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Bdellovibrio and Like Organisms

  • Or Rotem
  • Zohar Pasternak
  • Edouard JurkevitchEmail author
Reference work entry

Abstract

Bdellovibrio and like organisms (BALOs) are gram-negative, obligate predators of other gram-negative bacteria. These small bacteria interact with their prey as highly motile attack phase cells, attaching to the outer membrane and consuming the prey extracellularly (epibiotic predation) or penetrating their periplasm (periplasmic predation). The former divides in a binary fashion, while the latter grows as a polynucleotide filament to finally split as progeny attack cells. High-resolution microscopy, molecular genetics, genomics, and functional genomics have been applied to study the cell cycle of BALOs, revealing functions required for predation and for cellular organization. Until recently, Bdellovibrio bacteriovorus was the only recognized species of BALOs. Culture-dependent and culture-independent approaches have shown that these predators form diverse monophyletic groups, including the three families Bdellovibrionaceae, Bacteriovoraceae, and Peridibacteraceae in the δ-proteobacteria, and the genus Micavibrio in the α-proteobacteria. Based on this detailed taxonomical knowledge, it has become possible to track predator and prey interactions in natural systems, providing first evaluations of the impact of bacterial predation on community structure.

Keywords

Attack Phase Diaminopimelic Acid Infected Prey Modern Molecular Biology Prey Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abram D, CastroeMelo J, Chou D (1974) Penetration of Bdellovibrio bacteriovorus into host cells. J Bacteriol 118:663–680PubMedCentralPubMedGoogle Scholar
  2. Araki Y, Ruby EG (1988) A soluble enzyme activity that attaches free diaminopimelic acid to bdelloplast peptidoglycan. Biochemistry 27:2624–2629PubMedGoogle Scholar
  3. Atterbury RJ, Hobley L, Till R, Lambert C, Capeness MJ, Lerner TR, Fenton AK, Barrow P, Sockett RE (2011) Effects of orally administered Bdellovibrio bacteriovorus on the well-being and Salmonella colonization of young chicks. Appl Environ Microbiol 77:5794–5803PubMedCentralPubMedGoogle Scholar
  4. Baer ML, Ravel J, Chun J, Hill RT, Williams HN (2000) A proposal for the reclassification of Bdellovibrio stolpii and Bdellovibrio starrii into a new genus, Bacteriovorax gen. nov. as Bacteriovorax stolpii comb. nov. and Bacteriovorax starrii comb. nov., respectively. Int J Syst Evol Microbiol 50(Pt 1):219–224PubMedGoogle Scholar
  5. Baer ML, Ravel J, Pineiro SA, Guether-Borg D, Williams HN (2004) Reclassification of salt-water Bdellovibrio sp. as Bacteriovorax marinus sp. nov. and Bacteriovorax litoralis sp. nov. Int J Syst Evol Microbiol 54:1011–1016PubMedGoogle Scholar
  6. Barabote RD, Rendulic S, Schuster SC, Saier MH Jr (2007) Comprehensive analysis of transport proteins encoded within the genome of Bdellovibrio bacteriovorus. Genomics 90:424–446PubMedCentralPubMedGoogle Scholar
  7. Barel G, Sirota A, Volpin H, Jurkevitch E (2005) Fate of predator and prey proteins during browth of Bdellovibrio bacteriovorus on Escherichia coli and Pseudomonas syringae prey. J Bacteriol 187:329–335PubMedCentralPubMedGoogle Scholar
  8. Beck S, Schwudke D, Strauch E, Appel B, Linscheid M (2004) Bdellovibrio bacteriovorus strains produce a novel major outer membrane protein during predacious growth in the periplasm of prey bacteria. J Bacteriol 186:2766–2773PubMedCentralPubMedGoogle Scholar
  9. Borgnia MJ, Subramaniam S, Milne JLS (2008) Three-dimensional imaging of the highly bent architecture of Bdellovibrio bacteriovorus by using cryo-electron tomography. J Bacteriol 190:2588–2596PubMedCentralPubMedGoogle Scholar
  10. Butan C, Hartnell LM, Fenton AK, Bliss D, Sockett RE, Subramaniam S, Milne JLS (2011) Spiral architecture of the nucleoid in Bdellovibrio bacteriovorus. J Bacteriol 193:1341–1350PubMedCentralPubMedGoogle Scholar
