Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Research Article

Molecular and Genomic Characterization of PFAB2: A Non-virulent Bacillus anthracis Strain Isolated from an Indian Hot Spring

Author(s): Aparna Banerjee, Vikas K. Somani, Priyanka Chakraborty, Rakesh Bhatnagar, Rajeev K. Varshney, Alex Echeverría-Vega, Sara Cuadros-Orellana and Rajib Bandopadhyay*

Volume 20, Issue 7, 2019

Page: [491 - 507] Pages: 17

DOI: 10.2174/1389202920666191203121610

Price: $65

Abstract

Background: Thermophilic bacilli in both aerobic or facultative anaerobic forms have been isolated for over a hundred years from different mesophilic or thermophilic environments as they are potential source of bioactive secondary metabolites. But the taxonomic resolution in the Bacillus genus at species or at strain level is very challenging for the insufficient divergence of the 16S rRNA genes. One such recurring problem is among Bacillus anthracis, B. cereus and B. thuringiensis. The disease-causing B. anthracis strains have their characteristic virulence factors coded in two wellknown plasmids, namely pXO1 (toxin genes) and pXO2 (capsule genes).

Objective: The present study aimed at the molecular and genomic characterization of a recently reported thermophilic and environmental isolate of B. anthracis, strain PFAB2.

Methods: We performed comparative genomics between the PFAB2 genome and different strains of B. anthracis, along with closely related B. cereus strains.

Results: The pangenomic analysis suggests that the PFAB2 genome harbors no complete prophage genes. Cluster analysis of Bray-Kurtis similarity resemblance matrix revealed that gene content of PFAB2 is more closely related to other environmental strains of B. anthracis. The secretome analysis and the in vitro and in vivo pathogenesis experiments corroborate the avirulent phenotype of this strain. The most probable explanation for this phenotype is the apparent absence of plasmids harboring genes for capsule biosynthesis and toxins secretion in the draft genome. Additional features of PFAB2 are good spore-forming and germinating capabilities and rapid replication ability.

Conclusion: The high replication rate in a wide range of temperatures and culture media, the nonpathogenicity, the good spore forming capability and its genomic similarity to the Ames strain together make PFAB2 an interesting model strain for the study of the pathogenic evolution of B. anthracis.

Keywords: Bacillus anthracis, avirulence, comparative genomics, pangenomics, pathogenesis, secretome analysis.

