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Volume 67 Number 4
  • ISSN: 2056-5135


Microbubbles are famed for their large surface area-to-volume ratio, with the promise of intensification of interfacial phenomena, highlighted by more rapid gas exchange. However, for bioprocessing, it has been recognised for many decades that surfactant-rich fermentation media hinders mass transfer and possibly other interfacial processes due to surfactant loading on the interface. This article focuses on the roles of microbubble size and bubble bank, dispersed microbubbles that are sufficiently small to be non-buoyant, in mediating other modes of interfacial transfer collisions with microorganisms and self-assembled clusters of microorganisms and microbubbles. These provide a more direct route of mass transfer for product gases that can be released directly to the microbubble with ~104 faster diffusion rates than liquid mediated gas exchange. Furthermore, secreted external metabolites with amphoteric character are absorbed along the microbubble interface, providing a faster route for liquid solute transport than diffusion through the boundary layer. These mechanisms can be exploited by the emerging fields of symbiotic or microbiome engineering to design self-assembled artificial lichen dispersed structures that can serve as a scaffold for the selected constituents. Additionally, such designed scaffolds can be tuned, along with the controllable parameters of microbubble mediated flotation separations or hot microbubble stripping for simultaneous or product removal. Staging the product removal thus has benefits of decreasing the inhibitory effect of secreted external metabolites on the microorganism that produced them. Evidence supporting these hypotheses are produced from reviewing the literature. In particular, recent work in co-cultures of yeast and microalgae in the presence of a dispersed bubble bank, as well as anaerobic digestion (AD) intensification with dispersed, seeded microbubbles, is presented to support these proposed artificial lichen clusters.


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  1. Gilmour D. J., Zimmerman W. B., and Poole R. K. ‘Microbubble Intensification of Bioprocessing’, in “Advances in Microbial Physiology”, ed. Elsevier Ltd, London, UK, 2020, pp. 135 LINK [Google Scholar]
  2. Bailey J. E., and Ollis D. F. “Biochemical Engineering Fundamentals”, 2nd Edn., McGraw Hill, New York, USA, 1986 [Google Scholar]
  3. Al-Mashhadani M. K. H., Wilkinson S. J., and Zimmerman W. B. Chem. Eng. Sci., 2015, 137, 243 LINK [Google Scholar]
  4. Fan W., Desai P., Zimmerman W. B., Duan Y., Crittenden J. C., Wang C., and Huo M. J. Clean. Prod., 2021, 294, 126258 LINK [Google Scholar]
  5. Raghavendran V., Webb J. P., Cartron M. L., Springthorpe V., Larson T. R., Hines M., Mohammed H., Zimmerman W. B., Poole R. K., and Green J. Biotechnol. Biofuels, 2020, 13, 104 LINK [Google Scholar]
  6. Desai P. D., Turley M., Robinson R., and Zimmerman W. B. Chem. Eng. Process.: Process Intensif., 2022, 180, 108693 LINK [Google Scholar]
