Skip to main content

Advertisement

SpringerLink
Log in

Distribution of dTDP-glucose-4,6-dehydratase gene and diversity of potential glycosylated natural products in marine sediment-derived bacteria

  • Applied Genetics and Molecular Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

To investigate the distribution of dTDP-glucose-4,6-dehydratase (dTGD) gene and diversity of the potential 6-deoxyhexose (6DOH) glycosylated compounds in marine microorganisms, a total of 91 marine sediment-derived bacteria, representing 48 operational taxonomic units and belonging to 25 genera, were screened by polymerase chain reaction. In total, 84% of the strains were dTGD gene positive, suggesting 6DOH biosynthetic pathway is widespread in these marine sediment-derived bacteria. BLASTp results of dTGD gene fragments indicate a high chemical diversity of the potential 6DOH glycosylated compounds. Close phylogenetic relationship occurred between dTGDs involved in the production of same or similar 6DOH glycosylated compounds, suggesting dTGD can be used to predict the structure of potential 6DOH glycosylated compounds produced by new strains. In two cases, where dTGD shared ≥85% amino acid identity and close phylogenetic relationship with their counterparts, 6DOH glycosylated compounds were accurately predicted. Our results demonstrate that phylogenetic analysis of dTGD gene is useful for structure prediction of glycosylated compounds from newly isolated strains and can therefore guide the chemical purification and structure identification process. The rapid identification of strains that possess dTGD gene provides a bioinformatics assessment of the greatest potential to produce glycosylated compounds despite the absence of fully biosynthetic pathways or genome sequences.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24

    Article  CAS  Google Scholar 

  • Deckera H, Gaisserb S, Pelzera S, Schneidera P, Westrichb L, Wohllebena W, Bechtholdb A (1996) A general approach for cloning and characterizing dNDP-glucose dehydratase genes from actinomycetes. FEMS Microbiol Lett 141:195–201

    Article  Google Scholar 

  • Du Y, Li T, Wang YG, Xia H (2004) Identification and functional analysis of dTDP- glucose-4, 6-dehydratase gene and its linked gene cluster in an aminoglycoside antibiotics producer of Streptomyces tenebrarius H6. Curr Microbiol 49:99–107

    Article  CAS  Google Scholar 

  • Haltli BA (2005) Elaiophylin biosynthetic gene cluster. US patent number 7595187

  • Ichinose K, Ozawa M, Itou K, Kunieda K, Ebizuka Y (2003) Cloning, sequencing and heterologous expression of the medermycin biosynthetic gene cluster of Streptomyces sp. AM-7161: towards comparative analysis of the benzoisochromanequinone gene clusters. Microbiol 149:1633–1645

    Article  CAS  Google Scholar 

  • Jacin H, Mishkin AR (1965) Separation of carbohydrates on borate-impregnated silica gel G plates. J Chromatogr 18:170–173

    Article  CAS  Google Scholar 

  • Kaysser L, Lutsch L, Siebenberg S, Wemakor E, Kammerer B, Gust B (2009) Identification and manipulation of the caprazamycin gene cluster lead to new simplified liponucleoside antibiotics and give insights into the biosynthetic pathway. J Biol Chem 284:14987–14996

    Article  CAS  Google Scholar 

  • Kaysser L, Wemakor E, Siebenberg S, Salas JA, Sohng JK, Kammerer B, Gust B (2010) Formation and attachment of the deoxysugar moiety and assembly of the gene cluster for caprazamycin biosynthesis. Appl Environ Microbiol 76:4008–4018

    Article  CAS  Google Scholar 

  • Kirschning A, Bechthold AF, Rohr J (1997) Chemical and biochemical aspects of deoxysugars and deoxysugar oligosaccharides. Top Curr Chem 188:1–84

    Article  CAS  Google Scholar 

  • Liu HW, Thorson JS (1994) Pathways and mechanisms in the biogenesis of novel deoxysugars by bacteria. Annu Rev Microbiol 48:223–256

    Article  CAS  Google Scholar 

  • Liu W, Ahlert J, Gao QJ, Wendt-Pienkowski E, Shen B, Thorson JS (2003) Rapid PCR amplification of minimal enediyne polyketide synthase cassette leads to a predictive familial classification model. PNAS 100:11959–11963

    Article  CAS  Google Scholar 

  • Liu W, Nonaka K, Nie L, Zhang J, Christenson SD, Bae J, Lanen SGV, Zazopoulos E, Farnet CM, Yang CF, Shen B (2005) The neocarzinostatin biosynthetic gene cluster from Streptomyces carzinostaticus ATCC 15944 involving two iterative type I polyketide synthases. Chem Biol 12:293–302

    Article  CAS  Google Scholar 

  • Madduri K, Waldron C, Merlo DJ (2001) Rhamnose biosynthesis pathway supplies precursors for primary and secondary metabolism in Saccharopolyspora spinosa. J Bacteriol 183:5632–5638

    Article  CAS  Google Scholar 

  • McAlpine JB, Bachmann BO, Piraee M, Tremblay S, Alarco AM, Zazopoulos E, Farnet CM (2005) Microbial genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example. J Nat Prod 68:493–496

    Article  CAS  Google Scholar 

  • Miyamoto M, Kawamatsu Y, Kawashima K, Shinohara M, Tanaka K, Tatsuoka S, Nakanishi K (1967) Chromomycin A-2, A-3 and A-4. Tetrahedron 23:421–437

