To clarify the evolutionary relationships and classification of Bacillus species, comprehensive phylogenomic and comparative analyses were performed on >300 Bacillus/Bacillaceae genomes. Multiple genomic-scale phylogenetic trees were initially reconstructed to identify different monophyletic clades of Bacillus species. In parallel, detailed analyses were performed on protein sequences of genomes to identify conserved signature indels (CSIs) that are specific for each of the identified clades. We show that in different reconstructed trees, most of the Bacillus species, in addition to the Subtilis and Cereus clades, consistently formed 17 novel distinct clades. Additionally, some Bacillus species reliably grouped with the genera Alkalicoccus, Caldalkalibacillus, Caldibacillus, Salibacterium and Salisediminibacterium. The distinctness of identified Bacillus species clades is independently strongly supported by 128 identified CSIs which are unique characteristics of these clades, providing reliable means for their demarcation. Based on the strong phylogenetic and molecular evidence, we are proposing that these 17 Bacillus species clades should be recognized as novel genera, with the names Alteribacter gen. nov., Ectobacillus gen. nov., Evansella gen. nov., Ferdinandcohnia gen. nov., Gottfriedia gen. nov., Heyndrickxia gen. nov., Lederbergia gen. nov., Litchfieldia gen. nov., Margalitia gen. nov., Niallia gen. nov., Priestia gen. nov., Robertmurraya gen. nov., Rossellomorea gen. nov., Schinkia gen. nov., Siminovitchia gen. nov., Sutcliffiella gen. nov. and Weizmannia gen. nov. We also propose to transfer 'Bacillus kyonggiensis' to Robertmurraya kyonggiensis sp. nov. (type strain: NB22=JCM 17569T=DSM 26768). Additionally, we report 31 CSIs that are unique characteristics of either the members of the Subtilis clade (containing the type species B. subtilis) or the Cereus clade (containing B. anthracis and B. cereus). As most Bacillus species which are not part of these two clades can now be assigned to other genera, we are proposing an emended description of the genus Bacillus to restrict it to only the members of the Subtilis and Cereus clades.

Erratum: Robust demarcation of seventeen distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for emended genus Bacillus limiting it only to the members of the subtilis and cereus clades of species.

A novel Gram-stain-positive, rod-shaped, endospore-forming, motile, aerobic bacterium, designated as P2T, was isolated from a hot spring water sample collected from Ilica-Erzurum, Turkey. Phylogenetic analyses based on 16S rRNA gene sequence comparisons affiliated strain P2T with the genus Bacillus, and the strain showed the highest sequence identity to Bacillus azotoformans NBRC 15712T (96.7 %). However, the pairwise sequence comparisons of the 16S rRNA genes revealed that strain P2T shared only 94.7 % sequence identity with Bacillus subtilis subsp. subtilis NCIB 3610T, indicating that strain P2T might not be a member of the genus Bacillus. The digital DNA-DNA hybridization and average nucleotide identity values between strain P2T and B. azotoformans NBRC 15712T were 19.8 and 74.2 %, respectively. The cell-wall peptidoglycan of strain P2T contained meso-diaminopimelic acid. The polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, an aminophospholipid, five unidentified phospholipids and two unidentified lipids while the predominant isoprenoid quinone was MK-7. The major fatty acids were iso-C15 : 0 and iso-C16 : 0. The draft genome of strain P2T was composed of 82 contigs and found to be 3.5 Mb with 36.1 mol% G+C content. The results of phylogenomic and phenotypic analyses revealed that strain P2T represents a novel genus in the family Bacillaceae, for which the name Calidifontibacillus erzurumensis gen. nov., sp. nov. is proposed. The type strain of Calidifontibacillus erzurumensis is P2T (=CECT 9886T=DSM 107530T=NCCB 100675T). Based on the results of the present study, it is also suggested that Bacillus azotoformans and Bacillus oryziterrae should be transferred to this novel genus as Calidifontibacillus azotoformans comb. nov. and Calidifontibacillus oryziterrae comb. nov., respectively.

