Phages Preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, Present and Future
Abstract
:1. Introduction
“A strong feeling of adventure is animating those who are working on bacterial viruses, a feeling that they have a small part in the great drive towards a fundamental problem in biology”.—Max Delbrück, 1946 [1].
2. The B. cereus Group and Its Taxonomic Issues
Characteristics | B. anthracis | B. cereus | B. thuringiensis |
---|---|---|---|
Motility | No a | Yes | Yes |
Crystal parasporal inclusion(s) | No | No | Yes |
Lysis by Gamma phage | Yes | No b | No |
Mucoid colony (capsule synthesis on bicarbonate medium) | Yes | No | No |
Hemolytic activity on 5% blood agar (sheep or horse) | No a | Yes c | Yes c |
Penicillin resistance (β-lactamase production) | No a | Yes | Yes |
Phospholipase C activity | No | Yes c | Yes c |
Chitinase activity | No | Yes | Yes |
Tyrosine decomposition | No | Yes | Yes c |
Mutation non-sense in plcR regulator | Yes | No a | No a |
Four genomic prophages | Yes | No | No |
3. Pioneer Milestones
4. Phages of B. anthracis, B. cereus and B. thuringiensis
4.1. Classification of B. cereus Group Phages
Order | Family | Morphology | Shape | Virion Size (nm) | Schematic Representation a |
---|---|---|---|---|---|
Caudovirales | Myoviridae | Isometric head, contractile tail and a small base plate. | Tailed | Icosahedral heads: 50–145 Elongated heads: 80 × 110 Tail: 16–20 × 80–455 | |
Siphoviridae | Isometric head, long non-contractile tail. Some have elongated heads. | Tailed | Head: 40–80 Tail: 5–10 × 100–210 | ||
Podoviridae | Isometric head, short non-contractile tail. Some have elongated heads. | Tailed | Head: 60–70 Tail: 10–20 | ||
Unassigned | Tectiviridae | Isometric virion with apical spikes. Capsid encloses an inner membrane vesicle. | Polyhedral | Virion: 66 Spikes: 20 |
Morphology | Phage | (Original) Host | Estimated Genome Size | Lifestyle | Particular Features | References |
---|---|---|---|---|---|---|
Myoviridae | Bace-11 | B. cereus | ND | ND | Virion morphology related to the 0305ϕ8-36 jumbo phage. | [69,70,71] |
Myoviridae | BCP1-1 | B. cereus | ~150 kb | Virulent | Able to eradicate B. cereus from food. Divalent cations (Ca2+, Mg2+ or Mn2+) required for activity. | [72] |
Myoviridae | BCP8-2 | B. cereus | ~150 kb | Virulent | Able to eradicate B. cereus from food Divalent cations (Ca2+, Mg2+ or Mn2+) required for activity. | [72] |
Myoviridae (SPO1-like) | CP-51 | B. cereus NRRL 569 (ATCC 10876) | ~138 (88) kb a | ND | Mediates generalized transduction. Instability at low temperatures. Infects sporulating B. cereus cells. Related to B. subtilis phage SPO1. | [58,59,64,73,74] |
Myoviridae | CP-54 | B. thuringiensis sv. alesti NRRL 4041 | 84–116 (339) kb a | ND | Mediates generalized transduction. | [59] |
Myoviridae | CP-54Ber | B. thuringiensis sv. thuringiensis Berliner 1715 | 84–116 (339) kb a | ND | Mediates generalized transduction. | [75] |
Myoviridae | FWLBc1 | B. cereus | >90 kb | Virulent | Biocontrols B. cereus. | [76] |
Myoviridae | FWLBc2 | B. cereus | >90 kb | Virulent | Biocontrols B. cereus. | [76] |
Myoviridae | JBP901 | B. cereus | ~150 kb | Virulent | Biocontrols B. cereus in liquid cultures and in fermented Korean food products. | [77] |
Myoviridae | Tg13 | B. thuringiensis | 61 kb | ND | Mediates transduction. | [78] |
Myoviridae | TP-13 | B. thuringiensis | Possibly 380 kb | ND | Mediates generalized transduction. Converting phage for sporulation and crystal formation. Related to B. subtilis phages SP15. | [79] |
