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Lysinibacillus composti sp. nov., isolated from compost

Annals of Microbiology volume 64, pages 1081–1088 (2014)Cite this article

Abstract

A Gram-negative, motile, rod-shaped, endospore-forming bacterial strain, designated as NCCP-36T, was isolated from the compost of fruit and vegetable wastes. The strain NCCP-36T grew within a temperature range of 10–45 ○C (optimum 28 ○C) and a pH range of 6.5–8.5 (optimum 7.0), and its cells tolerated <50 mM boron (optimum growth without boron) and 0–5 % NaCl (w/v) in tryptic soya broth medium. Based on comparative analysis of 16S rRNA gene sequence, strain NCCP-36T showed the highest similarity to Lysinibacillus sinduriensis BLB-1T (97.52 %) and L. xylanilyticus XDB9T (96.96 %), and <97 % similarity with other closely related taxa. However, DNA–DNA relatedness between strain NCCP-36T and the closely related type strains of genus Lysinibacillus was ≤37 %. Phylogenetic and chemotaxonomic analyses [major polar lipids: diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, and phospholipids; predominant menaquinone: MK-7; major cellular fatty acids: iso-C15:0, antieso-C15:0, and iso-C16:0; DNA G+C contents: 37 mol %; Lys-Asp (type A4α) in cell-wall peptidoglycans as diagnostic amino acids] also support the affiliation of strain NCCP-36T to genus Lysinibacillus. Based upon DNA–DNA relatedness as well as distinctive chemotaxonomic, phylogenetic, and genotypic data, we conclude that strain NCCP-36T belongs to a novel species of genus Lysinibacillus, for which the name Lysinibacillus composti sp. nov. is proposed. The type strain is NCCP-36T (JCM 18777T = KCTC 13796T = DSMZ 24785T).

Introduction

Bacillus, a genus of Gram-positive, aerobic, endospore-forming motile bacteria, belongs to the family Bacillaceae (Claus and Berkeley 1986) and has wide genetic heterogeneity. Over the last decade, the genus Bacillus has been taxonomically dissected into five recognized groups (Ash et al. 1991), and several new genera have emerged based on differentiating polyphasic taxonomic features (Wisotzkey et al. 1992; Ash et al. 1993; Shida et al. 1996; Heyndrickx et al. 1998; Wainø et al. 1999; Yoon et al. 2001; Ahmed et al. 2007b; Albert et al. 2007; Krishnamurthi et al. 2009). Ahmed et al. (2007b) transferred two more rRNA group 2 Bacillus species, Bacillus fusiformis and B. sphaericus, into genus Lysinibacillus based on the single differentiating character of a cell-wall peptidoglycan containing lysine and aspartate. Although the presence of L-lysine peptidoglycans in Bacillus rRNA group 2 inspired researchers to re-evaluate the taxonomy of this group, this benchmark has remained under continuous criticism/observation since 1990 (Farrow et al. 1994; Rheims et al. 1999; Yoon et al. 2001; Albert et al. 2007; Zhang et al. 2007; Stackebrandt and Swiderski 2008; Jung et al. 2012).

For most of the Bacillus species in rRNA group 2 information is lacking on one or more of the chemotaxonomic standards (Krishnamurthi et al. 2009) required for describing new taxa (Kämpfer et al. 2006; Logan et al. 2009). La Duc et al. (2004) and Glazunova et al. (2006) described novel species Bacillus massiliensis and B. odysseyi, respectively, based on phenotypic characteristics and the 16S rRNA gene sequence. However, these authors did not report any data on cell-wall peptidoglycans, polar lipids, and menaquinone for these species. Bacillus massiliensis and B. odyssey are phylogenetically more closely related to Bacillus pycnus and Solibacillus silvestris (Albert et al. 2007; Krishnamurthi et al. 2009), but analysis of the 16S rRNA gene sequence phyletic line delineated that B. odyssey is closely related to Lysinibacillus boronitolerans KCTC 13709T sharing a sequence similarity of 96.1 % (Ahmed et al. 2007b). Recently, a proposal has been accepted to transfer Bacillus massiliensis and B. odyssey into the genus Lysinibacillus as L. massiliensis and L. odyssey, respectively, along with classification of L. sinduriensis through detailed examination of their fatty acid profile, polar lipids, cell-wall peptidoglycans, and menaquinone systems (Jung et al. 2012).