Graphical Abstract

[1]
Rainey, F.A.; Fritze, D.; Stackebrandt, E. The phylogenetic diversity of thermophilic members of the genus Bacillus as revealed by 16S rDNA analysis. FEMS Microbiol. Lett., 1994, 115(2-3), 205-211.
[http://dx.doi.org/10.1111/j.1574-6968.1994.tb06639.x] [PMID: 8138135]
[2]
Fritze, D. Taxonomy of the genus bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology, 2004, 94(11), 1245-1248.
[http://dx.doi.org/10.1094/PHYTO.2004.94.11.1245] [PMID: 18944461]
[3]
Helgason, E.; Økstad, O.A.; Caugant, D.A.; Johansen, H.A.; Fouet, A.; Mock, M.; Hegna, I.; Kolstø, A.B. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis--one species on the basis of genetic evidence. Appl. Environ. Microbiol., 2000, 66(6), 2627-2630.
[http://dx.doi.org/10.1128/AEM.66.6.2627-2630.2000] [PMID: 10831447]
[4]
Spotts Whitney, E.A.; Beatty, M.E.; Taylor, T.H., Jr; Weyant, R.; Sobel, J.; Arduino, M.J.; Ashford, D.A. Inactivation of Bacillus anthracis spores. Emerg. Infect. Dis., 2003, 9(6), 623-627.
[http://dx.doi.org/10.3201/eid0906.020377] [PMID: 12780999]
[5]
Ortatatli, M.; Canitez, K.; Sezigen, S.; Eyison, R.K.; Kenar, L. Evaluation of gamma-radiation inactivation of a bioterrorism agent, Bacillus anthracis spores, on different materials. Indian J. Microbiol., 2018, 58(1), 76-80.
[http://dx.doi.org/10.1007/s12088-017-0691-z] [PMID: 29434400]
[6]
Yu, G.X. Pathogenic Bacillus anthracis in the progressive gene losses and gains in adaptive evolution. BMC Bioinformatics, 2009, 10(Suppl. 1), S3.
[http://dx.doi.org/10.1186/1471-2105-10-S1-S3] [PMID: 19208130]
[7]
Turnbull, P.C.B.; Hutson, R.A.; Ward, M.J.; Jones, M.N.; Quinn, C.P.; Finnie, N.J.; Duggleby, C.J.; Kramer, J.M.; Melling, J. Bacillus anthracis but not always anthrax. J. Appl. Bacteriol., 1992, 72(1), 21-28.
[http://dx.doi.org/10.1111/j.1365-2672.1992.tb04876.x] [PMID: 1541596]
[8]
Dai, Z.; Koehler, T.M. Regulation of anthrax toxin activator gene (atxA) expression in Bacillus anthracis: temperature, not CO2/bicarbonate, affects AtxA synthesis. Infect. Immun., 1997, 65(7), 2576-2582.
[PMID: 9199422]
[9]
Radnedge, L.; Agron, P.G.; Hill, K.K.; Jackson, P.J.; Ticknor, L.O.; Keim, P.; Andersen, G.L. Genome differences that distinguish Bacillus anthracis from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol., 2003, 69(5), 2755-2764.
[http://dx.doi.org/10.1128/AEM.69.5.2755-2764.2003] [PMID: 12732546]
[10]
Venkateswaran, K.; Checinska Sielaff, A.; Ratnayake, S.; Pope, R.K.; Blank, T.E.; Stepanov, V.G.; Fox, G.E.; van Tongeren, S.P.; Torres, C.; Allen, J.; Jaing, C.; Pierson, D.; Perry, J.; Koren, S.; Phillippy, A.; Klubnik, J.; Treangen, T.J.; Rosovitz, M.J.; Bergman, N.H. Draft Genome sequences from a novel clade of Bacillus cereus Sensu Lato strains, isolated from the international space station. Genome Announc., 2017, 5(32), e00680-e17.
[http://dx.doi.org/10.1128/genomeA.00680-17] [PMID: 28798168]
[11]
Venkateswaran, K.; Singh, N.K.; Checinska Sielaff, A.; Pope, R.K.; Bergman, N.H.; van Tongeren, S.P.; Patel, N.B.; Lawson, P.A.; Satomi, M.; Williamson, C.H.D.; Sahl, J.W.; Keim, P.; Pierson, D.; Perry, J. Non-toxin-producing Bacillus cereus strains belonging to the B. anthracis clade isolated from the International Space Station. mSystems, 2017, 2(3), e00021-e17.
[http://dx.doi.org/10.1128/mSystems.00021-17] [PMID: 28680972]
[12]
Guimarães, L.C.; Florczak-Wyspianska, J.; de Jesus, L.B.; Viana, M.V.; Silva, A.; Ramos, R.T. Soares, Sde.C.; Soares, Sde.C. Inside the pan-genome-methods and software overview. Curr. Genomics, 2015, 16(4), 245-252.
