close
Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Jan 14:10:2821.
doi: 10.3389/fmicb.2019.02821. eCollection 2019.

Robust Demarcation of the Family Caryophanaceae (Planococcaceae) and Its Different Genera Including Three Novel Genera Based on Phylogenomics and Highly Specific Molecular Signatures

Radhey S Gupta  1 , Sudip Patel  1
Affiliations

Robust Demarcation of the Family Caryophanaceae (Planococcaceae) and Its Different Genera Including Three Novel Genera Based on Phylogenomics and Highly Specific Molecular Signatures

Radhey S Gupta et al. Front Microbiol. .

Abstract

The family Caryophanaceae/Planococcaceae is a taxonomically heterogeneous assemblage of >100 species classified within 13 genera, many of which are polyphyletic. Exhibiting considerable phylogenetic overlap with other families, primarily Bacillaceae, the evolutionary history of this family, containing the potent mosquitocidal species Lysinibacillus sphaericus, remains incoherent. To develop a reliable phylogenetic and taxonomic framework for the family Caryophanaceae/Planococcaceae and its genera, we report comprehensive phylogenetic and comparative genomic analyses on 124 genome sequences from all available Caryophanaceae/Planococcaceae and representative Bacillaceae species. Phylogenetic trees were constructed based on multiple datasets of proteins including 819 core proteins for this group and 87 conserved Firmicutes proteins. Using the core proteins, pairwise average amino acid identity was also determined. In parallel, comparative analyses on protein sequences from these species have identified 92 unique molecular markers (synapomorphies) consisting of conserved signature indels that are specifically shared by either the entire family Caryophanaceae/Planococcaceae or different monophyletic clades present within this family, enabling their reliable demarcation in molecular terms. Based on multiple lines of investigations, 18 monophyletic clades can be reliably distinguished within the family Caryophanaceae/Planococcaceae based on their phylogenetic affinities and identified molecular signatures. Some of these clades are comprised of species from several polyphyletic genera within this family as well as other families. Based on our results, we are proposing the creation of three novel genera within the family Caryophanaceae/Planococcaceae, namely Metalysinibacillus gen. nov., Metasolibacillus gen. nov., and Metaplanococcus gen. nov., as well as the transfer of 25 misclassified species from the families Caryophanaceae/Planococcaceae and Bacillaceae into these three genera and in Planococcus, Solibacillus, Sporosarcina, and Ureibacillus genera. These amendments establish a coherent taxonomy and evolutionary history for the family Caryophanaceae/Planococcaceae, and the described molecular markers provide novel means for diagnostic, genetic, and biochemical studies. Lastly, we are also proposing a consolidation of the family Planococcaceae within the emended family Caryophanaceae.

Keywords: Lysinibacillus; Metalysinibacillus gen. nov.; Metaplanococcus gen. nov.; Metasolibacillus gen. nov.; Planococcaceae and Caryophanaceae families; conserved signature indels for different clades; emended descriptions of the Caryophanaceae/Planococcaceae genera; phylogenomic and comparative genomic analyses.

