, Volume 87, Issue 6, pp 796–805 | Cite as

Bacteria from Poorly Studied Phyla as a Potential Source of New Enzymes: β-Galactosidases from Planctomycetes and Verrucomicrobia

  • D. G. Naumoff
  • S. N. Dedysh


Here, we present a phylogenetic analysis of a large group of the nearest homologues of a β-galactosidase, recently cloned from a soil metagenome and representing a new family of glycoside hydrolases. These proteins form an independent subfamily of hypothetical β-galactosidases and are almost exclusively represented in bacteria of the poorly studied phyla Planctomycetes and Verrucomicrobia, as well as Bacteroidetes. The phylogenetic tree of this subfamily consists of eleven highly stable clusters of branches, probably resulting from a series of gene duplications. An analysis of the tree topology suggested that the corresponding genes first evolved in Planctomycetes and most gene duplications occurred within this phylum. Later, these genes spread to several other bacterial phyla through horizontal transfers, the most numerous being transfers to Verrucomicrobia. The genomes of most Planctomycetes contain multiple paralogues of these genes of a different origin: in some cases, the horizontal transfers played a key role, while in other cases gene duplications played a key role. The importance of poorly studied groups of prokaryotes as a source of novel glycoside hydrolases is discussed.


glycoside hydrolase β-galactosidase TIGR02604 family Planctomycetes Verrucomicrobia protein phylogenetic tree protein evolution lateral gene transfer search of homologues gene annotation metagenome misannotation 



This work was performed as a part of budget-supported project no. 0104-2018-0034.