Genome-based classification of Calidifontibacillus erzurumensis gen. nov., sp. nov., isolated from a hot spring in Turkey, with reclassification of Bacillus azotoformans as Calidifontibacillus azotoformans comb. nov. and Bacillus oryziterrae as Calidifontibacillus oryziterrae comb. nov.

Methicillin-resistant Staphylococcus sciuri (MRSS) strain C2865 from a stranded dog in Nigeria was trimethoprim (TMP) resistant but lacked formerly described staphylococcal TMP-resistant dihydrofolate reductase genes (dfr). Whole-genome sequencing, comparative genomics, and pan-genome analyses were pursued to unveil the molecular bases for TMP resistance via resistome and mobilome profiling. MRSS C2865 comprised a species subcluster and positioned just above the intraspecies boundary. Lack of species host tropism was observed. S. sciuri exhibited an open pan-genome, while MRSS C2865 harbored the highest number of unique genes (75% associated with mobilome). Within this fraction, we discovered a transferable TMP resistance gene, named dfrE, which confers high-level TMP resistance in Staphylococcus aureus and Escherichia coli. dfrE was located in a novel multidrug resistance mosaic plasmid (pUR2865-34) encompassing adaptive, mobilization, and segregational stability traits. dfrE was formerly denoted as dfr_like in Exiguobacterium spp. from fish farm sediment in China but escaped identification in one macrococcal and diverse staphylococcal genomes in different Asian countries. dfrE shares the highest identity with dfr of soil-related Paenibacillus anaericanus (68%). Data analysis discloses that dfrE has emerged from a single ancestor and places S. sciuri as a plausible donor. C2865 unique fraction additionally enclosed novel chromosomal mobile islands, including a multidrug-resistant pseudo-SCCmec cassette, three apparently functional prophages (Siphoviridae), and an SaPI4-related staphylococcal pathogenicity island. Since dfrE seems not yet common in staphylococcal clinical specimens, our data promote early surveillance and enable molecular diagnosis. We evidence the genome plasticity of S. sciuri and highlight its role as a resourceful reservoir for adaptive traits. IMPORTANCE The discovery and surveillance of antimicrobial resistance genes (AMRG) and their mobilization platforms are critical to understand the evolution of bacterial resistance and to restrain further expansion. Limited genomic data are available on Staphylococcus sciuri; regardless, it is considered a reservoir for critical AMRG and mobile elements. We uncover a transferable staphylococcal TMP resistance gene, named dfrE, in a novel mosaic plasmid harboring additional resistance, adaptive, and self-stabilization features. dfrE is present but evaded detection in diverse species from varied sources geographically distant. Our analyses evidence that the dfrE-carrying element has emerged from a single ancestor and position S. sciuri as the donor species for dfrE spread. We also identify novel mobilizable chromosomal islands encompassing AMRG and three unrelated prophages. We prove high intraspecies heterogenicity and genome plasticity for S. sciuri. This work highlights the importance of genome-wide ecological studies to facilitate identification, characterization, and evolution routes of bacteria adaptive features.

The Resistome and Mobilome of Multidrug-Resistant Staphylococcus sciuri C2865 Unveil a Transferable Trimethoprim Resistance Gene, Designated dfrE, Spread Unnoticed.

Two strains isolated from soil samples were designated as YH-JAE5T and YH-JAE2. The isolates were facultative anaerobic, Gram-stain-variable, motile, rod-shaped bacteria. Phylogenetic analysis indicated that the isolates belonged to the genus Paenibacillus, but the 16S rRNA gene sequence similarities were <98 % when compared with other species within the genus. Analysis of rpoB gene revealed the isolates formed a sub-cluster with P. chibensis. The only menaquinone identified was MK-7. The two isolates contained meso-diaminopimelic acid within their cell wall peptidoglycan. The major polar lipids were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, phospholipid, aminophospholipids, and lipids. The major fatty acids were C15 : 0 anteiso and C15 : 0 iso. The average nucleotide identity, average amino acid identity, and digital DNA-DNA hybridization values between isolate YH-JAE5T and the most closely related reference strain (Paenibacillus chibensis KCTC 3758T) were 81.7, 84.8 and 23.4 %, respectively. The G+C content of the genomic DNA was 47.4 mol%. Thus, the polyphasic data revealed that YH-JAE2 (=KCTC 43239=JCM 34435) and YH-JAE5T (=KCTC 43059=JCM 33533) represent a new species. The name Paenibacillus dokdonensis sp. nov. is proposed.

