Genomic information of the arsenic-resistant bacterium Lysobacter arseniciresistens type strain ZS79T and comparison of Lysobacter draft genomes
© Liu et al. 2015
Received: 29 October 2014
Accepted: 8 October 2015
Published: 27 October 2015
Lysobacter arseniciresistens ZS79T is a highly arsenic-resistant,rod-shaped, motile, non-spore-forming, aerobic, Gram-negative bacterium. In this study, four Lysobacter type strains were sequenced and the genomic information of L. arseniciresistens ZS79T and the comparative genomics results of the Lysobacter strains were described. The draft genome sequence of the strain ZS79T consists of 3,086,721 bp and is distributed in 109 contigs. It has a G+C content of 69.5 % and contains 2,363 protein-coding genes including eight arsenic resistant genes.
KeywordsLysobacter Lysobacter arseniciresistens Comparative genomics Genome sequence Xanthomonadaceae
Lysobacter arseniciresistens type strain ZS79T (=CGMCC 1.10752T = KCTC 23365 T) belongs to family Xanthomonadaceae . It is an arsenic-resistant bacterium isolated from subsurface soil of Tieshan iron mine, Daye City, P. R. China . So far, there are 32 validly published species of Lysobacter . Most of these Lysobacter strains were isolated from soil except that Lysobacter brunescens  and Lysobacter oligotrophicus  were isolated from water, and Lysobacter concretionis , Lysobacter daecheongensis  Lysobacter spongiicola  were isolated from sludge, sediment and deep-sea sponge, respectively.
So far, the genomic sequences of two Lysobacter strains have been published ( Lysobacter capsici AZ78 [8, 9] and Lysobacter antibioticus 13-6 ), but the annotation of L. antibioticus 13-6 was not completed. In order to provide genome information of genus Lysobacter , we performed whole genome sequencing of four strains of Lysobacter ( L. arseniciresistens ZS79T, Lysobacter conceretionis Ko07T , Lysobacter daejeonensis GH1-9T , and Lysobacter defluvii IMMIB APB-9T ). In this study, the genome features of L. arseniciresistens ZS79T is provided and the comparative results of five genomes of Lysobacter are presented.
Classification and features
Members of genus Lysobacter are rod-shaped, aerobic, Gram-negative bacteria . Their G+C contents are 65.4–70.1 %. They use NO3 −, NH4 +, glutamate, asparaginate as sole nitrogen sources, Q-8 as the major respiratory quinone, and diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, phosphatidyl-N-methylethanolamine as the major polar lipids [3, 8]. In addition, they could lyse cells of many creatures including bacteria, filamentous fungi, yeasts, algae and nematodes .
Classification and general features of L. arseniciresistens ZS79T according to the MIGS recommendations 
Species Lysobacter arseniciresistens
Type strain: ZS79T (=CGMCC 1.10752T = KCTC 23365T).
pH range; Optimum
tyrosine, hippurate, gelatin, 3-hydroxybutyric acid
Habitat subsurface soil
0–4 % NaCl (w/v)
Daye City, Hubei province, China
The major ubiquinone is Q-8, the major cellular fatty acids (>10 %) are iso-C15 : 0, iso-C17 :1 ω9ϲ, iso-C16 :0, iso-C11 :0 and iso-C11 :0 3-OH. The polar lipids are diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and a kind of unknown phospholipid The C + G content is was 70.7 mol% (HPLC) .
Genome sequencing and annotation
Genome project history
Illumina Paired-End library (300 bp insert size)
Gene calling method
GenBank Date of Release
Source Material Identifier
Growth conditions and genomic DNA preparation
L. arseniciresistens ZS79T was cultured in 50 ml of LB (Luria–Bertani) medium at 28 °C for 3 days with 160 160 r/min shaking. About 10 mg cells were harvested by centrifugation and suspended in normal saline, and then lysed using lysozyme. DNA was isolated using cells were harvested by centrifugation and suspended in normal saline, and then lysed using lysozyme. The DNA was extracted and purified using the QiAamp kit according to the manufacturer’s instruction (Qiagen, Germany).
