenomena. In: Methods in experimental physics. Elsevier, pp 299–353

  47. Tscheschke B, Dreimann J, von der Ruhr JW et al (2015) Evaluation of a new mist-chamber bioreactor for biotechnological applications. Biotechnol Bioeng 112:1155–1164. https://doi.org/10.1002/BIT.25523

    Article  CAS  PubMed  Google Scholar 

  48. Urbanska N, Giebultowicz J, Olszowska O, Szypula WJ (2014) The growth and saponin production of Platycodon grandiflorum (Jacq.) A. DC. (Chinese bellflower) hairy roots cultures maintained in shake flasks and mist bioreactor. Acta Soc Bot Pol 83

  49. Hao Z, Ouyang F, Geng Y et al (1998) Propagation of potato tubers in a nutrient mist bioreactor. Biotechnol Tech 12:641–644

    Article  CAS  Google Scholar 

  50. Liu CZ, Wang YC, Zhao B et al (1999) Development of a nutrient mist bioreactor for growth of hairy roots. Vitr Cell Dev Biol 35:271–274

    Article  Google Scholar 

  51. Dilorio AA, Cheetham RD, Weathers PJ (1992) Growth of transformed roots in a nutrient mist bioreactor: reactor performance and evaluation. Appl Microbiol Biotechnol 37:457–462

    Article  Google Scholar 

  52. Sung L, Huang S (2006) Lateral root bridging as a strategy to enhance l-DOPA production in Stizolobium hassjoo hairy root cultures by using a mesh hindrance mist trickling bioreactor. Biotechnol Bioeng 94:441–447

    Article  CAS  PubMed  Google Scholar 

  53. Fei L, Weathers PJ (2014) From cells to embryos to rooted plantlets in a mist bioreactor. Plant Cell Tissue Organ Cult 116:37–46

    Article  CAS  Google Scholar 

  54. Mousavi M (2015) Improve Bougainvillea shoot growth in vitro using a modified temporary immersion system (TIS). Int J Rev Life Sci 5:325–330

    Google Scholar 

  55. Regueira M, Rial E, Blanco B et al (2018) Micropropagation of axillary shoots of Salix viminalis using a temporary immersion system. Trees 32:61–71

    Article  CAS  Google Scholar 

  56. Cham CL, Tan AH, Tan WH (2017) Identification of a multivariable nonlinear and time-varying mist reactor system. Control Eng Pract 63:13–23

    Article  Google Scholar 

  57. Cham CL, Tan AH, Tan WH (2016) Design and construction of a mist reactor system. In: 2016 IEEE Region 10 Conference (TENCON). IEEE, pp 3382–3385

  58. Cham CL, Tan AH, Tan WH (2020) Identification of a parameter-varying mist reactor for cell culture. IFAC-PapersOnLine 53:622–627

    Article  Google Scholar 

  59. Cham CL, Tan AH, Tan WH, Sarker MT (2020) Model predictive control with direct feedthrough with application on a mist reactor. IFAC-PapersOnLine 53:183–188

    Article  Google Scholar 

  60. Akita M, Shigeoka T, Koizumi Y, Kawamura M (1994) Mass propagation of shoots of Stevia rebaudiana using a large scale bioreactor. Plant Cell Rep 13:180–183

    CAS  PubMed  Google Scholar 

  61. Buer CS, Correll MJ, Smith TC et al (1996) Development of a nontoxic acoustic window nutrient-mist bioreactor and relevant growth data. Vitr Cell Dev Biol 32:299–304. https://doi.org/10.1007/BF02822703

    Article  Google Scholar 

  62. Rahman MZ, Islam SMS, Chowdhury AN, Subramaniam S (2015) Efficient microtuber production of potato in modified nutrient spray bioreactor system. Sci Hortic (Amsterdam) 192:369–374

    Article  CAS  Google Scholar 

  63. Piatczak E, Chmiel A, Wysokinska H (2005) Mist trickling bioreactor for Centaurium erythraea Rafn growth of shoots and production of secoiridoids. Biotechnol Lett 27:721–724

    Article  CAS  PubMed  Google Scholar 

  64. Olędzka H, Gajdzis-Kuls D, GąSKA A et al (2009) Paclitaxel and cephalomannine in in vitro cultures of Taxus cuspidata Sieb. et Zucc. shoots and plantlets. Herba Pol 55:231–237