[http://dx.doi.org/10.2174/1389202916666150423002311] [PMID: 27006628]
[13]
Banerjee, A.; Halder, U.; Chaudhry, V.; Varshney, R.K.; Mantri, S.; Bandopadhyay, R. Draft genome sequence of the nonpathogenic, thermotolerant, and exopolysaccharide-producing Bacillus anthracis strain PFAB2 from Panifala hot water spring in West Bengal, India. Genome Announc., 2016, 4(6), e01346-e16.
[http://dx.doi.org/10.1128/genomeA.01346-16] [PMID: 28007848]
[14]
Banerjee, A.; Rudra, S.G.; Mazumder, K.; Nigam, V.; Bandopadhyay, R. Structural and functional properties of exopolysaccharide excreted by a novel Bacillus anthracis (Strain PFAB2) of hot spring origin. Indian J. Microbiol., 2018, 58(1), 39-50.
[http://dx.doi.org/10.1007/s12088-017-0699-4] [PMID: 29434396]
[15]
Kumari, B.; Lohar, S.; Ghosh, M.; Ta, S.; Sengupta, A.; Banerjee, P.P.; Chattopadhyay, A.; Das, D. Structurally characterized Zn2+ selective ratiometric fluorescence probe in 100% water for hela cell imaging: experimental and computational studies. J. Fluoresc., 2016, 26(1), 87-103.
[http://dx.doi.org/10.1007/s10895-015-1688-9] [PMID: 26482592]
[16]
Pelczar, M.J. Manual Of Microbiological Methods-By The Society American Bacteriologists Commitiee On Bacteriological Technic; Mcgraw-Hill Book Company: New York, Toronto, London, 1957.
[17]
Dey, U.; Chatterjee, S.; Mondal, N.K. Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnol. Rep. (Amst.), 2016, 10, 1-7.
[http://dx.doi.org/10.1016/j.btre.2016.02.002] [PMID: 28352518]
[18]
Mikesell, P.; Ivins, B.E.; Ristroph, J.D.; Dreier, T.M. Evidence for plasmid-mediated toxin production in Bacillus anthracis. Infect. Immun., 1983, 39(1), 371-376.
[PMID: 6401695]
[19]
Altschul, S.F.; Madden, T.L.; Schäffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 1997, 25(17), 3389-3402.
[http://dx.doi.org/10.1093/nar/25.17.3389] [PMID: 9254694]
[20]
Goris, J.; Konstantinidis, K.T.; Klappenbach, J.A.; Coenye, T.; Vandamme, P.; Tiedje, J.M. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol., 2007, 57(Pt 1), 81-91.
[http://dx.doi.org/10.1099/ijs.0.64483-0] [PMID: 17220447]
[21]
Richter, M.; Rosselló-Móra, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA, 2009, 106(45), 19126-19131.
[http://dx.doi.org/10.1073/pnas.0906412106] [PMID: 19855009]
[22]
Lee, I.; Ouk Kim, Y.; Park, S.C.; Chun, J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol., 2016, 66(2), 1100-1103.
[http://dx.doi.org/10.1099/ijsem.0.000760] [PMID: 26585518]
[23]
Aziz, R.K.; Bartels, D.; Best, A.A.; DeJongh, M.; Disz, T.; Edwards, R.A.; Formsma, K.; Gerdes, S.; Glass, E.M.; Kubal, M.; Meyer, F.; Olsen, G.J.; Olson, R.; Osterman, A.L.; Overbeek, R.A.; McNeil, L.K.; Paarmann, D.; Paczian, T.; Parrello, B.; Pusch, G.D.; Reich, C.; Stevens, R.; Vassieva, O.; Vonstein, V.; Wilke, A.; Zagnitko, O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics, 2008, 9, 75.
[http://dx.doi.org/10.1186/1471-2164-9-75] [PMID: 18261238]
[24]
Ozer, E.A.; Allen, J.P.; Hauser, A.R. Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt. BMC Genomics, 2014, 15, 737.
[http://dx.doi.org/10.1186/1471-2164-15-737] [PMID: 25168460]
[25]
Pirooznia, M.; Nagarajan, V.; Deng, Y. GeneVenn- A web application for comparing gene lists using Venn diagrams. Bioinformation, 2007, 1(10), 420-422.
[http://dx.doi.org/10.6026/97320630001420] [PMID: 17597932]
[26]
Wu, S.; Zhu, Z.; Fu, L.; Niu, B.; Li, W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics, 2011, 12, 444.
[http://dx.doi.org/10.1186/1471-2164-12-444] [PMID: 21899761]
