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Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov.

¹ Microbial Genomics and Bioprocessing Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA
² Bioproducts and Biocatalysis Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA
³ Counterterrorism and Forensic Science Research Unit, Federal Bureau of Investigation Academy, Quantico, VA 22135, USA
⁴ Chemical-Biological Sciences Unit, Laboratory Division, Federal Bureau of Investigation, Quantico, VA 22135, USA

Correspondence
Alejandro P. Rooney
alejandro.rooney{at}ars.usda.gov

The Bacillus subtilis species complex is a tight assemblage of closely related species. For many years, it has been recognized that these species cannot be differentiated on the basis of phenotypic characteristics. Recently, it has been shown that phylogenetic analysis of the 16S rRNA gene also fails to differentiate species within the complex due to the highly conserved nature of the gene, yet DNA–DNA hybridization values fall well below 70 % for the same species comparisons. As a complementary approach, we propose that phylogenetic analysis of multiple protein-coding loci can be used as a means to detect and differentiate novel Bacillus taxa. Indeed, our phylogenetic analyses revealed the existence of a previously unknown group of strains closely related to, but distinct from, Bacillus subtilis subsp. spizizenii. Results of matrix-assisted laser desorption ionization-time of flight mass spectrometry analyses revealed that the group produces a novel surfactin-like lipopeptide with mass m/z 1120.8 that is not produced by the other currently recognized subspecies. In addition, the group displayed differences in the total cellular content of the fatty acids C_{16 : 0} and iso-C_{17 : 1}10c that distinguish it from the closely related B. subtilis subsp. spizizenii. Consequently, the correlation of these novel phenotypic traits with the phylogenetic distinctiveness of this previously unknown subspecies group showed that phylogenetic analysis of multiple protein-coding loci can be used as a means to detect and differentiate novel Bacillus taxa. Therefore, we propose that this new group should be recognized as representing a novel taxon, Bacillus subtilis subsp. inaquosorum subsp. nov., with the type strain NRRL B-23052^T (=KCTC 13429^T=BGSC 3A28^T).

The GenBank/EMBL/DDBJ accession numbers for the sequences generated in this study are EU138452–EU138865.

A maximum-parsimony cladogram of the Bacillus subtilis species complex and tables showing the mean values of synonymous and non-synonymous substitutions per site among protein-coding genes and the geographical origins, isolation substrates and maximum growth temperatures for B. subtilis subsp. inaquosorum subsp. nov., B. subtilis subsp. spizizenii and B. subtilis subsp. subtilis are available as supplementary material with the online version of this paper.