Skip to main content
  • Short genome report
  • Open access
  • Published:

Complete genome of Arthrobacter alpinus strain R3.8, bioremediation potential unraveled with genomic analysis

Abstract

Arthrobacter alpinus R3.8 is a psychrotolerant bacterial strain isolated from a soil sample obtained at Rothera Point, Adelaide Island, close to the Antarctic Peninsula. Strain R3.8 was sequenced in order to help discover potential cold active enzymes with biotechnological applications. Genome analysis identified various cold adaptation genes including some coding for anti-freeze proteins and cold-shock proteins, genes involved in bioremediation of xenobiotic compounds including naphthalene, and genes with chitinolytic and N-acetylglucosamine utilization properties and also plant-growth-influencing properties. In this genome report, we present a complete genome sequence of A. alpinus strain R3.8 and its annotation data, which will facilitate exploitation of potential novel cold-active enzymes.

Introduction

The production of cold-adapted enzymes by psychrotolerant bacteria has important scientific and industrial interest due to their highly specific activity and catalytic efficiency at low and moderate temperatures [1]. The use of cold-adapted enzymes offers various advantages such as the reduction of undesirable chemical reactions that take place at high temperature, rapid enzymatic inactivation through thermal treatment, and reduction in energy demand required to fuel industrial processes at higher temperatures [2,3,4]. These beneficial traits are particularly useful in the development of sequential molecular biology processes, low temperature detergents, food and industrial bio-catalytic enzymes, and for bioremediation agents applicable during cold seasons and in cold regions. In this study, we perform complete genome sequencing on a psychrotolerant bacterium, Arthrobacter alpinus strain R3.8 (=DSM 100969), originally isolated from soil collected from Rothera Point, Adelaide Island, maritime Antarctica. The optimum growth temperature range of this bacterium is 10–16 °C, which rendered it a promising source for discovery of novel cold-adapted enzymes. The complete genome sequence of A. alpinus strain R3.8 was generated using Single Molecule Real Time sequencing technology to provide a rapid and complete insight into its biotechnological potential. Here, we highlight various genome features that indicate the potential biotechnological value of A. alpinus strain R3.8 in the context of xenobiotic biodegradation and metabolism, chitin utilization, and as a potential component in bio-fertilizers.

Organism information

Classification and features

A. alpinus strain R3.8, is a psychrotolerant soil bacterium originally isolated from a soil sample collected at Rothera Research Station, close to Antarctic Special Protected Area No.129 (68°07′S, 67°34′W). Strain R3.8 was isolated using basal medium supplied with C6-HSL as sole carbon source. An isolation temperature of 4 °C was used to select for psychrophilic or psychrotolerant bacteria maintained on Luria Bertani (LB) agar [5, 6]. The strain exhibited a 98.6% 16S rRNA nucleotide sequence similarity with A. alpinus , the most phylogenetically closely related Arthrobacter species with standing in nomenclature (Fig. 1). The cells are Gram-positive, coccoid, and approximately 2.0 μM in width and 1.8 μM in length (Fig. 2). This pairwise 16S rRNA gene sequence similarity value suggested that strain R3.8 is A. alpinus , following the species delineation threshold recommended by Stackebrandt and Ebers [7]. API test strips (API 20 E, API 20 E and API ZYM) incubated at 20 °C were used according to the manufacturer’s instructions to determine the physiological and biochemical characteristics as well as enzyme activities of strain R3.8. The results were compared with type strain of A. alpinus strain S6-3T. Strain R3.8 showed a closely similar biochemical profile with S6-3T in all the API tests. Both strains did not produce catalase and cytochrome oxidase and were able to hydrolyze aesculin. Both strains were positive for activities of acidic phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, α-glucosidase, ß-glucosidase, α-galactosidase, ß-galactosidase, ß-glucuronidase and α-mannosidase, and could utilizes D-glucose, lactose, L-arabinose, maltose, D-mannose, D-mannitol and N-acetylglucosamine as sole carbon source. Both strains were negative in indole production, H2S production and citrate utilization. Both were also negative for activities of arginine dihydrolase, lysine dihydrolase, ornithine dihydrolase, lipase (C14), N-acetyl-ß-glucosaminidase, trypsin, α-chymotrypsin, and α-fucosidase, and negative for the fermentation of glucose, mannitol, sucrose, inositol, sorbitol, rhamnose, melibiose, and amygdalin. However, strain R3.8 was not able to hydrolyze urea, unlike strain S6-3T, in both API 20 E and API 20 NE tests. In the API 20 NE test, strain R3.8 was positive for nitrate reduction, differing from strain S6-3T. In the API 20 E test, strain R3.8 was positive for fermentation of L-arabinose but strain S6-3T was negative. In the API ZYM test, strain R3.8 did not produced alkaline phosphatase and naphthol-AS-BI- phosphohydrolase as produced by strain S6-3T.