Genome sequencing and assembly
The whole genome sequencing of L. arseniciresistens ZS79T was performed on Illumina Hiseq2000 with Paired-End library strategy (300 bp insert size) at Majorbio Biomedical Science and Technology Co. Ltd. DNA libraries with insert sizes from 300 to 500 bp was constructed using the established protocol . The obtained high quality data contains 4,528,542 × 2 pared reads and 194,996 single reads with an average read length of 91 bp. The sequencing depth was 272.6×. Using SOAPdenovo v1.05  the reads were assembled into 109 contigs with a cumulative genome size of 3,086,721 bp.
The draft sequence of L. arseniciresistens ZS79T was annotated using the National Center for Biotechnology Information Prokaryotic Genomes Annotation Pipeline . The functions of the predicted genes were determined through blast alignment against the NCBI protein database. Genes were identified using the gene caller GeneMarkS+ with the similarity-based gene detection approach . The different features were predicted by WebMGA , TMHMM  and SignalP .
% of Total
Genome size (bp)
DNA coding (bp)
DNA G+C (bp)
Protein coding genes
Genes in internal clusters
Genes with function prediction
Genes assigned to COGs
Genes with Pfam domains
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with general COG functional categories
Translation, ribosomal structure and biogenesis
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, Cell division, chromosome partitioning
Signal transduction mechanisms
Cell wall/membrane biogenesis
Intracellular trafficking and secretion
Posttranslational modification, protein turnover, chaperones
Energy production and conversion
Carbohydrate transport and metabolism
Amino acid transport and metabolism
Nucleotide transport and metabolism
Coenzyme transport and metabolism
Lipid transport and metabolism
Inorganic ion transport and metabolism
Secondary metabolites biosynthesis, transport and catabolism
General function prediction only
Not in COGs
Insights from the genome sequences
General features of the five Lysobacter genomesa
Contigs N50 (bp)
L. arseniciresistens ZS79T
L. conceretionis Ko07T
L. daejeonensis GH1-9T
Green house soils
L. defluvii IMMIB APB-9T
Municipal solid waste
L. capsici AZ78
Tobacco & tomato rhizosphere
In the genome of L. arseniciresistens ZS79T, we found that the genomic island distributions are consistent with the genome C + G content anomaly areas (Fig. 3). In addition, few gene sequences from the other four Lysobacter genomes could be aligned with these genomic island regions (Fig. 3, ring 6 to ring 9). These results indicated that the genes within the genomic islands were most probably acquired by horizontal transfer  and these regions are unique in the genome of L. arseniciresistens ZS79T.
According to Kyoto Encyclopedia of Genes and Genomes  annotation result, all of the five Lysobacter genomes have a nearly complete type II secretion system which could secret cell wall degrading enzymes . This result may correspond to the behavior of Lysobacter members that were able to lyse cells of many microorganisms . In addition, the genomes of L. arseniciresistens ZS79T, L. concretionis Ko07T and L. defluvii IMMIB APB-9T contain genes for flagellar assembly, whereas the genome of L. daejeonensis GH1-9T does not contain any genes for flagellar assembly and L. capsici AZ78 does not contain genes for flagellar filament (Additional file 1: Table S2). These genotypes correspond to the phenotype descriptions that L. daejeonensis and L. capsici are non-motile [8, 11].
Genomic analysis showed eight genes corresponding to arsenic resistance in the genomes of L. arseniciresistens ZS79T (Additional file 1: Table S3). This result well explained the arsenite resistance of this strain . By contrast, fewer arsenic resistance were found in the genomes of L. concretionis Ko07T, L. defluvii IMMIB APB-9T, L. capsici AZ78, and L. daejeonensis GH1-9T compared to strain ZS79T.
The genomic information of L. arseniciresistens ZS79T and the comparative genomics analysis of the five Lysobacter strains are obtained. The genomic based phylogeny is in agreement with the 16S rRNA gene based one indicating the usefulness of genomic information for bacterial taxonomic classification. Analysis of the genomes show certain correlation between the genotypes and the phenotypes.