    Article  CAS  Google Scholar 

  • Oh TJ, Mo SJ, Yoon YJ, Sohng JK (2007) Discovery and molecular engineering of sugar-containing natural product biosynthetic pathways in actinomycetes. J Microbiol Biotechnol 17:1909–1921

    CAS  PubMed  Google Scholar 

  • Okabe T, Nomoto K, Funabashi H, Okuda S, Suzuki H, Tanaka N (1985) Lactoquinomycin, a novel anticancer antibiotic. J Antibiot 38:1333–1336

    Article  CAS  Google Scholar 

  • Piepersberg W (1994) Pathway engineering in secondary metabolite-producing actinomycetes. Crit Rev Biotechnol 14:251–285

    Article  CAS  Google Scholar 

  • Poulsena SM, Kofoeda C, Vestera B (2000) Inhibition of the ribosomal peptidyl transferase reaction by the mycarose moiety of the antibiotics carbomycin, spiramycin and tylosin. J Mol Biol 304:471–481

    Article  Google Scholar 

  • Ramos A, Lombó F, Braña AF, Rohr J, Méndez C, Salas JA (2008) Biosynthesis of elloramycin in Streptomyces olivaceus requires glycosylation by enzymes encoded outside the aglycon cluster. Microbiol 154:781–788

    Article  CAS  Google Scholar 

  • Samuel G, Reeves P (2003) Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 338:2503–2519

    Article  CAS  Google Scholar 

  • Schnaitman CA, Klena JD (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Mol Biol Rev 57:655–682

    CAS  Google Scholar 

  • Stockmann M, Piepersberg W (1992) Gene probes for the detection of 6-deoxyhexose metabolism in secondary metabolite-producing Streptomycetes. FEMS Microbiol Lett 90:185–189

    Article  CAS  Google Scholar 

  • Takano S, Hasuda K, Ito A, Koide Y, Ishii F, Haneda I, Chihara S, Koyama Y (1976) A new antibiotic, medermycin. J Antibiot 29:765–768

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Thibodeaux CJ, Melançon CE, Liu HW (2007) Unusual sugar biosynthesis and natural product glycodiversification. Nature 446:1008–1016

    Article  CAS  Google Scholar 

  • Thiem J, Meyer B (1981) Studies on the structure of chromomycin A3 by 1H and 13C nuclear magnetic resonance spectroscopy. Tetrahedron 37:551–558

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Trefzer A, Salasb JA, Bechthold A (1999) Genes and enzymes involved in deoxysugar biosynthesis in bacteria. Nat Prod Rep 16:283–299

    Article  CAS  Google Scholar 

  • Udwary DW, Zeigler L, Asolkar RN, Singan V, Lapidus A, Fenical W, Jensen PR, Moore BS (2007) Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. PNAS 104:10376–10381

    Article  CAS  Google Scholar 

  • Wu XC, Chen WF, Qian CD, Li O, Li P, Wen YP (2007) Isolation and identification of newly isolated antagonistic Streptomyces sp. Strain AP 19-2 producing chromomycins. J Microbiol 45:499–504

    CAS  PubMed  Google Scholar 

  • Xu P, WJ LI, Xu LH, Jiang CL (2003) A microwave-based method for genomic DNA extraction from actinomycetes. Microbiology (Beijing) 30:82–84

    CAS  Google Scholar 

  • Yoshimura Y, Koenuma M, Matsumoto K, Tori K, Terui Y (1988) NMR studies of chromomycins, olivomycins, and their derivatives. J Antibiot 41:53–67

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Professor Yiwen Chu of Sichuan Industrial Institute of Antibiotics for his kind help of assigning the 1H and 13C chemical shift values for chromomycin A3. This work was supported by the Central Public-interest Scientific Institution Basal Research Fund (IMBF20060202) of the Ministry of Finance, Science, and Technology.

Author information

Authors and Affiliations

  1. Key Laboratory of Biotechnology of Antibiotics, Ministry of Health, Institute of Medicinal Biotechnology, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College (PUMC), Beijing, China

    Feifei Chen, Ling Lin, Yi Tan, Hongxia Zhou, Yiguang Wang & Weiqing He

  2. Sichuan Industrial Institute of Antibiotics, Chengdu, China

    Feifei Chen, Lu Wang & Yi Tan

  3. Northeast Agricultural University, Harbin, China

    Ling Lin

  4. Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Yong Wang

Authors
  1. Feifei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ling Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yi Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongxia Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yiguang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Weiqing He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yong Wang or Weiqing He.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

Comparison of dTDP-glucose-4,6-dehydratase involved in the biosynthesis of same or similar 6-deoxyhexose glycosylated compounds (DOC 351 kb)

Supplementary Table 2

1H and 13C NMR data of 16-2A-1(600 MHz, in CD3OD) (DOC 36 kb)

Supplementary Table 3

1H and 13C NMR data of 318-A (400 MHz, in CDCl3) (DOC 63 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, F., Lin, L., Wang, L. et al. Distribution of dTDP-glucose-4,6-dehydratase gene and diversity of potential glycosylated natural products in marine sediment-derived bacteria. Appl Microbiol Biotechnol 90, 1347–1359 (2011). https://doi.org/10.1007/s00253-011-3112-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3112-y

Keywords

Search

Navigation