Fig. 1
figure 1

Neighbour-joining phylogenetic tree based on complete 16S rRNA gene sequences of Arthrobacter alpinus strain R3.8 and closely related species of the genus Arthrobacter. Bootstrap values (expressed as percentages of 1000 replications) are shown at the branching points. Bar, 1 nt substitutions per 100 nt

Fig. 2
figure 2

Transmission electron micrograph of Arthrobacter alpinus strain R3.8. The image was taken under a scanning transmission electron microscope (STEM, LIBRA 120; Carl Zeiss AG, Germany) at an operation voltage of 80 kV. The scale bar represents 500 nm

Minimum Information about the Genome Sequence of A. alpinus strain R3.8 is summarized in Table 1.

Table 1 Classification and general features of Arthrobacter alpinus R3.8 according to the MIGS recommendations [34]

Genome sequencing information

Genome project history

The genome of A. alpinus strain R3.8 was sequenced to study its bioremediation properties, specifically focusing on naphthalene biodegradation. The assembled and annotated genome of A. alpinus strain R3.8 described in this paper has been deposited in GenBank (accession number of CP12677.1), the KEGG database (entry number of T04095) and the JGI portal with GOLD ID of Gp0124186 and IMG taxon ID of 2645727552. Sequencing, assembly and annotation of the complete genome were performed by the UM Omics Centre, University of Malaya, Malaysia. A summary of the project information is shown in Table 2.

Table 2 Project information

Growth conditions and genomic DNA preparation

A. alpinus strain R3.8 was grown aerobically in 5.0 ml LB broth at 16 °C. A volume of 1.0 ml was then centrifuged at 2500 x g for 5 min at 4 °C and genomic DNA was extracted and purified using the MasterPure™ Gram positive DNA purification kit (Epicenter Technologies, USA) following the manufacturer’s instructions. The purity and quality of the genomic DNA obtained were assessed using a NanoDrop 2000 UV-Vis spectrophotometer (Thermo Scientific, USA) and quantified using Qubit 2.0 fluorometer (Life Technologies, MA, USA).

Genome Sequencing and Assembly

The sheared genomic DNA of A. alpinus strain R3.8 was constructed into a 20 kb SMRTbell template library following the ‘Procedure and Checklist - 20 kb Template Preparation Using BluePippin™ Size-Selection System’ protocol [8, 9]. The purified and size-selected SMRTbell library was sequenced in five SMRT cells using P6C4 chemistry on a PacBio RS II sequencing system (Pacific Biosciences, USA). Sub-reads generated from the raw sequencing reads following adapter-removal were used as input data for de novo assembly using Hierarchical Genome Assembly Process version 2 [10]. The assembly of the A. alpinus strain R3.8 genome was based on 64,388 quality reads with a mean length of 7,335 bp resulting in a single circular chromosome consisting of 4,046,453 bp with 101.74-fold overall coverage.

Genome Annotation

Gene prediction and annotation were performed using the Rapid Annotation Search Tool [11], Rapid Prokaryotic Genome Annotation [12] and NCBI Prokaryotic Genome Annotation Pipeline based on the best-placed reference protein set and GeneMarkS+. Additional gene identification was made using the KEGG database [13], Carbohydrate-Active Enzymes Database ([14], Pathosystem Resource Integration Center [15], and IMG ER [16].