[27]
Arndt, D.; Grant, J.R.; Marcu, A.; Sajed, T.; Pon, A.; Liang, Y.; Wishart, D.S. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res., 2016, 44(W1), W16-W21.
[http://dx.doi.org/10.1093/nar/gkw387] [PMID: 27141966]
[28]
Lee, K.; Costerton, J.W.; Ravel, J.; Auerbach, R.K.; Wagner, D.M.; Keim, P.; Leid, J.G. Phenotypic and functional characterization of Bacillus anthracis biofilms. Microbiology, 2007, 153(Pt 6), 1693-1701.
[http://dx.doi.org/10.1099/mic.0.2006/003376-0] [PMID: 17526827]
[29]
Peeters, E.; Nelis, H.J.; Coenye, T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods, 2008, 72(2), 157-165.
[http://dx.doi.org/10.1016/j.mimet.2007.11.010] [PMID: 18155789]
[30]
Aggarwal, S.; Somani, V.K.; Bhatnagar, R. Phosphate starvation enhances the pathogenesis of Bacillus anthracis. Int. J. Med. Microbiol., 2015, 305(6), 523-531.
[http://dx.doi.org/10.1016/j.ijmm.2015.06.001] [PMID: 26143397]
[31]
Sinha, K.; Bhatnagar, R. Recombinant GroEL enhances protective antigen-mediated protection against Bacillus anthracis spore challenge. Med. Microbiol. Immunol. (Berl.), 2013, 202(2), 153-165.
[http://dx.doi.org/10.1007/s00430-012-0280-z] [PMID: 23263010]
[32]
Somani, V.K.; Aggarwal, S.; Singh, D.; Prasad, T.; Bhatnagar, R. Identification of novel raft marker protein, FlotP in Bacillus anthracis. Front. Microbiol., 2016, 7, 169.
[http://dx.doi.org/10.3389/fmicb.2016.00169] [PMID: 26925042]
[33]
Chauhan, V.; Singh, A.; Waheed, S.M.; Singh, S.; Bhatnagar, R. Constitutive expression of protective antigen gene of Bacillus anthracis in Escherichia coli. Biochem. Biophys. Res. Commun., 2001, 283(2), 308-315.
[http://dx.doi.org/10.1006/bbrc.2001.4777] [PMID: 11327699]
[34]
Gupta, P.; Batra, S.; Chopra, A.P.; Singh, Y.; Bhatnagar, R. Expression and purification of the recombinant lethal factor of Bacillus anthracis. Infect. Immun., 1998, 66(2), 862-865.
[PMID: 9453657]
[35]
Kumar, P.; Ahuja, N.; Bhatnagar, R. Purification of anthrax edema factor from Escherichia coli and identification of residues required for binding to anthrax protective antigen. Infect. Immun., 2001, 69(10), 6532-6536.
[http://dx.doi.org/10.1128/IAI.69.10.6532-6536.2001] [PMID: 11553601]
[36]
Russell, B.H.; Vasan, R.; Keene, D.R.; Xu, Y. Bacillus anthracis internalization by human fibroblasts and epithelial cells. Cell. Microbiol., 2007, 9(5), 1262-1274.
[http://dx.doi.org/10.1111/j.1462-5822.2006.00869.x] [PMID: 17474904]
[37]
Zwick, M.E.; Joseph, S.J.; Didelot, X.; Chen, P.E.; Bishop-Lilly, K.A.; Stewart, A.C.; Willner, K.; Nolan, N.; Lentz, S.; Thomason, M.K.; Sozhamannan, S.; Mateczun, A.J.; Du, L.; Read, T.D. Genomic characterization of the Bacillus cereus sensu lato species: backdrop to the evolution of Bacillus anthracis. Genome Res., 2012, 22(8), 1512-1524.
[http://dx.doi.org/10.1101/gr.134437.111] [PMID: 22645259]
[38]
Papazisi, L.; Rasko, D.A.; Ratnayake, S.; Bock, G.R.; Remortel, B.G.; Appalla, L.; Liu, J.; Dracheva, T.; Braisted, J.C.; Shallom, S.; Jarrahi, B.; Snesrud, E.; Ahn, S.; Sun, Q.; Rilstone, J.; Okstad, O.A.; Kolstø, A.B.; Fleischmann, R.D.; Peterson, S.N. Investigating the genome diversity of B. cereus and evolutionary aspects of B. anthracis emergence. Genomics, 2011, 98(1), 26-39.
[http://dx.doi.org/10.1016/j.ygeno.2011.03.008] [PMID: 21447378]
[39]
Landini, P. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res. Microbiol., 2009, 160(4), 259-266.
[http://dx.doi.org/10.1016/j.resmic.2009.03.001] [PMID: 19345733]
[40]