The genus Lysinibacillus was proposed based on lysine and aspartate (Lys-Asp) as diagnostic amino acids in peptidoglycans rather than meso-diaminopimelic acid, which is a specific characteristic of the genus Bacillus. All members of genus Lysinibacillus are characterized as strictly aerobic, rod-shaped, and spore-forming, which are positive for catalase but negative for the production of indole and H2S. Chemotaxonomically, these are characterized by the presence of diphosphatidylglycerol (DPG) and phosphatidylglycerol (PG) as the major polar lipids, MK-7 as the predominant menaquinone, iso-C15:0, antieso-C15:0, and iso-C16:0 as the major cellular fatty acids, and DNA G+C contents of 35–38.7 mol %. To date, the genus Lysinibacillus contains 13 validly recognized species, including Lysinibacillus boronitolerans, L. fusiformis, L. sphaericus (Ahmed et al. 2007b), L. parviboronicapiens (Miwa et al. 2009), L. xylanilyticus (Lee et al. 2010), L. sinduriensis, L. massiliensis, L. odyssey (Jung et al. 2012), L. macroides (Coorevits et al. 2012), L. mangiferihumi (Yang et al. 2012), L. contaminans (Kämpfer et al. 2013), and L. manganicus (Liu et al. 2013), and L. meyeri (Seiler et al. 2013). However, one new species, L. pakistanensis (Hayat et al. 2013), has recently been proposed. In this study, we describe a novel strain NCCP-36T in the genus Lysinibacillus as Lysinibacillus composti sp. nov. based on its phenotypic, phylogenetic, and chemotaxonomic relationship to the genus Lysinibacillus.

Materials and methods

Isolation, morphology, and phenotypic characterization

A bacterial strain, designated as NCCP-36T, was isolated from the compost of fruit and vegetable wastes prepared aerobically in a 1 m × 1 m × 1 m - (L × W × D) pit at the research farm of Pir Mehr Ali Shah Arid Agriculture University Rawalpindi, Pakistan. The waste was turned over on a weekly basis to maintain aerobic conditions at all depths. Following the required time for composting (approx. 100 days), we collected a sample of the compost and isolated bacteria by the dilution plate technique using a phosphate-buffered saline solution on tryptic soya agar (TSA; Difco Laboratories, Detroit, MI) and incubation at 28 °C. The purified strain was obtained through sub-culturing and was stored in glycerol (final concentration 35 % w/v) at −80 ○C for further characterization. The reference strains used in these studies were Lysinibacillus massiliensis KCTC13178T (Glazunova et al. 2006), L. xylanilyticus KCTC13423T (Lee et al. 2010), L. odyssey KCTC3961T (La Duc et al. 2004), L. sinduriensis KCTC13296T (Jung et al. 2012), L. fusiformis KCTC3454T (Priest et al. 1988), L. parviboronicapiens KCTC13154T (Miwa et al. 2009), L. boronitolerans KCTC13709T (Ahmed et al. 2007b), and L. sphaericus KCTC3346T (Claus and Berkeley 1986). All strains were routinely grown on TSA at 28 °C, unless otherwise mentioned.

Colonial morphology of the isolated strain NCCP-36T was observed on well-isolated colonies grown on TSA for 2 days. Cell morphology and motility were examined by light microscopy (model E600; Nikon, Tokyo, Japan). For pH optimization, various pH levels (4.0–10.0) were adjusted in tryptic soya broth (TSB; Difco) using Na2CO3 and HCl. The pH levels were confirmed after the media had been autoclaved. For NaCl tolerance, strain NCCP-36T was inoculated in TSB (pH 7.0) containing different NaCl concentrations from 0 to 10 % (w/v). Optimum growth temperature for NCCP-36T was determined by streaking bacterial strains on TSA plates (pH 7.0) and incubation at temperatures of 4, 10, 16, 22, 28, 32, 37, 45, and 50 °C. The boron tolerance of strain NCCP-36T was determined in TSB (pH 7.0) containing different levels of boron ranging from 0 to 150 mM (Ahmed et al. 2007b). Physiological and biochemical characteristics were examined using API kits (AP50CH, API 20E, API-ZYM; bioMérieux, Marcy l'Etoile, France) and the Biolog GP system (Biolog Inc., Hayward, CA) to determine the different metabolic features of the strains in accordance with the manufacturers’ instructions. Gram staining and the KOH reaction test were also performed by standard procedures as described earlier (Chang et al. 2002).

