Skip to main content
Log in

Pseudomonas nanhaiensis sp. nov., a lipase-producing bacterium isolated from deep-sea sediment of the South China Sea

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A bacterial lipase producing bacterium, designated SCS 2–3, was isolated from deep-sea sediment of the South China Sea. Phylogenetic analysis based on the 16S rRNA sequence revealed that strain SCS2-3 belonged to the genus Pseudomonas and had 98.56% similarity to P. xinjiangensis NRRL B-51270T as the closest relative strain. MLSA using four protein-coding genes (dnaK, gyrA, recA, and rpoB) showed strain SCS 2–3 to form a separate branch. ANI and in silico DDH values between strain SCS 2–3 and related type strains of Pseudomonas were less than 81.51% and 23.80%, respectively. Genome comparison showed that strain SCS 2–3 shared 1875 core gene families with other eight closely related type strains in Pseudomonas, and the number of strain-unique genes was 263. Through gene annotations, genes related to lipase were found in the genome. Furthermore, a combination of phenotypic, chemotaxonomic, phylogenetic and genotypic data clearly indicated that strain SCS 2–3 represents a novel species of the genus Pseudomonas, for which the name Pseudomonas nanhaiensis sp. nov. is proposed. The type strain is SCS 2–3T (= GDMCC 1.2219T = JCM 34440T).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bairoch A, Apweiler R (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33:W451–W454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buck JD (1982) Nonstaining (KOH) method for determination of gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan PP, Lowe TM (2019) tRNAscan-SE: searching for tRNA genes in genomic sequences. Gene prediction. Springer, New York, pp 1–14

    Google Scholar 

  • Chaudhari NM, Gupta VK, Dutta C (2016) BPGA-an ultra-fast pan-genome analysis pipeline. Sci Rep 6:1–10

    Article  CAS  Google Scholar 

  • Consortium U (2019) UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 47:D506–D515

    Article  CAS  Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679

    Article  CAS  PubMed  Google Scholar 

  • Driscoll JA, Brody SL, Kollef MH (2007) The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67:351–368

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    Article  CAS  PubMed  Google Scholar 

  • George M, Julia A, Timothy G (2005) Bergey’s manual of systematic bacteriology 2nded, vol 2. Springer, New York

    Google Scholar 

  • Gilbert EJ (1993) Pseudomonas lipases: biochemical properties and molecular cloning. Enzyme Microb Technol 15:634–645

    Article  CAS  PubMed  Google Scholar 

  • Guo Q, Zhou Z, Zhang L, Zhang C, Chen M, Wang B, Lin M, Wang W, Zhang W, Li X (2020) Skermanella pratensis sp. Nov. isolated from meadow soil, and emended description of the genus skermanella. Int J Syst Evol Microbiol 70(3):1605–1609

    Article  CAS  PubMed  Google Scholar 

  • Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. Appl Microbiol Biotechnol 64:763–781

    Article  CAS  PubMed  Google Scholar 

  • He T, Li Z, Sun Q, Xu Y, Ye Q (2016) Heterotrophic nitrification and aerobic denitrification by Pseudomonas tolaasii Y-11 without nitrite accumulation during nitrogen conversion. Bioresour Technol 200:493–499

    Article  CAS  PubMed  Google Scholar 

  • Hung JH, Weng Z (2016) Sequence alignment and homology search with BLAST and ClustalW. Cold Spring Harb Protoc 2016(11). https://doi.org/10.1101/pdb.prot093088

  • Hwang CY, Zhang GI, Kang S-H, Kim HJ, Cho BC (2009) Pseudomonas pelagia sp. nov., isolated from a culture of the Antarctic green alga Pyramimonas gelidicola. Int J Syst Evol Microbiol 59:3019–3024

    Article  CAS  PubMed  Google Scholar 

  • Jaeger K, Dijkstra B, Reetz M (1999) Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu Rev Microbiol 53:315–351

    Article  CAS  PubMed  Google Scholar 

  • Jensen LJ, Julien P, Kuhn M, von Mering C, Muller J, Doerks T, Bork P (2007) eggNOG: automated construction and annotation of orthologous groups of genes. Nucleic Acids Res 36:D250–D254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462