Sastalla, I.; Maltese, L.M.; Pomerantseva, O.M.; Pomerantsev, A.P.; Keane-Myers, A.; Leppla, S.H. Activation of the latent PlcR regulon in Bacillus anthracis. Microbiology, 2010, 156(Pt 10), 2982-2993.
[http://dx.doi.org/10.1099/mic.0.041418-0] [PMID: 20688829]
[41]
Popova, T.G.; Millis, B.; Chung, M.C.; Bailey, C.; Popov, S.G. Anthrolysin O and fermentation products mediate the toxicity of Bacillus anthracis to lung epithelial cells under microaerobic conditions. FEMS Immunol. Med. Microbiol., 2011, 61(1), 15-27.
[http://dx.doi.org/10.1111/j.1574-695X.2010.00740.x] [PMID: 20946354]
[42]
Feld, G.K.; Thoren, K.L.; Kintzer, A.F.; Sterling, H.J.; Tang, I.I.; Greenberg, S.G.; Williams, E.R.; Krantz, B.A. Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nat. Struct. Mol. Biol., 2010, 17(11), 1383-1390.
[http://dx.doi.org/10.1038/nsmb.1923] [PMID: 21037566]
[43]
Knaysi, G. Optical density of the endospore of Bacillus cereus and its relation to germination and resistance. J. Bacteriol., 1959, 78(2), 206-216.
[PMID: 16561835]
[44]
Brahmbhatt, T.N.; Janes, B.K.; Stibitz, E.S.; Darnell, S.C.; Sanz, P.; Rasmussen, S.B.; O’Brien, A.D. Bacillus anthracis exosporium protein BclA affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity. Infect. Immun., 2007, 75(11), 5233-5239.
[http://dx.doi.org/10.1128/IAI.00660-07] [PMID: 17709408]
[45]
Green, B.D.; Battisti, L.; Koehler, T.M.; Thorne, C.B.; Ivins, B.E. Demonstration of a capsule plasmid in Bacillus anthracis. Infect. Immun., 1985, 49(2), 291-297.
[PMID: 3926644]
[46]
Carrera, M.; Zandomeni, R.O.; Fitzgibbon, J.; Sagripanti, J.L. Difference between the spore sizes of Bacillus anthracis and other Bacillus species. J. Appl. Microbiol., 2007, 102(2), 303-312.
[http://dx.doi.org/10.1111/j.1365-2672.2006.03111.x] [PMID: 17241334]
[1]
Rainey, F.A.; Fritze, D.; Stackebrandt, E. The phylogenetic diversity of thermophilic members of the genus Bacillus as revealed by 16S rDNA analysis. FEMS Microbiol. Lett., 1994, 115(2-3), 205-211.
[http://dx.doi.org/10.1111/j.1574-6968.1994.tb06639.x] [PMID: 8138135]
[2]
Fritze, D. Taxonomy of the genus bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology, 2004, 94(11), 1245-1248.
[http://dx.doi.org/10.1094/PHYTO.2004.94.11.1245] [PMID: 18944461]
[3]
Helgason, E.; Økstad, O.A.; Caugant, D.A.; Johansen, H.A.; Fouet, A.; Mock, M.; Hegna, I.; Kolstø, A.B. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis--one species on the basis of genetic evidence. Appl. Environ. Microbiol., 2000, 66(6), 2627-2630.
[http://dx.doi.org/10.1128/AEM.66.6.2627-2630.2000] [PMID: 10831447]
[4]
Spotts Whitney, E.A.; Beatty, M.E.; Taylor, T.H., Jr; Weyant, R.; Sobel, J.; Arduino, M.J.; Ashford, D.A. Inactivation of Bacillus anthracis spores. Emerg. Infect. Dis., 2003, 9(6), 623-627.
[http://dx.doi.org/10.3201/eid0906.020377] [PMID: 12780999]
[5]
Ortatatli, M.; Canitez, K.; Sezigen, S.; Eyison, R.K.; Kenar, L. Evaluation of gamma-radiation inactivation of a bioterrorism agent, Bacillus anthracis spores, on different materials. Indian J. Microbiol., 2018, 58(1), 76-80.
[http://dx.doi.org/10.1007/s12088-017-0691-z] [PMID: 29434400]
[6]
Yu, G.X. Pathogenic Bacillus anthracis in the progressive gene losses and gains in adaptive evolution. BMC Bioinformatics, 2009, 10(Suppl. 1), S3.
[http://dx.doi.org/10.1186/1471-2105-10-S1-S3] [PMID: 19208130]
[7]
Turnbull, P.C.B.; Hutson, R.A.; Ward, M.J.; Jones, M.N.; Quinn, C.P.; Finnie, N.J.; Duggleby, C.J.; Kramer, J.M.; Melling, J. Bacillus anthracis but not always anthrax. J. Appl. Bacteriol., 1992, 72(1), 21-28.