    Google Scholar 

  65. Fei L, Weathers P (2015) From leaf explants to rooted plantlets in a mist reactor. Vitr Cell Dev Biol 51:669–681

    Article  CAS  Google Scholar 

  66. Fei L, Weathers P (2016) From leaf explants to hanging rooted plantlets in a mist reactor. Plant Cell Tissue Organ Cult 124:265–274

    Article  CAS  Google Scholar 

  67. Jesionek A, Kokotkiewicz A, Wlodarska P et al (2017) Bioreactor shoot cultures of Rhododendron tomentosum (Ledum palustre) for a large-scale production of bioactive volatile compounds. Plant Cell Tissue Organ Cult 131:51–64

    Article  CAS  Google Scholar 

  68. Weathers PJ, Cheetham RD, Giles KL (1988) Dramatic increases in shoot number and lengths for Musa, Cordyline, and Nephrylepsis using nutrient mists. In: Symposium on high technology in protected cultivation, vol 230. pp 39–44

  69. Correll MJ, Wu Y, Weathers PJ (2000) Controlling hyperhydration of carnations (Dianthus caryophyllus L.) grown in a mist reactor. Biotechnol Bioeng 71:307–314

    Article  CAS  PubMed  Google Scholar 

  70. Correll MJ, Weathers PJ (2001) Effects of light, CO 2 and humidity on carnation growth, hyperhydration and cuticular wax development in a mist reactor. Vitr Cell Dev Biol 37:405–413

    Article  Google Scholar 

  71. Correll MJ, Weathers PJ (2001) One-step acclimatization of plantlets using a mist reactor. Biotechnol Bioeng 73:253–258

    Article  CAS  PubMed  Google Scholar 

  72. Tisserat B, Jones D, Galletta PD (1993) Construction and use of an inexpensive in vitro ultrasonic misting system. HortTechnology 3:75–78

    Article  Google Scholar 

  73. Liu C-Z, Wang Y-C, Guo C et al (1998) Production of artemisinin by shoot cultures of Artemisia annua L. in a modified inner-loop mist bioreactor. Plant Sci 135:211–217

    Article  CAS  Google Scholar 

  74. Weathers PJ, Giles KL (1988) Regeneration of plants using nutrient mist culture. Vitr Cell Dev Biol 24:727–732

    Article  Google Scholar 

  75. Wang GR, Qi NM (2010) Influence of mist intervals and aeration rate on growth and second metabolite production of Pseudostellaria heterophylla adventitious roots in a siphon-mist bioreactor. Biotechnol Bioprocess Eng 15:1059–1064

    Article  CAS  Google Scholar 

  76. Simonetti G, Tocci N, Valletta A et al (2016) In vitro antifungal activity of extracts obtained from Hypericum perforatum adventitious roots cultured in a mist bioreactor against planktonic cells and biofilm of Malassezia furfur. Nat Prod Res 30:544–550

    Article  CAS  PubMed  Google Scholar 

  77. Towler MJ (2005) Effects of inoculum density, carbon concentration, and feeding scheme on the growth of transformed roots of Artemisia annua in a modified nutrient mist bioreactor. Worcester Polytechnic Institute

  78. Kurata K, Ibaraki Y, Goto E (1991) System for micropropagation by nutrient mist supply. Trans ASAE 34:621–624

    Article  Google Scholar 

  79. Whitney PJ (1990) Novel bio-reactors for plant root organ cultures. Abstr VII Intl Cong Plant Tissue Cell Cult, Amsterdam

  80. Whitney PJ (1992) Novel bioreactors for the growth of roots transformed by Agrobacterium rhizogenes. Enzyme Microb Technol 14:13–17

    Article  CAS  Google Scholar 

  81. Nuutila A-M, Lindqvist AS, Kauppinen V (1997) Growth of hairy root cultures of strawberry (Fragaria¥ ananassa Duch.) in three different types of bioreactors. Biotechnol Tech 11:363–366

    Article  CAS  Google Scholar 

  82. Bais HP, Suresh B, Rachavarao K, Ravishankar GA (2002) Performance of hairy root cultures of Cichorium intybus L. in bioreactors of different configurations. Vitr Cell Dev Biol 38:573–580

