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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Availability of data and materials
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).
References
Alcaraz L, Moreno-Hagelsieb G, Eguiarte LE, Souza V, Herrera-Estrella L, Olmedo G (2010) Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genom 11:332. https://doi.org/10.1186/1471-2164-11-332
Amor MGB, Siala M, Zayani M, Grosset N, Smaoui S, Messadi-Akrout F, Baron F, Jan S, Gautier M, Gdoura R (2018) Isolation, identification, prevalence, and genetic diversity of Bacillus cereus group bacteria from different foodstuffs in Tunisia. Front Microbiol 9:1–12. https://doi.org/10.3389/fmicb.2018.00447
Anderson I, Sorokin A, Kapatral V, Reznik G, Bhattacharya A, Mikhailova N, Burd H, Joukov V, Kaznadzey D, Walunas T, D’Souza M, Larsen N, Pusch G, Liolios K, Grechkin Y, Lapidus A, Goltsman E, Chu L, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N, Ivanova N (2005) Comparative genome analysis of Bacillus cereus group genomes with Bacillus subtilis. FEMS Microbiol Lett 250:175–184. https://doi.org/10.1016/j.femsle.2005.07.008
Apetroaie C, Andersson MA, Spröer C, Tsitko I, Shaheen R, Jääskeläinen EL, Wijnands LM, Heikkilä R, Salkinoja-Salonen MS (2005) Cereulide-producing strains of Bacillus cereus show diversity. Arch Microbiol 184:141–151. https://doi.org/10.1007/s00203-005-0032-1
Baek I, Lee K, Goodfellow M, Chun J (2019) Comparative genomic and phylogenomic analyses clarify relationships within and between Bacillus cereus and Bacillus thuringiensis: proposal for the recognition of two Bacillus thuringiensis Genomovars. Front Microbiol 10:1–11. https://doi.org/10.3389/fmicb.2019.01978
Bazinet AL (2017) Pan-genome and phylogeny of Bacillus cereus sensu lato. BMC Evol Biol 17:1–16. https://doi.org/10.1186/s12862-017-1020-1
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Beno SM, Orsi RH, Cheng RA, Kent DJ, Kovac J, Duncan DR, Martin NH, Wiedmann M (2019) Genes associated with psychrotolerant Bacillus cereus group isolates. Front Microbiol 10:1–14. https://doi.org/10.3389/fmicb.2019.00662
Bhandari V, Ahmod NZ, Shah HN, Gupta RS (2013) Molecular signatures for Bacillus species: Demarcation of the Bacillus subtilis and Bacillus cereus clades in molecular terms and proposal to limit the placement of new species into the genus Bacillus. Int J Syst Evol Microbiol 63:2712–2726. https://doi.org/10.1099/ijs.0.048488-0
Borowiec ML (2016) AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4:e1660. https://doi.org/10.7717/peerj.1660
Bradley PH, Nayfach S, Pollard KS (2018) Phylogeny-corrected identification of microbial gene families relevant to human gut colonization
Carlin F, Brillard J, Broussolle V, Clavel T, Duport C, Jobin M, Guinebretière MH, Auger S, Sorokine A, Nguyen-Thé C (2010) Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment. Food Res Int 43:1885–1894. https://doi.org/10.1016/j.foodres.2009.10.024
Carroll LM, Kovac J, Miller RA, Wiedmann M (2017) Rapid, high-throughput identification of anthrax-causing and emetic Bacillus cereus group genome assemblies via BTyper, a computational tool for virulence-based classification of Bacillus cereus group isolates by using nucleotide sequencing. Appl Environ Microbiol 83:1–19. https://doi.org/10.1128/aem.01096-17