  7. Zimmerman W. B., Zandi M., Bandulasena H. C. H., Tesař V., Gilmour D. J., and Ying K. Appl. Energy, 2011, 88, (10), 3357 LINK [Google Scholar]
  8. Hanotu J., Kong D., and Zimmerman W. B. Food Bioprod. Process., 2016, 100, (A), 424 LINK [Google Scholar]
  9. Harnby N., Edwards M. F., and Nienow A. W. “Mixing in the Process Industries”, 2nd Edn., Butterworth-Heinemann, Oxford, UK, 1992 [Google Scholar]
  10. Clift R., Grace J. R., and Weber M. E. “Bubbles, Drops, and Particles”, Academic Press Inc, New York, USA, 1978 [Google Scholar]
  11. Schulze G., and Schlünder E. U. Chem. Eng. Process.: Process Intensif., 1985, 19, (5), 257 LINK [Google Scholar]
  12. Rosso D., and Stenstrom M. K. Water Res., 2006, 40, (7), 1397 LINK [Google Scholar]
  13. Nienow A. W. Cytotechnology, 2006, 50, (1–3), 9 LINK [Google Scholar]
  14. Hanotu J., Bandulasena H. C. H., and Zimmerman W. B. Biotechnol. Bioeng., 2012, 109, (7), 1663 LINK [Google Scholar]
  15. Zimmerman W. B., Tesař V., and Bandulasena H. C. H. Curr. Opin. Colloid Interface Sci., 2011, 16, (4), 350 LINK [Google Scholar]
  16. Desai P. D., Hines M., Riaz Y., and Zimmerman W. Energies, 2018, 11, (10), 2680 LINK [Google Scholar]
  17. Rehman F., Medley G. J. D., Bandulasena H., and Zimmerman W. B. J. Environ. Res., 2015, 137, 32 LINK [Google Scholar]
  18. Bandyopadhyay B., Humphrey A. E., and Taguchi H. Biotechnol. Bioeng., 2009, 104, (5), 841 LINK [Google Scholar]
  19. Ying K., Gilmour D. J., and Zimmerman W. B. Int. J. Mol. Sci., 2015, 16, (5), 11509 LINK [Google Scholar]
  20. de Donder Th., “L’Affinité”, ed. and Van Rysselberghe P. Gauthier-Villars, Paris, France, 1936 [Google Scholar]
  21. Prigogine I. “From Being to Becoming: Time and Complexity in the Physical Sciences”, W. H. Freeman and Company, San Francisco, USA, 1980 [Google Scholar]
  22. Abdulrazzaq N. N., Al-Sabbagh B. H., Rees J. M., and Zimmerman W. B. Ind. Eng. Chem. Res., 2016, 55, (50), 12909 LINK [Google Scholar]
  23. Tesař V., Hung C.-H., and Zimmerman W. B. Sensors Actuators A: Phys., 2006, 125, (2), 159 LINK [Google Scholar]
  24. Kaye G. W. C., and Laby T. H. “Tables of Physical and Chemical Constants and Some Mathematical Functions”, 15th Edn., Longman, New York, USA, 1986, p. 219 [Google Scholar]
  25. Worden R. M., Bredwell M. D., and Grethlein A. J. ‘Engineering Issues in Synthesis-Gas Fermentations’, ACS Symposium Series, Vol. 666, Ch. 18, American Chemical Society, Washington, DC, USA, 1997, pp. 320335 LINK [Google Scholar]
  26. Al-Mashhadani M. K. H., Wilkinson S. J., and Zimmerman W. B. Chem. Eng. Sci., 2016, 156, 24 LINK [Google Scholar]
  27. Al-Mashhadani M. K. H. ‘Application of Microbubbles Generated by Fluidic Oscillation in the Anaerobic Digestion Process’, PhD Thesis, Chemical and Biological Engineering Department, University of Sheffield, UK, February, 2013, 276 pp LINK [Google Scholar]
  28. Al-Mashhadani M. K. H., Bandulasena H. C. H., and Zimmerman W. B. Ind. Eng. Chem. Res., 2012, 51, (4), 1864 LINK [Google Scholar]