Genotypic and chemotaxonomic analyses

To identify the strain, the nearly complete 16S rRNA gene was amplified by the PCR as described by Ahmed et al. (2007a) using forward (9F; 5′-GAGTTTGATCCTGGCTCAG-3′) and reverse (1510R; 5′-GGCTACCTTGTTACGA-3′) primers. The PCR product was purified using the PureLink PCR purification kit (Invitrogen, Carlsbad, CA) and sequenced by Macrogen Inc., Korea (www.dna.macrogen.com/eng) using four universal 16S rRNA gene primers, namely, 9F, 515F (5′-GTGCCAGCAGCCGCGGT-3′), 926R (5′-CCGTCAATTCCTTTGAGTTT-3′), and 1510R.

The strain NCCP-36T was identified using the sequence of 16S rRNA gene on the EzTaxon Server (http://eztaxon-e.ezbiocloud.net). To explore the exact taxonomic position of strain NCCP-36T, we performed phylogenetic analyses with all of the published species of genus Lysinibacillus as described previously (Roohi et al. 2012). Sequences of closely related type strains that had been validated were retrieved from the database of the EzTaxon Server (http://eztaxon-e.ezbiocloud.net) for constructing the phylogenetic tree. Molecular evolutionary analyses were performed using MEGA ver. 5.20 (Tamura et al. 2011), and phylogenetic trees were constructed using three algorithms: neighbor-joining (NJ), maximum parsimony (MP), and maximum likelihood (MLH). The stability of the relationship was assessed by bootstrap analysis (Felsenstein 2005) using 1,000 re-sampling for the tree topology of NJ data.

For DNA–DNA hybridization, genomic DNA of strain NCCP-36T and of closely related reference species were isolated using a previously described procedure (Marmur 1963; Ahmed et al. 2007a). DNA–DNA hybridization was performed by the microplate method, as previously described (Ezaki et al. 1989) with five replications for each sample. The plate was pre-hybridized for 30 min and then hybridized with photobiotin-labeled probes at 45 °C. The fluorescence intensity was measured by a Flouroskan Ascent Fluorescent plate reader (Thermo Life Sciences, Basingstoke, UK). The highest and lowest values were excluded from each sample, and the means of the remaining three values were taken as the DNA relatedness value (Chang et al. 2008). The G+C content of the extracted DNA was determined by high-performance liquid chromatography at column temperature of 40 ○C and wavelength of 270 nm using the mobile phase as 0.2 M ammonium phosphate: acetonitrile in the ratio of 40:1 (Mesbah et al. 1989).

Cellular fatty acid profiles of strain NCCP-36T and of the closely related reference species were determined by growing strains on TSA medium at 28 °C for 48 h. The analysis was carried out according to a standard protocol (Sherlock Microbial Identification System; MIDI, Microbial ID, Newark, DE). The fatty acids were separated on an automated gas chromatography system (model 6890 N and 7683 Autosampler; Agilent Technologies, Santa Clara, CA) and identified by the associated software package ver. 4.0 (Library TSBA 40; MIDI, Microbial ID). Respiratory quinones were analyzed as described by Xie and Yokota (2003). To determine the peptidoglycan structure, 2 g of wet cells grown in TSB for 24 h was harvested and the cell walls purified as described previously (Kawamoto et al. 1981). The purified cell walls were hydrolyzed and their amino acids quantitatively analyzed on an automatic amino acid analyzer (Hitachi, Tokyo, Japan). Polar lipids were extracted and separated from 100 mg freeze-dried cell material by the two-stage method described by Tindall (1990).

Results and discussion

The optimum pH for the growth of strain NCCP-36T was 7.0 (range 6.5–8.5). The strain did not show any growth at pH 6.0, whereas its closest species, Lysinibacillus sinduriensis, even grew at pH 5.0. Strain NCCP-36T tolerated up to 5 % (w/v) NaCl. Slight growth was observed at 10  ○C after 3 days of incubation, but it could not grow at ≥50 ○C. The optimum growth temperature was 28 ○C. Strain NCCP-36T could not tolerate ≥50 mM boron, whereas the reference Lysinibacillus boronitolerans can tolerate up to 150 mM boron (Ahmed et al. 2007b). Strain NCCP-36T was negative for oxidase (bioMérieux) and positive for catalase activity. The characteristics of strain NCCP-36T which differentiate it from closely related strains are given in Table 1.