  11. Chang CY, Hobley L, Till R, Capeness M, Kanna M, Burtt W, Jagtap P, Aizawa S, Sockett RE (2011) The Bdellovibrio bacteriovorus twin-arginine transport system has roles in predatory and prey-independent growth. Microbiology 157:3079–3093PubMedGoogle Scholar
  12. Chauhan A, Cherrier J, Williams HN (2009) Impact of sideways and bottom-up control factors on bacterial community succession over a tidal cycle. Proc Natl Acad of Sci USA 106(11):4301–4306. doi:10.1073/pnas.0809671106Google Scholar
  13. Chen H, Athar R, Zheng G, Williams HN (2011) Prey bacteria shape the community structure of their predators. ISME J 5(8):1314–1322PubMedCentralPubMedGoogle Scholar
  14. Chen H, Young S, Berhane T-K, Williams HN (2012) Predatory Bacteriovorax communities ordered by various prey species. PLoS One 7:e34174PubMedCentralPubMedGoogle Scholar
  15. Chu WH, Zhu W (2009) Isolation of Bdellovibrio as biological therapeutic agents used for the treatment of Aeromonas hydrophila infection in fish. Zoonoses and Public Health 57(4):258–64. doi:10.1111/j.1863-2378.2008.01224.xPubMedGoogle Scholar
  16. Cotter TW, Thomashow MF (1992a) A conjugation procedure for Bdellovibrio bacteriovorus and its use to identify DNA sequences that enhance the plaque-forming ability of a spontaneous host-independent mutant. J Bacteriol 174:6011–6017PubMedCentralPubMedGoogle Scholar
  17. Cotter TW, Thomashow MF (1992b) Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 174:6018–6024PubMedCentralPubMedGoogle Scholar
  18. Cover WH, Rittenberg SC (1984) Change in the surface hydrophobicity of substrate cells during bdelloplast formation by Bdellovibrio bacteriovorus 109J. J Bacteriol 157:391–397.PubMedCentralPubMedGoogle Scholar
  19. Dashiff A, Kadouri DE (2009) A new method for isolating host-independent variants of Bdellovibrio bacteriovorus using E. coli auxotrophs. Open Microbiol J 3:87–91PubMedCentralPubMedGoogle Scholar
  20. Dashiff A, Kadouri DE (2011) Predation of oral pathogens by Bdellovibrio bacteriovorus 109J. Mol Oral Microbiol 26:19–34PubMedGoogle Scholar
  21. Davidov Y, Jurkevitch E (2004) Diversity and evolution of Bdellovibrio-and-like organisms (BALOs), reclassification of Bacteriovorax starrii as Peredibacter starrii gen. nov., comb. nov., and description of the Bacteriovorax–Peredibacter clade as Bacteriovoracaceae fam. nov. Int J Syst Evol Microbiol 54:1439–1452PubMedGoogle Scholar
  22. Davidov Y, Jurkevitch E (2009) Predation between prokaryotes and the origin of eukaryotes. Bioessays 31:748–757PubMedGoogle Scholar
  23. Davidov Y, Friedjung A, Jurkevitch E (2006a) Structure analysis of a soil community of predatory bacteria using culture-dependent and culture-independent methods reveals a hitherto undetected diversity of Bdellovibrio-and-like organisms. Environ Microbiol 8:1667–1673PubMedGoogle Scholar
  24. Davidov Y, Huchon D, Koval SF, Jurkevitch E (2006b) A new α-proteobacterial clade of Bdellovibrio-like predators: implications for the mitochondrial endosymbiotic theory. Environ Microbiol 8:2179–2188PubMedGoogle Scholar
  25. Diedrich DL, Denny CF, Hashimoto T, Conti SF (1970) Facultatively parasitic strain of Bdellovibrio bacteriovorus. J Bacteriol 101:989–996PubMedCentralPubMedGoogle Scholar
  26. Diedrich DL, Portnoy Duran CA, Conti SF (1984) Acquisition of Escherichia coli outer membrane proteins by Bdellovibrio sp. strain 109D. J Bacteriol 159:329–334PubMedCentralPubMedGoogle Scholar
  27. Dori-Bachash M, Dassa B, Pietrokovski S, Jurkevitch E (2008) Proteome-based comparative analyses of growth stages reveal new cell cycle-dependent functions in the predatory bacterium Bdellovibrio bacteriovorus. Appl Environ Microbiol 74:7152–7162PubMedCentralPubMedGoogle Scholar
  28. Doskina TV (1973) Isolation of parasitic and saprophytic strains of Bdellovibrio bacteriovorus from natural waters. Gig Sanit 38:84–85PubMedGoogle Scholar