    Article  CAS  Google Scholar 

  83. Palazón J, Mallol A, Eibl R et al (2003) Growth and ginsenoside production in hairy root cultures of Panax ginseng using a novel bioreactor. Planta Med 69:344–349

    Article  PubMed  Google Scholar 

  84. Suresh B, Bais HP, Raghavarao K et al (2005) Comparative evaluation of bioreactor design using Tagetes patula L. hairy roots as a model system. Process Biochem 40:1509–1515

    Article  CAS  Google Scholar 

  85. Sivakumar G, Liu C, Towler MJ, Weathers PJ (2010) Biomass production of hairy roots of Artemisia annua and Arachis hypogaea in a scaled-up mist bioreactor. Biotechnol Bioeng 107:802–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Srivastava S, Srivastava AK (2012) In vitro azadirachtin production by hairy root cultivation of Azadirachta indica in nutrient mist bioreactor. Appl Biochem Biotechnol 166:365–378

    Article  CAS  PubMed  Google Scholar 

  87. Jaremicz Z, Luczkiewicz M, Kokotkiewicz A et al (2014) Production of tropane alkaloids in Hyoscyamus niger (black henbane) hairy roots grown in bubble-column and spray bioreactors. Biotechnol Lett 36:843–853

    Article  CAS  PubMed  Google Scholar 

  88. Kochan E, Szymczyk P, Szymańska G (2016) Nitrogen and phosphorus as the factors affecting ginsenoside production in hairy root cultures of Panax quinquefolium cultivated in shake flasks and nutrient sprinkle bioreactor. Acta Physiol Plant 38:149

    Article  CAS  Google Scholar 

  89. Patra N, Srivastava AK (2016) Artemisinin production by plant hairy root cultures in gas-and liquid-phase bioreactors. Plant Cell Rep 35:143–153

    Article  CAS  PubMed  Google Scholar 

  90. Kochan E, Balcerczak E, Lipert A et al (2018) Methyl jasmonate as a control factor of the synthase squalene gene promoter and ginsenoside production in American ginseng hairy root cultured in shake flasks and a nutrient sprinkle bioreactor. Ind Crops Prod 115:182–193

    Article  CAS  Google Scholar 

  91. Sitarek P, Kowalczyk T, Picot L et al (2018) Growth of Leonurus sibiricus L. roots with over-expression of AtPAP1 transcriptional factor in closed bioreactor, production of bioactive phenolic compounds and evaluation of their biological activity. Ind Crops Prod 122:732–739

    Article  CAS  Google Scholar 

  92. Wilson PDG, Hilton MG, Meehan PTH et al (1990) The cultivation of transformed roots from laboratory to pilot plant. In: Nijkamp HJJ, Van Der Plas LHW, Van Aartrijk J (eds) Progress in plant cellular and molecular biology. Springer, Dordrecht, pp 700–705

    Chapter  Google Scholar 

  93. Wilson PDG (1997) The Pilot-Scale Cultivation of 16 Transformed Roots. Hairy Roots 179

  94. Huang S-Y, Hung C-H, Chou S-N (2004) Innovative strategies for operation of mist trickling reactors for enhanced hairy root proliferation and secondary metabolite productivity. Enzyme Microb Technol 35:22–32

    Article  CAS  Google Scholar 

  95. Huang S-Y, Chou S-N (2006) Elucidation of the effects of nitrogen source on proliferation of transformed hairy roots and secondary metabolite productivity in a mist trickling reactor by redox potential measurement. Enzyme Microb Technol 38:803–813

    Article  CAS  Google Scholar 

  96. Liu C, Towler MJ, Medrano G et al (2009) Production of mouse interleukin-12 is greater in tobacco hairy roots grown in a mist reactor than in an airlift reactor. Biotechnol Bioeng 102:1074–1086

    Article  CAS  PubMed  Google Scholar 

  97. Chatterjee C, Correll MJ, Weathers PJ et al (1997) Simplified acoustic window mist bioreactor. Biotechnol Tech 11:155–158

    Article  CAS  Google Scholar 

  98. Weathers PJ, Wyslouzil BE, Wobbe KK et al (1999) The biological response of hairy roots to O 2 levels in bioreactors. Vitr Cell Dev Biol 35:286–289