Table 1 Characteristics that differentiate strain NCCP-36T from its closely related taxa
Full size table

The comparative analysis of the 16S rRNA gene sequence of NCCP-36T with that of its closely related strains indicated that strain NCCP-36 T belongs to Bacillus rRNA group 2. The highest sequence similarity of the 16S rRNA gene of strain NCCP-36T was 97.52 % with Lysinibacillus sinduriensis KCTC13296T (FJ169465); its sequence similarity with other closely related taxa was <97 % (Table 2). Strain NCCP-36T clustered with species of genus Lysinibacillus and was found to be closely associated to L. sinduriensis BLB-1T (FJ169465) with a high bootstrap value (82 %) in the NJ phylogenetic tree inferred from 16S rRNA gene sequences (Fig. 1). This coherent association of NCCP-36T with species of genus Lysinibacillus was also confirmed by MLH and MP algorithms.

Table 2 16S rRNA gene sequence similarity and DNA–DNA relatedness between strain NCCP-36T and closely related reference strains of genus Lysinibacillus
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Fig. 1
figure 1

Phylogenetic tree showing interrelationships of strain NCCP-36T with closely related species of Lysinibacillus and other related genera inferred from 16S rRNA gene sequences. The tree was generated using the neighbor-joining (NJ) method based on a comparison of approximately 1,324 nucleotides and was rooted using Paenibacillus polymyxa (D16276) as an outgroup. Bootstrap values (>50 %), expressed as percentage of 1,000 replications, are indicated at the nodes. Nodes denoted by open circles were recovered by at least two algorithms, whereas nodes denoted with filled circles were recovered by three algorithms (NJ, maximum parsimony and maximum likelihood). Number in parenthesis is the accession number of type strain

Full size image

The DNA–DNA hybridization values between strain NCCP-36T and the reference species were <37 % (Table 2). These values are below the threshold (70 %) for species delineation (Stackebrandt and Goebel 1994) and thus allow the strain to be classified as a new species. The DNA G+C contents of strain NCCP-36T were 37 mol% (Table 1). These data are in agreement with the values reported previously for genus Lysinibacillus (range 35–38.7 %; Ahmed et al. 2007b).

The predominant cellular fatty acids of strain NCCP-36T were iso-C15:0 (45.02 %) and anteiso-C15:0 (16.74 %) (Table 3), and MK-7 (88 %) was identified as the predominant menaquinone system. The whole cell hydrolysate of strain NCCP-36T contained Lys-Asp as diagnostic amino acids. The presence of Lys-Asp in cell-wall peptidoglycans corresponds to type A4α (Schleifer and Kandler 1972), which is in agreement with the description of genus Lysinibacillus (Ahmed et al. 2007b). The phylogenetic and chemotaxonomic analyses [major polar lipids: DPG, PG, phosphatidylethanolamine (PE), and phospholipids (PL); predominant menaquinone: MK-7; major cellular fatty acids: iso-C15:0, antieso-C15:0, and iso-C16:0; DNA G+C contents: 37 mol %; Lys-Asp (type A4α) in cell-wall peptidoglycans as diagnostic amino acids] also support the affiliation of strain NCCP-36T with genus Lysinibacillus.

Table 3 Cellular fatty acid profile of NCCP-36T in comparison with the closely related reference species of genus Lysinibacillus
Full size table

Strain NCCP-36T shared a similar polar lipid profile (Electronic Supplementary Material Fig. 1; Table 4) with Lysinibacillus massiliensis KCTC 13178T L. xylanilyticus KCTC13423T, L. odyssey KCTC3961T, L. fusiformis KCTC3454T, L. parviboronicapiens KCTC13154T, L. boronitolerans KCTC13709T, and L. sphaericus KCTC3346T, which consisted of predominantly DPG, PG and PE (Table 4).

Table 4 Comparison of polar lipids profile of NCCP-36T with the closely related reference species of genus Lysinibacillus
Full size table

On the basis of genotypic (DNA–DNA relatedness and DNA G+C contents) and phylogenetic analysis along with the phenotypic data presented in this paper, we assigned the isolated strain NCCP-36T to a novel species in the genus Lysinibacillus as Lysinibacillus composti sp. nov. This strain is described in detail in the following section.