  29. Evans KJ, Lambert C, Sockett RE (2007) Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 189:4850–4859PubMedCentralPubMedGoogle Scholar
  30. Fenton AK, Hobley L, Butan C, Subramaniam S, Sockett RE (2010a) A coiled-coil-repeat protein “Ccrp”in Bdellovibrio bacteriovorus prevents cellular indentation, but is not essential for vibroid cell morphology. FEMS Microbiol Lett 313:89–95PubMedGoogle Scholar
  31. Fenton AK, Kanna M, Woods RD, Aizawa SI, Sockett RE (2010b) Shadowing the actions of a predator: Backlit fluorescent microscopy reveals synchronous nonbinary septation of predatory Bdellovibrio inside prey and exit through discrete bdelloplast pores. J Bacteriol 192:6329–6335PubMedCentralPubMedGoogle Scholar
  32. Fenton AK, Lambert C, Wagstaff PC, Sockett RE (2010c) Manipulating each MreB of Bdellovibrio bacteriovorus gives diverse morphological and predatory phenotypes. J Bacteriol 192:1299–1311PubMedCentralPubMedGoogle Scholar
  33. Framatico PM, Cooke PH (1996) Isolation of bdellovibrios that prey on Escherichia coli 0157:H7 and Salmonella species and application for removal of prey from stainless steel surfaces. J Food Safety 16:161–173Google Scholar
  34. Friedberg D (1977) Effect of light on Bdellovibrio bacteriovorus. J Bacteriol 131:399–404PubMedCentralPubMedGoogle Scholar
  35. Fry J, Staples DG (1976) Distribution of Bdellovibrio bacteriovorus in sewage works, river water, and sediments. Appl Environ Microbiol 31:469–474PubMedCentralPubMedGoogle Scholar
  36. Gadkari D, Stolp H (1975) Energy metabolism of Bdellovibrio bacteriovorus. I. Energy production, ATP pool, energy charge. Arch Microbiol 102(3):179–185PubMedGoogle Scholar
  37. Gadkari D, Stolp H (1976) Energy metabolism of Bdellovibrio bacteriovorus. II. P/O ratio and ATP pool turnover rate. Arch Microbiol 108:125–132PubMedGoogle Scholar
  38. Gallet R, Alizon S, Comte P-A, Gutierrez A, Depaulis F, van Baalen M, Michel E, Muller-Graf CDM (2007) Predation and disturbance Interact to shape prey species diversity. Am Nat 170:143–154PubMedGoogle Scholar
  39. Gallet R, Tully T, Evans MKE (2009) Ecological conditions affect evolutionary trajectory in a predator–prey system. Evolution 63:641–651PubMedGoogle Scholar
  40. Germida JJ (1987) Isolation of Bdellovibrio spp. that prey on Azospirillum brasilense in soil. Can J Microbiol 33:459–461Google Scholar
  41. Gordon RF, Stein MA, Diedrich DL (1993) Heat shock-induced axenic growth of Bdellovibrio bacteriovorus. J Bacteriol 175:2157–2161PubMedCentralPubMedGoogle Scholar
  42. Gray KM, Ruby EG (1990) Prey-derived signals regulating duration of the developmental growth phase of Bdellovibrio bacteriovorus. J Bacteriol 172:4002–4007PubMedCentralPubMedGoogle Scholar
  43. Gray KM, Ruby EG (1991) Intercellular signalling in the bdellovibrio developmental growth cycle. Microbial Cell-Cell Interactions ASM, Washington, DCGoogle Scholar
  44. Guerrero R, Pedros-Alio C, Esteve I, Mas J, Chase D, Margulis L (1986) Predatory prokaryotes: predation and primary consumption evolved in bacteria. Proc Natl Acad Sci U S A 83:2138–2142PubMedCentralPubMedGoogle Scholar
  45. Hespell RB, Odelson DA (1978) Metabolism of RNA-ribose by Bdellovibrio bacteriovorus during intraperiplasmic growth on Escherichia coli. J Bacteriol 136:936–946PubMedCentralPubMedGoogle Scholar
  46. Hespell RB, Rosson RA, Thomashow MF, Rittenberg SC (1973) Respiration of Bdellovibrio bacteriovorus strain 109J and its energy substrates for intraperiplasmic growth. J Bacteriol 113:1280–1288PubMedCentralPubMedGoogle Scholar
  47. Hespell R, Thomashow MF, Rittenberg SC (1974) Changes in cell composition and viability of Bdellovibrio bacteriovorus during starvation. Arch Microbiol 97:313–327PubMedGoogle Scholar
  48. Hobley L, Fung RK, Lambert C, Harris MA, Dabhi JM, King SS, Basford SM, Uchida K, Till R, Ahmad R, Aizawa S, Gomelsky M, Sockett RE (2012a) Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus. PLoS Pathog 8:e1002493PubMedCentralPubMedGoogle Scholar