    Article  CAS  Google Scholar 

  99. Wyslouzil BE, Waterbury RG, Weathers PJ (2000) The growth of single roots of Artemisia annua in nutrient mist reactors. Biotechnol Bioeng 70:143–150

    Article  CAS  PubMed  Google Scholar 

  100. Kim Y, Wyslouzil B, Weathers P (2001) A comparative study of mist and bubble column reactors in the in vitro production of artemisinin. Plant Cell Rep 20:451–455

    Article  CAS  Google Scholar 

  101. Souret FF, Kim Y, Wyslouzil BE et al (2003) Scale-up of Artemisia annua L. hairy root cultures produces complex patterns of terpenoid gene expression. Biotechnol Bioeng 83:653–667

    Article  CAS  PubMed  Google Scholar 

  102. Towler MJ, Wyslouzil BE, Weathers PJ (2007) Using an aerosol deposition model to increase hairy root growth in a mist reactor. Biotechnol Bioeng 96:881–891

    Article  CAS  PubMed  Google Scholar 

  103. DiIorio AA, Cheetham RD, Weathers PJ (1992) Carbon dioxide improves the growth of hairy roots cultured on solid medium and in nutrient mists. Appl Microbiol Biotechnol 37:463–467

    Article  CAS  Google Scholar 

  104. Weathers P, Giles K (1989) Mist cultivation of cells

  105. Kim YJ, Weathers PJ, Wyslouzil BE (2002) Growth of Artemisia annua hairy roots in liquid-and gas-phase reactors. Biotechnol Bioeng 80:454–464

    Article  CAS  PubMed  Google Scholar 

  106. Ooshima H, Yamane Y, Nakamura Y et al (1998) Design of a spray-cycle bioreactor and its application for riboflavin production. Appl Biochem Biotechnol 73:51–58

    Article  CAS  Google Scholar 

  107. Sharaf-Eldin MA, Weathers PJ (2006) Movement and containment of microbial contamination in the nutrient mist bioreactor. Vitr Cell Dev Biol 42:553–557

    Article  Google Scholar 

  108. Fadavi A, Gholami Banadkoki O, Mansouri A (2021) Performance evaluation of ultrasonic transducer in a mist bioreactor by different nutrient media. Biotechnol Lett. https://doi.org/10.1007/s10529-021-03168-0

    Article  PubMed  Google Scholar 

  109. Jackson MB (2002) Ventilation of plant tissue cultures. In: First international symposium on liquid systems for in vitro mass propagation of plants. Cost, pp 56–57

  110. Fujiwara K, Kozai T (1995) Physical microenvironment and its effects. In: Automation and environmental control in plant tissue culture. Springer, pp 319–369

  111. McAlister BG (2003) In vitro propagation of eucalytpus clones using a temporary immersion bioreactor system (RITA)

  112. Cortes-Morales JA, López-Laredo AR, Zamilpa A et al (2018) Morphogenesis and secondary metabolites production in the medicinal plant Castilleja tenuiflora Benth. under nitrogen deficiency and starvation stress in a temporary immersion system. Rev Mex Ing Química 17:229–242

    Article  CAS  Google Scholar 

  113. Ellis DD, Webb DT (1993) Light regimes used in conifer tissue culture. In: Micropropagation of woody plants. Springer, pp 31–55

  114. Polzin F, Sylvestre I, Déchamp E et al (2014) Effect of activated charcoal on multiplication of African yam (Dioscorea cayenensis-rotundata) nodal segments using a temporary immersion bioreactor (RITA®). Vitr Cell Dev Biol 50:210–216

    Article  CAS  Google Scholar 

  115. Du C, Yan J (2017) Plasma remediation technology for environmental protection. Springer

    Book  Google Scholar 

  116. Hsiao TY, Bacani FT, Carvalho EB, Curtis WR (1999) Development of a low capital investment reactor system: application for plant cell suspension culture. Biotechnol Prog 15:114–122

    Article  CAS  PubMed  Google Scholar 

  117. Sodian R, Lemke T, Loebe M et al (2001) New pulsatile bioreactor for fabrication of tissue-engineered patches. J Biomed Mater Res 58:401–405