Carroll LM, Wiedmann M, Mukherjee M, Nicholas DC, Mingle LA, Dumas NB, Cole JA, Kovac J (2019) Characterization of emetic and diarrheal Bacillus cereus strains from a 2016 foodborne outbreak using whole-genome sequencing: addressing the microbiological, epidemiological, and bioinformatic challenges. Front Microbiol. https://doi.org/10.3389/fmicb.2019.00144
Carroll LM, Wiedmann M, Kovac J (2020) Proposal of a taxonomic nomenclature for the Bacillus cereus group which reconciles genomic definitions of bacterial species with clinical and industrial phenotypes. MBio 11:1–15. https://doi.org/10.1128/mBio.00034-20
Ceuppens S, Boon N, Uyttendaele M (2013) Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles. FEMS Microbiol Ecol 84:433–450. https://doi.org/10.1111/1574-6941.12110
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.0.002516
Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K, Turner S, Brover S, Schoch CL, Kimchi A, DiCuccio M (2018) Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 68:2386–2392. https://doi.org/10.1099/ijsem.0.002809
Didelot X, Barker M, Falush D, Priest FG (2009) Evolution of pathogenicity in the Bacillus cereus group. Syst Appl Microbiol 32:81–90. https://doi.org/10.1016/j.syapm.2009.01.001
EFSA BIOHAZ Panel (2016) Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs EFSA panel on biological hazards (BIOHAZ). https://doi.org/10.2903/j.efsa.2016.4524
Ehling-Schulz M, Fricker M, Grallert H, Rieck P, Wagner M, Scherer S (2006) Cereulide synthetase gene cluster from emetic Bacillus cereus: Structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiol 6:1–11. https://doi.org/10.1186/1471-2180-6-20
Espariz M, Zuljan FA, Esteban L, Magni C (2016) Taxonomic Identity resolution of highly phylogenetically related strains and selection of phylogenetic markers by using genome-scale methods: the Bacillus pumilus group case. PLoS ONE 11:e0163098. https://doi.org/10.1371/journal.pone.0163098
Fagerlund A, Ween O, Lund T, Hardy SP, Granum PE (2004) Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology. https://doi.org/10.1099/mic.0.26975-0
Felis GE, Dellaglio F (2007) On species descriptions based on a single strain: proposal to introduce the status species proponenda (sp. pr.). Int J Syst Evol Microbiol 57:2185–2187. https://doi.org/10.1099/ijs.0.64931-0
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. https://doi.org/10.1086/284325
Garufi G, Butler E, Missiakas D (2008) ESAT-6-like protein secretion in Bacillus anthracis. J Bacteriol 190:7004–7011. https://doi.org/10.1128/JB.00458-08
Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739. https://doi.org/10.1038/nrmicro1236
Guérin A, Rønning HT, Dargaignaratz C, Clavel T, Broussolle V, Mahillon J, Granum PE, Nguyen-The C (2017) Cereulide production by Bacillus weihenstephanensis strains during growth at different pH values and temperatures. Food Microbiol. https://doi.org/10.1016/j.fm.2017.02.006
Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P (2008) Ecological diversification in the Bacillus cereus Group. Environ Microbiol 10:851–865. https://doi.org/10.1111/j.1462-2920.2007.01495.x
Guinebretière MH, Velge P, Couvert O, Carlin F, Debuyser ML, Nguyen-The C (2010) Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. J Clin Microbiol 48:3388–3391. https://doi.org/10.1128/JCM.00921-10
Guinebretière MH, Auger S, Galleron N, Contzen M, de Sarrau B, de Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, de Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. Int J Syst Evol Microbiol 63:31–40. https://doi.org/10.1099/ijs.0.030627-0