Description of Lysinibacillus composti sp. nov.

Lysinibacillus composti (com.pos′ti. N.L. gen. n. composti, of compost, from which the organism was isolated).

Cells are Gram-negative, aerobic, endospore-forming, and motile. The colonies are smooth with a shiny surface and opaque; the texture is butyrous and elevation is convex. The colony has a diameter of 1–2 mm after 24 h of incubation 28 ○C on TSA, and it has a circular form with an entire margin. The pigmentation is light yellow. The temperature range and pH range for cell growth are 10–45 ○C (optimum 28 ○C) and 6.5–8.5 (optimum pH 7.0), respectively. Cells tolerate up to 5 % (w/v) NaCl but not 6 %, and they tolerate 0–50 mM boron in TSA but boron is not required for growth. Negative for nitrate reduction, oxidase, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, citrate utilization, urease, geletinase, production of H2S, indole, hydrolysis of casein, and starch. Positive for reduction of NO3 to N2, Voges–Proskauer test, and catalase activity; however, only weakly positive for tryptophane deaminase. No sugar is fermented in the API 50 CH strips using CHB/E suspension medium and in the API 20E strips (bio-Merieux). The cells show strong enzyme activity for alkaline phosphatase and acid phosphatase, but weak activity for esterase lipase (C8) and naphtol-AS-BI-phosphohydrolase and no activity for esterase (C4), lipase (C14), leucine arylamidase, valine arylamidase, cystine arylamidase, trypsin, α-chymotrypsin, α-galactosidase, β-galactosidase, β-glucuronidase, α-glucosidase, β-glucosidase, N-acetyl-β-glucosaminidase, α-mannosidase, α-fucosidase (API-ZYM; bio-Merieux). Biolog results revealed that the strain is positive for acetic acid dextrin, but it is negative for α-ketovaleric acid, pyruvatic acid methyl ester, pyruvic acid, L-alaninamide, L-alanine, L-glutamate, adenosine, thymidine, thymidine-5′-monophosphate, β-hydroxybutyric acid, D-lactic acid methyl ester, and succinic acid mono-methyl ester. The dominant polar lipids are DPG, PG, PE, and PL. Cell-wall peptidoglycan contains Lys-Asp as the diagnostic amino acids, corresponding to peptidoglycan type A4α. The predominant cellular fatty acids are iso-C15:0, anteiso-C15:0, iso-C16:0, anteiso-C17:0, iso-C17:0, C16:1 ω7c alcohol, iso-C17:1 ω10c, C16:0, C16:1 ω11c, iso-C14:0. The major menaquinone is MK-7. The G+C contents of the type strain is 37 mol%.

The strain NCCP-36T (=JCM 18777T = KCTC 13796T; DSMZ 24785T) was isolated from compost of fruit and vegetable wastes prepared aerobically.

References

  • Ahmed I, Yokota A, Fujiwara T (2007a) A novel highly boron tolerant bacterium, Bacillus boroniphilus sp. nov., isolated from soil, that requires boron for its growth. Extremophiles 11:217–224

    Article  CAS  PubMed  Google Scholar 

  • Ahmed I, Yokota A, Yamazoe A, Fujiwara T (2007b) 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. doi:10.1099/ijs.0.63867-0

    Article  CAS  PubMed  Google Scholar 

  • Albert RA, Archambault J, Lempa M, Hurst B, Richardson C, Gruenloh S, Duran M, Worliczek HL, Huber BE, Rossello-Mora R, Schumann P, Busse HJ (2007) Proposal of Viridibacillus gen. nov. and reclassification of Bacillus arvi, Bacillus arenosi and Bacillus neidei as Viridibacillus arvi gen. nov., comb. nov., Viridibacillus arenosi comb. nov. and Viridibacillus neidei comb. nov. Int J Syst Evol Microbiol 57(12):2729–2737. doi:10.1099/ijs.0.65256-0

    Article  CAS  PubMed  Google Scholar 

  • Ash C, Farrow JAE, Wallbanks S, Collins MD (1991) Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences. Lett Appl Microbiol 13(4):202–206. doi:10.1111/j.1472-765X.1991.tb00608.x