Genome Properties

With 101.74 fold of coverage, the genome of A. alpinus strain R3.8 was assembled into a 4046,4553 bp circular chromosome with an average GC content of 62.2% (Table 3). No plasmid sequence was identified in this assembly (Table 1 and Fig. 3). A total of 3697 genes was predicted of which 3268 genes were identified as protein coding genes. A total of 69 RNA genes were also identified consisting of 18 rRNA (6 5S rRNA, 6 16S rRNA, and 6 23S rRNA) and 51 tRNA genes. 169 (5.17%) were designated as pseudo genes, 57 (1.74%) genes were frameshifted (Table 3). Furthermore, 61.54% of the predicted genes (3892) are represented by COG functional categories. Distribution of these genes and their percentage representation are listed in Table 4. The genome sequence is deposited in GenBank (accession number of CP12677.1), from which the genome sequence data can be accessed in the format of FASTA, annotated GenBank flat file, graphical and ASN.1 file.

Table 3 Genome statistics of Arthrobacter alpinus R3.8
Fig. 3
figure 3

The genome graphical map of strain R3.8. From the outside to the center: genes on forward stand and genes on reverse strand (color by COG categories see legend), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew

Table 4 Number of genes associated with general COG functional categories

Insights from the genome sequence

Functional annotation results of this genome are accessible from the complete genome directory of the KEGG ORGANISMS database with the organism prefix of aaq. Further, through the aaq hyperlink, cross-reference information is available in the form of protein, and small-molecules interaction network maps, BRITE biological systems hierarchical classifications, KEGG modules, and a whole genome map which can be visualized using genome map browser can be accessed through the subdirectory panel.

Cold-adaptation genes

An antifreeze protein [AOC05_08780], a gene encoding a protein with ice-nucleation activity reported to be secreted by psychrotolerant bacterium into the surrounding medium at low temperatures to prevent the formation of ice crystals [17,18,19], was identified in the genome. Various temperature stress response genes were also identified. For example, the cold shock protein family that has been shown to allow bacterial response to rapid temperature shift, allowing bacteria cells to function to survive above their thermal optimum by serving as nucleic acid chaperones that may prevent the formation of secondary structures in mRNA at low temperature [20]. The NCBI locus tags for the cold shock proteins that were identified are AOC05_RS02130, AOC05_13125, and AOC05_RS01570.

Biodegradation genes

Naphthalene is a group C (possible human carcinogen) benzenoid polycyclic aromatic hydrocarbon and is a pollutant widely encountered in nature [21, 22]. In 1990, naphthalene was recognized as one of the priority pollutants required to be controlled by the Environmental Protection Agency of the United States. In the genome of A. alpinus strain R3.8, various genes that are involved in naphthalene biodegradation were identified, including salicylate 1-monooxygenase [AOC05_08330], imidazole glycerol phosphate synthase cyclase [AOC05_05535] that is involved in 1- and 2-methylnaphthalene degradation, and other genes involved in 1,4-dichlorobenzene degradation, namely enoyl-CoA hydratase [AOC05_00980, AOC05_05365, AOC05_11215, AOC05_11270, AOC05_11290, AOC05_11310, AOC05_13700, AOC05_13710], alkaline phosphatase [AOC05_01425, AOC05_03310, AOC05_12520], nitrilotriacetate monooxygenase [AOC05_10370] and aliphatic amidase amiE [AOC05_16895].

Furthermore, two genes involved in the production of urease were also identified in the genome of A. alpinus strain R3.8, urease alpha subunit [AOC05_06080] and urease gamma subunit [AOC05_18490]). Urease is important in catalyzing one of the metabolic pathways involved in microbial-induced calcite precipitation. MICP is a promising approach in the containment of heavy metals such as lead and cadmium in contaminated soils [23, 24].

Various other xenobiotic biodegradation genes and pathways of A. alpinus strain R3.8 are available from the PATRIC server.

Genes with chitinolytic and N-acetylglucosamine utilization properties

Chitinase is a biotechnologically-important enzyme widely used in waste management industries for the degradation of chitinous waste into simpler depolymerized substances [25], in agricultural industries for engineering of transgenic crops with resistance to fungal infection [26] and in healthcare industries for the therapeutic treatment of fungal infections [25, 27]. A range of recent tudies have identified and characterized novel cold-active chitinase enzymes with higher catalytic efficiency at low temperatures [28,29,30,31].