Hagan AK, Plotnick YM, Dingle RE, Mendel ZI, Cendrowski SR, Sherman DH, Tripathi A, Hanna PC (2018) Petrobactin protects against oxidative stress and enhances sporulation efficiency in Bacillus anthracis sterne. MBio 9:1–14. https://doi.org/10.1128/mBio.02079-18
Han CS, Xie G, Challacombe JF, Altherr MR, Bhotika SS, Bruce D, Campbell CS, Campbell ML, Chen J, Chertkov O, Cleland C, Dimitrijevic M, Doggett NA, Fawcett JJ, Glavina T, Goodwin LA, Hill KK, Hitchcock P, Jackson PJ, Keim P, Kewalramani AR, Longmire J, Lucas S, Malfatti S, Mcmurry K, Meincke LJ, Misra M, Moseman BL, Mundt M, Munk AC, Okinaka RT, Reilly LP, Richardson P, Robinson DL, Rubin E, Saunders E, Tapia R, Tesmer JG, Thayer N, Thompson LS, Tice H, Ticknor LO, Wills PL, Brettin TS, Gilna P (2006) Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis ISOLATES CLOSELY RELATED to Bacillus anthracis†. 188:3382–3390. https://doi.org/10.1128/JB.188.9.3382
Hong HA, Le HD, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29:813–835. https://doi.org/10.1016/j.femsre.2004.12.001
Huppert LA, Ramsdell TL, Chase MR, Sarracino DA, Fortune SM, Burton BM (2014) The ESX system in Bacillus subtilis mediates protein secretion. PLoS ONE. https://doi.org/10.1371/journal.pone.0096267
Ives AR, Garland T (2010) Phylogenetic logistic regression for binary dependent variables. Syst Biol 59:9–26. https://doi.org/10.1093/sysbio/syp074
Ives AR, Garland T (2014) Phylogenetic regression for binary dependent variables. Mod Phylogenetic Comp Methods Appl Evol Biol 59:231–261. https://doi.org/10.1007/978-3-662-43550-2_9
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of 90 K prokaryotic genomes reveals clear species boundaries. Nat Commun. https://doi.org/10.1038/s41467-018-07641-9
Jiménez G, Urdiain M, Cifuentes A, López-López A, Blanch AR, Tamames J, Kämpfer P, Kolstø AB, Ramón D, Martínez JF, Codoñer FM, Rosselló-Móra R (2013) Description of Bacillus toyonensis sp. nov., a novel species of the Bacillus cereus group, and pairwise genome comparisons of the species of the group by means of ANI calculations. Syst Appl Microbiol 36:383–391. https://doi.org/10.1016/j.syapm.2013.04.008
Johler S, Kalbhenn EM, Heini N, Brodmann P, Gautsch S, Bagcioglu M, Contzen M, Stephan R, Ehling-Schulz M (2018) Enterotoxin production of Bacillus thuringiensis isolates from biopesticides, foods, and outbreaks. Front Microbiol 9:1–11. https://doi.org/10.3389/fmicb.2018.01915
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. https://doi.org/10.1093/nar/gkn201
Jolley KA, Maiden MCJ (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-11-595
Jung MY, Paek WK, Park IS, Han JR, Sin Y, Paek J, Rhee MS, Kim H, Song HS, Chang YH (2010) Bacillus gaemokensis sp. nov., isolated from foreshore tidal flat sediment from the Yellow Sea. J Microbiol 48:867–871. https://doi.org/10.1007/s12275-010-0148-0
Kolstø A-B, Tourasse NJ, Økstad OA (2009) What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63:451–476. https://doi.org/10.1146/annurev.micro.091208.073255
Lazarte JN, Lopez RP, Ghiringhelli PD, Berón CM (2018) Bacillus wiedmannii biovar thuringiensis: a specialized mosquitocidal pathogen with plasmids from diverse origins. Genome Biol Evol 10:2823–2833. https://doi.org/10.1093/gbe/evy211
Lee I, Kim YO, Park SC, Chun J (2016) OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760
Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478. https://doi.org/10.1093/nar/gkr201