Myoviridae | TP-18 | B. thuringiensis | 55 kb | ND | Mediates generalized transduction. | [60] |
Myoviridae | Tt91 | B. thuringiensis | ND | Virulent | Mediates specialized transduction. | [80] |
Siphoviridae | ϕ20 | B. anthracis Sterne 34F2 (pXO1+ pXO2−) | 48.7 kb | ND | Has a circular plasmidial prophage state. | [81] |
Siphoviridae | CP-53 | B. cereus ATCC 6464 | 25 kb | ND | Mediates generalized transduction. | [73,74] |
Siphoviridae | J7W-1 | B. thuringiensis sv. sotto/dendrolimus AF101 | 48 kb | Temperate | Integrates into the 69 kb plasmid pAF101. Is induced by temperature or during mating. | [82,83,84] |
Siphoviridae | MZTP01 | B. thuringiensis sv. kurstaki MZ1 | ND | Temperate | None. | [85] |
Siphoviridae | Px1 | B. thuringiensis sv. galleriae 69/6 | ND | Temperate | Mediates transduction. Very sensitive to chloroform. | [86] |
Siphoviridae | TP21-H | B. thuringiensis | ND | Temperate | None. | [87,88] |
Siphoviridae | SU-11 | B. thuringiensis sv. israelensis | ND | ND | Has a circular plasmidial prophage state. | [89] |
Tectiviridae | Emet | B. cereus 5975c | ~15 kb | Temperate | Isolated from an emetic B. cereus. Has a linear plasmidial prophage state. | [90] |
Tectiviridae | Sand | B. cereus VD184 | ~15 kb | Temperate | Has a linear plasmidial prophage state. | [90] |
Tectiviridae | Sato | B. cereus AND1284 | ~15 kb | Temperate | Isolated from an emetic B. cereus. Has a linear plasmidial prophage state. | [90] |
Tectiviridae | Sole | B. cereus VD166 | ~15 kb | Temperate | Has a linear plasmidial prophage state. | [90] |
ND | - | B. anthracis | ND | Virulent | First phage isolated for this bacterium. | [41] |
ND | ϕ42 | B. thuringiensis sv. gelechiae Bt1134 | ND | ND | Mediates generalized transduction. | [91] |
ND | ϕ63 | B. thuringiensis | ND | ND | Mediates generalized transduction. | [91] |
ND | ϕ64 | B. thuringiensis sv. alesti | 79–85 kb | ND | Mediates generalized transduction. Possibly a mutant of ϕ63. | [92] |
ND | ϕHD67 | B. thuringiensis sv. alesti | 45.7 kb | Temperate | Mediates generalized transduction. | [93,94,95] |
ND | ϕHD130 | B. thuringiensis | 38.1 kb | Temperate | Mediates transduction. | [93,94,95] |
ND | ϕHD228 | B. thuringiensis | 36 kb | Temperate | Mediates transduction. | [93,94,95] |
ND | ϕHD248 | B. thuringiensis | 47.1 kb | Temperate | Mediates transduction. Used for fine-structure chromosomal mapping. | [93,94,95] |
ND | TP-21 (TP21-T) | B. thuringiensis sv. kurstaki HD-1 (HD1-9) | ND | ND | Mediates specialized transduction. Plasmidial phage. | [96,97] |
ND | 12826 | B. cereus WS2453 | ND | ND | Its endolysin (Ply12) lysis several Bacillus sp. | [98] |
ND | BcpI | ND | ND | ND | Its endolysin (PlyB) has a potent lytic action against B. anthracis. | [99] |
ND | TP-10 | B. thuringiensis | ND | ND | Mediates generalized transduction. | [79] |
ND | W | B. cereus W (ATCC 11950) | ND | Temperate | Parental phage for Gamma phage, probably same as Wβ. | [100] |
ND | Wα | B. cereus W (ATCC 11950) | ND | Virulent | Rare virulent mutant of phage W. | [101] |
ND | wx | B. cereus W (ATCC 11950) | ND | Temperate | Cryptic plasmid involved in lysogenic conversion to phospholipase A production. | [102,103] |
ND | wxc | B. cereus W (ATCC 11950) | ND | Virulent | Virulent mutant of phage wx | [102] |
Morphology b | Phage | Host | Genome Size (bp) | GC% | Predicted ORFs | No. tRNAs | Lifestyle | GenBank Accession No. | Reference |
---|---|---|---|---|---|---|---|---|---|
