Skip to main content
SpringerLink
Log in

Distribution of 1-aminocyclopropane-1-carboxylate deaminase and d-cysteine desulfhydrase genes among type species of the genus Methylobacterium

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

Abstract

The presence of 1-aminocyclopropane-1-carboxylate (ACC) deaminase determines the ability of bacteria to increase the resistance of plants to various types of stress. The genes of ACC deaminase (acdS) and the closely related enzyme d-cysteine desulfhydrase (dcyD) were searched in type strains of various representatives of the genus Methylobacterium. Using PCR screening and in silico searching in the available complete genome sequences of type strains, the genes were found in 28 of 48 species of the genus. Phylogenetic analysis of amino acid sequences of proteins revealed two large groups of sequences of the AcdS protein and one of the DcyD protein. The distribution of these groups correlates well with the phylogenetic tree based on the sequences of the 16S rRNA genes, which apparently indicates a different evolutionary adaptation to association with plants in the representatives of these groups. For the first time for aerobic methylotrophs it was demonstrated that the gene dcyD encodes d-cysteine desulfhydrase by cloning and recombinant protein characterization.

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
Fig. 4

Similar content being viewed by others

References

  • Austin B, Goodfellow M (1979) Pseudomonas mesophilica, a new species of pink bacteria isolated from leaf surfaces. Int J Syst Evol Microbiol 29(4):373–378

    Google Scholar 

  • Doronina N, Torgonskaya M, Fedorov D, Trotsenko YA (2015) Aerobic methylobacteria as promising objects of modern biotechnology. Appl Biochem Microbiol 51(2):125

    Article  CAS  Google Scholar 

  • Ekimova G, Fedorov D, Doronina N, Trotsenko YA (2015) 1-aminocyclopropane-1-carboxylate deaminase of the aerobic facultative methylotrophic actinomycete Amycolatopsis methanolica 239. Microbiology 84(4):584–586

    Article  CAS  Google Scholar 

  • Fedorov D, Doronina N, Trotsenko YA (2010) Cloning and characterization of indolepyruvate decarboxylase from Methylobacterium extorquens AM1. Biochemistry (Moscow) 75(12):1435–1443

    Article  CAS  Google Scholar 

  • Fedorov D, Doronina N, Trotsenko YA (2011) Phytosymbiosis of aerobic methylobacteria: new facts and views. Microbiology 80(4):443

    Article  CAS  Google Scholar 

  • Fedorov DN, Ekimova GA, Doronina NV, Trotsenko YA (2013) 1-Aminocyclopropane-1-carboxylate (ACC) deaminases from Methylobacterium radiotolerans and Methylobacterium nodulans with higher specificity for ACC. FEMS Microbiol Lett 343(1):70–76

    Article  CAS  Google Scholar 

  • Galbally I, Kirstine W (2002) The production of methanol by flowering plants and the global cycle of methanol. JAtC 43(3):195–229

    CAS  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39

    Article  CAS  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119(3):329–339

    Article  CAS  Google Scholar 

  • Guo H, Xiao T, Zhou H, Xie Y, Shen W (2016) Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38(1):16

    Article  Google Scholar 

  • Hontzeas N, Zoidakis J, Glick BR, Abu-Omar MM (2004) Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: a key enzyme in bacterial plant growth promotion. Biochim Biophys Acta Proteins Proteomics 1703(1):11–19

    Article  CAS  Google Scholar 

  • Ito H, Iizuka H (1971) Taxonomic studies on a radio-resistant Pseudomonas: part XII. Studies on the microorganisms of cereal grain. Agric Biol Chem 35(10):1566–1571

    Google Scholar 

  • Kane SR, Chakicherla AY, Chain PS, Schmidt R, Shin MW, Legler TC, Scow KM, Larimer FW, Lucas SM, Richardson PM (2007) Whole-genome analysis of the methyl tert-butyl ether-degrading beta-proteobacterium Methylibium petroleiphilum PM1. J Bacteriol 189(5):1931–1945

    Article  CAS  Google Scholar 

  • Kang Y-S, Kim J, Shin H-D, Nam Y-D, Bae J-W, Jeon CO, Park W (2007) Methylobacterium platani sp. nov., isolated from a leaf of the tree Platanus orientalis. Int J Syst Evol Microbiol 57(12):2849–2853

