The assessment of leading traits in the taxonomy of the Bacillus cereus group

Authors: TORRES MANNO, MARIANO - National University Of Rosario; REPIZO, GUILLERMO - National University Of Rosario; MAGNI, CHRISTIAN - National University Of Rosario; Dunlap, Christopher; ESPARIZ, MARTIN - National University Of Rosario

Submitted to: Antonie Van Leeuwenhoek
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/23/2020
Publication Date: 11/12/2020
Citation: Torres Manno, M.A., Repizo, G.D., Magni, C., Dunlap, C.A., Espariz, M. 2020. The assessment of leading traits in the taxonomy of the Bacillus cereus group. Antonie Van Leeuwenhoek. 113:2223-2242. https://doi.org/10.1007/s10482-020-01494-3.
DOI: https://doi.org/10.1007/s10482-020-01494-3

Interpretive Summary: ARS researchers from Peoria, IL collaborated with Argentinian researchers to evaluate an important class of bacteria and determine their taxonomic position under the most advanced methods of taxonomy. The bacteria that belong to the Bacillus cereus group are very important to agriculture. The genus encompasses species that are important as biological control agents, plant growth promoters, probiotics, sources of food processing enzymes, food fermentation inoculants, food poisoning agents, human and livestock pathogens. This study describes the latest methods for correctly identifying these organisms. Correct identification is very important for regulatory concerns, intellectual property and communication of ideas. This research benefits farmers, business owners and consumers that depend on products affected by bacteria of this genus.

Technical Abstract: Bacillus cereus sensu lato strains (B. cereus group) are widely distributed in nature and have received interest for decades due to their importance in insect pest management, food production and their positive and negative repercussions in human health. Consideration of practical uses such as virulence, physiology, morphology, or ill-defined features have been applied to describe and classify species of the group. However, current comparative studies have exposed inconsistencies between evolutionary relatedness and biological significance among species of the B. cereus group. Here, in order to update the species circumscriptions within B. cereus group, core-based phylogenetic and all versus all Average Nucleotide Identity value analyses of 2,116 strains were conducted. These analyses suggested the existence of 57 species, 37 of which are novel, thus indicating that the taxonomic identities of more than 39% of the analyzed strains should be revised or updated. In addition, we found that whole-genome in silico analyses were suitable to differentiate species such as B. anthracis, B. cereus and B. thuringiensis. The prevalence of toxin and virulence factors coding genes in each of the species of the B. cereus group was also examined, using phylogeny-aware methods at wide-genome scale. Remarkably, Cry and emetic toxins, commonly assumed to be associated with B. thuringiensis and emetic B. cereus, respectively, did not show a positive correlation with those species. On the other hand, anthrax-like toxin coding genes were positively correlated with B. anthracis species, despite not being present in all strains, and with presumably non-pathogenic species. Hence, despite these features have been so far considered relevant for industrial or medical classification of related species of the B. cereus group, they resulted inappropriate for their circumscription. In this study, species of the group were accurately affiliated and representative strains defined, generating a rational framework that will allow comparative analysis in epidemiological or ecological studies. Based on this classification the role of specific markers such as Type VII secretion system, cytolysin, bacillolysin, and siderophores such as Petrobactin were pointed out for further analysis.