1887

Abstract

A range of bacteria and archaea produce gas vesicles as a means to facilitate flotation. These gas vesicles have been purified from a number of species and their applications in biotechnology and medicine are reviewed here. sp. NRC-1 gas vesicles have been engineered to display antigens from eukaryotic, bacterial and viral pathogens. The ability of these recombinant nanoparticles to generate an immune response has been quantified both and . These gas vesicles, along with those purified from and , have been developed as an acoustic reporter system. This system utilizes the ability of gas vesicles to retain gas within a stable, rigid structure to produce contrast upon exposure to ultrasound. The susceptibility of gas vesicles to collapse when exposed to excess pressure has also been proposed as a biocontrol mechanism to disperse cyanobacterial blooms, providing an environmental function for these structures.

Funding
This study was supported by the:
  • George P. C. Salmond , Biotechnology and Biological Sciences Research Council , (Award BB/K001833/1 and BB/N008081/1)
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2020-04-22
2020-06-02
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References

  1. Pfeifer F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol 2012; 10:705–715 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  2. Bowen CC, Jensen TE. Blue-Green algae: fine structure of the gas vacuoles. Science 1965; 147:1460–1462 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  3. Walsby AE. Gas vesicles. Microbiol Rev 1994; 58:94–144
    [Google Scholar]
  4. Gosink JJ, Herwig RP, Staley JT. Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst Appl Microbiol 1997; 20:356–365
    [Google Scholar]
  5. Ramsay JP, Williamson NR, Spring DR, Salmond GPC. A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium. Proc Natl Acad Sci U S A 2011; 108:14932–14937 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Li N, Cannon MC. Gas vesicle genes identified in Bacillus megaterium and functional expression in Escherichia coli. J Bacteriol 1998; 180:2450–2458 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Huang R, Lin J, Gao D, Zhang F, Yi L et al. Discovery of gas vesicles in Streptomyces sp. CB03234-S and potential effects of gas vesicle gene overexpression on morphological and metabolic changes in streptomycetes. Appl Microbiol Biotechnol 2019; 103:5751–5761 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. Houwink AL. Flagella, gas vacuoles and cell-wall structure in Halobacterium halobium; an electron microscope study. J Gen Microbiol 1956; 15:146–150 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Englert C, Horne M, Pfeifer F. Expression of the major gas vesicle protein gene in the halophilic archaebacterium Haloferax mediterranei is modulated by salt. Mol Gen Genet 1990; 222:225–232 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Walsby AE. A square bacterium. Nature 1980; 283:69–71 [CrossRef]
    [Google Scholar]
  11. Bolhuis H, Poele EMT, Rodriguez-Valera F. Isolation and cultivation of Walsby's square archaeon. Environ Microbiol 2004; 6:1287–1291 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. DasSarma S, Damerval T, Jones JG, Tandeau de Marsac N. A plasmid-encoded gas vesicle protein gene in a halophilic archaebacterium. Mol Microbiol 1987; 1:365–370 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  13. Englert C, Krüger K, Offner S, Pfeifer F. Three different but related gene clusters encoding gas vesicles in halophilic archaea. J Mol Biol 1992; 227:586–592 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M et al. Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A 2000; 97:12176–12181 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  15. Surek B, Pillay B, Rdest U, Beyreuther K, Goebel W. Evidence for two different gas vesicle proteins and genes in Halobacterium halobium. J Bacteriol 1988; 170:1746–1751 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Horne M, Englert C, Wimmer C, Pfeifer F. A DNA region of 9 kbp contains all genes necessary for gas vesicle synthesis in halophilic archaebacteria. Mol Microbiol 1991; 5:1159–1174 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Hayes PK, Powell RS. The gvpA/C cluster of Anabaena flos-aquae has multiple copies of a gene encoding GvpA. Arch Microbiol 1995; 164:50–57 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Kinsman R, Hayes PK. Genes encoding proteins homologous to halobacterial Gvps N, J, K, F & L are located downstream of gvpC in the cyanobacterium Anabaena flos-aquae. DNA Seq 1997; 7:97–106 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Tashiro Y, Monson RE, Ramsay JP, Salmond GPC. Molecular genetic and physical analysis of gas vesicles in buoyant enterobacteria. Environ Microbiol 2016; 18:1264–1276 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  20. Mlouka A, Comte K, Castets A-M, Bouchier C, Tandeau de Marsac N. The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. J Bacteriol 2004; 186:2355–2365 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Blaurock AE, Walsby AE. Crystalline structure of the gas vesicle wall from Anabaena flos-aquae. J Mol Biol 1976; 105:183–199 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Walsby AE. The permeability of blue-green algal gas-vacuole membranes to gas. Proc R Soc London Ser B Biol Sci 1969; 173:235–255