  49. Hobley L, Lerner TR, Williams LE, Lambert C, Till R, Milner DS, Basford SM, Capeness MJ, Fenton AK, Atterbury RJ, Harris MA, Sockett RE (2012b) Genome analysis of a simultaneously predatory and prey-independent, novel Bdellovibrio bacteriovorus from the River Tiber, supports in silico predictions of both ancient and recent lateral gene transfer from diverse bacteria. BMC Genomics 13:670PubMedCentralPubMedGoogle Scholar
  50. Iida Y, Hobley L, Lambert C, Fenton AK, Sockett RE, Aizawa S (2009) Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus. J Mol Biol 394:1011–1021PubMedCentralPubMedGoogle Scholar
  51. Ishiguro EE (1974) Minimum nutritional requirements for growth of host-independent derivatives of Bdellovibrio bacteriovorus strain 109 Davis. Can J Microbiol 20:263–264PubMedGoogle Scholar
  52. Jurkevitch E, Minz D, Ramati B, Barel G (2000) Prey range characterization, ribotyping, and diversity of soil and rhizosphere Bdellovibrio spp. isolated on phytopathogenic bacteria. Appl Environ Microbiol 66:2365–2371PubMedCentralPubMedGoogle Scholar
  53. Kadouri D, O'Toole GA (2005) Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 71:4044–4051PubMedCentralPubMedGoogle Scholar
  54. Kadouri D, Venzon NC, O'Toole GA (2007) Vulnerability of pathogenic biofilms to Micavibrio aeruginosavorus. Appl Environ Microbiol 73:605–614PubMedCentralPubMedGoogle Scholar
  55. Karunker I, Rotem O, Dori-Bachash M, Jurkevitch E, Sorek R (2013) A global transcriptional switch between the attack and growth forms of Bdellovibrio bacteriovorus. PLoS One 8:e61850PubMedCentralPubMedGoogle Scholar
  56. Kelley J, Turng B, Williams H, Baer M (1997) Effects of temperature, salinity, and substrate on the colonization of surfaces in situ by aquatic bdellovibrios. Appl Environ Microbiol 63:84–90PubMedCentralPubMedGoogle Scholar
  57. Kessel M, Shilo M (1976) Relationship of Bdellovibrio elongation and fission to host cell size. J Bacteriol 128:477–480PubMedCentralPubMedGoogle Scholar
  58. Kikuchi Y, Bomar L, Graf J (2009) Stratified bacterial community in the bladder of the medicinal leech, Hirudo verbana. Environ Microbiol 11:2758–2770PubMedGoogle Scholar
  59. Koval SF, Hynes SH, Flannagan RS, Pasternak Z, Davidov Y, Jurkevitch E (2012) Bdellovibrio exovorus sp. nov., a novel predator of Caulobacter crescentus. Int J Syst Evol Microbiol 63(Pt 1):146–151PubMedGoogle Scholar
  60. Kuenen JG, Rittenberg SC (1975) Incorporation of long-chain fatty acids of the substrate organism by Bdellovibrio bacteriovorus during intraperiplasmic growth. J Bacteriol 121:1145–1157PubMedCentralPubMedGoogle Scholar
  61. LaMarre AG, Straley SC, Conti SF (1977) Chemotaxis toward amino acids by Bdellovibrio bacteriovorus. J Bacteriol 131:201–207PubMedCentralPubMedGoogle Scholar
  62. Lambert C, Smith MC, Sockett RE (2003) A novel assay to monitor predator–prey interactions for Bdellovibrio bacteriovorus 109J reveals a role for methyl-accepting chemotaxis proteins in predation. Environ Microbiol 5:127–132PubMedGoogle Scholar
  63. Lambert C, Evans KJ, Till R, Hobley L, Capeness M, Rendulic S, Schuster SC, Aizawa S, Sockett RE (2006) Characterizing the flagellar filament and the role of motility in bacterial prey-penetration by Bdellovibrio bacteriovorus. Mol Microbiol 60:274–286PubMedCentralPubMedGoogle Scholar
  64. Lambert C, Chang CY, Capeness MJ, Sockett RE (2010a) The first bite–profiling the predatosome in the bacterial pathogen Bdellovibrio. PLoS One 5:e8599PubMedCentralPubMedGoogle Scholar
  65. Lambert C, Ivanov P, Sockett RE (2010b) A transcriptional “Scream” early response of E. coli prey to predatory invasion by Bdellovibrio. Curr Microbiol 60:419–427PubMedCentralPubMedGoogle Scholar
  66. Lambert C, Fenton AK, Hobley L, Sockett RE (2011) Predatory Bdellovibrio bacteria use gliding motility to scout for prey on surfaces. J Bacteriol 193:3139–3141PubMedCentralPubMedGoogle Scholar