    Article  CAS  PubMed  Google Scholar 

  118. Bijonowski BM, Miller WM, Wertheim JA (2013) Bioreactor design for perfusion-based, highly vascularized organ regeneration. Curr Opin Chem Eng 2:32–40

    Article  PubMed  PubMed Central  Google Scholar 

  119. Moreau M, Orange N, Feuilloley MGJ (2008) Non-thermal plasma technologies: new tools for bio-decontamination. Biotechnol Adv 26:610–617

    Article  CAS  PubMed  Google Scholar 

  120. Zieliński M, Dębowski M (2018) The possibility of hybrid-bioreactor heating by the microwave radiation. Int J Chem React Eng. https://doi.org/10.1515/ijcre-2016-0115

    Article  Google Scholar 

  121. Correia V, Panadero JA, Ribeiro C et al (2016) Design and validation of a biomechanical bioreactor for cartilage tissue culture. Biomech Model Mechanobiol 15:471–478

    Article  CAS  PubMed  Google Scholar 

  122. Kamaroddin MF, Hanotu J, Gilmour DJ, Zimmerman WB (2016) In-situ disinfection and a new downstream processing scheme from algal harvesting to lipid extraction using ozone-rich microbubbles for biofuel production. Algal Res 17:217–226

    Article  Google Scholar 

  123. Bulso LA (2006) Modeling the effect of the separation of gas stream from droplet stream on the growth rate of transformed roots of Artemisia annua in a nutrient mist bioreactor. Worcester Polytechnic Institute

  124. Huang LX, Kumar K, Mujumdar AS (2006) A comparative study of a spray dryer with rotary disc atomizer and pressure nozzle using computational fluid dynamic simulations. Chem Eng Process Process Intensif 45:461–470

    Article  CAS  Google Scholar 

  125. Lefebvre AH (1990) Energy considerations in twin-fluid atomization. J Am Soc Mech Eng. https://doi.org/10.1115/90-GT-003

    Article  Google Scholar 

  126. Dalmoro A, d’Amore M, Barba AA (2013) Droplet size prediction in the production of drug delivery microsystems by ultrasonic atomization. Transl Med UniSa 7:6

    PubMed  PubMed Central  Google Scholar 

  127. Ramisetty KA, Pandit AB, Gogate PR (2013) Investigations into ultrasound induced atomization. Ultrason Sonochem 20:254–264

    Article  CAS  PubMed  Google Scholar 

  128. Mackay WA, Kitto SL (1988) Factors affecting in vitro shoot proliferation of French tarragon. J Am Soc Hortic Sci 113:282–287

    Article  CAS  Google Scholar 

  129. Wyslouzil BE, Whipple M, Chatterjee C et al (1997) Mist deposition onto hairy root cultures: aerosol modeling and experiments. Biotechnol Prog 13:185–194

    Article  CAS  PubMed  Google Scholar 

  130. Flagan RC, Seinfeld JH (1988) Fundamentals of air pollution engineering.(I. Prentice-Hall, Ed.). New Jersey

  131. Kuwabara S (1959) The forces experienced by randomly distributed parallel circular cylinders or spheres in a viscous flow at small Reynolds numbers. J Phys Soc Japan 14:527–532

    Article  Google Scholar 

  132. Crawford M (1976) Air pollution control theory. McGraw-Hill Companies

  133. Tervasmäki P, Latva-Kokko M, Taskila S, Tanskanen J (2018) Effect of oxygen transfer on yeast growth—Growth kinetic and reactor model to estimate scale-up effects in bioreactors. Food Bioprod Process 111:129–140

    Article  CAS  Google Scholar 

  134. Botella C, Hernandez JE, Webb C (2019) Dry weight model, capacitance and metabolic data as indicators of fungal biomass growth in solid state fermentation. Food Bioprod Process 114:144–153

    Article  CAS  Google Scholar 

  135. Rončević Z, Grahovac J, Dodić S et al (2019) Utilisation of winery wastewater for xanthan production in stirred tank bioreactor: Bioprocess modelling and optimisation. Food Bioprod Process 117:113–125

    Article  CAS  Google Scholar 

  136. Kaleybar LS, Khoshfetrat AB, Charoudeh HN (2020) Modeling and performance prediction of a conceptual bioprocess for mass production of suspended stem cells. Food Bioprod Process 122:254–268

