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Genomic comparison of 93 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity.

Grose JH, Jensen GL, Burnett SH, Breakwell DP - BMC Genomics (2014)

Bottom Line: In addition, 3,058 (62%) of phams were orphams (phams containing a gene product from a single phage).These included several genes that may contribute to the pathogenicity of Bacillus strains.The presence of sparsely populated clusters, the high ratio of singletons to clusters, and the large number of uncharacterized, conserved proteins confirms the need for more Bacillus phage isolation in order to understand the full extent of their diversity as well as their impact on host evolution.

View Article: PubMed Central - PubMed

Affiliation: Microbiology and Molecular Biology Department, Brigham Young University, Provo, UT, USA. julianne_grose@byu.edu.

ABSTRACT

Background: The Bacillus genus of Firmicutes bacteria is ubiquitous in nature and includes one of the best characterized model organisms, B. subtilis, as well as medically significant human pathogens, the most notorious being B. anthracis and B. cereus. As the most abundant living entities on the planet, bacteriophages are known to heavily influence the ecology and evolution of their hosts, including providing virulence factors. Thus, the identification and analysis of Bacillus phages is critical to understanding the evolution of Bacillus species, including pathogenic strains.

Results: Whole genome nucleotide and proteome comparison of the 93 extant Bacillus phages revealed 12 distinct clusters, 28 subclusters and 14 singleton phages. Host analysis of these clusters supports host boundaries at the subcluster level and suggests phages as vectors for genetic transfer within the Bacillus cereus group, with B. anthracis as a distant member of the group. Analysis of the proteins conserved among these phages reveals enormous diversity and the uncharacterized nature of these phages, with a total of 4,922 protein families (phams) of which only 951 (19%) had a predicted function. In addition, 3,058 (62%) of phams were orphams (phams containing a gene product from a single phage). The most populated phams were those encoding proteins involved in DNA metabolism, virion structure and assembly, cell lysis, or host function. These included several genes that may contribute to the pathogenicity of Bacillus strains.

Conclusions: This analysis provides a basis for understanding and characterizing Bacillus phages and other related phages as well as their contributions to the evolution and pathogenicity of Bacillus cereus group bacteria. The presence of sparsely populated clusters, the high ratio of singletons to clusters, and the large number of uncharacterized, conserved proteins confirms the need for more Bacillus phage isolation in order to understand the full extent of their diversity as well as their impact on host evolution.

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Analysis of fully sequencedBacillusphage genomes belonging to clusters I through L reveals 13 subclusters. (I-L) Bacillus phage clusters I through L, respectively. Subcluster divisions are provided by blue lines and are indicated on the Y-axis when there are more than one per cluster. Individual phages are separated by red lines. Phage names are provided on the X-axis and Y-axis with host abbreviation from which the phages were isolated indicated on the Y-axis. Hosts abbreviations are Bacillus anthracis (A), Bacillus cereus (C), Bacillus sp. (B), Bacillus megaterium (M), Bacillus pumulis (P), Bacillus subtilis (S), Bacillus thuringiensis (T), and Bacillus weihenstephanensis MG1, (W). Dot plots were produced using Gepard [61].
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Fig3: Analysis of fully sequencedBacillusphage genomes belonging to clusters I through L reveals 13 subclusters. (I-L) Bacillus phage clusters I through L, respectively. Subcluster divisions are provided by blue lines and are indicated on the Y-axis when there are more than one per cluster. Individual phages are separated by red lines. Phage names are provided on the X-axis and Y-axis with host abbreviation from which the phages were isolated indicated on the Y-axis. Hosts abbreviations are Bacillus anthracis (A), Bacillus cereus (C), Bacillus sp. (B), Bacillus megaterium (M), Bacillus pumulis (P), Bacillus subtilis (S), Bacillus thuringiensis (T), and Bacillus weihenstephanensis MG1, (W). Dot plots were produced using Gepard [61].

Mentions: Each cluster was further analyzed by nucleotide dot plot to reveal groups of high similarity, or subclusters (FiguresĀ 2 and 3). These subclusters were chosen based on natural divisions in phage similarity seen in the dot plot, but could be more strictly defined by ANI values of at least 66% between two phages within the subcluster. The subcluster assignments indicate great diversity in the relatedness within each Bacillus phage cluster. It is unknown whether this diversity represents evolutionary forces that constrain certain types of phages or if it is an artifact of phage isolation. Further phage isolation is necessary for this distinction.Figure 2


Genomic comparison of 93 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity.