PubMed Disclaimer

Figures

FIGURE 1
FIGURE 1
Maximum-likelihood phylogenetic trees for 124 genome sequenced members of the family Caryophanaceae/Planococcaceae and some representative members of the family “Bacillaceae” based on (A) 819 core proteins for this group of species, and (B) a set of 87 conserved proteins that are part of the phyloeco marker set for the phylum Firmicutes (Wang and Wu, 2013). Both trees were rooted using genome sequences of Streptococcus pyogenes, Streptococcus mitis, Lactococcus piscium, and Lactococcus lactis (labeled as Lactobacillales). SH-like statistical support values are indicated at each branch node. All clades observed in this study are labeled and presented with square brackets. The specific clades of interest are indicated in bold. A superscript “T” indicates the type species of a specific genus and the asterisk (∗) indicates the genome of Psychrobacillus quisquiliarum seems to be contaminated. The scale bars at the bottom represent 0.05 changes per amino acid position for each tree.
FIGURE 2
FIGURE 2
Maximum-likelihood phylogenetic tree for 109 Caryophanaceae/Planococcaceae and Bacillaceae species based on 16S rRNA gene sequences retrieved from the All-Species Living Tree Project (Yilmaz et al., 2014). The evolutionary history was inferred based on the Kimura 2-parameter model (Kimura, 1980). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The scale bar at the bottom represents 0.05 changes per nucleotide position. All species which had their 16S rRNA gene sequence of their type strains are indicated by (T) followed by the name of the strains. The proposed clades seen in this tree are labeled with square brackets and all non-genome-sequenced species which are part of these clades are highlighted in red with the species which we have proposed be transferred labeled with an asterisk (∗). This tree is unrooted.
FIGURE 3
FIGURE 3
A matrix indicating the percentage of average amino acid identities shared by members of the family Caryophanaceae/Planococcaceae analyzed in this study based on 819 core proteins for this set of species. Higher amino acid identity shared by a pair of species are colored more darkly (red). The specific clades observed based on higher interspecies similarity are boxed with blue borders and labeled with arrows. The mean and standard deviation in AAI values for different clades of interest are indicated. The “Caryophanon” and “Flavidum” clades have only 1 AAI similarity values and hence the mean and standard deviation values for these clades could not be determined. The family Bacillaceae and the genus Jeotgalibacillus are indicated with boxes with black borders. A detailed amino acid matrix with the numerical values underlying this amino acid matrix and the species names is provided in Supplementary Figure 2.
FIGURE 4
FIGURE 4
Partial sequence alignment of the phenylalanine–tRNA ligase subunit alpha protein showing a one amino acid deletion (boxed) that is exclusively shared by all members of the emended family Caryophanaceae. Sequence information for a limited number of Caryophanaceae species and other bacteria are shown here, but unless otherwise indicated, similar CSIs were detected in all members of the indicated group and not detected in any other species in the top 1000 BLASTp hits. The dashes (-) in this alignment and all other alignments presented in this paper indicate identity with the residue in their respective top sequences. Accession numbers for each sequence are indicated in the second column. Detailed sequence alignments for this CSI as well as additional CSIs specific for the family Caryophanaceae are presented in Supplementary Figures 3–15 and some of their characteristics are summarized in Table 1.
FIGURE 5
FIGURE 5
Partial sequence alignment of (A) the bacillithiol biosynthesis deacetylase BshB2 protein showing a one amino acid insertion (boxed) that is exclusively shared by all members of the Lysinibacillus sensu stricto clade, and (B) the arginine-binding extracellular protein ArtP precursor containing an 11 amino acid insertion that is exclusively shared by all members of the Jejuensis clade. Detailed sequence alignments for these CSIs as well as additional CSIs specific for these clades are presented in Supplementary Figures 16–21 for the Lysinibacillus sensu stricto clade and Supplementary Figures 22–38 for the Jejuensis clade and some of their characteristics are summarized in Table 2.
FIGURE 6
FIGURE 6
Partial sequence alignments of (A) the MFS transporter protein showing a one amino acid insertion (boxed) that is exclusively shared by all members of the Ureibacillus clade and (B) the DUF456 domain-containing protein containing a one amino acid deletion (boxed) that is exclusively shared by all members within the Meyeri clade. Detailed sequence alignments for these CSIs as well as additional CSIs specific for these clades are presented in Supplementary Figures 39–41 for the Ureibacillus clade and Supplementary Figures 42–53 for the Meyeri clade and some of their characteristics are summarized in Table 3.
FIGURE 7
FIGURE 7
Partial sequence alignments of (A) the flagellar hook–basal body protein showing a one amino acid insertion (boxed) that is exclusively shared by all members of the Solibacillus clade, and (B) the aspartate–tRNA ligase protein containing a two amino acid deletion (boxed) that is exclusively shared by all members of the Sporosarcina clade. Detailed sequence alignments for these CSIs as well as additional CSIs specific for these clades are presented in Supplementary Figures 54–65 for the Solibacillus clade, and Supplementary Figures 66–73 for the Sporosarcina clade and some of their characteristics are summarized in Table 3.
FIGURE 8
FIGURE 8
Partial sequence alignments of (A) the penicillin-binding protein 2 protein showing a two amino acid insertion (boxed) that is exclusively shared by all members of the Planococcus/Planomicrobium clade, (B) the ABC transporter substrate-binding protein containing a three amino acid insertion (boxed) that is exclusively shared by all members within the Flavidum clade, and (C) the DNA-directed RNA polymerase subunit beta protein containing an eight amino acid insertion that is exclusively shared by all members of the genus Caryophanon. Detailed sequence alignments for these CSIs as well as additional CSIs specific for these clades are presented in Supplementary Figures 74–78 for the Planococcus/Planomicrobium clade, Supplementary Figures 79–86 for the Flavidum clade, and Supplementary Figures 87–94 for the genus Caryophanon and some of their characteristics are summarized in Table 4.
FIGURE 9
FIGURE 9
A conceptual diagram based on results obtained from phylogenetic studies, AAI similarity analysis, and several identified CSIs indicating the evolutionary relationships among the Caryophanaceae species. The total numbers of identified CSIs that are specifically shared by species from each of these clades are indicated at their respective nodes. All clades analyzed in this study are shown in boxes containing the species they comprise. Of these species, the ones in bold are genome-sequenced while the rest are placed within these clades based on our 16S rRNA analysis.
See this image and copyright information in PMC

References

    1. Adeolu M., Alnajar S., Naushad S., Gupta R. S. (2016). Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int. J. Syst. Evol. Microbiol. 66 5575–5599. 10.1099/ijsem.0.001485 - DOI - PubMed
    1. Adeolu M., Gupta R. S. (2014). A phylogenomic and molecular marker based proposal for the division of the genus Borrelia into two genera: the emended genus Borrelia containing only the members of the relapsing fever Borrelia, and the genus Borreliella gen. nov. containing the members of the Lyme disease Borrelia (Borrelia burgdorferi sensu lato complex). Antonie Van Leeuwenhoek 105 1049–1072. 10.1007/s10482-014-0164-x - DOI - PubMed
    1. Ahmed I., Yokota A., Yamazoe A., Fujiwara T. (2007). Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int. J. Syst. Evol. Microbiol. 57 1117–1125. - PubMed
    1. Andersson M., Laukkanen M., Nurmiaho-Lassila E. L., Rainey F. A., Niemela S. I., Salkinoja-Salonen M. (1996). Bacillus thermosphaericus sp. nov. In list no. 56, validation of the publication of new names and new combinations previously effectively published outside the IJSEB. Int. J. Syst. Bacteriol. 46 362–363.
    1. Arora P. K., Chauhan A., Pant B., Korpole S., Mayilraj S., Jain R. K. (2011). Chryseomicrobium imtechense gen. nov., sp. nov., a new member of the family Planococcaceae. Int. J. Syst. Evol. Microbiol. 61 1859–1864. 10.1099/ijs.0.023184-0 - DOI - PubMed

LinkOut - more resources