    Article  CAS  Google Scholar 

  • Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Proposal for the creation of a new genus Paenibacillus. Antonie Van Leeuwenhoek 64(3–4):253–260

    CAS  PubMed  Google Scholar 

  • Chang YH, Han JI, Chun JS, Lee KC, Rhee MS, Kim YB, Bae KS (2002) Comamonas koreensis sp. nov., a non-motile species from wetland in Woopo, Korea. Int J Syst Evol Microbiol 52:377–381. doi:10.1099/ijs.0.01734-0

    CAS  PubMed  Google Scholar 

  • Chang YH, Jung MY, Park IS, Oh HM (2008) Sporolactobacillus vineae sp nov., a spore-forming lactic acid bacterium isolated from vineyard soil. Int J Syst Evol Microbiol 58:2316–2320. doi:10.1099/ijs.0.65608-0

    Article  CAS  PubMed  Google Scholar 

  • Claus D, Berkeley RCW (1986) Genus Bacillus Cohn. In: Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (eds) Bergey’s manual systematic bacteriology, vol 3: The firmicutes. Williams & Wilkins, Baltimore, pp 1105–1139

  • Coorevits A, Dinsdale AE, Heyrman J, Schumann P, Van Landschoot A, Logan NA, De Vos P (2012) Lysinibacillus macroides sp. nov., nom. rev. Int J Syst Evol Microbiol 62(5):1121–1127. doi:10.1099/ijs.0.027995-0

    Article  CAS  PubMed  Google Scholar 

  • Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229

    Article  Google Scholar 

  • Farrow JAE, Wallbanks S, Collins MD (1994) Phylogenetic interrelationships of round-spore-forming bacilli containing cell-walls based on lysine and the non-spore-forming genera Caryophanon, Exiguobacterium, Kurthia, and Planococcus. Int J Syst Bacteriol 44(1):74–82

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package). Version 3.6. distributed by the author. Department of Genome Sciences, University of Washington, Seattle

    Google Scholar 

  • Glazunova OO, Raoult D, Roux V (2006) Bacillus massiliensis sp. nov., isolated from cerebrospinal fluid. Int J Syst Evol Microbiol 56(Pt 7):1485–1488. doi:10.1099/ijs.0.63982-0

    Article  CAS  PubMed  Google Scholar 

  • Hayat R, Ahmed I, Paek J, Ehsan M, Iqbal M, Chang YH (2013) A moderately boron-tolerant candidatus novel soil bacterium Lysinibacillus pakistanensis sp. nov. cand., isolated from soybean (Glycine max L.) rhizosphere. Pak J Bot 45(S1):41–50

    Google Scholar 

  • Heyndrickx M, Lebbe L, Kersters K, De Vos P, Forsyth C, Logan NA (1998) Virgibacillus: a new genus to accommodate Bacillus pantothenticus (Proom and Knight 1950). Emended description of Virgibacillus pantothenticus. Int J Syst Bacteriol 48:99–106

    Article  Google Scholar 

  • Jung MY, Kim J-S, Paek WK, Styrak I, Park I-S, Sin Y, Paek J, Park KA, Kim H, Kim HL, Chang Y-H (2012) Description of Lysinibacillus sinduriensis sp. nov., and transfer of Bacillus massiliensis and Bacillus odysseyi to the genus Lysinibacillus as Lysinibacillus massiliensis comb. nov. and Lysinibacillus odysseyi comb. nov. with emended description of the genus Lysinibacillus. Int J Syst Evol Microbiol 62(10):2347–2355. doi:10.1099/ijs.0.033837-0

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P, Rossello-Mora R, Falsen E, Busse HJ, Tindall BJ (2006) Cohnella thermotolerans gen. nov., sp. nov., and classification of 'Paenibacillus hongkongensis' as Cohnella hongkongensis sp. nov. Int J Syst Evol Microbiol 56:781–786. doi:10.1099/ijs.0.63985-0

    Article  PubMed  Google Scholar 

  • Kämpfer P, Martin K, Glaeser SP (2013) Lysinibacillus contaminans sp. nov., isolated from a surface water. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.049593-0

    Google Scholar 

  • Kawamoto I, Oka T, Nara T (1981) Cell-wall composition of Micromonospora olivoasterospora, Micromonospora agamiensis, and related organisms. J Bacteriol 146(2):527–534