This work was supported by the National High Technology Research and Development Program of China (2012AA101402) and the National Natural Science Foundation of China (31470226).
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Luo G, Shi Z, Wang G. Lysobacter arseniciresistens sp. nov., an arsenite-resistant bacterium isolated from iron-mined soil. Int J Syst Evol Microbiol. 2012;62:1659–65. PubMed http://www.ncbi.nlm.nih.gov/pubmed/21890727.View ArticlePubMedGoogle Scholar
- NCBI Taxonomy Browser http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi
- Christensen P, Cook FD. Lysobacter, a New Genus of Nonfruiting, Gliding Bacteria with a High Base Ratio. Int J Syst Bacteriol. 1978;28:27. http://ijs.sgmjournals.org/cgi/content/abstract/28/3/367.View ArticleGoogle Scholar
- Fukuda W, Kimura T, Araki S, Miyoshi Y, Atomi H, Imanaka T. Lysobacter oligotrophicus sp. nov., isolated from an Antarctic freshwater lake in Antarctica. Int J Syst Evol Microbiol. 2013;63:3313–8. PubMed http://www.ncbi.nlm.nih.gov/pubmed/23475347.View ArticlePubMedGoogle Scholar
- Bae HS, Im WT, Lee ST. Lysobacter concretionis sp. nov., isolated from anaerobic granules in an upflow anaerobic sludge blanket reactor. Int J Syst Evol Microbiol. 2005;55:1155–61. PubMed http://www.ncbi.nlm.nih.gov/pubmed/15879248.View ArticlePubMedGoogle Scholar
- Ten LN, Jung HM, Im WT, Yoo SA, Lee ST. Lysobacter daecheongensis sp. nov., isolated from sediment of stream near the Daechung dam in South Korea. J Microbiol. 2008;46:519–24. PubMed http://www.ncbi.nlm.nih.gov/pubmed/18974952.View ArticlePubMedGoogle Scholar
- Romanenko LA, Uchino M, Tanaka N, Frolova GM, Mikhailov VV. Lysobacter spongiicola sp. nov., isolated from a deep-sea sponge. Int J Syst Evol Microbiol. 2008;58:370–4. PubMed http://www.ncbi.nlm.nih.gov/pubmed/18218933.View ArticlePubMedGoogle Scholar
- Park JH, Kim R, Aslam Z, Jeon CO, Chung YR. Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. Int J Syst Evol Microbiol. 2008;58:387–92. PubMed http://www.ncbi.nlm.nih.gov/pubmed/18218936.View ArticlePubMedGoogle Scholar
- Puopolo G, Sonego P, Engelen K, Pertot I. Draft Genome Sequence of Lysobacter capsici AZ78, a Bacterium Antagonistic to Plant-Pathogenic Oomycetes. Genome Announc. 2014;2. PubMed http://www.ncbi.nlm.nih.gov/pubmed/24762937.
- Zhou L, Li M, Yang J, Wei L, Ji G. Draft Genome Sequence of Antagonistic Agent Lysobacter antibioticus 13-6. Genome Announc. 2014;2. PubMed http://www.ncbi.nlm.nih.gov/pubmed/25301638.
- Weon HY, Kim BY, Baek YK, Yoo SH, Kwon SW, Stackebrandt E, et al. Two novel species, Lysobacter daejeonensis sp. nov. and Lysobacter yangpyeongensis sp. nov., isolated from Korean greenhouse soils. Int J Syst Evol Microbiol. 2006;56:947–51. PubMed http://www.ncbi.nlm.nih.gov/pubmed/16627636.View ArticlePubMedGoogle Scholar
- Yassin AF, Chen WM, Hupfer H, Siering C, Kroppenstedt RM, Arun AB, et al. Lysobacter defluvii sp. nov., isolated from municipal solid waste. Int J Syst Evol Microbiol. 2007;57:1131–6. PubMed http://www.ncbi.nlm.nih.gov/pubmed/17473271.View ArticlePubMedGoogle Scholar
- Illumina official website http://www.illumina.com
- Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2012;1:18. PubMed http://www.ncbi.nlm.nih.gov/pubmed/23587118.PubMed CentralView ArticlePubMedGoogle Scholar
- Prokaryotic Genome Annotation Pipeline http://www.ncbi.nlm.nih.gov/genome/annotation_prok.
- Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001;29(12):2607–18. PubMed http://www.ncbi.nlm.nih.gov/pubmed/11410670.PubMed CentralView ArticlePubMedGoogle Scholar
- Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011;12:444. PubMed http://www.ncbi.nlm.nih.gov/pubmed/21899761.PubMed CentralView ArticlePubMedGoogle Scholar
- Krogh A, Larsson BÈ, Von Heijne G, et al. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80. PubMed http://www.ncbi.nlm.nih.gov/pubmed/11152613.View ArticlePubMedGoogle Scholar
- Dyrlov Bendtsen J, Nielsen H, von Heijne G. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340(4):783–95. PubMed http://www.ncbi.nlm.nih.gov/pubmed/15223320.View ArticleGoogle Scholar
- Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003;4:41. PubMed http://www.ncbi.nlm.nih.gov/pubmed/12969510.PubMed CentralView ArticlePubMedGoogle Scholar
- Li L, Stoeckert Jr CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178–89. PubMed http://www.ncbi.nlm.nih.gov/pubmed/12952885.PubMed CentralView ArticlePubMedGoogle Scholar
- Darling AC, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–403. PubMed http://www.ncbi.nlm.nih.gov/pubmed/15231754.PubMed CentralView ArticlePubMedGoogle Scholar
- Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. PubMed http://www.ncbi.nlm.nih.gov/pubmed/19346325.View ArticlePubMedGoogle Scholar
- Langille MG, Hsiao WW, Brinkman FS. Detecting genomic islands using bioinformatics approaches. Nat Rev Microbiol. 2010;8:373–82. PubMed http://www.ncbi.nlm.nih.gov/pubmed/20395967.View ArticlePubMedGoogle Scholar
- Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42:D199–205. PubMed http://www.ncbi.nlm.nih.gov/pubmed/24214961.PubMed CentralView ArticlePubMedGoogle Scholar
- Cianciotto NP. Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 2005;13:581–8. PubMed http://www.ncbi.nlm.nih.gov/pubmed/16216510.View ArticlePubMedGoogle Scholar
- Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7. PubMed http://www.ncbi.nlm.nih.gov/pubmed/18464787.PubMed CentralView ArticlePubMedGoogle Scholar
- Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9. PubMed http://www.ncbi.nlm.nih.gov/pubmed/2112744.PubMed CentralView ArticlePubMedGoogle Scholar
- Garrity G, Bell J, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity G, Brenner D, Krieg N, Staley J, editors. Bergey’s Manual of Systematic Bacteriology, vol. 2. 2nd ed. New York: Springer; 2005. p. 1.View ArticleGoogle Scholar
- Validation of publication of new names and new combinations previously effectively published outside the IJSEM. Int J Syst Evol Microbiol. 2005; 55:1743–5. PubMed [http://www.ncbi.nlm.nih.gov/pubmed/16166658].
- Saddler G, Bradbury J. Order III. Xanthomonadales ord. nov. In: Garrity G, Brenner D, Krieg N, Staley J, editors. Bergey’s Manual of Systematic Bacteriology, vol. 2. 2nd ed. New York: Springer; 2005. p. 63.View ArticleGoogle Scholar
- Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9. PubMed http://www.ncbi.nlm.nih.gov/pubmed/10802651.PubMed CentralView ArticlePubMedGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30:2725–9. PubMed http://www.ncbi.nlm.nih.gov/pubmed/24132122.PubMed CentralView ArticlePubMedGoogle Scholar
- Langille MG, Brinkman FS. IslandViewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics. 2009;25:664–5. PubMed http://www.ncbi.nlm.nih.gov/pubmed/19151094.PubMed CentralView ArticlePubMedGoogle Scholar