Description of Paenibacillus dokdonensis s p. nov., a new bacterium isolated from soil

Four methicillin-resistant Staphylococcus sciuri (MRSS) strains isolated from stranded dogs showed trimethoprim (TMP) resistance, while all staphylococcal TMP resistant dihydrofolate reductase genes (dfr) were negative. An in-depth whole-genome-sequencing approach on strain C2865 was followed for resistome and mobilome profiling, and for comparative genomics with S. sciuri group available genomes. Lack of species host tropism was observed, with MRSS C2865 placed at a separate sub-branch within S. sciuri species, close to the average nucleotide identity to be considered a different species (95-96%). S. sciuri proved a pronounced accessory genome (73% of genes), while MRSS C2865 distinctively harboured the highest total gene number and highest number of unique genes, with 75% associated to the recognised mobilome. A novel multidrug resistance mosaic plasmid (pUR2865-34) with several adaptive, mobilization (oriT mimic) and segregational stability (Type Ib par system) traits and two small single resistance plasmids were identified. Plasmid pUR2865-34 enclosed a novel staphylococcal TMP resistance gene, named dfrE, which shared highest identity with dfr of soil-related Paenibacillus anaericanus (68%). DfrE conferred high-level TMP resistance in S. aureus and Escherichia coli. Database searches revealed that dfrE was formerly denoted (dfr_like) in an Exiguobacterium spp. from a fish-farm sediment and that was present but unnoticed in several staphylococcal and onemacrococcal genomes with different epidemiological backgrounds. Novel chromosomal site-specific mobile islands with resourceful traits were identified, including a multidrug-resistant SCCmec cassette lacking cassette chromosome recombinase (Ccr) genes, a staphylococcal pathogenicity island of the SaPI4 family, and three unrelated siphoviridae prophages, two of which enclosed recombinases with the conserved Ccr-motif. We reveal a novel staphylococcal TMP resistance dfrE gene already present in diverse bacterial backgrounds. We confirm the ubiquity, high genome plasticity and low host tropism of S. sciuri highlighting its role as a resourceful reservoir for evolutionary novel features contributing to its extraordinary versatility and adaptability. Author summary Staphylococcus spp. are ubiquitous bacteria present in diverse ecological niches, including humans, animals and the environment. They are clinically relevant opportunistic pathogens and are notorious for their ability to acquire antimicrobial resistance (AMR) and virulence properties, resulting in a significant impact for Public Health. Mobile genetic elements (MGEs) play a central role in this adaptation process and are a means to transfer genetic information across bacterial species. Staphylococcus sciuri represents one of the most ancestral species in the genus and has been suggested a reservoir for AMR genes. Here, following a refined whole genome sequencing approach we determined the entire genome of an animal and environment-associated multidrug resistant (MDR) S. sciuri strain uncovering a novel acquired staphylococcal TMP resistance gene already spread among different bacterial species from different epidemiological backgrounds. We also reveal several additional MGEs, including a novel MDR mobilizable plasmid that encloses several adaptive and stabilization features, and novel mobilizable chromosomal islands with resourceful traits, including three unrelated prophages. Together with comparative genomics, we confirm the ubiquity, high intraspecies heterogenicity, genome plasticity and low host tropism of this species, highlighting its role as resourceful reservoir for evolutionary novel features contributing to its extraordinary versatility and adaptability.

