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 genomospecies of the B. cereus group. Here, the combined analyses of core-based phylogeny and all versus all Average Nucleotide Identity values based on 2116 strains were conducted to update the genomospecies circumscriptions within B. cereus group. These analyses suggested the existence of 57 genomospecies, 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 genomospecies such as B. anthracis, B. cereus and B. thuringiensis. The prevalence of toxin and virulence factors coding genes in each of the genomospecies 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. paranthracis, respectively, did not show a positive correlation with those genomospecies. On the other hand, anthrax-like toxin and capsule-biosynthesis coding genes were positively correlated with B. anthracis genomospecies, despite not being present in all strains, and with presumably non-pathogenic genomospecies. Hence, despite these features have been so far considered relevant for industrial or medical classification of related species of the B. cereus group, they were inappropriate for their circumscription. In this study, genomospecies 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.
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All data analyzed during the current study were downloaded from public databases (NCBI), and dates of download are provided in the text. A list of all assembly accessions used in this study is provided in Supplementary Table S1. ANI values of the 4.665.600 genome comparisons, all alignments as well as their corresponding phylogenetic trees in Newick format are available in the GitHub repository (https://github.com/torresmanno/Bacillus-cereus-data).
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Acknowledgements
We would like to thank Agencia Nacional de Promoción Científica y Tecnológica for financial support. MATM is CONICET fellow; CM, GDR, and ME are researchers of the same institution. CAD is a researcher at USDA. We would also like to thank Prunello M. from UNR for assistance with statistical analysis of the results that greatly improved the manuscript. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture. The mention of firm names or trade products does not imply that they are endorsed or recommended by the USDA over other firms or similar products not mentioned. USDA is an equal opportunity provider and employer.
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This study was funded by Agencia Nacional de Promoción Científica y Tecnológica PICT 2018-01872 to ME, PICT2017-3536, PIP2017-11220170100377CO to GDR, and Agricultural Research Service Project Number 5010-22410-019-00-D to CAD.
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All authors contributed conception and design of the study; MATM and CAD performed the in silico analyses; MATM performed the statistical analysis; All authors interpreted the evolutionary relationships; ME wrote the first draft of the manuscript; All authors wrote sections of the manuscript, contributed to manuscript revision, read and approved the submitted version.
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Torres Manno, M.A., Repizo, G.D., Magni, C. et al. The assessment of leading traits in the taxonomy of the Bacillus cereus group. Antonie van Leeuwenhoek 113, 2223–2242 (2020). https://doi.org/10.1007/s10482-020-01494-3
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DOI: https://doi.org/10.1007/s10482-020-01494-3