Skip to main content

Advertisement

Log in

Genome Sequence of Microbulbifer mangrovi DD-13T Reveals Its Versatility to Degrade Multiple Polysaccharides

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Microbulbifer mangrovi strain DD-13T is a novel-type species isolated from the mangroves of Goa, India. The draft genome sequence of strain DD-13 comprised 4,528,106 bp with G+C content of 57.15%. Out of 3479 open reading frames, functions for 3488 protein coding sequences were predicted on the basis of similarity with the cluster of orthologous groups. In addition to protein coding sequences, 34 tRNA genes and 3 rRNA genes were detected. Analysis of nucleotide sequence of predicted gene using a Carbohydrate-Active Enzymes (CAZymes) Analysis Toolkit indicates that strain DD-13 encodes a large set of CAZymes including 255 glycoside hydrolases, 76 carbohydrate esterases, 17 polysaccharide lyases, and 113 carbohydrate-binding modules (CBMs). Many genes from strain DD-13 were annotated as carbohydrases specific for degradation of agar, alginate, carrageenan, chitin, xylan, pullulan, cellulose, starch, β-glucan, pectin, etc. Some of polysaccharide-degrading genes were highly modular and were appended at least with one CBM indicating the versatility of strain DD-13 to degrade complex polysaccharides. The cell growth of strain DD-13 was validated using pure polysaccharides such as agarose or alginate as carbon source as well as by using red and brown seaweed powder as substrate. The homologous carbohydrase produced by strain DD-13 during growth degraded the polysaccharide, ensuring the production of metabolizable reducing sugars. Additionally, several other polysaccharides such as carrageenan, xylan, pullulan, pectin, starch, and carboxymethyl cellulose were also corroborated as growth substrate for strain DD-13 and were associated with concomitant production of homologous carbohydrase.

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

Similar content being viewed by others

References

  • Abbott DW, Boraston AB (2008) Structural biology of pectin degradation by Enterobacteriaceae. Microbiol Mol Biol Rev 72:301–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boraston AB, McLean BW, Chen G, Li A, Warren RA, Kilburn DG (2002) Cooperative binding of triplicate carbohydrate-binding modules from a thermophilic xylanase. Mol Microbiol 43:87–194

    Article  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238

    Article  CAS  PubMed  Google Scholar 

  • Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freelove AC, Bolam DN, White P, Hazlewood GP, Gilbert HJ (2001) A novel carbohydrate-binding protein is a component of the plant cell wall-degrading complex of Piromycesequi. J Biol Chem 276:43010–43017

    Article  CAS  PubMed  Google Scholar 

  • Galperin MY, Koonin EV (2004) ‘Conserved hypothetical’ proteins: prioritization of targets for experimental study. Nucleic Acids Res 32:5452–5463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutcheson SW, Zhang H, Suvorov M (2011) Carbohydrase systems of Saccharophagus degradans degrading marine complex polysaccharides. Mar drugs 9:645–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Jonnadula R, Verma P, Shouche YS, Ghadi SC (2009) Characterization of Microbulbifer strain CMC-5, a new biochemical variant of Microbulbifer elongatus type strain DSM6810T isolated from decomposing seaweeds. Curr Microbiol 59:600–607

    Article  CAS  PubMed  Google Scholar 

  • Kang S, Kim JK (2015) Reuse of red seaweed waste by a novel bacterium, Bacillus sp. SYR4 isolated from a sandbar. World J Microbiol Biotechnol 31:209–217

    Article  PubMed  Google Scholar 

  • Kim EJ, Fathoni A, Jeong GT, Do Jeong H, Nam TJ, Kong IS, Kim JK (2013) Microbacteriumoxydans, a novel alginate-and laminarin-degrading bacterium for the reutilization of brown-seaweed waste. J Environ Manag 130:153–159

    Article  CAS  Google Scholar 

  • Kurata A, Nishimura M, Kishimoto N, Kobayashi T (2014) Draft genome sequence of a deep-sea bacterium, Bacillus niacini strain JAM F8, involved in the degradation of glycosaminoglycans. Genome Announc 2:e00983–e00914

    PubMed  PubMed Central  Google Scholar 

  • Kwak MJ, Song JY, Kim BK, Chi WJ, Kwon SK, Choi S, Kim JF (2012) Genome sequence of the agar-degrading marine bacterium Alteromonadaceae sp. strain G7. J Bacteriol 194:6961–6962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lagesen K, Hallin P, Rødland EA, Stærfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Yi Z, Cai Y, Zeng R (2015) Draft genome sequence of algal polysaccharides degradation bacterium, Flammeovirga sp. OC4. Mar Genomics 21:21–22

    Article  CAS  PubMed  Google Scholar 

  • Lombard V, Golaconda RH, 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 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynd LR, Van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583

    Article  CAS  PubMed  Google Scholar 

  • Mann AJ, Hahnke RL, Huang S, Werner J, Xing P, Barbeyron T, Glöckner FO (2013) The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides. Appl Environ Microbiol 79:6813–6822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCann MC, Carpita NC (2008) Designing the deconstruction of plant cell walls. Curr Opin Biotechnol 11:314–320

    CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  • Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC (2010) CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20:1574–1584

    Article  CAS  PubMed  Google Scholar 

  • Roh H, Yun EJ, Lee S, Ko HJ, Kim S, Kim BY, Choi IG (2012) Genome sequence of Vibrio sp. strain EJY3, an agarolytic marine bacterium metabolizing 3, 6-anhydro-L-galactose as a sole carbon source. J Bacteriol 194:2773–2774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun C, Chen YJ, Zhang XQ, Pan J, Cheng H, Wu M (2014) Draft genome sequence of Microbulbifer elongatus strain HZ11, a brown seaweed-degrading bacterium with potential ability to produce bioethanol from alginate. Mar Genomics 18:83–85

    Article  PubMed  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28(1):33–6

  • Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Koonin EV (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vashist P, Nogi Y, Ghadi SC, Verma P, Shouche YS (2013) Microbulbifer mangrovi sp. nov., a polysaccharide-degrading bacterium isolated from an Indian mangrove. Int J Syst Evol Microbiol 63:2532–2537

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi M, Sakatoku A, Noda F, Noda M, Tanaka D, Nakamura S (2012) Isolation and characterization of Microbulbifer species 6532A degrading seaweed thalli to single cell detritus particles. Biodegradation 23:93–105

    Article  CAS  PubMed  Google Scholar 

  • Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CNS, Kim PB, Lakshmanaswamy A (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335:308–313

    Article  CAS  PubMed  Google Scholar 

  • Weiner RM, Taylor LE II, Henrissat B, Hauser L, Land M, Coutinho PM, Bayer EA (2008) Complete genome sequence of the complex carbohydrate-degrading marine bacterium, Saccharophagus degradans strain 2-40 T. PLoS Genet 4:e1000087

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgment

Md. Imran acknowledges the Department of Biotechnology, New Delhi, Govt. of India, for the financial support as JRF and SRF throughout the tenure of this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sanjeev C. Ghadi.

Additional information

Accession No.

This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBankunder the accession LZDE00000000. The version described in this paper is version LZDE01000000.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Imran, M., Pant, P., Shanbhag, Y.P. et al. Genome Sequence of Microbulbifer mangrovi DD-13T Reveals Its Versatility to Degrade Multiple Polysaccharides. Mar Biotechnol 19, 116–124 (2017). https://doi.org/10.1007/s10126-017-9737-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-017-9737-9

Keywords

Navigation