The full chitinolytic potential of A. alpinus strain R3.8 was also identified here, with various genes involved in chitin and N-acetylglucosamine utilization being identified, including beta-hexosaminidase (EC 3.2.1.52) [AOC05_10575, AOC05_02140], eukaryotic type N-acetylglucosamine kinase (EC 2.7.1.59) [AOC05_12050], PTS system, N-acetylglucosamine (EC 2.7.1.69) [AOC05_12345], N-acetylglucosamine-6-phosphate deacetylase (EC 3.5.1.25) [AOC05_15120], eukaryotic type N-acetylglucosamine kinase (EC 2.7.1.59) [AOC05_15120], chitinase (EC 3.2.1.14) [AOC05_02965], N-acetyl-glucosamine kinase 2, ROK family (EC 2.7.1.59) [AOC05_03295], transcriptional regulator of N-acetylglucosamine utilization, GntR family [AOC05_07215] and glucosamine-6-phosphate deaminase (EC 3.5.99.6) [AOC05_10045].

Potential plant growth promoting properties

Application of psychrotrophic PGP bacteria to vegetation can promote growth and improve cold tolerance of crops [32]. From the RAST analysis, a total of 22 PGP genes were identified in the genome of A. alpinus strain R3.8. The genes that are involved in the glutamine synthetase (GS)-glutamate synthase (GOGAT) pathway of bacterial ammonia assimilation are glutamine synthetase (GS) [AOC05_04790] and glutamate synthase (GOGAT) [AOC05_05585]. Full details of these genes, including nitrogen regulatory protein [AOC05_18400] and ammonium transporter [AOC05_09335] are available in Additional file 1: Table S1. Furthermore, five genes involved in plant hormone biosynthesis, indole acetic acid biosynthesis, including monoamine oxidase [AOC05_17530], tryptophan synthase [AOC05_05570, AOC05_05575], anthranilate phosphoribosyltransferase [AOC05_07190] and N-(5′-phosphoribosyl) anthranilate isomerase [AOC05_12350] were identified. Production of bacterial IAA is important to assist plants to overcome abiotic stresses and inhibitory compounds, and thus contributes to plant growth stimulation [33]. Several other PGP-relevant genes involved in trehalose synthesis [AOC05_15010, AOC05_00140, AOC05_00145, AOC05_00495, and AOC05_00500] and involved in spermidine synthesis [AOC05_16565] were also identified in the genome.

Conclusions

We report the complete genome sequence of Arthrobacter alpinus strain R3.8 that was originally isolated from the soil collected from Rothera Point, Adelaide Island, maritime Antarctica. The strain was sequenced to explore its biotechnological potential. By analyzing the complete genome of A. alpinus strain R3, we identified genes involved in xenobiotic biodegradation and metabolism, and chitin utilization, as well as genes that potentially promote plant growth. Further comparative genomic studies with related isolates together with functional studies will provide better understanding of the potential biotechnological value of this strain.

Abbreviations

HGAP:

Hierarchical Genome Assembly Process

IAA:

Indole acetic acid

MICP:

Microbial-induced calcite precipitation

MIGS:

Minimum Information about the Genome Sequences

PATRIC:

Pathosystem Resource Integration Center

PGP:

Plant Growth Promoting

RAST:

Rapid Prokaryotic Genome Annotation

SMRT:

Single Molecule Real Time

References

  1. Huston AL. Biotechnological aspects of cold-adapted enzymes. In: Psychrophiles: from biodiversity to biotechnology. Springer: Heidelberg-Berlin, Germany; 2008. p. 347–363.

  2. Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, D’Amico S, Dumont J, Garsoux G, Georlette D. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 2000;18(3):103–7.

    Article  CAS  PubMed  Google Scholar 

  3. Russell NJ. Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. In: Biotechnology of Extremophiles. Springer: Heidelberg-Berlin, Germany; 1998. p. 1–21.