    [Google Scholar]
  23. Walsby AE, Revsbech NP, Griffel DH. The gas permeability coefficient of the cyanobacterial gas vesicle wall. J Gen Microbiol 1992; 138:837–845 [CrossRef]
    [Google Scholar]
  24. Hayes PK, Buchholz B, Walsby AE. Gas vesicles are strengthened by the outer-surface protein, GvpC. Arch Microbiol 1992; 157:229–234 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Walsby AE, Hayes PK. The minor cyanobacterial gas vesicle protein, GvpC, is attached to the outer surface of the gas vesicle. Microbiology 1988; 134:2647–2657 [CrossRef]
    [Google Scholar]
  26. Jones JG, Young DC, DasSarma S. Structure and organization of the gas vesicle gene cluster on the Halobacterium halobium plasmid pNRC100. Gene 1991; 102:117–122 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Walsby AE, Bleything A. The dimensions of cyanobacterial gas vesicles in relation to their efficiency in providing buoyancy and withstanding pressure. Microbiology 1988; 134:2635–2645 [CrossRef]
    [Google Scholar]
  28. Walsby AE, Buckland B. Isolation and purification of intact gas vesicles from a Blue–Green alga. Nature 1969; 224:716–717 [CrossRef]
    [Google Scholar]
  29. Walsby AE. The mechanical properties of the Microcystis gas vesicle. J Gen Microbiol 1991; 137:2401–2408 [CrossRef]
    [Google Scholar]
  30. Lakshmanan A, Lu GJ, Farhadi A, Nety SP, Kunth M et al. Preparation of biogenic gas vesicle nanostructures for use as contrast agents for ultrasound and MRI. Nat Protoc 2017; 12:2050–2080 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Offner S, Ziese U, Wanner G, Typke D, Pfeifer F. Structural characteristics of halobacterial gas vesicles. Microbiology 1998; 144:1331–1342 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  32. Belenky M, Meyers R, Herzfeld J. Subunit structure of gas vesicles: a MALDI-TOF mass spectrometry study. Biophys J 2004; 86:499–505 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. DasSarma S, DasSarma P. Gas vesicle nanoparticles for antigen display. Vaccines 2015; 3:686–702 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS et al. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol 2014; 9:311–316 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  35. Leclercq DJJ, Howard CQ, Hobson P, Dickson S, Zander AC et al. Controlling cyanobacteria with ultrasound. Inter-noise 2014 pp 1–10
    [Google Scholar]
  36. Kreuter J. Nanoparticles and microparticles for drug and vaccine delivery. J Anat 1996; 189:503–505[PubMed][PubMed]
    [Google Scholar]
  37. Gregory AE, Titball R, Williamson D. Vaccine delivery using nanoparticles. Front Cell Infect Microbiol 2013; 3:13 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Zhao L, Seth A, Wibowo N, Zhao C-X, Mitter N et al. Nanoparticle vaccines. Vaccine 2014; 32:327–337 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  39. Stuart ES, Morshed F, Sremac M, DasSarma S. Antigen presentation using novel particulate organelles from halophilic archaea. J Biotechnol 2001; 88:119–128 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  40. DasSarma P, Negi VD, Balakrishnan A, Karan R, Barnes S et al. Haloarchaeal gas vesicle nanoparticles displaying Salmonella SopB antigen reduce bacterial burden when administered with live attenuated bacteria. Vaccine 2014; 32:4543–4549 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  41. Balakrishnan A, DasSarma P, Bhattacharjee O, Kim JM, DasSarma S et al. Halobacterial nano vesicles displaying murine bactericidal permeability-increasing protein rescue mice from lethal endotoxic shock. Sci Rep 2016; 6:33679 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  42. Stuart ES, Morshed F, Sremac M, DasSarma S. Cassette-Based presentation of SIV epitopes with recombinant gas vesicles from halophilic archaea. J Biotechnol 2004; 114:225–237 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. DasSarma P, Negi VD, Balakrishnan A, Kim J-M, Karan R et al. Haloarchaeal gas vesicle nanoparticles displaying Salmonella antigens as a novel approach to vaccine development. Procedia Vaccinol 2015; 9:16–23 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Dutta S, DasSarma P, DasSarma S, Jarori GK. Immunogenicity and protective potential of a Plasmodium spp. enolase peptide displayed on archaeal gas vesicle nanoparticles. Malar J 2015; 14:406 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  45. Pecher WT, Kim J-M, DasSarma P, Karan R, Sinnis P. Halobacterium expression system for production of full-length Plasmodium falciparum circumsporozoite protein. In Rampelotto PH. editor Biotechnology of Extremophiles Switzerland: Springer International Publishing; 2016 pp 699–709