  67. Lambert C, Till R, Hobley L, Sockett RE (2012) Mutagenesis of RpoE-like sigma factor genes in Bdellovibrio reveals differential control of groEL and two groES genes. BMC Microbiol 12:99PubMedCentralPubMedGoogle Scholar
  68. Lambina VA, Afinogenova AV, Romai Penabad S, Konovalona SM, Pushkareva AP (1982) Micavibrio admirandus gen. et sp. nov. Mikrobiologiya 51:114–117Google Scholar
  69. Lerner TR, Lovering AL, Bui NK, Uchida K, Aizawa S-I, Vollmer W, Sockett RE (2012) Specialized peptidoglycan hydrolases sculpt the intra-bacterial niche of predatory Bdellovibrio and increase population fitness. PLoS Pathog 8:e1002524PubMedCentralPubMedGoogle Scholar
  70. Mahmoud KK, Koval SF (2010) Characterization of type IV pili in the life cycle of the predator bacterium Bdellovibrio. Microbiology 156:1040–1051PubMedGoogle Scholar
  71. Martinez V, Jurkevitch E, Garcia JL, Prieto MA (2012) Reward for bdellovibrio bacteriovorus for preying on a polyhydroxyalkanoate producer. Environ MicrobiolGoogle Scholar
  72. Marbach A, Shilo M (1978) Dependence of marine bdellovibrios on potassium, calcium, and magnesium ions. Appl Environ Microbiol 36:169–177PubMedCentralPubMedGoogle Scholar
  73. McCann MP, Solimeo HT, Cusick F Jr, Panunti B, McCullen C (1998) Developmentally regulated protein synthesis during intraperiplasmic growth of Bdellovibrio bacteriovorus 109J. Can J Microbiol 44:50–55PubMedGoogle Scholar
  74. Medina AA, Kadouri DE (2009) Biofilm formation of Bdellovibrio bacteriovorus host-independent derivatives. Res Microbiol 160:224–231PubMedGoogle Scholar
  75. Medina AA, Shanks RM, Kadouri DE (2008) Development of a novel system for isolating genes involved in predator-prey interactions using host independent derivatives of Bdellovibrio bacteriovorus 109J. BMC Microbiol 8:33PubMedCentralPubMedGoogle Scholar
  76. Mills E, Pultz IS, Kulasekara HD, Miller SI (2011) The bacterial second messenger c-di-GMP: mechanisms of signalling. Cell Microbiol 13:1122–1129PubMedGoogle Scholar
  77. Monnappa AF, Dwidar M, Mitchell RJ (2013) Application of bacterial predation to mitigate recombinant bacterial populations and their DNA. Soil Biol Biochem 57:427–435Google Scholar
  78. Morehouse KA, Hobley L, Capeness M, Sockett RE (2011) Three motAB stator gene products in Bdellovibrio bacteriovorus contribute to motility of a single flagellum during predatory and prey-independent growth. J Bacteriol 193:932–943PubMedCentralPubMedGoogle Scholar
  79. Muller FD, Beck S, Strauch E, Linscheid MW (2011) Bacterial predators possess unique membrane lipid structures. Lipids 46:1129–1140PubMedGoogle Scholar
  80. Nakamura M (1972) Alteration of Shigella pathogenicity by other bacteria. Am J Clin Nutr 25:1441–1451PubMedGoogle Scholar
  81. Nguyen NA, Sallans L, Kaneshiro ES (2008) The major glycerophospholipids of the predatory and parasitic bacterium Bdellovibrio bacteriovorus HID5. Lipids 43:1053–1063PubMedGoogle Scholar
  82. Parker CA, Grove PL (1970) Bdellovibrio bacteriovorus parasitizing Rhizobium in Western Australia. J Appl Microbiol 33:253–255Google Scholar
  83. Pasternak Z, Pietrokovski S, Rotem O, Gophna U, Lurie-Weinberger MN, Jurkevitch E (2012) By their genes ye shall know them: genomic signatures of predatory bacteria. ISME J 7(4):756–769PubMedCentralPubMedGoogle Scholar
  84. Pineiro S, Stine CO, Chauhan A, Steyert SR, Smith R, Williams HN (2007) Global survey of diversity among environmental saltwater Bacteriovoracaceae. Environ Microbiol 9:2441–2450PubMedGoogle Scholar
  85. Pineiro SA, Williams HN, Stine OC (2008) Phylogenetic relationships amongst the saltwater members of the genus Bacteriovorax using rpoB sequences and reclassification of Bacteriovorax stolpii as Bacteriolyticum stolpii gen. nov., comb. nov. Int J Syst Evol Microbiol 58:1203–1209PubMedGoogle Scholar