  1. 1.
    Boedeker, C., Schüler, M., Reintjes, G., Jeske, O., van Teeseling, M.C.F., Jogler, M., Rast, P., Borchert, D., Devos, D.P., Kucklick, M., Schaffer, M., Kolter, R., van Niftrik, L., Engelmann, S., Amann, R., et al., Determining the bacterial cell biology of Planctomycetes, Nat. Commun., 2017, vol. 8, art. 14853.CrossRefGoogle Scholar
  2. 2.
    Cabello-Yeves, P.J., Ghai, R., Mehshad, M., Picazo, A., Camacho, A., and Rodriguez-Valera, F., Reconstruction of diverse verrucomicrobial genomes from metagenome datasets of freshwater reservoirs, Front. Microbiol., 2017, vol. 8, art. 2131.CrossRefGoogle Scholar
  3. 3.
    Chandrasekar, B. and van der Hoorn, R.A., Beta-galactosidases in Arabidopsis and tomato–a mini review, Biochem. Soc. Trans., 2016, vol. 44, pp. 150–158.CrossRefGoogle Scholar
  4. 4.
    Cheng, J., Romantsov, T., Engel, K., Doxey, A.C., Rose, D.R., Neufeld, J.D., and Charles, T.C., Functional metagenomics reveals novel β-galactosidases not predictable from gene sequences, PLoS One, 2017, vol. 12, art. e0172545.CrossRefGoogle Scholar
  5. 5.
    Devos, D.P., PVC bacteria: variation of, but not exception to, the Gram-negative cell plan, Trends Microbiol., 2014, vol. 22, pp. 14–20.CrossRefGoogle Scholar
  6. 6.
    Fuerst, J.A., The PVC superphylum: exceptions to the bacterial definition?, Antonie van Leeuwenhoek, 2013, vol. 104, pp. 451–466.CrossRefGoogle Scholar
  7. 7.
    Glöckner, F.O., Kube, M., Bauer, M., Teeling, H., Lombardot, T., Ludwig, W., Gade, D., Beck, A., Borzym, K., Rabus, R., Schlesner, H., Amann, R., and Reinhardt, R., Complete genome sequence of the marine planctomycete Pirellula sp. strain 1, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, pp. 8298–8303.CrossRefGoogle Scholar
  8. 8.
    Haft, D.H., Selengut, J.D., Richter, R.A., Harkins, D., Basu, M.K., and Beck, E., TIGRFAMs and genome properties in 2013, Nucleic Acids Res., 2013, vol. 41 (Database issue), pp. D387–D395.CrossRefGoogle Scholar
  9. 9.
    Hahnke, R.L., Meier-Kolthoff, J.P., García-López, M., Mukherjee, S., Huntemann, M., Ivanova, N.N., Woyke, T., Kyrpides, N.C., Klenk, H.P., and Göker, M., Genome-based taxonomic classification of Bacteroidetes, Front. Microbiol., 2016, vol. 7, art. 2003.CrossRefGoogle Scholar
  10. 10.
    Husain, Q., Beta-galactosidases and their potential applications: a review, Crit. Rev. Biotechnol., 2010, pp. 30, pp. 41–62.Google Scholar
  11. 11.
    Ivanova, A.A., Naumoff, D.G., Miroshnikov, K.K., Liesack, W., and Dedysh, S.N., Comparative genomics of four Isosphaeraceae Planctomycetes: a common pool of plasmids and glycoside hydrolase genes shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and strain SH-PL62, Front. Microbiol., 2017, vol. 8, art. 412.CrossRefGoogle Scholar
  12. 12.
    Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M., and Henrissat, B., The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res., 2014, vol. 42 (Database issue), pp. D490–D495.CrossRefGoogle Scholar
  13. 13.
    Luis, A.S., Briggs, J., Zhang, X., Farnell, B., Ndeh, D., Labourel, A., Baslé, A., Cartmell, A., Terrapon, N., Stott, K., Lowe, E.C., McLean, R., Shearer, K., Schückel, J., Venditto, I., et al., Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides, Nat. Microbiol., 2018, vol. 3, pp. 210–219.CrossRefGoogle Scholar
  14. 14.
    Naumoff, D.G., β-Fructosidase superfamily: homology with some α-L-arabinases and β-D-xylosidases, Prot. Struct. Funct. Genet., 2001, vol. 42, pp. 66–76.CrossRefGoogle Scholar
  15. 15.
    Naumoff, D.G., Development of a hierarchical classification of the TIM-barrel type glycoside hydrolases, Proc. 5th Int. Conf. Bioinformat. Genome Regul. Structure, July 16–22, 2006, Novosibirsk, Russia, 2006, vol. 1, pp. 294–298. ( BGRS_2006_V1_067.pdf).Google Scholar
  16. 16.
    Naumoff, D.G., Furanosidase superfamily: search of homologues, Mol. Biol. (Moscow), 2012, vol. 46, pp. 322–327.CrossRefGoogle Scholar
  17. 17.
    Naumoff, D.G., GH101 family of glycoside hydrolases: subfamily structure and evolutionary connections with other families, J. Bioinform. Comput. Biol., 2010, vol. 8, pp. 437–451.CrossRefGoogle Scholar
  18. 18.
    Naumoff, D.G., Hierarchical classification of glycoside hydrolases, Biochemistry (Moscow), 2011, vol. 76, pp. 622–635.Google Scholar
  19. 19.
    Naumoff, D.G., Hierarchical classification of glycoside hydrolases, FEBS J., 2014, vol. 281, no. S1, p. 569.Google Scholar
  20. 20.
    Naumoff, D.G., Multiple lateral transfers and duplications of genes as sources of diversity of α-L-rhamnosidases in Clostridium methylpentosum DSM5476, Microbiology (Moscow), 2013, vol. 82, pp. 415–422.CrossRefGoogle Scholar
  21. 21.
    Naumoff, D.G. and Dedysh, S.N., Lateral gene transfer between the Bacteroidetes and Acidobacteria: the case of α‑L-rhamnosidases, FEBS Lett., 2012, vol. 586, pp. 3843–3851.CrossRefGoogle Scholar
  22. 22.
    Naumoff, D.G., Ivanova, A.A., and Dedysh, S.N., Phylogeny of β-xylanases from Planctomycetes, Mol. Biol. (Moscow), 2014, vol. 48, pp. 439–447.CrossRefGoogle Scholar
  23. 23.
    Rivas-Marin, E. and Devos, D.P. The paradigms they are a‑Changin’: past, present and future of PVC bacteria research, Antonie van Leeuwenhoek, 2018, vol. 111, pp. 785–799.CrossRefGoogle Scholar
  24. 24.
    Saqib, S., Akram, A., Halim, S.A., and Tassaduq, R., Sources of β-galactosidase and its applications in food industry, 3 Biotech., 2017, vol. 7, no. 1, art. 79.Google Scholar
  25. 25.
    Terrapon, N., Lombard, V., Drula, E., Coutinho, P.M., and Henrissat, B., Chapter 6. The CAZy database/the Carbohydrate-Active Enzyme (CAZy) database: principles and usage guidelines, in A Practical Guide to Using Glycomics Databases, Aoki-Kinoshita, K.F., Ed., Tokyo: Springer, 2017, pp. 117–131.Google Scholar
  26. 26.
    Wagner, M. and Horn, M., The Planctomycetes, Verrucomicrobia, Chlamydia and sister phyla comprise a superphylum with biotechnological and medical relevance, Curr. Opin. Biotechnol., 2006, vol. 17, pp. 241–249.CrossRefGoogle Scholar
  27. 27.
    Ward, N. L., Challacombe, J.F., Janssen, P.H., Henrissat, B., Coutinho, P.M., Wu, M., Xie, G., Haft, D. H., Sait, M., Badger, J., Barabote, R.D., Bradley, B., Brettin, T.S., Brinkac, L.M., Bruce, D., et al., Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils, Appl. Environ. Microbiol., 2009, vol. 75, pp. 2046–2056.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of SciencesMoscowRussia

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