High-quality-draft genome sequence of the multiple heavy metal resistant bacterium Pseudaminobacter manganicus JH-7T

Standards in Genomic Sciences, Oct 2018

Pseudaminobacter manganicus JH-7T (= KCTC 52258T = CCTCC AB 2016107T) is a Gram-staining-negative, aerobic and non-motile strain that was isolated from a manganese mine. The strain JH-7T shows multiple heavy metal resistance and can effectively remove Mn2+ and Cd2+. In addition, it is able to produce exopolysaccharides (EPS), which may contribute to metal remove/adsorption. Thus, strain JH-7T shows a great potential in bioremediation of heavy metal-contaminated environment. In this study, we report the draft genomic sequence of P. manganicus JH-7T and compare it to related genomes. Strain JH-7T has a 4,842,937 bp genome size with a G + C content of 61.2%, containing 4504 protein-coding genes and 71 RNA genes. A large number of putative genes associated with heavy metal resistance and EPS synthesis are found in the genome.

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High-quality-draft genome sequence of the multiple heavy metal resistant bacterium Pseudaminobacter manganicus JH-7T

Standards in Genomic Sciences December 2018, 13:29 | Cite as High-quality-draft genome sequence of the multiple heavy metal resistant bacterium Pseudaminobacter manganicus JH-7T AuthorsAuthors and affiliations Xian XiaJiahong LiZijie ZhouDan WangJing HuangGejiao Wang Open Access Short genome report First Online: 25 October 2018 10 Downloads Abstract Pseudaminobacter manganicus JH-7T (= KCTC 52258T = CCTCC AB 2016107T) is a Gram-staining-negative, aerobic and non-motile strain that was isolated from a manganese mine. The strain JH-7T shows multiple heavy metal resistance and can effectively remove Mn2+ and Cd2+. In addition, it is able to produce exopolysaccharides (EPS), which may contribute to metal remove/adsorption. Thus, strain JH-7T shows a great potential in bioremediation of heavy metal-contaminated environment. In this study, we report the draft genomic sequence of P. manganicus JH-7T and compare it to related genomes. Strain JH-7T has a 4,842,937 bp genome size with a G + C content of 61.2%, containing 4504 protein-coding genes and 71 RNA genes. A large number of putative genes associated with heavy metal resistance and EPS synthesis are found in the genome. KeywordsCadmium Exopolysaccharides Heavy metal resistance and adsorption Manganese,Pseudaminobacter  Abbreviations EPS Exopolysaccharides MIC Minimal inhibition concentration Xian Xia and Jiahong Li contributed equally to this work. Electronic supplementary material The online version of this article ( https://doi.org/10.1186/s40793-018-0330-2) contains supplementary material, which is available to authorized users. Introduction Genus Pseudaminobacter was established by Kämpfer et al. in 1999 and contains three species represented by Pseudaminobacter salicylatoxidans BN12T (type species) [1], Pseudaminobacter defluvii THI 051T [1] and Pseudaminobacter manganicus JH-7T [2]. The common characteristics of Pseudaminobacter strains are Gram-staining-negative, rod-shaped and aerobic [1, 2]. P. salicylatoxidans BN12T contains a peculiar ring-fission dioxygenase with the ability to cleave salicylate in 1, 2-position to 2-oxohepta-3, 5-dienedioic acid [3]. P. manganicus JH-7T was isolated from a sludge sample of a wastewater ditch in Dalong manganese mine in 2015 [2]. It shows multiple heavy metal resistance and can effectively remove Mn2+ and Cd2+. In addition, the strain produces EPS, which may facilitate heavy metal resistance and adsorption [4, 5, 6]. These features show great interests because of its potential applications in bioremediation of heavy metal contaminated environments. So far, only the genome of an atypical Pseudaminobacter strain Pseudaminobacter salicylatoxidans KCT001 has been sequenced [7]. Strain KCT001 