    CAS  PubMed Central  PubMed  Google Scholar 

  • Krishnamurthi S, Chakrabarti T, Stackebrand E (2009) Re-examination of the taxonomic position of Bacillus silvestris Rheims et al. 1999 and proposal to transfer it to Solibacillus gen. nov as Solibacillus silvestris comb. nov. Int J Syst Evol Microbiol 59:1054–1058. doi:10.1099/ijs.0.65742-0

    Article  CAS  PubMed  Google Scholar 

  • La Duc MT, Satomi M, Venkateswaran K (2004) Bacillus odysseyi sp. nov., a round-spore-forming bacillus isolated from the Mars Odyssey spacecraft. Int J Syst Evol Microbiol 54:195–201. doi:10.1099/Ijs.0.02747

    Article  PubMed  Google Scholar 

  • Lee CS, Jung Y-T, Park S, Oh T-K, Yoon J-H (2010) Lysinibacillus xylanilyticus sp. nov., a xylan-degrading bacterium isolated from forest humus. Int J Syst Evol Microbiol 60(2):281–286. doi:10.1099/ijs.0.013367-0

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Song Y, Chen F, Zheng S, Wang G (2013) Lysinibacillus manganicus sp. nov., isolated from manganese mining soil. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.050492-0

    Google Scholar 

  • Logan NA, Berge O, Bishop AH, Busse HJ, De Vos P, Fritze D, Heyndrickx M, Kampfer P, Rabinovitch L, Salkinoja-Salonen MS, Seldin L, Ventosa A (2009) Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol 59(8):2114–2121. doi:10.1099/ijs.0.013649-0

    Article  CAS  PubMed  Google Scholar 

  • Marmur J (1963) A procedure for the isolation of deoxyribonucleic acid from microorganisms. Method Enzymol 6:726–738. doi:10.1016/0076-6879(63)06240-6

    Article  CAS  Google Scholar 

  • Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic-acid by high-performance liquid-chromatography. Int J Syst Bacteriol 39(2):159–167

    Article  CAS  Google Scholar 

  • Miwa H, Ahmed I, Yokota A, Fujiwara T (2009) Lysinibacillus parviboronicapiens sp nov., a low-boron-containing bacterium isolated from soil. Int J Syst Evol Microbiol 59:1427–1432. doi:10.1099/ijs.0.65455-0

    Article  CAS  PubMed  Google Scholar 

  • Priest FG, Goodfellow M, Todd C (1988) A numerical classification of the genus Bacillus. J Gen Microbiol 134:1847–1882

    CAS  PubMed  Google Scholar 

  • Rheims H, Fruhling A, Schumann P, Rohde M, Stackebrandt E (1999) Bacillus silvestris sp. nov., a new member of the genus Bacillus that contains lysine in its cell wall. Int J Syst Bacteriol 49:795–802

    Article  PubMed  Google Scholar 

  • Roohi A, Ahmed I, Iqbal M, Jamil M (2012) Preliminary isolation and characterization of halotolerant and halophilic bacteria from salt mines of Karak, Pakistan. Pak J Bot 44(SI 1):365–370

    CAS  Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36(4):407–477

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seiler H, Scherer S, Wenning M (2013) Lysinibacillus meyeri sp. nov., isolated from a medical practice. Int J Syst Evol Microbiol 63(Pt 4):1512–1518. doi:10.1099/ijs.0.039420-0

    Article  PubMed  Google Scholar 

  • Shida O, Takagi H, Kadowaki K, Komagata K (1996) Proposal for two new genera, Brevibacillus gen nov and Aneurinibacillus gen nov. Int J Syst Bacteriol 46(4):939–946

    Article  CAS  PubMed  Google Scholar 

  • Stakebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849

    Google Scholar 

  • Stackebrandt E, Swiderski J (2008) From phylogeny to systematics: the dissection of the genus Bacillus. In: Berkeley R, Heyndrickx M, Logan N, De Vos P (eds) Applications and systematics of Bacillus and relatives. Blackwell Science Ltd, Oxford, pp 8–22. doi:10.1002/9780470696743.ch2

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tindall BJ (1990) A comparative-study of the lipid-composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 13(2):128–130