    Article  CAS  Google Scholar 

  137. Ranjan R, Katuri SR, Khanna R (2015) Discrete modeling of growth of hairy roots in a mist bioreactor. Chem Eng Technol 38:391–398

    Article  CAS  Google Scholar 

  138. Woo SH, Park JM, Yang J-W (1997) Induction of branch roots by cutting method in t Hyoscyamus niger root culture. Plant Cell Tissue Organ Cult 48:131–134

    Article  Google Scholar 

  139. Taya M, Kino-oka M, Tone S, Kobayashi T (1989) A kinetic model of branching growth of plant hairy root. J Chem Eng Japan 22:698–700

    Article  Google Scholar 

  140. Nakashimada Y, Uozumi N, Kobayashi T (1994) Stimulation of emergence of root apical meristems in horseradish hairy root by auxin supplementation and its kinetic model. J Ferment Bioeng 77:178–182

    Article  CAS  Google Scholar 

  141. Kim S, Hopper E, Hjortso M (1995) Hairy root growth models: effect of different branching patterns. Biotechnol Prog 11:178–186

    Article  CAS  Google Scholar 

  142. Chavarria-Krauser A, Schurr U (2004) A cellular growth model for root tips. J Theor Biol 230:21–32

    Article  CAS  PubMed  Google Scholar 

  143. Ranjan R, Ahmed N, Khanna R, Mishra BN (2009) Design of an ON/OFF mist duty cycle in mist bioreactors for the growth of hairy roots. Biotechnol Bioprocess Eng 14:38–45

    Article  CAS  Google Scholar 

  144. Palavalli RR, Srivastava S, Srivastava AK (2012) Development of a mathematical model for growth and oxygen transfer in in vitro plant hairy root cultivations. Appl Biochem Biotechnol 167:1831–1844

    Article  CAS  PubMed  Google Scholar 

  145. Sharp JM, Doran PM (1990) Characteristics of growth and tropane alkaloid synthesis in Atropa belladonna roots transformed by Agrobacterium rhizogenes. J Biotechnol 16:171–185

    Article  CAS  Google Scholar 

  146. Ranjan R, Khanna R, Mishra BN (2011) Sustained operation of nutrient mist reactor to grow hairy roots. Asia-Pacific J Chem Eng 6:23–28

    Article  CAS  Google Scholar 

  147. Ranjan R, Rao SK, Khanna R (2014) A strategy to choose process parameters for sustained operation of nutrient mist reactor to grow hairy roots. Int J Eng Invent 4:46–54

    Google Scholar 

  148. Doriya K, Kumar DS (2018) Optimization of solid substrate mixture and process parameters for the production of L-asparaginase and scale-up using tray bioreactor. Biocatal Agric Biotechnol 13:244–250

    Article  Google Scholar 

  149. Ashok A, Doriya K, Rao DRM, Kumar DS (2017) Design of solid state bioreactor for industrial applications: an overview to conventional bioreactors. Biocatal Agric Biotechnol 9:11–18

    Article  Google Scholar 

  150. Elsayed EA, Danial EN, Wadaan MA, El-Enshasy HA (2019) Production of β-galactosidase in shake-flask and stirred tank bioreactor cultivations by a newly isolated Bacillus licheniformis strain. Biocatal Agric Biotechnol 20:101231

    Article  Google Scholar 

  151. Nie J, Sun Y, Peng F et al (2020) Pseudorabies virus production using a serum-free medium in fixed-bed bioreactors with low cell inoculum density. Biotechnol Lett 42:2551–2560

    Article  CAS  PubMed  Google Scholar 

  152. Maiorano AE, da Silva ES, Perna RF et al (2020) Effect of agitation speed and aeration rate on fructosyltransferase production of Aspergillus oryzae IPT-301 in stirred tank bioreactor. Biotechnol Lett 42:2619–2629

    Article  CAS  PubMed  Google Scholar 

  153. Wang C, Wang J, Chen M et al (2018) Ultra-low carbon dioxide partial pressure improves the galactosylation of a monoclonal antibody produced in Chinese hamster ovary cells in a bioreactor. Biotechnol Lett 40:1201–1208