  86. Qi Z, Zhang X-H, Boon N, Bossier P (2009) Probiotics in aquaculture of China – Current state, problems and prospect. Aquaculture 290:15–21Google Scholar
  87. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans KJ, Goesmann A, Meyer F, Sockett ER, Schuster S (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303:689–692PubMedGoogle Scholar
  88. Rice TD, Williams HN, Turng BF (1998) Susceptibility of bacteria in estuarine environments to autochthonous bdellovibrios. Microb Ecol 35:256–264PubMedGoogle Scholar
  89. Richardson IR (1990) The incidence of Bdellovibrio spp. in man-made water systems: coexistence with legionellas. J Appl Bacteriol 69:134–140PubMedGoogle Scholar
  90. Rittenberg SC, Hespell RB (1975) Energy efficiency of intraperiplasmic growth of Bdellovibrio bacteriovorus. J Bacteriol 121:1158–1165PubMedCentralPubMedGoogle Scholar
  91. Rittenberg SC, Shilo M (1970) Early host damage in the infection cycle of Bdellovibrio bacteriovorus. J Bacteriol 102:149–160PubMedCentralPubMedGoogle Scholar
  92. Roschanski N, Klages S, Reinhardt R, Linscheid M, Strauch E (2011) Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 193:1745–1756PubMedCentralPubMedGoogle Scholar
  93. Rosson RT, Rittenberg SC (1979) Regulated breakdown of Escherichia coli deoxyribonucleic acid during intraperiplasmic growth of Bdellovibrio bacteriovorus 109J. J Bacteriol 140:620–633PubMedCentralPubMedGoogle Scholar
  94. Ruby EG (1991) The genus Bdellovibrio. In: Balows HGTA, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York, pp 3400–3415Google Scholar
  95. Ruby EG, McCabe JB (1986) An ATP transport system in the intracellular bacterium, Bdellovibrio bacteriovorus 109J. J Bacteriol 167:1066–1070PubMedCentralPubMedGoogle Scholar
  96. Ruby EG, Rittenberg SC (1983) Differentiation after premature release of intraperiplasmically growing Bdellovibrio bacteriovorous. J Bacteriol 154:32–40PubMedCentralPubMedGoogle Scholar
  97. Ruby EG, Rittenberg SC (1984) Attachment of diaminopimelic acid to bdelloplast peptidoglycan during intraperiplasmic growth of Bdellovibrio bacteriovorus 109J. J Bacteriol 158:597–602PubMedCentralPubMedGoogle Scholar
  98. Ruby EG, McCabe JB, Barke JI (1985) Uptake of intact nucleoside monophosphates by Bdellovibrio bacteriovorus 109J. J Bacteriol 163:1087–1094PubMedCentralPubMedGoogle Scholar
  99. Sanchez-Amet A, Torrella F (1990) Formation of stable bdelloplasts as a starvation-survival strategy of marine bdellovibrios. Appl Environ Microbiol 56(9):2717–2725Google Scholar
  100. Schelling M, Conti S (1986) Host receptor sites involved in the attachment of Bdellovibrio bacteriovorus and Bdellovibrio stolpii. FEMS Microbial Lett 36:319–323Google Scholar
  101. Scherff RH (1973) Control of bacterial blight of soybean by Bdellovibrio bacteriovorus. Phytopathology 63:400–402Google Scholar
  102. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedCentralPubMedGoogle Scholar
  103. Schoeffield AJ, Williams HN (1990) Efficiencies of recovery of bdellovibrios from brackish-water environments by using various bacterial species as prey. Appl Environ Microbiol 56:230–236PubMedCentralPubMedGoogle Scholar
  104. Schwudke D, Strauch E, Krueger M, Appel B (2001) Taxonomic studies of predatory bdellovibrios based on 16S rRNA analysis, ribotyping and the hit locus and characterization of isolates from the gut of animals. Syst Appl Microbiol 24:385–394PubMedGoogle Scholar
  105. Schwudke D, Linscheid M, Strauch E, Appel B, Zahringer U, Moll H, Muller M, Brecker L, Gronow S, Lindner B (2003) The obligate predatory Bdellovibrio bacteriovorus possesses a neutral lipid A containing alpha-D-Mannoses that replace phosphate residues: similarities and differences between the lipid As and the lipopolysaccharides of the wild type strain B. bacteriovorus HD100 and its host-independent derivative HI100. J Biol Chem 278:27502–27512PubMedGoogle Scholar