Levy A, Salas Gonzalez I, Mittelviefhaus M, Clingenpeel S, Herrera Paredes S, Miao J, Wang K, Devescovi G, Stillman K, Monteiro F, Rangel Alvarez B, Lundberg DS, Lu T-Y, Lebeis S, Jin Z, McDonald M, Klein AP, Feltcher ME, Rio TG, Grant SR, Doty SL, Ley RE, Zhao B, Venturi V, Pelletier DA, Vorholt JA, Tringe SG, Woyke T, Dangl JL (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150. https://doi.org/10.1038/s41588-017-0012-9
Liu B, Liu GH, Hu GP, Cetin S, Lin NQ, Tang JY, Tang WQ, Lin YZ (2014) Bacillus bingmayongensis sp. nov., isolated from the pit soil of Emperor Qin’s Terra-cotta warriors in China. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 105:501–510. https://doi.org/10.1007/s10482-013-0102-3
Liu Y, Lai Q, Göker M, Meier-Kolthoff JP, Wang M, Sun Y, Wang L, Shao Z (2015) Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 5:1–11. https://doi.org/10.1038/srep14082
Liu Y, Du J, Lai Q, Zeng R, Ye D, Xu J, Shao Z (2017a) Proposal of nine novel species of the Bacillus cereus group. Int J Syst Evol Microbiol 67:2499–2508. https://doi.org/10.1099/ijsem.0.001821
Liu Y, Lai Q, Du J, Shao Z (2017b) Genetic diversity and population structure of the Bacillus cereus group bacteria from diverse marine environments. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-00817-1
Mandic-mulec I, Stefanic P, Elsas JANDVAN (2015) Ecology of Bacillaceae. Bact Spore Mol Syst. https://doi.org/10.1128/microbiolspec.TBS-0017-2013
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: Functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw1129
Maughan H, Van der Auwera G (2011) Bacillus taxonomy in the genomic era finds phenotypes to be essential though often misleading. Infect Genet Evol 11:789–797. https://doi.org/10.1016/j.meegid.2011.02.001
Mazzantini D, Celandroni F, Salvetti S, Gueye SA, Lupetti A, Senesi S, Ghelardi E (2016) FlhF is required for swarming motility and full pathogenicity of Bacillus cereus. Front Microbiol 7:1–9. https://doi.org/10.3389/fmicb.2016.01644
Méric G, Mageiros L, Pascoe B, Woodcock DJ, Mourkas E, Lamble S, Bowden R, Jolley KA, Raymond B, Sheppard SK (2018) Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group. Mol Ecol 27:1524–1540. https://doi.org/10.1111/mec.14546
Miller RA, Beno SM, Kent DJ, Carroll LM, Martin NH, Boor KJ, Kovac J (2016) Bacillus wiedmannii sp. nov., a psychrotolerant and cytotoxic Bacillus cereus group species isolated from dairy foods and dairy environments. Int J Syst Evol Microbiol 66:4744–4753. https://doi.org/10.1099/ijsem.0.001421
Miller RA, Jian J, Beno SM, Wiedmann M, Kovac J (2018) Intraclade variability in toxin production and cytotoxicity of Bacillus cereus group type strains and dairy-associated isolates. Appl Environ Microbiol 84:1–15. https://doi.org/10.1128/AEM.02479-17
Okinaka R, Pearson T, Keim P (2006) Anthrax, but Not Bacillus anthracis? PLoS Pathog 2:e122. https://doi.org/10.1371/journal.ppat.0020122
Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, Fookes M, Falush D, Keane JA, Parkhill J (2015) Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics. https://doi.org/10.1093/bioinformatics/btv421
Pallen MJ (2002) The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol 10:209–212. https://doi.org/10.1016/S0966-842X(02)02345-4
Patiño-Navarrete R, Sanchis V (2017) Evolutionary processes and environmental factors underlying the genetic diversity and lifestyles of Bacillus cereus group bacteria. Res Microbiol 168:309–318. https://doi.org/10.1016/j.resmic.2016.07.002
Rasko DA, Altherr MR, Han CS, Ravel J (2005) Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29:303–329