[http://dx.doi.org/10.1111/j.1365-2672.1992.tb04876.x] [PMID: 1541596]
[8]
Dai, Z.; Koehler, T.M. Regulation of anthrax toxin activator gene (atxA) expression in Bacillus anthracis: temperature, not CO2/bicarbonate, affects AtxA synthesis. Infect. Immun., 1997, 65(7), 2576-2582.
[PMID: 9199422]
[9]
Radnedge, L.; Agron, P.G.; Hill, K.K.; Jackson, P.J.; Ticknor, L.O.; Keim, P.; Andersen, G.L. Genome differences that distinguish Bacillus anthracis from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol., 2003, 69(5), 2755-2764.
[http://dx.doi.org/10.1128/AEM.69.5.2755-2764.2003] [PMID: 12732546]
[10]
Venkateswaran, K.; Checinska Sielaff, A.; Ratnayake, S.; Pope, R.K.; Blank, T.E.; Stepanov, V.G.; Fox, G.E.; van Tongeren, S.P.; Torres, C.; Allen, J.; Jaing, C.; Pierson, D.; Perry, J.; Koren, S.; Phillippy, A.; Klubnik, J.; Treangen, T.J.; Rosovitz, M.J.; Bergman, N.H. Draft Genome sequences from a novel clade of Bacillus cereus Sensu Lato strains, isolated from the international space station. Genome Announc., 2017, 5(32), e00680-e17.
[http://dx.doi.org/10.1128/genomeA.00680-17] [PMID: 28798168]
[11]
Venkateswaran, K.; Singh, N.K.; Checinska Sielaff, A.; Pope, R.K.; Bergman, N.H.; van Tongeren, S.P.; Patel, N.B.; Lawson, P.A.; Satomi, M.; Williamson, C.H.D.; Sahl, J.W.; Keim, P.; Pierson, D.; Perry, J. Non-toxin-producing Bacillus cereus strains belonging to the B. anthracis clade isolated from the International Space Station. mSystems, 2017, 2(3), e00021-e17.
[http://dx.doi.org/10.1128/mSystems.00021-17] [PMID: 28680972]
[12]
Guimarães, L.C.; Florczak-Wyspianska, J.; de Jesus, L.B.; Viana, M.V.; Silva, A.; Ramos, R.T. Soares, Sde.C.; Soares, Sde.C. Inside the pan-genome-methods and software overview. Curr. Genomics, 2015, 16(4), 245-252.
[http://dx.doi.org/10.2174/1389202916666150423002311] [PMID: 27006628]
[13]
Banerjee, A.; Halder, U.; Chaudhry, V.; Varshney, R.K.; Mantri, S.; Bandopadhyay, R. Draft genome sequence of the nonpathogenic, thermotolerant, and exopolysaccharide-producing Bacillus anthracis strain PFAB2 from Panifala hot water spring in West Bengal, India. Genome Announc., 2016, 4(6), e01346-e16.
[http://dx.doi.org/10.1128/genomeA.01346-16] [PMID: 28007848]
[14]
Banerjee, A.; Rudra, S.G.; Mazumder, K.; Nigam, V.; Bandopadhyay, R. Structural and functional properties of exopolysaccharide excreted by a novel Bacillus anthracis (Strain PFAB2) of hot spring origin. Indian J. Microbiol., 2018, 58(1), 39-50.
[http://dx.doi.org/10.1007/s12088-017-0699-4] [PMID: 29434396]
[15]
Kumari, B.; Lohar, S.; Ghosh, M.; Ta, S.; Sengupta, A.; Banerjee, P.P.; Chattopadhyay, A.; Das, D. Structurally characterized Zn2+ selective ratiometric fluorescence probe in 100% water for hela cell imaging: experimental and computational studies. J. Fluoresc., 2016, 26(1), 87-103.
[http://dx.doi.org/10.1007/s10895-015-1688-9] [PMID: 26482592]
[16]
Pelczar, M.J. Manual Of Microbiological Methods-By The Society American Bacteriologists Commitiee On Bacteriological Technic; Mcgraw-Hill Book Company: New York, Toronto, London, 1957.
[17]
Dey, U.; Chatterjee, S.; Mondal, N.K. Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnol. Rep. (Amst.), 2016, 10, 1-7.
[http://dx.doi.org/10.1016/j.btre.2016.02.002] [PMID: 28352518]
[18]
Mikesell, P.; Ivins, B.E.; Ristroph, J.D.; Dreier, T.M. Evidence for plasmid-mediated toxin production in Bacillus anthracis. Infect. Immun., 1983, 39(1), 371-376.
[PMID: 6401695]
[19]
Altschul, S.F.; Madden, T.L.; Schäffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 1997, 25(17), 3389-3402.