  106. Seidler RJ, Starr MP (1968) Structure of the flagellum of Bdellovibrio bacteriovorus. J Bacteriol 95:1952–1955PubMedCentralPubMedGoogle Scholar
  107. Seidler R, Starr MMP (1969a) Factors affecting the intracellular parasitic growth of Bdellovibrio bacteriovorus developing within Escherichia coli. J Bacteriol 97:912–923PubMedCentralPubMedGoogle Scholar
  108. Seidler RJ, Starr MP (1969b) Isolation and characterization of host-independent bdellovibrios. J Bacteriol 100:769–785PubMedCentralPubMedGoogle Scholar
  109. Shemesh Y, Jurkevitch E (2004) Plastic phenotypic resistance to predation by Bdellovibrio and like organisms in bacterial prey. Environ Microbiol 6:12–18PubMedGoogle Scholar
  110. Shemesh Y, Yaacov D, Susan K, Jurkevitch E (2003) Small eats big: ecology and diversity of Bdellovibrio and like organisms, and their dynamics in predator–prey interactions. Agronomie 23:433–439Google Scholar
  111. Shilo M, Bruff B (1965) Lysis of gram-negative bacteria by host-independent ectoparasitic Bdellovibrio bacteriovorus isolates. J Gen Microbiol 40:317–328PubMedGoogle Scholar
  112. Snyder AR, Williams HN, Baer ML, Walker SOC (2002) 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int J Syst Evol Microbiol 52:2089–2094PubMedGoogle Scholar
  113. Sockett ER, Lambert C (2004) Bdellovibrio as therapeutic agents: a predatory renaissance? Nat Rev Microbiol 2:669–675PubMedGoogle Scholar
  114. Sourjik V, Wingreen NS (2012) Responding to chemical gradients: bacterial chemotaxis. Curr Opin Cell Biol 24:262–268PubMedCentralPubMedGoogle Scholar
  115. Starr MP (1975) Bdellovibrio as a symbiont: the association of bdellovibrios with other bacteria interpreted in terms of a generalized scheme for classifying organismic associations. Symp Soc Exp Biol 29:93–124PubMedGoogle Scholar
  116. Stein MA, McAllister SA, Torian BE, Diedrich DL (1992) Acquisition of apparently intact and unmodified lipopolysaccharides from Escherichia coli by Bdellovibrio bacteriovorus. J Bacteriol 174:2858–2864PubMedCentralPubMedGoogle Scholar
  117. Stolp H (1967) Lysis von bacterien durch den parasiten Bdellovibrio bacteriovorus, Film C972. I.W.F., GottingenGoogle Scholar
  118. Stolp H (1968) Ein rauberischer backterienparasit. Die Naturwissenschaften 55:57–63Google Scholar
  119. Stolp H (1981) The genus Bdellovibrio. In: Starr MP, Stolp H, Troper HG, Balows A, Schegel HG (eds) The prokaryotes. Springer, Berlin, pp 618–629Google Scholar
  120. Stolp H, Petzold H (1962) Untersuchungen uber einen obligat parasitischen Mikroorganismus mit lytischer Aktivitiit fur Pseudomonas Bakterien. Phytopathol Z 45:364–370Google Scholar
  121. Stolp H, Starr MP (1963) Bdellovibrio bacteriovorus gen. et sp. n., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29:217–248PubMedGoogle Scholar
  122. Straley SC, Conti SF (1977) Chemotaxis by Bdellovibrio bacteriovorus toward prey. J Bacteriol 132:628–640PubMedCentralPubMedGoogle Scholar
  123. Straley SC, LaMarre AG, Lawrence LJ, Conti SF (1979) Chemotaxis of Bdellovibrio bacteriovorus toward pure compounds. J Bacteriol 140:634–642PubMedCentralPubMedGoogle Scholar
  124. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  125. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739PubMedCentralPubMedGoogle Scholar
  126. Thomashow MF, Cotter TW (1992) Bdellovibrio host dependence: the search for signal molecules and genes that regulate the intraperiplasmic growth cycle. J Bacteriol 174:5767–5771PubMedCentralPubMedGoogle Scholar
  127. Thomashow MF, Rittenberg SC (1978a) Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: solubilization of Escherichia coli peptidoglycan. J Bacteriol 135:998–1007PubMedCentralPubMedGoogle Scholar
  128. Thomashow MF, Rittenberg SC (1978b) Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: N-deacetylation of Escherichia coli peptidoglycan amino sugars. J Bacteriol 135:1008–1014PubMedCentralPubMedGoogle Scholar