  4. Cavicchioli R, Charlton T, Ertan H, Omar SM, Siddiqui KS, Williams TJ. Biotechnological uses of enzymes from psychrophiles. Microb Biotechnol. 2011;4(4):449–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. See-Too WS, Ee R, Lim YL, Convey P, Pearce DA, Yin WF, Chan KG. AidP, a novel N-acyl homoserine lactonase gene from Antarctic Planococcus sp. Sci Rep. 2017;7:42968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. See-Too WS, Ee R, Madhaiyan M, Kwon SW, Tan JY, Lim YL, Convey P, Pearce DA, Yin WF, Chan KG. Planococcus versutus sp nov, isolated from Antarctic soil. Int J Syst Evol Microbiol. 2016;67:944–50.

    Google Scholar 

  7. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today. 2006;33(4):152.

    Google Scholar 

  8. See-Too WS, Convey P, Pearce DA, Lim YL, Ee R, Yin WF, Chan KG. Complete genome of Planococcus rifietoensis M8T, a halotolerant and potentially plant growth promoting bacterium. J Biotechnol. 2016;221:114–5.

    Article  CAS  PubMed  Google Scholar 

  9. See-Too WS, Tan JY, Ee R, Lim YL, Convey P, Pearce DA, Yin WF, Chan KG. De novo assembly of complete genome sequence of Planococcus kocurii ATCC 43650T, a potential plant growth promoting bacterium. Mar Genomics. 2016;28:33–5.

    Article  PubMed  Google Scholar 

  10. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods. 2013;10(6):563–9.

    Article  CAS  PubMed  Google Scholar 

  11. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9(1):1.

    Article  Google Scholar 

  12. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9.

    Article  CAS  PubMed  Google Scholar 

  13. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2015;44(D1):457–62.

    Article  Google Scholar 

  14. Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42(D1):490–5.

    Article  Google Scholar 

  15. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 2014;42(D1):581–91.

    Article  Google Scholar 

  16. Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics. 2009;25(17):2271–8.

    Article  CAS  PubMed  Google Scholar 

  17. Duman JG, Olsen TM. Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology. 1993;30(3):322–8.

    Article  Google Scholar 

  18. Sun X, Griffith M, Pasternak JJ, Glick BR. Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol. 1995;41(9):776–84.

    Article  CAS  PubMed  Google Scholar 

  19. Xu H, Griffith M, Patten CL, Glick BR. Isolation and characterization of an antifreeze protein with ice nucleation activity from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol. 1998;44(1):64–73.

    Article  CAS  Google Scholar 

  20. Keto-Timonen R, Hietala N, Palonen E, Hakakorpi A, Lindström M, Korkeala H: Cold Shock Proteins: A Minireview with Special Emphasis on Csp-family of Enteropathogenic Yersinia. Front. Microbiol. 2016; 7.

  21. Pathak H, Kantharia D, Malpani A, Madamwar D. Naphthalene degradation by Pseudomonas sp. HOB1: in vitro studies and assessment of naphthalene degradation efficiency in simulated microcosms. J Hazard Mater. 2009;166(2):1466–73.

  22. Buckpitt A, Kephalopoulos S, Koistinen K, Kotzias D, Morawska L, Sagunski H: Naphthalene. 2010.

  23. Achal V, Pan X, Zhang D, Fu QL. Bioremediation of Pb-contaminated soil based on microbially induced calcite precipitation. J Microbiol Biotechnol. 2012;22(2):244–7.

    Article  PubMed  Google Scholar 

  24. Kang CH, Choi JH, Noh J, Kwak DY, Han SH, So JS. Microbially induced calcite precipitation-based sequestration of strontium by Sporosarcina pasteurii WJ-2. Appl Biochem Biotechnol. 2014;174(7):2482–91.

    Article  CAS  PubMed  Google Scholar 

  25. Hamid R, Khan MA, Ahmad M, Ahmad MM, Abdin MZ, Musarrat J, Javed S. Chitinases: an update. J Pharm Bioallied Sci. 2013;5(1):21.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Melchers LS, Stuiver MH. Novel genes for disease-resistance breeding. Curr Opin Plant Biol. 2000;3(2):147–52.

    Article  CAS  PubMed  Google Scholar 

  27. Oranusi NA, Trinci AP. Growth of bacteria on chitin, fungal cell walls and fungal biomass, and the effect of extracellular enzymes produced by these cultures on the antifungal activity of amphotericin B. Microbios. 1984;43(172):17–30.