  29. Desai P. D., Ng W. C., Hines M. J., Riaz Y., Tesar V., and Zimmerman W. B. Colloids Interfaces, 2019, 3, (4), 65 LINK [Google Scholar]
  30. Chatterjee D., Jain P., and Sarkar K. Phys. Fluids, 2005, 17, (10), 100603 LINK [Google Scholar]
  31. Zimmerman W. B., Al-Mashhadani M. K. H., and Bandulasena H. C. H. Chem. Eng. Sci., 2013, 101, 865 LINK [Google Scholar]
  32. Tesař V. Chem. Eng. J., 2014, 235, 368 LINK [Google Scholar]
  33. Krzan M., Zawala J., and Malysa K. Colloids Surf. A: Physicochem. Eng. Asp., 2007, 298, (1–2), 42 LINK [Google Scholar]
  34. Dhanarajan G., Patra P., Rangarajan V., Somasundaran P., and Sen R. ACS Sustain. Chem. Eng., 2018, 6, (3), 4046 LINK [Google Scholar]
  35. Singhal S., Moser C. C., and Wheatley M. A. Langmuir, 1993, 9, (9), 2426 LINK [Google Scholar]
  36. Takahashi M. J. Phys. Chem. B, 2005, 109, (46), 21858 LINK [Google Scholar]
  37. Xu Q., Nakajima M., Ichikawa S., Nakamura N., Roy P., Okadome H., and Shiina T. J. Colloid Interface Sci., 2009, 332, (1), 208 LINK [Google Scholar]
  38. Edzwald J. K. Water Res., 2010, 44, (7), 2077 LINK [Google Scholar]
  39. Dai Z., Fornasiero D., and Ralston J. Adv. Colloid Interface Sci., 2000, 85, (2–3), 231 LINK [Google Scholar]
  40. Kitchener J. A., and Gochin R. J. Water Res., 1981, 15, (5), 585 LINK [Google Scholar]
  41. Teixeira M. R., and Rosa M. J. Sep. Purif. Technol., 2006, 52, (1), 84 LINK [Google Scholar]
  42. Teixeira M. R., Sousa V., and Rosa M. J. Water Res., 2010, 44, (11), 3337 LINK [Google Scholar]
  43. Hanotu J., Bandulasena H. C. H., Chiu T. Y., and Zimmerman W. B. Int. J. Multiph. Flow, 2013, 56, 119 LINK [Google Scholar]
  44. Hanotu J., Karunakaran E., Bandulasena H., Biggs C., and Zimmerman W. B. Biochem. Eng. J., 2014, 82, 174 LINK [Google Scholar]
  45. Fuerstenau D. W. Adv. Colloid Interface Sci., 2005, 114115, 9 LINK [Google Scholar]
  46. Feynman R. P. Eng. Sci., 1960, 23, (5), 22 [Google Scholar]
  47. Weaire D., and Hutzler S. “The Physics of Foams”, Oxford University Press Inc, New York, USA, 1999 [Google Scholar]
  48. Farajzadeh R., Vincent-Bonnieu S., and Bourada Bourada N. J. Soft Matter, 2014, 145352 LINK [Google Scholar]
  49. Yehia A., and Al-Wakeel M. I. Miner. Eng., 2000, 13, (1), 111 LINK [Google Scholar]
  50. Wang J., Wang L., Hanotu J., and Zimmerman W. B. Fuel Process. Technol., 2017, 165, 131 LINK [Google Scholar]
  51. Lemlich R. AIChE J., 1966, 12, (4), 802 LINK [Google Scholar]
  52. Fields P. R., Fryer P. J., Slater N. K. H., and Woods G. P. Chem. Eng. J., 1983, 27, (1), B 3 LINK [Google Scholar]
  53. Suzuki A., Maruyama H., and Seki H. J. Chem. Eng. Japan, 1996, 29, (5), 794 LINK [Google Scholar]
  54. Taylor S. F. R., Brittle S. A., Desai P., Jacquemin J., Hardacre C., and Zimmerman W. A. Phys. Chem. Chem. Phys., 2017, 19, (22), 14306 LINK [Google Scholar]
  55. Sanderson K. Nature, 2012 LINK [Google Scholar]