can utilize tetrathionate as the substrate for sulfur-oxidizing chemolithotrophic growth [8]. For better understanding the mechanism of bacterial resistance and removal of heavy metals, here we analyze the genome of P. manganicus JH-7T. Organism information Classification and features The phylogenetic relationship of P. manganicus JH-7T to the related members is shown in a 16S rRNA gene based neighbor-joining tree. Strain JH-7T is closely related to P. salicylatoxidans BN12T, P. defluvii THI 051T and P. salicylatoxidans KCT001 (Fig. 1). Strain JH-7T is Gram-staining-negative, aerobic, non-motile and rod-shaped (0.3–0.8 × 1–2 μm) (Fig. 2). The colonies are white, circular, entire, slightly raised and smooth on LB agar plates. It is positive for oxidase and catalase activities and hydrolysis of casein [2]. The major fatty acids are C18:1 ω7c, C19:0 cyclo ω8c and C16:0 and the G + C content is 61.2 mol% [2]. The major polyamine is sym-homospermidine and the respiratory quinone is ubiquinone-10. The polar lipids are phosphatidylmonomethylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylcholine, two aminolipids and two lipids [2]. Table 1 shows the general features of P. manganicus JH-7T. Open image in new window Fig. 1 Phylogenetic tree highlighting the phylogenetic position of Pseudaminobacter manganicus JH-7T. The phylogenetic tree was constructed based on the 16S rRNA gene sequences. The analysis was inferred by MEGA 6.0 [41] with neighbor-joining algorithm and 1000 bootstrap repetitions were computed to estimate the reliability of the tree. Bar, 0.005 substitutions per nucleotide position Open image in new window Fig. 2 Transmission electron micrograph image of strain JH-7T. Bar, 0.5 μm Table 1 Classification and general features of P. manganicus JH-7T [42] MIGS ID Property Term Evidence codea   Classification Domain Bacteria TAS [43]   Phylum Proteobacteria TAS [44, 45]   Class Alphaproteobacteria TAS [46]   Order Rhizobiales TAS [46, 47]   Family Phyllobacteriaceae TAS [46, 47]   Genus Pseudaminobacter TAS [1, 2]   Species manganicus TAS [2]   Type strain JH-7T (= KCTC 52258T = CCTCC AB 2016107T) TAS [2]   Gram stain negative TAS [2]   Cell shape rod-shaped TAS [2]   Motility no TAS [2]   Sporulation no TAS [2]   Temperature range 15–40 °C TAS [2]   Optimum temperature 28 °C TAS [2]   pH range; Optimum 5–9; 7 TAS [2]   Carbon source D-glucose, L-arabinose, D-fructose and D-mannose TAS [2] MIGS-6 Habitat Mine sludge TAS [2] MIGS-6.3 Salinity 0–6% NaCl (w/v) TAS [2] MIGS-22 Oxygen requirement aerobic TAS [2] MIGS-15 Biotic relationship free-living TAS [2] MIGS-14 Pathogenicity non-pathogen NAS MIGS-4 Geographic location Tongren city, Guizhou province, P. R. China TAS [2] MIGS-5 Sample collection 2015 TAS [2] MIGS-4.1 Latitude N27° 43′ 8" TAS [2] MIGS-4.2 Longitude E108° 31′ 42" TAS [2] MIGS-4.4 Altitude not reported   These evidence codes are from the Gene Ontology project [48] IDA Inferred from Direct Assay, TAS Traceable Author Statement (i.e., a direct report exists in the literature), NAS Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence) aEvidence codes The resistant levels of P. manganicus JH-7T to multiple metal(loid)s were tested with the MIC on LB agar plates incubated at 28 °C for 7 days. The MICs for MnCl2, CdCl2, PbCl2, CuCl2, ZnSO4 and NiSO4 are100, 2, 10, 5, 5 and 5 mmol/L respectively. The MICs for K2CrO4 and Na3AsO3 are both 0.1 mmol/L that are lower than the above six metals. Specifically, strain JH-7T could remove nearly 60% of 5 mmol/L Mn2+ and nearly 80% of 0.1 mmol/L Cd2+ (Fig. 3), respectively. In addition, strain JH-7T could produce EPS based on the aniline blue reaction incubated on LB agar in 3–7 days [9] (data not shown). This phenomenon is consistent with the cell image observed by TEM (Fig. 2). A lay of shadow around the strain was similar to the EPS observed in strain Bifidobacterium