    Article  CAS  PubMed  Google Scholar 

  • Ke X, Feng S, Wang J, Lu W, Zhang W, Chen M, Lin M (2019) Effect of inoculation with nitrogen-fixing bacterium Pseudomonas stutzeri A1501 on maize plant growth and the microbiome indigenous to the rhizosphere. Syst Appl Microbiol 42:248–260

    Article  CAS  PubMed  Google Scholar 

  • Khan NH, Ahsan M, Taylor WD, Kogure K (2010) Culturability and survival of marine, freshwater and clinical Pseudomonas aeruginosa. Microbes Environ 25(4):266–274

    Article  PubMed  Google Scholar 

  • Kim KK, Song HK, Shin DH, Hwang KY, Suh SW (1997) The crystal structure of a triacylglycerol lipase from Pseudomonas cepacia reveals a highly open conformation in the absence of a bound inhibitor. Structure 5:173–185

    Article  CAS  PubMed  Google Scholar 

  • Kim K-H, Roh SW, Chang H-W, Nam Y-D, Yoon J-H, Jeon CO, Oh H-M, Bae J-W (2009) Pseudomonas sabulinigri sp. nov., isolated from black beach sand. Int J Syst Evol Microbiol 59:38–41

    Article  CAS  PubMed  Google Scholar 

  • Kouker G, Jaeger K-E (1987) Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53:211–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee I, Kim YO, Park S-C, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wang L-H, Xiang F-G, Ding W-L, Xi L-J, Wang M-Q, Xiao Z-J, Liu J-G (2020) Pseudomonas phragmitis sp. nov., isolated from petroleum polluted river sediment. Int J Syst Evol Microbiol 70:364–372

    Article  PubMed  Google Scholar 

  • Liu M, Luo X, Zhang L, Dai J, Wang Y, Tang Y, Li J, Sun T, Fang C (2009) Pseudomonas xinjiangensis sp. nov., a moderately thermotolerant bacterium isolated from desert sand. Int J Syst Evol Microbiol 59:1286–1289

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Li M, Yan Y (2017) Heterologous expression and characterization of a new lipase from Pseudomonas fluorescens Pf0–1 and used for biodiesel production. Sci Rep 7(1):15711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  CAS  PubMed  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1:2047-2217X

    Article  Google Scholar 

  • Ma J, Xu L, Jia L (2012) Degradation of polycyclic aromatic hydrocarbons by Pseudomonas sp. JM2 isolated from active sewage sludge of chemical plant. J Environ Sci 24:2141–2148 (China)

    Article  CAS  Google Scholar 

  • Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. PNAS 95:3140–3145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:1–14

    Article  Google Scholar 

  • Mulet M, Sánchez D, Rodríguez AC, Nogales B, Bosch R, Busquets A, Gomila M, Lalucat J, García-Valdés E (2018) Pseudomonas gallaeciensis sp. nov., isolated from crude-oil-contaminated intertidal sand samples after the Prestige oil spill. Syst Appl Microbiol 41:340–347

    Article  CAS  PubMed  Google Scholar 

  • Nagarajan S (2012) New tools for exploring “old friends—microbial lipases.” Appl Biochem Biotechnol 168:1163–1196

    Article  CAS  PubMed  Google Scholar 

  • Nardini M, Lang DA, Liebeton K, Jaeger K-E, Dijkstra BW (2000) Crystal structure of Pseudomonas aeruginosa lipase in the open conformation: the prototype for family I. 1 of bacterial lipases. J Biol Chem 275:31219–31225

    Article  CAS  PubMed  Google Scholar 

  • Noble M, Cleasby A, Johnson L, Egmond M, Frenken L (1993) The crystal structure of triacylglycerol lipase from Pseudomonas glumae reveals a partially redundant catalytic aspartate. FEBS Lett 331:123–128

    Article  CAS  PubMed  Google Scholar 

  • Novik G, Savich V, Kiseleva E (2015) An insight into beneficial Pseudomonas bacteria. Microbiol Agric Human Health 1:73–105

    Google Scholar 

  • Oueslati M, Mulet M, Gomila M, Berge O, Hajlaoui MR, Lalucat J, Sadfi-Zouaoui N, García-Valdés E (2019) New species of pathogenic Pseudomonas isolated from citrus in Tunisia: proposal of Pseudomonas kairouanensis sp. nov. and Pseudomonas nabeulensis sp. nov. Syst Appl Microbiol 42:348–359