  56. Desai P., Jaffe S., and Zimmerman W. ‘Leidenfrost Like Effect Exhibited by Microbubbles for Biological Systems such as Anaerobic Fermenters’, Biotech France 2017 International Conference and Exhibition, Paris, France, 28th–30th June, 2017, Setcor Media FZ-LLC, Dubai, UAE, 2017 [Google Scholar]
  57. Al-yaqoobi A., Hogg D., and Zimmerman W. B. Int. J. Chem. Eng., 2016, 5210865 LINK [Google Scholar]
  58. “Adsorptive Bubble Separation Techniques”, ed. Lemlich R. Academic Press Inc, New York, USA, 1972 [Google Scholar]
  59. Clarke A. N., and Wilson D. J. “Foam Flotation: Theory and Applications”, Marcel Dekker, New York, USA, 1983 [Google Scholar]
  60. Alexandrova L., and Grigorov L. Int. J. Miner. Process., 1996, 48, (1–2), 111 LINK [Google Scholar]
  61. Santander M., Valderrama L., Guevara M., and Rubio J. Miner. Eng., 2011, 24, (9), 1010 LINK [Google Scholar]
  62. Pooja G., Kumar P. S., and Indraganti S. Chemosphere, 2022, 287, (2), 132231 LINK [Google Scholar]
  63. Waters K. E., Hadler K., and Cilliers J. J. Miner. Eng., 2008, 21, (12–14), 918 LINK [Google Scholar]
  64. Franklin B. AECOM Design Build, UK, private communication, 2015
  65. Alwared A. I., Abdulrazzaq N., and Al-Sabbagh B. Iraqi J. Chem. Pet. Eng., 2019, 20, (2), 1 LINK [Google Scholar]
  66. Yuan X. Z., Meng Y. T., Zeng G. M., Fang Y. Y., and Shi J. G. Colloids Surfaces A: Physicochem. Eng. Asp., 2008, 317, (1–3), 256 LINK [Google Scholar]
  67. Nafi A. W., and Taseidifar M. J. Environ. Manage., 2022, 319, 115666 LINK [Google Scholar]
  68. Bi P., Dong H., and Dong J. J. Chromatogr. A, 2010, 1217, (16), 2716 LINK [Google Scholar]
  69. Chew K. W., Chia S. R., Krishnamoorthy R., Tao Y., Chu D.-T., and Show P. L. Bioresour. Technol., 2019, 288, 121519 LINK [Google Scholar]
  70. Sankaran R., Cruz R. A. P., Show P. L., Haw C. Y., Lai S. H., Ng E.-P., and Ling T. C. Fluid Phase Equilib., 2019, 501, 112271 LINK [Google Scholar]
  71. Zeng J., Wang W., Lin J., Zhang Y., Li H., Liu J., Yan C., Gu Y., and Wei Y. J. Chromatogr. A, 2022, 1674, 463125 LINK [Google Scholar]
  72. Khoo K. S., Ooi C. W., Chew K. W., Chia S. R., Foo S. C., Ng H. S., and Show P. L. J. Chromatogr. A, 2022, 1668, 462915 LINK [Google Scholar]
  73. Padilha C. E. de A., Nogueira C. da C., Almeida H. N., de Medeiros W. R. D. B., Oliveira Filho M. A., de Araújo J. S., and dos Santos E. S. Food Bioprod. Process., 2020, 120, 151 LINK [Google Scholar]
  74. Peleka E. N., and Matis K. A. Open Chem., 2016, 14, (1), 132 LINK [Google Scholar]
  75. Rulyov N. ‘Colloidal-Hydrodynamic Theory of Flotation’, Science Direct Working Paper No. S1574-0331(04)70477-4, SSRN–Elsevier, New York, USA, March, 2001, 22 pp LINK [Google Scholar]
  76. Grammatika M., and Zimmerman W. B. Dyn. Atmos. Ocean., 2001, 34, (2–4), 327 LINK [Google Scholar]
  77. Kyzas G. Z., and Mitropoulos A. C. Nanomaterials, 2021, 11, (10), 2592 LINK [Google Scholar]
  78. Mesa D., van Heerden M., Cole K., Neethling S. J., and Brito-Parada P. R. Chem. Eng. Sci., 2022, 260, 117842 LINK [Google Scholar]
  79. Grassia P., Neethling S. J., and Cilliers J. J. Eur. Phys. J. E, 2002, 8, (S1), 517 LINK [Google Scholar]