longum 35,624 [10]. Open image in new window Fig. 3 Mn2+ and Cd2+ removed by P. manganicus JH-7T. Control stands for null LB medium. Strain JH-7T was incubated until OD600 reach 1.0, and then amended with 5000 μmol/L MnCl2 (a) and 100 μmol/L CdCl2 (b), respectively. The cultures were removed at 24 h intervals. After centrifuging at 12,000 rpm for 10 min, the supernatant was used to determine the residual concentration of Mn2+ and Cd2+ by the atomic absorption spectrometry AAS (AAS; 986A, Beijing Puxi General Instrument 197 Co., Beijing, China). Bars represent the mean ± SD of three biological replicates Genome sequencing information Genome project history This organism was selected for sequencing particularly due to its multiple heavy metals resistance and heavy metal removal ability. Genome sequencing was performed by Wuhan Bio-Broad Co., Ltd., Wuhan, China in 2016. The draft genome sequence of strain P. manganicus JH-7T has been deposited at DDBJ/EMBL/GenBank under accession number MDET00000000. The project information is summarized in Table 2. Table 2 Project information MIGS ID Property Term MIGS-31 Finishing quality High-quality draft MIGS-28 Libraries used Illumina Paired-End library (300 bp insert size) MIGS-29 Sequencing platforms Illumina Miseq 2000 MIGS-31.2 Fold coverage 624.94× MIGS-30 Assemblers SOAPdenovo v2.04 MIGS-32 Gene calling method GeneMarkS+ Locus TAG BFN67 Genbank ID MDET00000000 Genbank Date of Release 31, March, 2017 GOLD ID Gp0291525 Bioproject PRJNA338732 MIGS-13 Source material identifier CCTCC AB 2016107T Project relevance Bioremediation Growth conditions and genomic DNA preparation P. manganicus JH-7T was grown under aerobic conditions in LB medium at 28 °C for 40 h. DNA extraction was performed using the QiAamp kit (Qiagen, Germany) as the manufacturer’s instructions. A NanoDrop Spectrophotometer 2000 was used to determine the quality and quantity of the DNA. Seven microgram of DNA was sent to Bio-broad Technogoly Co., Ltd., Wuhan, China for sequencing. Genome sequencing and assembly The genome of strain JH-7T was sequenced on Illumina Hiseq2000 [11] and assembled by Bio-broad Technogoly Co., Ltd., Wuhan using SOAPdenovo v2.04 [12]. An Illumina standard shotgun library was constructed and sequenced, which generated 19,404,755 reads totaling 2,885,684,230 bp and average of 625 times genome coverage. The total size of the genome is 4,842,937 bp and a total of 60 scaffolds were obtained after arranging 68 contigs together. The part gaps of assembly were filled and the error bases were revised using GapCloser v1.12 [13]. Genome annotation The draft genome was annotated through the NCBI Prokaryotic Genome Annotation Pipeline (PGAP), and genes were identified using the gene caller GeneMarkS+ with the similarity-based gene detection approach [14]. The predicted CDSs were translated and were submitted to the Pfam protein family database [15] and KEGG database [16]. The genes in internal clusters were performed by OrthoMCL [17, 18]. The protein function classification, transmembrane helices and signal peptides were predicted by WebMGA [19], TMHMM v. 2.0 [20] and SignalP 4.1 [21], respectively. In addition, the CRISPRfinder program [22] was used to predict CRISPRs in the genome. Genome properties The draft genome size of strain JH-7T is 4,842,937 bp with 61.2 mol% G + C content and contains 60 scaffolds. The genome properties and statistics are shown in Table 3. From a total of 4685 genes, 4504 (96.2%) are protein coding genes, 110 (2.3%) are pseudo genes and the rest are 71 predicted RNA genes, including 54 tRNA, 12 rRNAs and 5 ncRNA. In addition, 3729 (82.8%) protein coding genes are distributed into COG functional categories (Table 4). Table 3 Genome statistics Attribute Value % of totala Genome size (bp) 4,842,937 100 DNA coding (bp) 4,238,496 87.5 DNA G + C (bp) 2,963,726 61.2 DNA scaffolds 60 100 