Grose JH, Jensen GL, Burnett SH, Breakwell DP - BMC Genomics (2014)

Analysis of fully sequencedBacillusphage genomes belonging to clusters I through L reveals 13 subclusters. (I-L) Bacillus phage clusters I through L, respectively. Subcluster divisions are provided by blue lines and are indicated on the Y-axis when there are more than one per cluster. Individual phages are separated by red lines. Phage names are provided on the X-axis and Y-axis with host abbreviation from which the phages were isolated indicated on the Y-axis. Hosts abbreviations are Bacillus anthracis (A), Bacillus cereus (C), Bacillus sp. (B), Bacillus megaterium (M), Bacillus pumulis (P), Bacillus subtilis (S), Bacillus thuringiensis (T), and Bacillus weihenstephanensis MG1, (W). Dot plots were produced using Gepard [61].
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4197329&req=5

Fig3: Analysis of fully sequencedBacillusphage genomes belonging to clusters I through L reveals 13 subclusters. (I-L) Bacillus phage clusters I through L, respectively. Subcluster divisions are provided by blue lines and are indicated on the Y-axis when there are more than one per cluster. Individual phages are separated by red lines. Phage names are provided on the X-axis and Y-axis with host abbreviation from which the phages were isolated indicated on the Y-axis. Hosts abbreviations are Bacillus anthracis (A), Bacillus cereus (C), Bacillus sp. (B), Bacillus megaterium (M), Bacillus pumulis (P), Bacillus subtilis (S), Bacillus thuringiensis (T), and Bacillus weihenstephanensis MG1, (W). Dot plots were produced using Gepard [61].
Mentions: Each cluster was further analyzed by nucleotide dot plot to reveal groups of high similarity, or subclusters (FiguresĀ 2 and 3). These subclusters were chosen based on natural divisions in phage similarity seen in the dot plot, but could be more strictly defined by ANI values of at least 66% between two phages within the subcluster. The subcluster assignments indicate great diversity in the relatedness within each Bacillus phage cluster. It is unknown whether this diversity represents evolutionary forces that constrain certain types of phages or if it is an artifact of phage isolation. Further phage isolation is necessary for this distinction.Figure 2

Bottom Line: In addition, 3,058 (62%) of phams were orphams (phams containing a gene product from a single phage).These included several genes that may contribute to the pathogenicity of Bacillus strains.The presence of sparsely populated clusters, the high ratio of singletons to clusters, and the large number of uncharacterized, conserved proteins confirms the need for more Bacillus phage isolation in order to understand the full extent of their diversity as well as their impact on host evolution.

View Article: PubMed Central - PubMed

Affiliation: Microbiology and Molecular Biology Department, Brigham Young University, Provo, UT, USA. julianne_grose@byu.edu.

ABSTRACT

Background: The Bacillus genus of Firmicutes bacteria is ubiquitous in nature and includes one of the best characterized model organisms, B. subtilis, as well as medically significant human pathogens, the most notorious being B. anthracis and B. cereus. As the most abundant living entities on the planet, bacteriophages are known to heavily influence the ecology and evolution of their hosts, including providing virulence factors. Thus, the identification and analysis of Bacillus phages is critical to understanding the evolution of Bacillus species, including pathogenic strains.

Results: Whole genome nucleotide and proteome comparison of the 93 extant Bacillus phages revealed 12 distinct clusters, 28 subclusters and 14 singleton phages. Host analysis of these clusters supports host boundaries at the subcluster level and suggests phages as vectors for genetic transfer within the Bacillus cereus group, with B. anthracis as a distant member of the group. Analysis of the proteins conserved among these phages reveals enormous diversity and the uncharacterized nature of these phages, with a total of 4,922 protein families (phams) of which only 951 (19%) had a predicted function. In addition, 3,058 (62%) of phams were orphams (phams containing a gene product from a single phage). The most populated phams were those encoding proteins involved in DNA metabolism, virion structure and assembly, cell lysis, or host function. These included several genes that may contribute to the pathogenicity of Bacillus strains.

Conclusions: This analysis provides a basis for understanding and characterizing Bacillus phages and other related phages as well as their contributions to the evolution and pathogenicity of Bacillus cereus group bacteria. The presence of sparsely populated clusters, the high ratio of singletons to clusters, and the large number of uncharacterized, conserved proteins confirms the need for more Bacillus phage isolation in order to understand the full extent of their diversity as well as their impact on host evolution.

Show MeSH
Related in: MedlinePlus