    Article  CAS  PubMed  Google Scholar 

  • Pandey A, Benjamin S, Soccol CR, Nigam P, Krieger N, Soccol VT (1999) The realm of microbial lipases in biotechnology. Biotechnol Appl Biochem 29:119–131

    CAS  PubMed  Google Scholar 

  • Peix A, Ramírez-Bahena M-H, Velázquez E (2009) Historical evolution and current status of the taxonomy of genus Pseudomonas. Infect Genet Evol 9:1132–1147

    Article  PubMed  Google Scholar 

  • Phukon LC, Chourasia R, Kumari M, Godan TK, Sahoo D, Parameswaran B, Rai AK (2020) Production and characterisation of lipase for application in detergent industry from a novel Pseudomonas helmanticensis HS6. Bioresour Technol 309:123352

    Article  CAS  PubMed  Google Scholar 

  • Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romanenko LA, Uchino M, Falsen E, Frolova GM, Zhukova NV, Mikhailov VV (2005) Pseudomonas pachastrellae sp. nov., isolated from a marine sponge. Int J Syst Evol Microbiol 55:919–924

    Article  CAS  PubMed  Google Scholar 

  • Rosenau F, Jaeger K-E (2000) Bacterial lipases from Pseudomonas: regulation of gene expression and mechanisms of secretion. Biochimie 82:1023–1032

    Article  CAS  PubMed  Google Scholar 

  • Spencer DF, Schnare MN, Gray MW (1984) Pronounced structural similarities between the small subunit ribosomal RNA genes of wheat mitochondria and Escherichia coli. PNAS 81:493–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genom 14:1–8

    Article  CAS  Google Scholar 

  • Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296–W303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wayne L, Brenner D, Colwell R, Grimont P, Kandler O, Krichevsky M, Moore L, Moore W, Murray R, Stackebrandt E (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 37:463–464

    Article  Google Scholar 

  • Wei Y, Mao H, Xu Y, Zou W, Fang J, Blom J (2018) Pseudomonas abyssi sp. nov., isolated from the abyssopelagic water of the Mariana Trench. Int J Syst Evol Microbiol 68:2462–2467

    Article  CAS  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Lu W, Wang J, Chen M, Zhang W, Lin M, Zhou Z, Liu Z (2021) Characterization of estdr4, a novel cold-adapted insecticides-metabolizing esterase from Deinococcus radiodurans. Appl Sci 11(4):1864

    Article  CAS  Google Scholar 

  • Zhao X, El-Zahab B, Brosnahan R, Perry J, Wang P (2007) An organic soluble lipase for water-free synthesis of biodiesel. Appl Biochem Biotechnol 143:236–243

    Article  CAS  PubMed  Google Scholar 

  • Zhong Z-P, Liu Y, Hou T-T, Liu H-C, Zhou Y-G, Wang F, Liu Z-P (2015) Pseudomonas salina sp. nov., isolated from a salt lake. Int J Syst Evol Microbiol 65:2846–2851

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by National Key R&D Program of China (No.2018YFA0901000, 2018YFA0901003), the National Transgenic Major Program of China (No. 2019ZX08010-004), the National Natural Science Foundation of China (No. 31930004). We also appreciate the support of the Agricultural Science and Technology Innovation Program of CAAS (No. CAAS-ZDRW202009).

Author information

Authors and Affiliations

Authors

Contributions

Z.Z. and W.Z. designed research and project outline. Y.P., Y.Z., MR.C., and M.C. performed isolation, deposition and polyphasic taxonomy. Y.P. and Y.Y. performed genome analysis. W.L. and W.Z. contributed to the polar lipid analysis. Y.P. and Z.Z. drafted the manuscript. M.L. revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Wei Zhang or Zhengfu Zhou.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1151 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pang, Y., Zhang, Y., Chen, M. et al. Pseudomonas nanhaiensis sp. nov., a lipase-producing bacterium isolated from deep-sea sediment of the South China Sea. Antonie van Leeuwenhoek 114, 1791–1804 (2021). https://doi.org/10.1007/s10482-021-01639-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-021-01639-y

Keywords

Navigation