Raymond B, Bonsall MB (2013) Cooperation and the evolutionary ecology of bacterial virulence: The Bacillus cereus group as a novel study system. BioEssays 35:706–716. https://doi.org/10.1002/bies.201300028
Rong X, Huang Y (2014) Multi-locus sequence analysis: Taking prokaryotic systematics to the next level. In: Methods in microbiology, 1st edn. Elsevier, Amsterdam, pp 221–251
Rooney AP, Price NPJ, Ehrhardt C, Sewzey JL, Bannan JD (2009) Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. Int J Syst Evol Microbiol 59:2429–2436. https://doi.org/10.1099/ijs.0.009126-0
Rosselló-Móra R (2012) Towards a taxonomy of Bacteria and Archaea based on interactive and cumulative data repositories. Environ Microbiol 14:318–334. https://doi.org/10.1111/j.1462-2920.2011.02599.x
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics. https://doi.org/10.1093/bioinformatics/btu153
Shapiro BJ, Leducq J-B, Mallet J (2016) What is speciation? PLoS Genet 12:e1005860. https://doi.org/10.1371/journal.pgen.1005860
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. https://doi.org/10.1038/msb.2011.75
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stenfors Arnesen LP, Fagerlund A, Granum PE (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32:579–606. https://doi.org/10.1111/j.1574-6976.2008.00112.x
Stevens MJA, Tasara T, Klumpp J, Stephan R, Ehling-Schulz M, Johler S (2019) Whole-genome-based phylogeny of Bacillus cytotoxicus reveals different clades within the species and provides clues on ecology and evolution. Sci Rep. https://doi.org/10.1038/s41598-018-36254-x
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Torres Manno M, Zuljan F, Alarcón S, Esteban L, Blancato V, Espariz M, Magni C (2018) Genetic and phenotypic features defining industrial relevant Lactococcus lactis, L. cremoris and L. lactis biovar. diacetylactis strains. J Biotechnol 282:25–31. https://doi.org/10.1016/j.jbiotec.2018.06.345
Torres Manno MA, Pizarro MD, Prunello M, Magni C, Daurelio LD, Espariz M (2019) GeM-Pro: a tool for genome functional mining and microbial profiling. Appl Microbiol Biotechnol 103:3123–3134. https://doi.org/10.1007/s00253-019-09648-8
Van der Auwera GA, Feldgarden M, Kolter R, Mahillon J (2013) Whole-Genome Sequences of 94 Environmental Isolates of Bacillus cereus sensu lato. Genome Announc 1:1–4. https://doi.org/10.1128/genomeA.00380-13
Whitman WB (2014) The need for change: embracing the genome. In: Methods in microbiology, 1st edn. Elsevier, Amsterdam, pp 1–12
Wu H, Gu Q, Xie Y, Lou Z, Xue P, Fang L, Yu C, Jia D, Huang G, Zhu B, Schneider A, Blom J, Lasch P, Borriss R, Gao X (2019) Cold-adapted Bacilli isolated from the Qinghai-Tibetan Plateau are able to promote plant growth in extreme environments. Environ Microbiol 21:3505–3526. https://doi.org/10.1111/1462-2920.14722
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Zheng J, Gao Q, Liu L, Liu H, Wang Y, Peng D, Ruan L, Raymond B, Sun M (2017) Comparative genomics of Bacillus thuringiensis reveals a path to specialized exploitation of multiple invertebrate hosts. MBio 8:1–14. https://doi.org/10.1128/mBio.00822-17
Zwick ME, Joseph SJ, Didelot X, Chen PE, Bishop-Lilly KA, Stewart AC, Willner K, Nolan N, Lentz S, Thomason MK, Sozhamannan S, Mateczun AJ, Du L, Read TD (2012) Genomic characterization of the Bacillus cereus sensu lato species: Backdrop to the evolution of Bacillus anthracis. Genome Res 22:1512–1524. https://doi.org/10.1101/gr.134437.111
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