Phylogenetic and protein prediction analysis reveals the taxonomically diverse distribution of virulence factors in Bacillus cereus strains.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101285081 Publication Model: eCollection Cited Medium: Internet ISSN: 1932-6203 (Electronic) Linking ISSN: 19326203 NLM ISO Abbreviation: PLoS One Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science

Bacillus cereus*/metabolism ; Virulence Factors*/metabolism; Enterotoxins/genetics ; Phylogeny ; Virulence/genetics

Bacillus cereus is a food contaminant with widely varying enterotoxic potential due to its virulence proteins. In this article, phylogenetic analysis of the amino acid sequences from the whole-genomes of 41 strains, evolutionary distance calculation of the amino acid sequences of the virulence genes, and functional and structural predictions of the virulence proteins were performed to reveal the taxonomically diverse distribution of virulence factors. The genome evolution of the strains showed a clustering trend based on the protein-coding virulence genes. The strains of B. cereus have evolved into non-toxic risk and toxic risk clusters with medium-high- and medium-low-risk subclusters. The evolutionary transfer distances of incomplete virulence genes relative to housekeeping genes were greater than those of complete virulence genes, and the distance values of HblACD were higher than those of nheABC and CytK among the complete virulence genes. Cytoplasmic localization was impossible for all the virulence proteins, and NheB, NheC, Hbl-B, and Hbl-L1 were predicted to be extracellular. Nhe and Hbl proteins except CytK had similar spatial structures. The predicted structures of Nhe and Hbl mainly showed 'head' and 'tail' domains. The 'head' of NheA and Hbl-B, including two α-helices separated by β-tongue strands, might play a special role in the formation of Nhe trimers and Hbl trimers, respectively. The 'cap' of CytK, which includes two 'latches' with many β-sheets, formed a β-barrel structure with pores, and a 'rim' balanced the structure. The evolution of B. cereus strains showed a clustering tendency based on the protein-coding virulence genes, and the complete virulence-gene operon combination had higher relative genetic stability. The beta-tongue or latch associated with β-sheet folding might play an important role in the binding of virulence structures and pore-forming toxins in B. cereus.
Competing Interests: The authors have declared that no competing interests exist.

J Dermatol Sci. 2005 Nov;40(2):141-3. (PMID: 16199139)
PLoS One. 2016 Oct 21;11(10):e0165135. (PMID: 27768742)
BMC Genomics. 2015 Jan 22;16:6. (PMID: 25608745)
Toxins (Basel). 2021 Mar 31;13(4):. (PMID: 33807365)
Genomics Proteomics Bioinformatics. 2021 Aug;19(4):662-667. (PMID: 34119695)
Microbiology (Reading). 2008 Mar;154(Pt 3):693-704. (PMID: 18310016)
Int J Syst Evol Microbiol. 2017 Aug;67(8):2499-2508. (PMID: 28792367)
Nat Biotechnol. 2019 Apr;37(4):420-423. (PMID: 30778233)
Mol Biol Evol. 2013 Dec;30(12):2725-9. (PMID: 24132122)
Bioinformatics. 2016 Mar 15;32(6):929-31. (PMID: 26576653)
Chem Biol Interact. 2008 Jan 30;171(2):236-49. (PMID: 17434157)
mBio. 2020 Feb 25;11(1):. (PMID: 32098810)
BMC Evol Biol. 2017 Aug 02;17(1):176. (PMID: 28768476)
PLoS One. 2013 Sep 10;8(9):e74748. (PMID: 24040335)
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549. (PMID: 29722887)
Trends Food Sci Technol. 2019 Nov;93:94-105. (PMID: 31764911)
Compr Rev Food Sci Food Saf. 2020 Jul;19(4):1605-1657. (PMID: 33337102)
EMBO J. 2006 Jun 7;25(11):2652-61. (PMID: 16688219)
Environ Microbiol. 2008 Apr;10(4):851-65. (PMID: 18036180)
Nucleic Acids Res. 2021 Jan 8;49(D1):D458-D460. (PMID: 33104802)
Cell. 2000 Jan 21;100(2):265-76. (PMID: 10660049)
Antonie Van Leeuwenhoek. 2020 Dec;113(12):2223-2242. (PMID: 33179199)
Appl Environ Microbiol. 2005 Dec;71(12):8214-20. (PMID: 16332805)
Sci Rep. 2015 Sep 16;5:14082. (PMID: 26373441)
Microbiology (Reading). 2004 Dec;150(Pt 12):3959-67. (PMID: 15583149)
Bioinformatics. 2001 Jul;17(7):646-53. (PMID: 11448883)
Genomics Proteomics Bioinformatics. 2015 Oct;13(5):321-31. (PMID: 26563468)
Nucleic Acids Res. 2016 Jan 4;44(D1):D663-8. (PMID: 26602691)
Biophys J. 2011 Dec 7;101(11):2679-83. (PMID: 22261056)
J Food Prot. 2019 Jul;82(7):1210-1216. (PMID: 31233363)
Appl Environ Microbiol. 2000 Jun;66(6):2627-30. (PMID: 10831447)
Acta Crystallogr Sect F Struct Biol Cryst Commun. 2012 Sep 1;68(Pt 9):1073-6. (PMID: 22949198)
Toxicon. 2015 Dec 15;108:226-31. (PMID: 26428390)
Appl Environ Microbiol. 2008 Feb;74(3):850-60. (PMID: 18083872)
Nature. 2021 Aug;596(7873):583-589. (PMID: 34265844)
Proteins. 2008 May 1;71(2):534-40. (PMID: 18175317)
Appl Environ Microbiol. 2002 Jun;68(6):3147-51. (PMID: 12039781)
Toxins (Basel). 2021 Jan 28;13(2):. (PMID: 33525722)
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W252-8. (PMID: 24782522)
Arch Microbiol. 2021 Aug;203(6):3577-3590. (PMID: 33961074)
Nature. 2009 Jun 4;459(7247):726-30. (PMID: 19421192)
Genome Res. 2015 Jul;25(7):1043-55. (PMID: 25977477)
Bioinformatics. 2013 Nov 1;29(21):2722-8. (PMID: 23986568)
BMC Evol Biol. 2015 Nov 10;15:246. (PMID: 26555390)
FEMS Microbiol Lett. 2006 Apr;257(2):293-8. (PMID: 16553866)
BMC Genomics. 2013 Dec 23;14:913. (PMID: 24365132)
J Appl Microbiol. 2006 Sep;101(3):579-93. (PMID: 16907808)
Toxicon. 2014 Jan;77:49-57. (PMID: 24211313)
Biochimie. 1996;78(5):364-9. (PMID: 8905155)
Curr Microbiol. 2018 May;75(5):531-540. (PMID: 29332140)
Front Microbiol. 2015 Jun 10;6:560. (PMID: 26113843)
Syst Appl Microbiol. 2009 Apr;32(2):81-90. (PMID: 19200684)
Toxins (Basel). 2019 May 20;11(5):. (PMID: 31137585)
BMC Genomics. 2016 Aug 09;17:581. (PMID: 27507015)

0 (Enterotoxins)
0 (Virulence Factors)

Date Created: 20220519 Date Completed: 20220523 Latest Revision: 20220627

20250114

PMC9119529

10.1371/journal.pone.0262974

35588435