  80. Neethling S. J., and Cilliers J. J. Int. J. Miner. Process., 2009, 93, (2), 141 LINK [Google Scholar]
  81. Wang G., Ge L., Mitra S., Evans G. M., Joshi J. B., and Chen S. Miner. Eng., 2018, 127, 153 LINK [Google Scholar]
  82. Quintanilla P., Neethling S. J., and Brito-Parada P. R. Miner. Eng., 2021, 162, 106718 LINK [Google Scholar]
  83. Rees-Zimmerman C. R., and Routh A. F. J. Fluid Mech., 2021, 928, A 15 LINK [Google Scholar]
  84. Thomas A., Winkler M. A., “Topics in Enzyme and Fermentation Biotechnology”, ed. and Wiseman A. Ellis Horwood, Chichester, UK, 1977 [Google Scholar]
  85. Pedley T. J., Hill N. A., and Kessler J. O. J. Fluid Mech., 1988, 195, 223 LINK [Google Scholar]
  86. Hill N. A., and Pedley T. J. Fluid Dynam. Res., 2005, 37, (1–2), 1 LINK [Google Scholar]
  87. Ouchi K., and Akiyama H. Agric. Biol. Chem., 1971, 35, (7), 1024 LINK [Google Scholar]
  88. Flor-Parra I., Bernal M., Zhurinsky J., and Daga R. R. Biol. Open, 2014, 3, (1), 108 LINK [Google Scholar]
  89. Ghose D., Jacobs K., Ramirez S., Elston T., and Lew D. Proc. Natl. Acad. Sci., 2021, 118, (22), e2025445118 LINK [Google Scholar]
  90. Palmieri M. C., Greenhalf W., and Laluce C. Biotechnol. Bioeng., 1996, 50, (3), 248 LINK<248::aid-bit3>;2-g [Google Scholar]
  91. Hu W., Gladue R., Hansen J., Wojnar C., and Chalmers J. J. Biotechnol. Prog., 2010, 26, (1), 79 LINK [Google Scholar]
  92. Ding Y.-D., Zhao S., Zhu X., Liao Q., Fu Q., and Huang Y. Clean Technol. Environ. Policy, 2016, 18, (7), 2039 LINK [Google Scholar]
  93. Pei H.-S., Guo C.-L., Zhang G.-F., Tang Q.-Y., and Guo F.-Q. Int. J. Heat Mass Transf., 2017, 110, 873 LINK [Google Scholar]
  94. Hossain A. I., Baghirzade B. S., Apul O., Kirisits M. J., Dev S., Das S., Islam S., Lai C.-Y., Huntington H. P., Umanzor S., Chen W.-T., Aggarwal S., and Saleh N. B. ACS EST Engg., 2022, 2, (4), 606 LINK [Google Scholar]
  95. Lawson C. E., Harcombe W. R., Hatzenpichler R., Lindemann S. R., Löffler F. E., O’Malley M. A., García Martín H., Pfleger B. F., Raskin L., Venturelli O. S., Weissbrodt D. G., Noguera D. R., and McMahon K. D. Nat. Rev. Microbiol., 2019, 17, (12), 725 LINK [Google Scholar]
  96. Samo T. J., Kimbrel J. A., Nilson D. J., Pett-Ridge J., Weber P. K., and Mayali X. Environ. Microbiol., 2018, 20, (12), 4385 LINK [Google Scholar]
  97. Kazamia E., Czesnick H., Van Nguyen T. T., Croft M. T., Sherwood E., Sasso S., Hodson S. J., Warren M. J., and Smith A. G. Environ. Microbiol., 2012, 14, (6), 1466 LINK [Google Scholar]
  98. Ramanan R., Kim B.-H., Cho D.-H., Oh H.-M., and Kim H.-S. Biotechnol. Adv., 2016, 34, (1), 14 LINK [Google Scholar]
  99. Fei C., Ochsenkühn M. A., Shibl A. A., Isaac A., Wang C., and Amin S. A. Environ. Microbiol., 2020, 22, (11), 4761 LINK [Google Scholar]
  100. de Carvalho C. C. C. R. Front. Mar. Sci., 2018, 5, 126 LINK [Google Scholar]
  101. Zheng Z., Cai Y., Zhang Y., Zhao Y., Gao Y., Cui Z., Hu Y., and Wang X. Water Res., 2021, 188, 116466 LINK [Google Scholar]

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