    Article  CAS  PubMed  Google Scholar 

  154. Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30:528–537

    Article  CAS  PubMed  Google Scholar 

  155. González EJ (2005) Mass propagation of tropical crops in temporary immersion systems. In: Liquid culture systems for in vitro plant propagation. Springer, pp 197–211

  156. Welander M, Persson J, Asp H, Zhu LH (2014) Evaluation of a new vessel system based on temporary immersion system for micropropagation. Sci Hortic (Amsterdam) 179:227–232

    Article  CAS  Google Scholar 

  157. Williams GRC, Doran PM (1999) Investigation of liquid–solid hydrodynamic boundary layers and oxygen requirements in hairy root cultures. Biotechnol Bioeng 64:729–740

    Article  CAS  PubMed  Google Scholar 

  158. Shiao T, Doran PM (2000) Root hairiness: effect on fluid flow and oxygen transfer in hairy root cultures. J Biotechnol 83:199–210

    Article  CAS  PubMed  Google Scholar 

  159. Bais HP, Ravishankar GA (2001) Cichorium intybus L–cultivation, processing, utility, value addition and biotechnology, with an emphasis on current status and future prospects. J Sci Food Agric 81:467–484

    Article  CAS  Google Scholar 

  160. Huang T-K, McDonald KA (2012) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol Adv 30:398–409

    Article  CAS  PubMed  Google Scholar 

  161. Georgiev VG, Bley T, Pavlov AI (2013) Bioreactors for the cultivation of red beet hairy roots. In: Red beet biotechnology. Springer, pp 251–281

  162. Patra N, Srivastava AK (2015) Use of model-based nutrient feeding for improved production of artemisinin by hairy roots of Artemisia annua in a modified stirred tank bioreactor. Appl Biochem Biotechnol 177:373–388

    Article  CAS  PubMed  Google Scholar 

  163. Taki M, Rohani A, Rahmati-Joneidabad M (2018) Solar thermal simulation and applications in greenhouse. Inf Process Agric 5:83–113

    Google Scholar 

  164. Cai W, Wei R, Xu L, Ding X (2021) A method for modelling greenhouse temperature using gradient boost decision tree. Inf Process Agric. https://doi.org/10.1016/j.inpa.2021.08.004

    Article  Google Scholar 

  165. Pawar SB (2018) Computational fluid dynamics (CFD) analysis of airlift bioreactor: effect of draft tube configurations on hydrodynamics, cell suspension, and shear rate. Bioprocess Biosyst Eng 41:31–45

    Article  CAS  PubMed  Google Scholar 

  166. Kazemzadeh A, Elias C, Tamer M, Ein-Mozaffari F (2018) Hydrodynamic performance of a single-use aerated stirred bioreactor in animal cell culture: applications of tomography, dynamic gas disengagement (DGD), and CFD. Bioprocess Biosyst Eng 41:679–695

    Article  CAS  PubMed  Google Scholar 

  167. Habibi A, Nalband M, Jalilnejad E (2019) Experimentation and CFD modeling of continuous degradation of formaldehyde by immobilized Ralstonia eutropha in a semi-pilot-scale plug flow bioreactor. Bioprocess Biosyst Eng 42:485–497

    Article  CAS  PubMed  Google Scholar 

  168. Gamborg OL, Miller R, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  CAS  PubMed  Google Scholar 

  169. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  170. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50:199–204

    Article  CAS  Google Scholar 

  171. Lloyd G, McCown B (1981) Commercially-feasible micro-propagation of Mountain Laurel, Kalmia latifolia, by use of shoot-tip culture. Proc Int Plant Propagators Soc 30:421–427

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the University of Tehran and Dr. Mohammad Hassan Torabi.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ali Hajiahmad.

Ethics declarations

Conflict of interest

The authors declare they have no financial interests or non-financial interests. Besides, all authors certify that they have no affiliations with or involvement in any organization or entity with any financial or non-financial interest in the subject matter or materials discussed in this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mirzabe, A.H., Hajiahmad, A., Fadavi, A. et al. Design of nutrient gas-phase bioreactors: a critical comprehensive review. Bioprocess Biosyst Eng 45, 1239–1265 (2022). https://doi.org/10.1007/s00449-022-02728-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-022-02728-6

Keywords

Navigation