[http://dx.doi.org/10.1093/nar/25.17.3389] [PMID: 9254694]
[20]
Goris, J.; Konstantinidis, K.T.; Klappenbach, J.A.; Coenye, T.; Vandamme, P.; Tiedje, J.M. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol., 2007, 57(Pt 1), 81-91.
[http://dx.doi.org/10.1099/ijs.0.64483-0] [PMID: 17220447]
[21]
Richter, M.; Rosselló-Móra, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA, 2009, 106(45), 19126-19131.
[http://dx.doi.org/10.1073/pnas.0906412106] [PMID: 19855009]
[22]
Lee, I.; Ouk Kim, Y.; Park, S.C.; Chun, J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol., 2016, 66(2), 1100-1103.
[http://dx.doi.org/10.1099/ijsem.0.000760] [PMID: 26585518]
[23]
Aziz, R.K.; Bartels, D.; Best, A.A.; DeJongh, M.; Disz, T.; Edwards, R.A.; Formsma, K.; Gerdes, S.; Glass, E.M.; Kubal, M.; Meyer, F.; Olsen, G.J.; Olson, R.; Osterman, A.L.; Overbeek, R.A.; McNeil, L.K.; Paarmann, D.; Paczian, T.; Parrello, B.; Pusch, G.D.; Reich, C.; Stevens, R.; Vassieva, O.; Vonstein, V.; Wilke, A.; Zagnitko, O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics, 2008, 9, 75.
[http://dx.doi.org/10.1186/1471-2164-9-75] [PMID: 18261238]
[24]
Ozer, E.A.; Allen, J.P.; Hauser, A.R. Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt. BMC Genomics, 2014, 15, 737.
[http://dx.doi.org/10.1186/1471-2164-15-737] [PMID: 25168460]
[25]
Pirooznia, M.; Nagarajan, V.; Deng, Y. GeneVenn- A web application for comparing gene lists using Venn diagrams. Bioinformation, 2007, 1(10), 420-422.
[http://dx.doi.org/10.6026/97320630001420] [PMID: 17597932]
[26]
Wu, S.; Zhu, Z.; Fu, L.; Niu, B.; Li, W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics, 2011, 12, 444.
[http://dx.doi.org/10.1186/1471-2164-12-444] [PMID: 21899761]
[27]
Arndt, D.; Grant, J.R.; Marcu, A.; Sajed, T.; Pon, A.; Liang, Y.; Wishart, D.S. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res., 2016, 44(W1), W16-W21.
[http://dx.doi.org/10.1093/nar/gkw387] [PMID: 27141966]
[28]
Lee, K.; Costerton, J.W.; Ravel, J.; Auerbach, R.K.; Wagner, D.M.; Keim, P.; Leid, J.G. Phenotypic and functional characterization of Bacillus anthracis biofilms. Microbiology, 2007, 153(Pt 6), 1693-1701.
[http://dx.doi.org/10.1099/mic.0.2006/003376-0] [PMID: 17526827]
[29]
Peeters, E.; Nelis, H.J.; Coenye, T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods, 2008, 72(2), 157-165.
[http://dx.doi.org/10.1016/j.mimet.2007.11.010] [PMID: 18155789]
[30]
Aggarwal, S.; Somani, V.K.; Bhatnagar, R. Phosphate starvation enhances the pathogenesis of Bacillus anthracis. Int. J. Med. Microbiol., 2015, 305(6), 523-531.
[http://dx.doi.org/10.1016/j.ijmm.2015.06.001] [PMID: 26143397]
[31]
Sinha, K.; Bhatnagar, R. Recombinant GroEL enhances protective antigen-mediated protection against Bacillus anthracis spore challenge. Med. Microbiol. Immunol. (Berl.), 2013, 202(2), 153-165.
[http://dx.doi.org/10.1007/s00430-012-0280-z] [PMID: 23263010]
[32]
Somani, V.K.; Aggarwal, S.; Singh, D.; Prasad, T.; Bhatnagar, R. Identification of novel raft marker protein, FlotP in Bacillus anthracis. Front. Microbiol., 2016, 7, 169.
[http://dx.doi.org/10.3389/fmicb.2016.00169] [PMID: 26925042]
[33]
Chauhan, V.; Singh, A.; Waheed, S.M.; Singh, S.; Bhatnagar, R. Constitutive expression of protective antigen gene of Bacillus anthracis in Escherichia coli. Biochem. Biophys. Res. Commun., 2001, 283(2), 308-315.
[http://dx.doi.org/10.1006/bbrc.2001.4777] [PMID: 11327699]
[34]
Gupta, P.; Batra, S.; Chopra, A.P.; Singh, Y.; Bhatnagar, R. Expression and purification of the recombinant lethal factor of Bacillus anthracis. Infect. Immun., 1998, 66(2), 862-865.