    [Google Scholar]
  46. DasSarma S, Arora P. Genetic analysis of the gas vesicle gene cluster in haloarchaea. FEMS Microbiol Lett 1997; 153:1–10 [CrossRef]
    [Google Scholar]
  47. Ng WV, Ciufo SA, Smith TM, Bumgarner RE, Baskin D et al. Snapshot of a large dynamic replicon in a halophilic archaeon: megaplasmid or minichromosome?. Genome Res 1998; 8:1131–1141 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  48. Halladay JT, Jones JG, Lin F, MacDonald AB, DasSarma S. The rightward gas vesicle operon in Halobacterium plasmid pNRC100: identification of the gvpA and gvpC gene products by use of antibody probes and genetic analysis of the region downstream of gvpC. J Bacteriol 1993; 175:684–692 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  49. Strunk T, Hamacher K, Hoffgaard F, Engelhardt H, Zillig MD et al. Structural model of the gas vesicle protein GvpA and analysis of GvpA mutants in vivo. Mol Microbiol 2011; 81:56–68 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  50. Sremac M, Stuart ES. Recombinant gas vesicles from Halobacterium sp. displaying SIV peptides demonstrate biotechnology potential as a pathogen peptide delivery vehicle. BMC Biotechnol 2008; 8:9 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  51. Ezzeldin HM, Klauda JB, Solares SD. Modeling of the major gas vesicle protein, GvpA: from protein sequence to vesicle wall structure. J Struct Biol 2012; 179:18–28 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  52. Stoeckenius W, Kunau WH. Further characterization of particulate fractions from lysed cell envelopes of Halobacterium halobium and isolation of gas vacuole membranes. J Cell Biol 1968; 38:337–357 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  53. DasSarma S. Mechanisms of genetic variability in Halobacterium halobium: the purple membrane and gas vesicle mutations. Can J Microbiol 1989; 35:65–72 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  54. DasSarma S, Halladay JT, Jones JG, Donovan JW, Giannasca PJ et al. High-frequency mutations in a plasmid-encoded gas vesicle gene in Halobacterium halobium. Proc Natl Acad Sci U S A 1988; 85:6861–6865 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  55. Ng W-L, Arora P, DasSarma S. Large deletions in class III gas vesicle-deficient mutants of Halobacterium halobium. Syst Appl Microbiol 1993; 16:560–568 [CrossRef]
    [Google Scholar]
  56. DasSarma S, Arora P, Lin F, Molinari E, Yin LR. Wild-type gas vesicle formation requires at least ten genes in the gvp gene cluster of Halobacterium halobium plasmid pNRC100. J Bacteriol 1994; 176:7646–7652 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  57. Delchambre M, Gheysen D, Thines D, Thiriart C, Jacobs E et al. The gag precursor of simian immunodeficiency virus assembles into virus-like particles. Embo J 1989; 8:2653–2660 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  58. Henderson LE, Benveniste RE, Sowder R, Copeland TD, Schultz AM et al. Molecular characterization of gag proteins from simian immunodeficiency virus (SIVMne). J Virol 1988; 62:2587–2595 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  59. Tikhonov I, Ruckwardt TJ, Hatfield GS, Pauza CD. Tat-neutralizing antibodies in vaccinated macaques. J Virol 2003; 77:3157–3166 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  60. Goldstein G. Hiv-1 Tat protein as a potential AIDS vaccine. Nat Med 1996; 2:960–964 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  61. Noviello CM, Pond SLK, Lewis MJ, Richman DD, Pillai SK et al. Maintenance of Nef-mediated modulation of major histocompatibility complex class I and CD4 after sexual transmission of human immunodeficiency virus type 1. J Virol 2007; 81:4776–4786 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  62. Fang J, Kubota S, Yang B, Zhou N, Zhang H et al. A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev. Virology 2004; 330:471–480 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  63. Coleman SH, Day JR, Guatelli JC. The HIV-1 Nef protein as a target for antiretroviral therapy. Expert Opin Ther Targets 2001; 5:1–22 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  64. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D et al. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 2009; 6:54–67 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  65. Sremac M, Stuart ES. SIVsm Tat, Rev, and Nef1: functional characteristics of r-GV internalization on isotypes, cytokines, and intracellular degradation. BMC Biotechnol 2010; 10:54 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  66. Childs TS, Webley WC. In vitro assessment of halobacterial gas vesicles as a Chlamydia vaccine display and delivery system. Vaccine 2012; 30:5942–5948 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  67. Baehr W, Zhang YX, Joseph T, Su H, Nano FE et al. Mapping antigenic domains expressed by Chlamydia trachomatis major outer membrane protein genes. Proc Natl Acad Sci U S A 1988; 85:4000–4004 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  68. Zhu S, Chen J, Zheng M, Gong W, Xue X et al. Identification of immunodominant linear B-cell epitopes within the major outer membrane protein of Chlamydia trachomatis. Acta Biochim Biophys Sin 2010; 42:771–778 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  69. Crane DD, Carlson JH, Fischer ER, Bavoil P, Hsia R et al. Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc Natl Acad Sci U S A 2006; 103:1894–1899
    [Google Scholar]
  70. Fraser A, Paul M, Goldberg E, Acosta CJ, Leibovici L. Typhoid fever vaccines: systematic review and meta-analysis of randomised controlled trials. Vaccine 2007; 25:7848–7857 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  71. Ghosh AK, Coppens I, Gårdsvoll H, Ploug M, Jacobs-Lorena M. Plasmodium ookinetes coopt mammalian plasminogen to invade the mosquito midgut. Proc Natl Acad Sci U S A 2011; 108:17153–17158 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  72. Schultz H, Weiss JP. The bactericidal/permeability-increasing protein (BPI) in infection and inflammatory disease. Clin Chim Acta 2007; 384:12–23 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  73. DasSarma S, Karan R, DasSarma P, Barnes S, Ekulona F et al. An improved genetic system for bioengineering buoyant gas vesicle nanoparticles from haloarchaea. BMC Biotechnol 2013; 13:112 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  74. DasSarma P, Karan R, Kim J-M, Pecher W, DasSarma S. Bioengineering novel floating nanoparticles for protein and drug delivery. Mater Today Proc 2016; 3:206–210 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  75. Tilney NL. The systemic distribution of soluble antigen injected into the footpad of the laboratory rat. Immunology 1970; 19:181–184[PubMed][PubMed]
    [Google Scholar]
  76. Tavlaridou S, Winter K, Pfeifer F. The accessory gas vesicle protein GvpM of haloarchaea and its interaction partners during gas vesicle formation. Extremophiles 2014; 18:693–706 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  77. Winter K, Born J, Pfeifer F. Interaction of haloarchaeal gas vesicle proteins determined by Split-GFP. Front Microbiol 2018; 9:9 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  78. Andar AU, Karan R, Pecher WT, DasSarma P, Hedrich WD et al. Microneedle-Assisted skin permeation by nontoxic Bioengineerable gas vesicle nanoparticles. Mol Pharm 2017; 14:953–958 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  79. Gilad AA, Winnard PT, van Zijl PCM, Bulte JWM. Developing MR reporter genes: promises and pitfalls. NMR Biomed 2007; 20:275–290 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  80. Borden M, Sirsi S. Better contrast with vesicles. Nat Nanotechnol 2014; 9:248–249 [CrossRef]
    [Google Scholar]
  81. Ferrara K, Pollard R, Borden M. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng 2007; 9:415–447 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  82. Farhadi A, Ho G, Kunth M, Ling B, Lakshmanan A et al. Recombinantly expressed gas vesicles as nanoscale contrast agents for ultrasound and hyperpolarized MRI. AIChE J 2018; 64:2927–2933 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  83. Ntziachristos V. Going deeper than microscopy: the optical imaging frontier in biology. Nat Methods 2010; 7:603–614 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  84. Piraner DI, Farhadi A, Davis HC, Wu D, Maresca D et al. Going deeper: biomolecular tools for acoustic and magnetic imaging and control of cellular function. Biochemistry 2017; 56:5202–5209 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  85. Shapiro MG, Ramirez RM, Sperling LJ, Sun G, Sun J et al. Genetically encoded reporters for hyperpolarized xenon magnetic resonance imaging. Nat Chem 2014; 6:629–634 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  86. Walker TG, Happer W. Spin-Exchange optical pumping of noble-gas nuclei. Rev Mod Phys 1997; 69:629–642 [CrossRef]
    [Google Scholar]
