The Phylogeny of Bacillus cereus sensu lato
- Authors: Richard T. Okinaka1, Paul Keim2
- Editors: Patrick Eichenberger3, Adam Driks4
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 1: Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, AZ 86011-4073; 2: Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, AZ 86011-4073; 3: New York University, New York, NY; 4: Loyola University Medical Center, Maywood, IL
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Received 17 October 2012 Accepted 15 December 2015 Published 12 February 2016
- Correspondence: Richard Okinaka, [email protected]

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Abstract:
The three main species of the Bacillus cereus sensu lato, B. cereus, B. thuringiensis, and B. anthracis, were recognized and established by the early 1900s because they each exhibited distinct phenotypic traits. B. thuringiensis isolates and their parasporal crystal proteins have long been established as a natural pesticide and insect pathogen. B. anthracis, the etiological agent for anthrax, was used by Robert Koch in the 19th century as a model to develop the germ theory of disease, and B. cereus, a common soil organism, is also an occasional opportunistic pathogen of humans. In addition to these three historical species designations, are three less-recognized and -understood species: B. mycoides, B. weihenstephanensis, and B. pseudomycoides. All of these “species” combined comprise the Bacillus cereus sensu lato group. Despite these apparently clear phenotypic definitions, early molecular approaches to separate the first three by various DNA hybridization and 16S/23S ribosomal sequence analyses led to some “confusion” because there were limited differences to differentiate between these species. These and other results have led to frequent suggestions that a taxonomic change was warranted to reclassify this group to a single species. But the pathogenic properties of B. anthracis and the biopesticide applications of B. thuringiensis appear to “have outweighed pure taxonomic considerations” and the separate species categories are still being maintained. B. cereus sensu lato represents a classic example of a now common bacterial species taxonomic quandary.
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Citation: Okinaka R, Keim P. 2016. The Phylogeny of Bacillus cereus sensu lato. Microbiol Spectrum 4(1):TBS-0012-2012. doi:10.1128/microbiolspec.TBS-0012-2012.




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Abstract:
The three main species of the Bacillus cereus sensu lato, B. cereus, B. thuringiensis, and B. anthracis, were recognized and established by the early 1900s because they each exhibited distinct phenotypic traits. B. thuringiensis isolates and their parasporal crystal proteins have long been established as a natural pesticide and insect pathogen. B. anthracis, the etiological agent for anthrax, was used by Robert Koch in the 19th century as a model to develop the germ theory of disease, and B. cereus, a common soil organism, is also an occasional opportunistic pathogen of humans. In addition to these three historical species designations, are three less-recognized and -understood species: B. mycoides, B. weihenstephanensis, and B. pseudomycoides. All of these “species” combined comprise the Bacillus cereus sensu lato group. Despite these apparently clear phenotypic definitions, early molecular approaches to separate the first three by various DNA hybridization and 16S/23S ribosomal sequence analyses led to some “confusion” because there were limited differences to differentiate between these species. These and other results have led to frequent suggestions that a taxonomic change was warranted to reclassify this group to a single species. But the pathogenic properties of B. anthracis and the biopesticide applications of B. thuringiensis appear to “have outweighed pure taxonomic considerations” and the separate species categories are still being maintained. B. cereus sensu lato represents a classic example of a now common bacterial species taxonomic quandary.

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Figures

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FIGURE 1
AFLP-based phylogenetic tree of B. cereus sensu lato. This is a schematic representation redrawn from Hill et al. ( 12 ) of 332 isolates. While 10 distinct branches were identified, they formed three main clusters labeled as 1, 2, and 3 to correspond to subgroups identified by Priest et al. ( 15 ) to maintain consistency between AFLP and MLST trees based on the positions of known matching isolates in both trees.

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FIGURE 2
An example of homologous recombination identified in MLST profiles. (A) The diversity of an original MLST subclade (Sotto) based on seven MLST fragments ( 15 ). The same branch is shown, but is now dissected by ClonalFrame ( 33 ) and separated into six consistent fragments (B) and a second inconsistent fragment (ilv) (C) to show that the ilv fragment has two sequence types, 55 and 49, that had experienced recombination events with two other distinct clades.

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FIGURE 3
A graph of the distribution of gene families across B. cereus sensu lato genomes redrawn from Zwick et al. ( 41 ). This figure is based on the definition of the extended core as genes encoding proteins present in 49 or more genomes and accessory genes as those present in <6 genomes. The class between these extremes defined the character gene set.

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FIGURE 4
Whole-genome phylogeny of B. cereus sensu lato. This tree was redrawn based on data sets of concatenated, conserved protein sequences by using a neighbor-joining algorithm ( 41 ). Note that the relative distribution of the isolates based on a conserved whole-genome phylogeny is essentially the same as those observed in numerous MLST and AFLP studies and separated into three major clades.
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