  129. Thomashow MF, Rittenberg SC (1978c) Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: attachment of long-chain fatty acids to Escherichia coli peptidoglycan. J Bacteriol 135:1015–1023PubMedCentralPubMedGoogle Scholar
  130. Thomashow LS, Rittenberg SC (1985) Isolation and composition of sheathed flagella from Bdellovibrio bacteriovorus 109J. J Bacteriol 163:1047–1054PubMedCentralPubMedGoogle Scholar
  131. Tudor JJ, Conti SF (1977) Characterization of bdellocysts of Bdellovibrio sp. J Bacteriol 131(1):314–322PubMedCentralPubMedGoogle Scholar
  132. Tudor J, Conti SF (1978) Characterization of germination and activation of Bdellovibrio bdellocysts. J Bacteriol 133:130–138PubMedCentralPubMedGoogle Scholar
  133. Tudor JJ, McCann MP, Acrich IA (1990) A new model for the penetration of prey cells by bdellovibrios. J Bacteriol 172:2421–2426PubMedCentralPubMedGoogle Scholar
  134. Uematsu T (1980) Ecology of Bdellovibrio parasitic to rice bacterial leaf blight pathogen, Xanthomonas oryzae. Rev Plant Protect Res 13:12–26Google Scholar
  135. Van Essche M, Quirynen M, Sliepen I, Van Eldere J, Teughels W (2009a) Bdellovibrio bacteriovorus attacks Aggregatibacter actinomycetemcomitans. J Dent Res 88:182–186PubMedGoogle Scholar
  136. Van Essche M, Sliepen I, Loozen G, Van Eldere J, Quirynen M, Davidov Y, Jurkevitch E, Boon N, Teughels W (2009b) Development and performance of a quantitative PCR for the enumeration of Bdellovibrionaceae. Environ Microbiol Rep 1:228–233PubMedGoogle Scholar
  137. Varon M (1979) Selection of predation-resistant bacteria in a continuous culture. Nature 277:386–388Google Scholar
  138. Varon M, Seijffers J (1975) Symbiosis-independent and symbiosis-incompetent mutants of Bdellovibrio bacteriovorus 109J. J Bacteriol 124:1191–1197PubMedCentralPubMedGoogle Scholar
  139. Varon M, Shilo M (1968) Interaction of Bdellovibrio bacteriovorus and host bacteria: I Kinetic studies of attachment and invasion of Escherichia coli B by Bdellovibrio bacteriovorus. J Bacteriol 95:744–753PubMedCentralPubMedGoogle Scholar
  140. Varon M, Shilo M (1969) Attachment of Bdellovibrio bacteriovorus to cell wall mutants of Salmonella spp. and Escherichia coli. J Bacteriol 97:977–979PubMedCentralPubMedGoogle Scholar
  141. Wang Z, Kadouri D, Wu M (2011) Genomic insights into an obligate epibiotic bacterial predator: Micavibrio aeruginosavorus ARL-13. BMC Genomics 12:453PubMedCentralPubMedGoogle Scholar
  142. Westergaard JM, Kramer TT (1977) Bdellovibrio and the intestinal flora of vertebrates. Appl Environ Microbiol 34:506–511PubMedCentralPubMedGoogle Scholar
  143. Wilkinson MHF (2007) Mathematical modelling of predatory prokaryotes. In: Jurkevitch E (ed) Predatory prokaryotes, vol 4. Springer, Berlin/Heidelberg, pp 93–130Google Scholar
  144. Williams HN (1988) A study of the distribution of bdellovibrios in estuarine sediment over an annual cycle. Microb Ecol 15:9–20PubMedGoogle Scholar
  145. Williams H, Falkler W, Shay D (1982) Seasonal distribution of bdellovibrios at the mouth of the Patuxent river in the Chesapeake bay. Can J Microbiol 28:111–116PubMedGoogle Scholar
  146. Williams HN, Schoeffied AJ, Guether D, Kelley J, Shah D, Falkler WA (1995) Recovery of bdellovibrios from submerged surfaces and other aquatic habitats. Microb Ecol 29:39–48PubMedGoogle Scholar
  147. Wurtzel O, Dori-Bachash M, Pietrokovski S, Jurkevitch E, Sorek R (2010) Mutation detection with next-generation resequencing through a mediator genome. PLoS One 5:e15628PubMedCentralPubMedGoogle Scholar
  148. Zheng G, Wang C, Williams HN, Pineiro SA (2008) Development and evaluation of a quantitative real-time PCR assay for the detection of saltwater Bacteriovorax. Environ Microbiol 10:2515–2526PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Plant Pathology and Microbiology, Faculty of Agriculture, Food and Environmental SciencesThe Hebrew University of JerusalemRehovotIsrael

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