  87. Lakshmanan A, Farhadi A, Nety SP, Lee-Gosselin A, Bourdeau RW et al. Molecular engineering of acoustic protein nanostructures. ACS Nano 2016; 10:7314–7322 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  88. Lu GJ, Farhadi A, Szablowski JO, Lee-Gosselin A, Barnes SR et al. Acoustically modulated magnetic resonance imaging of gas-filled protein nanostructures. Nat Mater 2018; 17:456–463 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  89. Cherin E, Melis JM, Bourdeau RW, Yin M, Kochmann DM et al. Acoustic behavior of Halobacterium salinarum gas vesicles in the high-frequency range: experiments and modeling. Ultrasound Med Biol 2017; 43:1016–1030 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  90. Maresca D, Sawyer DP, Renaud G, Lee-Gosselin A, Shapiro MG. Nonlinear X-Wave ultrasound imaging of acoustic biomolecules. Phys Rev X 2018; 8:041002 [CrossRef]
    [Google Scholar]
  91. Maresca D, Lakshmanan A, Lee-Gosselin A, Melis JM, Ni Y-L et al. Nonlinear ultrasound imaging of nanoscale acoustic biomolecules. Appl Phys Lett 2017; 110:073704 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  92. Bourdeau RW, Lee-Gosselin A, Lakshmanan A, Farhadi A, Kumar SR et al. Acoustic reporter genes for noninvasive imaging of microorganisms in mammalian hosts. Nature 2018; 553:86–90 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  93. Farhadi A, Ho GH, Sawyer DP, Bourdeau RW, Shapiro MG. Ultrasound imaging of gene expression in mammalian cells. Science 2019; 365:1469–1475 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  94. Szablowski JO, Bar-Zion A, Shapiro MG. Achieving spatial and molecular specificity with ultrasound-targeted biomolecular nanotherapeutics. Acc Chem Res 2019; 52:2427–2434 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  95. Merel S, Walker D, Chicana R, Snyder S, Baurès E et al. State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 2013; 59:303–327 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  96. Visser PM, Ibelings BW, Bormans M, Huisman J. Artificial mixing to control cyanobacterial blooms: a review. Aquat Ecol 2016; 50:423–441 [CrossRef]
    [Google Scholar]
  97. Reynolds CS, Wiseman SW, Godfrey BM, Butterwick C. Some effects of artificial mixing on the dynamics of phytoplankton populations in large limnetic enclosures. J Plankton Res 1983; 5:203–234 [CrossRef]
    [Google Scholar]
  98. Damerval T, Castets AM, Guglielmi G, Houmard J, Tandeau de Marsac N. Occurrence and distribution of gas vesicle genes among cyanobacteria. J Bacteriol 1989; 171:1445–1452 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  99. Clark AE, Walsby AE. The occurrence of gas-vacuolate bacteria in lakes. Arch Microbiol 1978; 118:223–228 [CrossRef]
    [Google Scholar]
  100. Lee TJ, Nakano K, Matsumara M. Ultrasonic irradiation for blue-green algae bloom control. Environ Technol 2001; 22:383–390 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  101. Rajasekhar P, Fan L, Nguyen T, Roddick FA. A review of the use of sonication to control cyanobacterial blooms. Water Res 2012; 46:4319–4329 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  102. Tang JW, Wu QY, Hao HW, Chen Y, Wu M. Effect of 1.7 MHz ultrasound on a gas-vacuolate cyanobacterium and a gas-vacuole negative cyanobacterium. Colloids Surf B Biointerfaces 2004; 36:115–121 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  103. Tang J, Wu Q, Hao H, Chen Y, Wu M. Growth inhibition of the cyanobacterium Spirulina (Arthrospira) platensis by 1.7 MHz ultrasonic irradiation. J Appl Phycol 2003; 15:37–43 [CrossRef]
    [Google Scholar]
  104. Ahn CY, Joung SH, Choi A, Kim HS, Jang KY et al. Selective control of cyanobacteria in eutrophic pond by a combined device of ultrasonication and water pumps. Environ Technol 2007; 28:371–379 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  105. Nakano K, Lee TJ, Matsumura M. In situ algal bloom control by the integration of ultrasonic radiation and jet circulation to flushing. Environ Sci Technol 2001; 35:4941–4946 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  106. Rodriguez-Molares A, Dickson S, Hobson P, Howard C, Zander A et al. Quantification of the ultrasound induced sedimentation of Microcystis aeruginosa. Ultrason Sonochem 2014; 21:1299–1304 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  107. Wu X, Joyce EM, Mason TJ. Evaluation of the mechanisms of the effect of ultrasound on Microcystis aeruginosa at different ultrasonic frequencies. Water Res 2012; 46:2851–2858 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  108. Ma B, Chen Y, Hao H, Wu M, Wang B et al. Influence of ultrasonic field on microcystins produced by bloom-forming algae. Colloids Surf B Biointerfaces 2005; 41:197–201 [CrossRef][PubMed][PubMed]
    [Google Scholar]
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