    Article  CAS  Google Scholar 

  • Keppler F, Hamilton JT, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439(7073):187–191

    Article  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sa T (2007a) Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226(4):867–876

    Article  CAS  Google Scholar 

  • Madhaiyan M, Kim B-Y, Poonguzhali S, Kwon S-W, Song M-H, Ryu J-H, Go S-J, Koo B-S, Sa T-M (2007b) Methylobacterium oryzae sp. nov., an aerobic, pink-pigmented, facultatively methylotrophic, 1-aminocyclopropane-1-carboxylate deaminase-producing bacterium isolated from rice. Int J Syst Evol Microbiol 57(2):326–331

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Kwon S-W, Sa T-M (2009) Methylobacterium phyllosphaerae sp. nov., a pink-pigmented, facultative methylotroph from the phyllosphere of rice. Int J Syst Evol Microbiol 59(1):22–27

    Article  CAS  Google Scholar 

  • McDonnell L, Plett JM, Andersson-Gunnerås S, Kozela C, Dugardeyn J, Van Der Straeten D, Glick BR, Sundberg B, Regan S (2009) Ethylene levels are regulated by a plant encoded 1-aminocyclopropane-1-carboxylic acid deaminase. Physiol Plant 136(1):94–109

    Article  CAS  Google Scholar 

  • Nagasawa T, Ishii T, Kumagai H, Yamada H (1985) d-Cysteine desulfhydrase of Escherichia coli. Purification and characterization. Eur J Biochem 153(3):541–551

    Article  CAS  Google Scholar 

  • Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS ONE 9(6):e99168

    Article  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants-from the field to the test tube and back. Plant Biol 9(05):582–588

    Article  CAS  Google Scholar 

  • Reasoner DJ, Geldreich E (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49(1):1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272(5):1291–1304

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Soutourina J, Blanquet S, Plateau P (2001) Role of d-cysteine desulfhydrase in the adaptation of Escherichia coli to d-cysteine. J Biol Chem 276(44):40864–40872

    Article  CAS  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, De Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183(1):214–220

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  Google Scholar 

  • Todorovic B, Glick BR (2008) The interconversion of ACC deaminase and d-cysteine desulfhydrase by directed mutagenesis. Planta 229(1):193–205

    Article  CAS  Google Scholar 

  • Van de Poel B, Van Der Straeten D (2014) 1-Aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:640

    PubMed  PubMed Central  Google Scholar 

  • Yamada H, Nagasawa T, Ohkishi H, Kawakami B, Tani Y (1981) Synthesis of d-cysteine from 3-chloro-d-alanine and hydrogen sulfide by 3-chloro-d-alanine hydrogen chloride-lyase (deaminating) of Pseudomonas putida. Biochem Biophys Res Commun 100(3):1104–1110

    Article  CAS  Google Scholar 

  • Zhang H, Hu S-L, Zhang Z-J, Hu L-Y, Jiang C-X, Wei Z-J, Liu J, Wang H-L, Jiang S-T (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60(3):251–257

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The work was supported by the grant of the Russian Fund for Basic Research RFBR 16-04-00381_a.

Author information

Authors and Affiliations

  1. G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms RAS, Prospect Nauki, 5, Pushchino, Moscow Region, Russia, 142290

    Galina A. Ekimova, Dmitry N. Fedorov, Nina V. Doronina & Yuri A. Trotsenko

  2. Pushchino State Institute of Natural Sciences, Prospect Nauki, 5, Pushchino, Moscow Region, Russia, 142290

    Galina A. Ekimova

  3. Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, Kurashiki, Okayama, 710-0046, Japan

    Akio Tani

Authors
  1. Galina A. Ekimova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dmitry N. Fedorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akio Tani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nina V. Doronina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuri A. Trotsenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dmitry N. Fedorov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ekimova, G.A., Fedorov, D.N., Tani, A. et al. Distribution of 1-aminocyclopropane-1-carboxylate deaminase and d-cysteine desulfhydrase genes among type species of the genus Methylobacterium. Antonie van Leeuwenhoek 111, 1723–1734 (2018). https://doi.org/10.1007/s10482-018-1061-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-018-1061-5

Keywords

Search

Navigation