Total genesb 4685 100 Protein-coding genes 4504 96.2 RNA genes 71 1.7 Pseudo genes 110 2.3 Genes in internal clusters 1725 38.3 Genes with function prediction 3228 68.9 Genes assigned to COGs 3729 79.6 Genes with Pfam domains 3926 83.8 Genes with signal peptides 392 8.4 Genes with transmembrane helices 1119 23.9 CRISPR repeats 5   aThe total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome bAlso includes 110 pseudogenes, 54 tRNA genes, 12 rRNAs and 5 ncRNA Table 4 Number of genes associated with the 25 general COG functional categories Code Value % of totala Description J 181 4.02 Translation A 0 0.00 RNA processing and modification K 299 6.64 Transcription L 233 5.17 Replication, recombination and repair B 3 0.07 Chromatin structure and dynamics D 39 0.87 Cell cycle control, mitosis and meiosis Y 0 0.00 Nuclear structure V 46 1.02 Defense mechanisms T 134 2.98 Signal transduction mechanisms M 217 4.82 Cell wall/membrane biogenesis N 35 0.78 Cell motility Z 0 0.00 Cytoskeleton W 0 0.00 Extracellular structures U 106 2.35 Intracellular trafficking and secretion O 156 3.46 Posttranslational modification, protein turnover, chaperones C 240 5.33 Energy production and conversion G 312 6.93 Carbohydrate transport and metabolism E 482 10.70 Amino acid transport and metabolism F 87 1.93 Nucleotide transport and metabolism H 158 3.51 Coenzyme transport and metabolism I 153 3.40 Lipid transport and metabolism P 209 4.64 Inorganic ion transport and metabolism Q 91 2.02 Secondary metabolites biosynthesis, transport and catabolism R 453 10.06 General function prediction only S 444 9.86 Function unknown – 775 17.21 Not in COGs aThe total is based on the total number of protein coding genes in the annotated genome Insights from the genome sequence Strain JH-7T could tolerant multiple heavy metals (Mn2+, Cd2+, Pb2+, Cu2+, Zn2+ and Ni2+) and remove Mn2+ and Cd2+, suggesting that it has developed a number of evolutionary strategies to adapt the mine environment. According to the genome annotation results, strain JH-7T harbors various putative proteins related to heavy metal(loid)s resistance including transporters, resistance proteins and metal reductases (Additional file 1: Table S1). MntH [23] and metal ABC transport system [24] are involved in cation uptake. Heavy metal-transporting ATPase is responsible for the efflux of Pb2+, Zn2+, Cd2+ and Ni2+ [25, 26, 27, 28]. The genome contains Cu2+ efflux system CopABC [29], mercuric reductase MerA and regulator MerR [30]. Athough the MICs for Cr6+ and As3+ are not high, the Cr6+ efflux protein ChrA [27, 31] and As3+ resistant proteins (ArsRHC and ACR3) [32, 33, 34] are present. EPS are long-chain polysaccharides consisting of branched, repeating units of sugars or sugar derivatives [35]. Stain JH-7T could produce EPS and all essential proteins for EPS production are found in the genome. Four complete nucleotide sugar synthesis (EPS precursor) pathways are identified based on KEGG analysis (Additional file 1: Table S2) including the syntheses of UDP-glucose, UDP-galactose, UDP-GlcNAc and GDP-D-mannose (Fig. 4a). EPS assembly gene clusters were also found in the genome of strain JH-7T [36] (Additional file 1: Table S3, Fig. 4b). Based on gene analysis, it is suggested that the EPS assembly in strain JH-7T might belong to Wzx/Wzy-dependent pathway [37], e.g., repeat units are assembled by glycosyltransferases (EpsI) and translocated across the cytoplasmic membrane to periplasm by flippase (Wzx) [37] and WbaP [38]. Next, Wzy (RfaL), polysaccharide co-polymerase (GumC) and the outer membrane polysaccharide exporter (GumB) transports the polymerized repeat units to cell surface [37, 39]. EPS has been reported to contribute to heavy metal removal/adsorption in bacteria [3, 4, 5, 6]. Hence, the ability of EPS may contribute to Mn2+ and Cd2+ removal. Open image in new window Fig. 4 Putative nucleotide