Myoviridae | 0305ϕ8-36 | B. thuringiensis | 218,948 | 41.80 | 247 | 2 | Virulent | EF583821 | [104] |
Myoviridae (Twort-like) | B4 | B. cereus | 162,596 | 37.71 | 277 | 0 | Virulent | JN790865 | [105] |
Myoviridae (Twort-like) | B5S | B. cereus | 162,598 | 37.71 | 272 | 0 | Virulent | JN797796 | [67] |
Myoviridae (Twort-like) | Bastille | B. cereus | 153,962 | 38.14 | 273 | 7 | Virulent | JF966203 | [64] |
Myoviridae | BCD7 | B. cereus | 93,839 | 38.04 | 140 | 0 | Virulent | JN712910 | - |
Myoviridae | BCP78 | B. cereus | 156,176 | 39.86 | 227 | 18 | Virulent | JN797797 | [106] |
Myoviridae | BCU4 | B. cereus | 154,371 | 39.86 | 223 | 19 | Virulent | JN797798 | [67] |
Myoviridae | BigBertha | B. thuringiensis | 162,661 | 37.80 | 287 | 0 | Virulent ? | KF669647 | [107] |
Myoviridae | BPS10C | B. cereus | 159,590 | 38.74 | 271 | 0 | Virulent | KC430106 | [108,109] |
Myoviridae | BPS13 | B. cereus | 158,305 | 38.75 | 268 | 0 | Virulent | JN654439 | [108,109] |
Myoviridae | JL | B. cereus | 137,918 | 40.80 | 22 | 4 | ND | KC595512 | [110] |
Myoviridae | Shanette | B. cereus | 138,877 | 40.80 | 223 | 3 | ND | KC595513 | [110] |
Myoviridae | Spock | B. thuringiensis | 161,497 | 38.20 | 280 | 0 | Virulent ? | KF669662 | [111] |
Myoviridae | Troll | B. thuringiensis | 163,019 | 37.80 | 289 | 0 | ND | KF208639 | [112] |
Myoviridae (Twort-like) | vB_BceM_Bc431v3 | B. cereus | 158,621 | 39.98 | 239 | 20 | Virulent | JX094431 | [68] |
Myoviridae | W.Ph. | B. cereus | 156,897 | 36.45 | 274 | 0 | Virulent | HM144387 | - |
Siphoviridae | 11143 | B. cereus | 39,077 | 34.96 | 49 | 0 | Temperate | GU233956 | [113] |
Siphoviridae | 250 | B. cereus | 56,505 | 36.45 | 54 | 0 | Temperate | GU229986 | [114] |
Siphoviridae | Basilisk | B. cereus | 81,790 | 33.90 | 140 | 2 | ND | KC595511 | [110] |
Siphoviridae | BceA1 | B. cereus | 42,932 | 35.66 | 63 | 0 | Temperate | HE614282 | [115] |
Siphoviridae | BMBtp2 | B. thuringiensis | 36,932 | 37.79 | 53 | 0 | Temperate | JX887877 | [116] |
Siphoviridae | BtCS33 | B. thuringiensis | 41,992 | 35.22 | 57 | 0 | Temperate | JN191664 | [117] |
Siphoviridae | Cherry c | B. anthracis | 36,615 | 35.26 | 51 | 0 | Virulent | DQ222851 | [118] |
Siphoviridae | Fah c | B. anthracis | 37,974 | 34.94 | 50 | 0 | Virulent | DQ150593 | [119] |
Siphoviridae | Gamma USAMRIID c | B. anthracis | 37,253 | 35.22 | 53 | 0 | Virulent | DQ222853 | [118] |
Siphoviridae | Gamma LSU c | B. anthracis | 38,067 | 35.63 | 50 | 0 | Virulent | DQ222855 | [118] |
Siphoviridae | Gamma isolate d’Herelle c | B. anthracis | 37,373 | 35.12 | 53 | 0 | Virulent | DQ289556 | [120] |
Siphoviridae | Gamma Porton c | B. anthracis | 36,083 | 35.10 | ND | 0 | Virulent | DQ221100 | - |
Siphoviridae | MZTP02 | B. thuringiensis | 15,717 | 37.55 | 20 | 0 | Temperate | AY894696 | [121] |
Siphoviridae | PBC1 | B. cereus | 41,164 | 41.68 | 50 | 0 | Virulent | JQ619704 | [122] |
Siphoviridae | phIS3501 | B. thuringiensis | 44,401 | 34.86 | 53 | 1 | Temperate | JQ062992 | [123] |
Siphoviridae | phiCM3 | B. thuringiensis | 38,772 | 35.46 | 56 | 0 | Virulent | KF296718 | [124] |
Siphoviridae | TP21-L | B. cereus | 37,456 | 37.80 | 56 | 0 | Temperate | EU887664 | [88,98] |
Siphoviridae | vB_BanS-Tsamsa | B. anthracis | 168,876 | 37.80 | 272 | 19 | Temperate | KC481682 | [125] |
Siphoviridae | vB_BceS-IEBH | B. cereus | 53,104 | 36.42 | 86 | 0 | Temperate | EU874396 | [126] |
Siphoviridae | Wβ | B. cereus | 40,867 | 35.26 | 53 | 0 | Temperate | DQ289555 | [120] |
Podoviridae | MG-B1 | B. weihenstephanensis | 27,190 | 30.75 | 43 | 0 | Virulent | KC685370 | [127] |