/pdf/staphylococcus-sciuri-c2865-from-a-distinct-subspecies-1r3x7xdp5u.pdf

Staphylococcus sciuri C2865 from a distinct subspecies cluster as reservoir of the novel transferable trimethoprim resistance gene, dfrE, and adaptation driving mobile elements

A Gram-stain-positive, rod-shaped, motile bacterial strain, designated 3-2-2T, was isolated from field topsoil collected from a western suburb of Nanyang city, Henan province, China. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain 3-2-2T was a member of the genus 
Bacillus
and most closely related to 
Bacillus fortis
R-6514T (98.9 % similarity), 
Bacillus terrae
RA9T (98.0 %) and 
Bacillus fordii
R-7190T (97.7 %). A draft genome sequence determined for strain 3-2-2T revealed a DNA G+C content of 42.2 mol%. The average nucleotide identity and digital DNA–DNA hybridization values between 3-2-2T and the closely related Bacillus species ranged 79.4–84.2 % and 23.4–24.6 %. The major fatty acids of strain 3-2-2T were iso-C15 : 0, anteiso-C15 : 0, iso-C14 : 0 and iso-C16 : 0. The major isoprenoid quinone was MK-7. meso-Diaminopimelic acid was detected in the peptidoglycan. The polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, an unidentified phospholipid and an unidentified lipid. The results of phylogenetic analyses, in silico genomic comparisons, and chemotaxonomic and phenotypic analyses clearly indicated that strain 3-2-2T represents a novel species within the genus 
Bacillus
, for which the name 
Bacillus
acidinfaciens sp. nov. is proposed. The type strain is 3-2-2T (=CGMCC 1.13685T=LMG 30839T).

Bacillus acidinfaciens sp. nov., isolated from farmland soil

A Gram-stain-negative, rod-shaped, motile bacterial strain, designated 3-5-3T, was isolated from maize-cultivated soil artificially contaminated with cadmium, in Nanyang, Henan Province, China. Strain 3-5-3T was oxidase- and catalase-positive. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain 3-5-3T was affiliated with the genus 
Paenibacillus
and most closely related to 
Paenibacillus anaericanus
MH2T (96.5 % similarity). The average nucleotide identity and digital DNA–DNA hybridization values between 3-5-3T and the closely related species ranged 69.4–84.5 % and 18.1–18.4 %. The genomic G+C content was 53.8 mol%. Anteiso-C15 : 0 was the major fatty acid and MK-7 was the only menaquinone. The diamino acid in the cell-wall peptidoglycan contains meso-diaminopimelic acid. The polar lipid profile contained diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, phosphatidylmethylethanolamine, two unidentified glycolipids, two unidentified aminolipids, one unidentified phospholipid, one unidentified phosphoaminolipid and six unidentified lipids. On the basis of the results obtained in this study, strain 3-5-3T is considered to represent a novel species of the genus 
Paenibacillus
, for which the name 
Paenibacillus
zei soli sp. nov. is proposed. The type strain is 3-5-3T (=CGMCC 1.13686T=KCTC 33998T).

Paenibacillus zeisoli sp. nov., isolated from maize-cultivated soil artificially contaminated with cadmium

In a survey of endophytic bacteria in Miscanthus sinensis, a strain of Gram-negative, non-endospore-forming, rod-shaped, aerobic bacterium was isolated and designated as RS10T. Phylogenetic analysis based on its 16S rRNA gene sequence showed that the strain RS10T was affiliated with the genus 
Pedobacter
and exhibited the highest sequence similarities to 
Pedobacter kyungheensis
KACC 16221T (97.78 %), 
Pedobacter roseus
KCTC 22187T (97.75 %), 
Pedobacter humicola
KACC 18452T (97.29 %) and 
Pedobacter soli
KACC 14939T (97.23 %). The novel strain contained iso-C15 : 0, iso-C17 : 0-3OH and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c) as major fatty acids. The only isoprenoid quinone detected in strain RS10T was MK-7. Strain RS10T contains phosphatidylethanolamine and one kind of aminophospholipid as its major polar lipids. The DNA G+C content for RS10T was 39.8 mol%. Based on the results of phenotypic and genomic characterizations, we concluded that strains RS10T represents a novel species of 
Pedobacter
, for which the name 
Pedobacter
miscanthi sp. nov. is proposed. The type strain is RS10T (=KCTC 62786T=GDMCC 1.1415T).

Pedobacter miscanthi sp. nov., isolated from Miscanthus sinensis.

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Bacillus acidinfaciens sp. nov., isolated from farmland soil

Paenibacillus zeisoli sp. nov., isolated from maize-cultivated soil artificially contaminated with cadmium

Pedobacter miscanthi sp. nov., isolated from Miscanthus sinensis.