sugars biosynthesis pathway and EPS synthesis gens in P. manganicus JH-7T. a The predicted nucleotide sugars biosynthesis pathway. The numbers refer to the enzymes involved: 1, Glucokinase; 2, α-D-glucose phosphate-specific phosphoglucomutase; 3, UTP--glucose-1-phosphate uridylyltransferase; 4, UDP-glucose 4-epimerase GalE; 5, Glucose-6-phosphate isomerase; 6, Fructokinase; 7, Glutamine--fructose-6-phosphate aminotransferase; 8, Phosphoglucosamine mutase; 9, UDP-N-acetylglucosamine; 10, Glucose-6-phosphate isomerase; 11, Mannose-6-phosphate isomerase; 12, PTS-Man-EIIA, ManX; 13, Phosphoglucomutase; 14, Mannose-1-phosphate guanylyltransferase. b The EPS synthesis gene cluster in strain JH-7T To gain more insight, the genomic features of strain JH-7T is compared with the available genome P. salicylatoxidans KCT001 [7]. Strain JH-7T has similar genome size (4.84 Mbp) and G + C content (61.2 mol%) compared to strain KCT001 (4.61 Mbp; 62.8 mol%). A total of 2408 core proteins are shared between the two strains. Strain JH-7T has 1724 strain-specific CDSs. Figure 5 shows the genome comparison results of strain JH-7T and strain KCT001 using CGview comparison tool [40]. Comparing to P. salicylatoxidans KCT001, strain JH-7T was unable to utilize tetrathionate for chemolithoautotrophy (data not shown). However, it harbors high quantitative and diverse heavy metal resistance genes. Open image in new window Fig. 5 A graphical circular map of the comparison between strain P. manganicus JH-7T and P. salicylatoxidans KCT001. From outside to center, rings 1, 4 show protein-coding genes colored by COG categories on forward/reverse strand; rings 2, 3 denote genes on forward/reverse strand; rings 5 show the CDS vs CDS BLAST results of strain JH-7T with strain KCT001; ring 6 shows G + C % content plot and the innermost ring shows GC skew Conclusions To the best of our knowledge, this study provides the first typical strain genomic information of the genus Pseudaminobacter and revealed a consistency of important characters between genotypes and phenotypes. Strain JH-7T is resistant to multiple heavy metals and capable of removal Mn2+/Cd2+. Genome analysis reveal various genes responsible for multiple heavy metal resistance, which provides the genomic basis for this strain to adapt the harmful environment. Notes Funding This study was supported by National key research and development program of China (2016YFD0800702). Authors’ contributions XX and JL performed the sequence annotation and genomic analysis and prepared the draft manuscript. ZZ, DW and JH performed the heavy metals resistance and removal tests. GW designed the study and revised the manuscript. All authors read and approved the final manuscript. Competing interests The authors declare that they have no competing interests. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Supplementary material 40793_2018_330_MOESM1_ESM.xlsx (12 kb) Additional file 1: Table S1. Putative heavy metal(loid)s resistance proteins. Table S2. Putative nucleotide sugars biosynthesis proteins for EPS production. Table S3. Putative proteins for EPS production. (XLSX 11 kb) References 1. Kämpfer P, Müller C, Mau M, Neef A, Auling G, Busse HJ, et al. Description of Pseudaminobacter gen. 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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. Authors and Affiliations Xian Xia1Jiahong Li1Zijie Zhou1Dan Wang1Jing Huang1Gejiao Wang1Email author1.State Key Laboratory of Agricultural MicrobiologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China

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Xian Xia, Jiahong Li, Zijie Zhou, Dan Wang, Jing Huang, Gejiao Wang. High-quality-draft genome sequence of the multiple heavy metal resistant bacterium Pseudaminobacter manganicus JH-7T, Standards in Genomic Sciences, 2018, 29, DOI: 10.1186/s40793-018-0330-2