Tectiviridae | AP50 d | B. anthracis | 14,398 | 38.65 | 31 | 0 | Temperate | EU408779 | [128] |
Tectiviridae | Bam35 d | B. thuringiensis | 14,935 | 39.72 | 32 | 0 | Temperate | AY257527 | [129] |
Tectiviridae | GIL01 | B. thuringiensis | 14,931 | 39.73 | 30 | 0 | Temperate | AJ536073 | [130] |
Tectiviridae | GIL16 d | B. thuringiensis | 14,844 | 40.07 | 31 | 0 | Temperate | AY701338 | [131] |
Tectiviridae | Wip1 | B. anthracis | 14,319 | 36.84 | 27 | 0 | Temperate | KF188458 | [132] |
ND | lambdaBa01 | B. anthracis | 50,482 | 35.3 | ND | 0 | Temperate | AE016879 | [16] |
ND | lambdaBa02 | B. anthracis | 44,043 | 35.0 | ND | 0 | Temperate | AE016879 | [16] |
ND | lambdaBa03 | B. anthracis | 16,759 | 35.0 | ND | 0 | Temperate | AE016879 | [16] |
ND | lambdaBa04 | B. anthracis | 37,385 | 34.0 | ND | 0 | Temperate | AE016879 | [16] |
ND | phBC6A51 | B. cereus | 61,395 | 37.69 | 75 | 0 | Temperate | NC_004820 | [17] |
ND | phBC6A52 | B. cereus | 38,472 | 34.72 | 49 | 0 | Temperate | NC_004821 | [17] |
ND | proCM3 | B. thuringiensis | 43,278 | 37.40 | 58 | 0 | Temperate | KF296717 | [124] |
Characteristics | CP-51 | CP-53 | CP-54 | CP-54Ber |
---|---|---|---|---|
Family | Myoviridae | Siphoviridae | Myoviridae | Myoviridae |
Head diameter (nm) | 90 | 66 | 120–122 | 120 |
Tail length (nm) | 160–185 | 276 | 198–200 | 200 |
Estimated genome size (kb) | 138 (88) a | 25 | 84–116 (339) b | 84–116 (339) b |
GC% | 43.9 | 37 | 43 | 43 |
Genome particular features | Fixed ends, HMU c | No unusual bases | HMU | HMU |
Lifestyle | Virulent | Temperate | Virulent | Temperate |
Transduction frequencies | 10−7–10−5 | 10−7–10−6 | 10−7–10−5 | 10−7–10−5 |
Host range | Active on different B. thuringiensis, B.cereus and B. anthracis strains | ND | Broader than CP-51 | Narrower than CP-54, but active on B.thuringiensis sv. thuringiensis strain Berliner 1715 |
Stability at 4 °C | No | Yes | No (more cold sensitive than CP-51) | No |
Stability at 15 °C (plus divalent cations) | Yes | ND | Yes (less than CP-51) | Yes (less than CP-51) |
Infection of sporulating cells | Yes | ND | Yes | Yes |
4.2. The Transducing Phages
4.2.1. Phages CP-51, CP-53, CP-54 and CP-54Ber
4.2.2. Phages TP-13 and TP-18
4.2.3. Phages ϕ63 and its Derivative Mutant ϕ64
4.2.4. Other Transducing Phages
4.3. Phages with a Chromosomal Prophage State
The γ-Like Phages
4.4. Phages with a Plasmidial Prophage State
4.4.1. Circular Plasmidial Prophages
4.4.2. Tectiviruses
4.5. The Jumbo Phages
4.6. Other Remarkable Phages
5. What about Phages in Other Members of the B. cereus Group?
6. Applications of B. cereus Group Phages
6.1. Phage Typing
6.2. Biocontrol
7. Concluding Remarks
Acknowledgments
Conflicts of Interest
References and Notes
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Gillis, A.; Mahillon, J. Phages Preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, Present and Future. Viruses 2014, 6, 2623-2672. https://doi.org/10.3390/v6072623
Gillis A, Mahillon J. Phages Preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, Present and Future. Viruses. 2014; 6(7):2623-2672. https://doi.org/10.3390/v6072623
Chicago/Turabian StyleGillis, Annika, and Jacques Mahillon. 2014. "Phages Preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, Present and Future" Viruses 6, no. 7: 2623-2672. https://doi.org/10.3390/v6072623
APA StyleGillis, A., & Mahillon, J. (2014). Phages Preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, Present and Future. Viruses, 6(7), 2623-2672. https://doi.org/10.3390/v6072623