    Article  CAS  Google Scholar 

  • Wainø M, Tindall BJ, Schumann P, Ingvorsenl K (1999) Gracilibacillus gen. nov., with description of Gracilibacillus halotolerans gen. nov., sp. nov. ; transfer of Bacillus dipsosauri to Gracilibacillus dipsosauri comb. nov., and Bacillus salexigens to the genus Salibacillus gen. nov., as Salibacillus salexigens comb. nov. Int J Syst Bacteriol 49:821–831

    Article  PubMed  Google Scholar 

  • Wisotzkey JD, Jurtshuk P Jr, Fox GE, Deinhard G, Poralla K (1992) Comparative sequence analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int J Syst Bacteriol 42(2):263–269

    Article  CAS  PubMed  Google Scholar 

  • Xie CH, Yokota A (2003) Phylogenetic analyses of Lampropedia hyalina based on the 16S rRNA gene sequence. J Gen Appl Microbiol 49(6):345–349. doi:10.2323/Jgam.49.345

    Article  CAS  PubMed  Google Scholar 

  • Yang LL, Huang Y, Liu J, Ma L, Mo MH, Li WJ, Yang FX (2012) Lysinibacillus mangiferihumi sp. nov., a new bacterium producing nematicidal volatiles. Antonie Van Leeuwenhoek 102(1):53–59. doi:10.1007/s10482-012-9712-4

  • Yoon JH, Weiss N, Lee KC, Lee IS, Kang KH, Park YH (2001) Jeotgalibacillus alimentarius gen. nov., sp nov., a novel bacterium isolated from jeotgal with L-lysine in the cell wall, and reclassification of Bacillus marinus Ruger 1983 as Marinibacillus marinus gen. nov., comb. nov. Int J Syst Evol Microbiol 51:2087–2093

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Xu Z, Patel BK (2007) Bacillus decisifrondis sp. nov., isolated from soil underlying decaying leaf foliage. Int J Syst Evol Microbiol 57(5):974–978. doi:10.1099/ijs.0.64440-0

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We gratefully acknowledge the kind help of Dr. Takuji Kudo from JCM, Tsukuba, Japan in the analysis of cell-wall peptidoglycans. This work was partially supported by PSDP Project “Research for Agricultural Development Program (RADP)” funded by Pakistan Agricultural Research Council (PARC) and by the KRIBB Research Initiative Program funded by the Ministry of Education, Science and Technology, Republic of Korea. Initial funds for these studies were provided by the Higher Education Commission of Pakistan under talent training program for young faculty members for training at National Institute for Genomics and Advanced Biotechnology, NARC, Islamabad, Pakistan and also at the Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

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Authors and Affiliations

  1. National Culture Collection of Pakistan (NCCP), National Institute for Genomics and Advanced Biotechnology (NIGAB), National Agricultural Research Centre (NARC), Park Road, Islamabad, 45500, Pakistan

    Rifat Hayat, Iftikhar Ahmed, Muhammad Ehsan & Muhammad Iqbal

  2. Department of Soil Science & SWC, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, 46300, Pakistan

    Rifat Hayat & Muhammad Ehsan

  3. Korean Collection for Type Cultures, Biological Resources Centre, Korea Research Institute of Bioscience and Biotechnology (KRIBB), 125 Gwahak-ro, Yuseong-gu, Daejeon, 305-806, Republic of Korea

    Jayoung Paek, Yeseul Sin & Young H. Chang

  4. Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Bunkyo-Ku, Tokyo, 113-8657, Japan

    Rifat Hayat & Akira Yokota

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  1. Rifat Hayat
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  2. Iftikhar Ahmed
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  3. Jayoung Paek
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  4. Yeseul Sin
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  5. Muhammad Ehsan
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  6. Muhammad Iqbal
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  7. Akira Yokota
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  8. Young H. Chang
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Corresponding authors

Correspondence to Iftikhar Ahmed or Young H. Chang.

Additional information

The DDBJ/EMBL/GenBank accession number for the 16S rRNA gene sequence of strain NCCP-36T (=JCM 18777T = KCTC 13796 T; DSMZ 24785 T) is AB547124.

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Hayat, R., Ahmed, I., Paek, J. et al. Lysinibacillus composti sp. nov., isolated from compost. Ann Microbiol 64, 1081–1088 (2014). https://doi.org/10.1007/s13213-013-0747-1

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Keywords

Annals of Microbiology

ISSN: 1869-2044

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