    Google Scholar 

  28. Mavromatis K, Feller G, Kokkinidis M, Bouriotis V. Cold adaptation of a psychrophilic chitinase: a mutagenesis study. Protein Eng. 2003;16(7):497–503.

    Article  CAS  PubMed  Google Scholar 

  29. Kuddus M. Statistical optimization of cold-active chitinase production by mutagenized cells of multi-enzyme producing Bacillus cereus GA6. Rendiconti Lincei. 2015;26(3):271–80.

    Article  Google Scholar 

  30. Ramli AN, Mahadi NM, Rabu A, Murad AM, Bakar FD, Illias RM. Molecular cloning, expression and biochemical characterisation of a cold-adapted novel recombinant chitinase from Glaciozyma antarctica PI12. Microb Cell Factories. 2011;10(1):1.

    Article  Google Scholar 

  31. Kim D, Park HJ, Kim IC, Yim JH. A new approach for discovering cold-active enzymes in a cell mixture of pure-cultured bacteria. Biotechnol Lett. 2014;36(3):567–73.

    Article  CAS  PubMed  Google Scholar 

  32. Barka EA, Nowak J, Clément C. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol. 2006;72(11):7246–52.

    Article  CAS  Google Scholar 

  33. Bianco C, Defez R. Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot. 2009;60(11):3097–107.

    Article  CAS  PubMed  Google Scholar 

  34. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26(5):541–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci. 1990;87(12):4576–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Goodfellow M: Phylum XXVI Actinobacteria phyl. nov. Bergey’s Manual of Systematic Bacteriology. Edited by: Goodfellow M, Kampfer P, Busse HJ, Tru-jillo ME, Suzuki K, Ludwig W, Whitman WB. 2012, 33–34. 2.

  37. Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Evol Microbiol. 1997;47(2):479–91.

    Google Scholar 

  38. Zhi XY, Li WJ, Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol. 2009;59(3):589–608.

    Article  CAS  PubMed  Google Scholar 

  39. Skerman VBD, McGowan V, Sneath PHA. Approved lists of bacterial names. Int J Syst Evol Microbiol. 1980;30(1):225–420.

    Article  Google Scholar 

  40. Buchanan R. Studies in the nomenclature and classification of the bacteria II. The primary subdivisions of the schizomycetes. J Bacteriol. 1917;2(2):155–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Pribram E. A contribution to the classification of microorganisms. J Bacteriol. 1929;18(6):361.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang DC, Schumann P, Liu HC, Xin YH, Zhou YG, Schinner F, Margesin R. Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from alpine soil. Int J Syst Evol Microbiol. 2010;60(9):2149–53.

    Article  CAS  PubMed  Google Scholar 

  43. Conn H, Dimmick I. Soil bacteria similar in morphology to Mycobacterium and Corynebacterium. J Bacteriol. 1947;54(3):291.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the University of Malaya High Impact Research Grants (UM-MOHE HIR Grant UM.C/625/1/HIR/MOHE/CHAN/14/1, Grant No. H-50001-A000027; UM-MOHE HIR Grant UM.C/625/1/HIR/MOHE/CHAN/01, Grant No. A-000001-50001) awarded to Kok-Gan Chan. Peter Convey is supported by NERC core funding to the British Antarctic Survey’s ‘Biodiversity, Evolution and Adaptation’ Team.

Author information

Authors and Affiliations

Authors

Contributions

WSST conceived and designed the experiments. WSST and YLL performed the sequencing and assembly experiments. WSST drafted the manuscript, with input and revisions from RE, YLL, PC, DP, TBMM, WFY and KGC. All authors commented on the manuscript before submission. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Kok Gan Chan.

Ethics declarations

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.

Additional file

Additional file 1:

Table S1. Genes involved in chitin degradation identified from RAST analysis. (DOCX 18 kb)

Rights and permissions

Open Access This 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

See-Too, WS., Ee, R., Lim, YL. et al. Complete genome of Arthrobacter alpinus strain R3.8, bioremediation potential unraveled with genomic analysis. Stand in Genomic Sci 12, 52 (2017). https://doi.org/10.1186/s40793-017-0264-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s40793-017-0264-0

Keywords