[PMID: 9453657]
[35]
Kumar, P.; Ahuja, N.; Bhatnagar, R. Purification of anthrax edema factor from Escherichia coli and identification of residues required for binding to anthrax protective antigen. Infect. Immun., 2001, 69(10), 6532-6536.
[http://dx.doi.org/10.1128/IAI.69.10.6532-6536.2001] [PMID: 11553601]
[36]
Russell, B.H.; Vasan, R.; Keene, D.R.; Xu, Y. Bacillus anthracis internalization by human fibroblasts and epithelial cells. Cell. Microbiol., 2007, 9(5), 1262-1274.
[http://dx.doi.org/10.1111/j.1462-5822.2006.00869.x] [PMID: 17474904]
[37]
Zwick, M.E.; Joseph, S.J.; Didelot, X.; Chen, P.E.; Bishop-Lilly, K.A.; Stewart, A.C.; Willner, K.; Nolan, N.; Lentz, S.; Thomason, M.K.; Sozhamannan, S.; Mateczun, A.J.; Du, L.; Read, T.D. Genomic characterization of the Bacillus cereus sensu lato species: backdrop to the evolution of Bacillus anthracis. Genome Res., 2012, 22(8), 1512-1524.
[http://dx.doi.org/10.1101/gr.134437.111] [PMID: 22645259]
[38]
Papazisi, L.; Rasko, D.A.; Ratnayake, S.; Bock, G.R.; Remortel, B.G.; Appalla, L.; Liu, J.; Dracheva, T.; Braisted, J.C.; Shallom, S.; Jarrahi, B.; Snesrud, E.; Ahn, S.; Sun, Q.; Rilstone, J.; Okstad, O.A.; Kolstø, A.B.; Fleischmann, R.D.; Peterson, S.N. Investigating the genome diversity of B. cereus and evolutionary aspects of B. anthracis emergence. Genomics, 2011, 98(1), 26-39.
[http://dx.doi.org/10.1016/j.ygeno.2011.03.008] [PMID: 21447378]
[39]
Landini, P. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res. Microbiol., 2009, 160(4), 259-266.
[http://dx.doi.org/10.1016/j.resmic.2009.03.001] [PMID: 19345733]
[40]
Sastalla, I.; Maltese, L.M.; Pomerantseva, O.M.; Pomerantsev, A.P.; Keane-Myers, A.; Leppla, S.H. Activation of the latent PlcR regulon in Bacillus anthracis. Microbiology, 2010, 156(Pt 10), 2982-2993.
[http://dx.doi.org/10.1099/mic.0.041418-0] [PMID: 20688829]
[41]
Popova, T.G.; Millis, B.; Chung, M.C.; Bailey, C.; Popov, S.G. Anthrolysin O and fermentation products mediate the toxicity of Bacillus anthracis to lung epithelial cells under microaerobic conditions. FEMS Immunol. Med. Microbiol., 2011, 61(1), 15-27.
[http://dx.doi.org/10.1111/j.1574-695X.2010.00740.x] [PMID: 20946354]
[42]
Feld, G.K.; Thoren, K.L.; Kintzer, A.F.; Sterling, H.J.; Tang, I.I.; Greenberg, S.G.; Williams, E.R.; Krantz, B.A. Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nat. Struct. Mol. Biol., 2010, 17(11), 1383-1390.
[http://dx.doi.org/10.1038/nsmb.1923] [PMID: 21037566]
[43]
Knaysi, G. Optical density of the endospore of Bacillus cereus and its relation to germination and resistance. J. Bacteriol., 1959, 78(2), 206-216.
[PMID: 16561835]
[44]
Brahmbhatt, T.N.; Janes, B.K.; Stibitz, E.S.; Darnell, S.C.; Sanz, P.; Rasmussen, S.B.; O’Brien, A.D. Bacillus anthracis exosporium protein BclA affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity. Infect. Immun., 2007, 75(11), 5233-5239.
[http://dx.doi.org/10.1128/IAI.00660-07] [PMID: 17709408]
[45]
Green, B.D.; Battisti, L.; Koehler, T.M.; Thorne, C.B.; Ivins, B.E. Demonstration of a capsule plasmid in Bacillus anthracis. Infect. Immun., 1985, 49(2), 291-297.
[PMID: 3926644]
[46]
Carrera, M.; Zandomeni, R.O.; Fitzgibbon, J.; Sagripanti, J.L. Difference between the spore sizes of Bacillus anthracis and other Bacillus species. J. Appl. Microbiol., 2007, 102(2), 303-312.
[http://dx.doi.org/10.1111/j.1365-2672.2006.03111.x] [PMID: 17241334]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy