Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Microbiology Resource Announcements
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Latest Articles
    • Archive
  • Types of Resources
    • Amplicon Sequence Collections
    • Culture Collections/Mutant Libraries
    • Databases and Software
    • Omics Data Sets
    • Other Genetic Resources
    • Genome Sequences
  • For Authors
    • Getting Started
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About MRA
    • Editor in Chief
    • Board of Editors
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Microbiology Resource Announcements
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Microbiology Resource Announcements
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Latest Articles
    • Archive
  • Types of Resources
    • Amplicon Sequence Collections
    • Culture Collections/Mutant Libraries
    • Databases and Software
    • Omics Data Sets
    • Other Genetic Resources
    • Genome Sequences
  • For Authors
    • Getting Started
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About MRA
    • Editor in Chief
    • Board of Editors
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
Genome Sequences

Complete Genome Sequence of Helicobacter suis Strain SNTW101c, Originally Isolated from a Patient with Nodular Gastritis

Emiko Rimbara, Masato Suzuki, Hidenori Matsui, Masahiko Nakamura, Hirotaka Kobayashi, Shigetarou Mori, Keigo Shibayama
Steven R. Gill, Editor
Emiko Rimbara
aDepartment of Bacteriology II, National Institute of Infectious Diseases, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Emiko Rimbara
Masato Suzuki
bAntimicrobial Resistance Research Center, National Institute of Infectious Diseases, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hidenori Matsui
cKitasato Institute for Life Sciences, Kitasato University, Tokyo, Japan
dGraduate School of Control Sciences, Kitasato University, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Masahiko Nakamura
eSchool of Pharmaceutical Sciences, Kitasato University, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hirotaka Kobayashi
fDepartment of Pathology, National Institute of Infectious Diseases, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Shigetarou Mori
aDepartment of Bacteriology II, National Institute of Infectious Diseases, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Keigo Shibayama
aDepartment of Bacteriology II, National Institute of Infectious Diseases, Tokyo, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Steven R. Gill
University of Rochester School of Medicine and Dentistry
Roles: Editor
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/MRA.01340-19
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Helicobacter suis strain SNTW101c, which was originally obtained from a patient with nodular gastritis, has been maintained in mouse stomach because of difficulty culturing it in vitro. Recently, we succeeded in culturing this strain in vitro. Here, we report the complete genome sequence of H. suis strain SNTW101c.

ANNOUNCEMENT

Helicobacter suis frequently colonizes pig stomach and causes gastric diseases, including mucosa-associated lymphoid tissue (MALT) lymphoma, in humans (1). H. suis strain SNTW101 was originally isolated from a patient with nodular gastritis in 2008; thereafter, it has been passaged in mice because the bacteria could not be grown in vitro. We previously reported a draft genome sequence of strain SNTW101 that was determined using bacterial cells purified from SNTW101-colonized mouse stomach with anti-Helicobacter pylori antibody-coated magnetic beads (2). Recently, the bacteria were successfully isolated from the infected stomach and grown in vitro by a method described previously (3, 4). Here, we report the complete genome sequence of the resulting H. suis strain, named SNTW101c.

SNTW101c was isolated as described previously (3, 4). The colonies appeared 20 days after inoculation (Fig. 1A), and each single colony was further subcultured in a biphasic medium containing Brucella broth and agar with Vitox and Skirrow supplements (Thermo Fisher Scientific), 0.05% HCl, and 20% fetal bovine serum (Sigma-Aldrich). The morphology of H. suis SNTW101c included a tightly coiled body with sheathed bipolar flagella (Fig. 1B), which contribute to the high level of motility of these bacteria (see https://youtu.be/l70zI-9N74A). A DNA library was prepared, using a rapid barcoding kit (product number SQK-RBK004; Oxford Nanopore Technologies), from genomic DNA extracted using Qiagen Genomic-tips 20/G and buffers (Qiagen). Nanopore sequencing using the MinION platform with R9.4.1 flow cells (Oxford Nanopore Technologies) provided a total of 11,701 reads (N50 = 11,501 bp), with an average coverage depth of 26.7; Guppy v3.1.5 (Oxford Nanopore Technologies) was used for base calling and adapter trimming, with default parameters. De novo assembly was performed with Unicycler v0.4.8 (5), with default parameters, and three contigs, including one chromosome and two putative plasmids, were constructed. The overlap region in the assembled contig was detected by a genome-scale sequence comparison using LAST (http://last.cbrc.jp) and was trimmed manually. The genomic DNA was also sequenced on an Illumina MiniSeq system, with a MiniSeq high-output reagent kit (300 cycles), using a 151-bp paired-end library prepared with the Nextera XT DNA library preparation kit (insert size, 500 to 900 bp); this resulted in a total of 263,361 reads (N50 = 151 bp) and an average coverage depth of 46.1. Illumina reads were mapped onto the sequences assembled de novo from MinION reads, and sequencing errors were corrected by extracting the consensus of the mapped reads three times using CLC Genomics Workbench v11.0.1 (Qiagen), with default parameters. The resulting sequences were annotated using DFAST v1.1.0 (6), with default parameters. The genome size of SNTW101c was 1,680,021 bp, comprising 1,744 protein-coding sequences (CDSs) and 5 ribosomal RNAs, with a GC content of 40%. The genome size of SNTW101c was similar to that estimated for SNTW101 (1,608,632 bp) (2). The putative plasmids pSNTW101c_1 (9,051 bp) and pSNTW101c_2 (5,825 bp) coded for 6 CDSs each.

FIG 1
  • Open in new tab
  • Download powerpoint
FIG 1

Helicobacter suis strain SNTW101c: (A) colonies on an agar plate; (B) scanning electron microscopy image.

As suggested by previous studies (1, 7), both CagA and VacA, the major virulence factors of the human gastric pathogen Helicobacter pylori (8), were absent in strain SNTW101c, indicating that unknown virulence factors contribute to bacterial pathogenesis. Regarding the plasmids, pSNTW101c_1 possessed genes encoding a type IIS restriction-modification system.

This is the first report of the complete genome sequence of an H. suis strain and will aid in understanding the mechanism of chronic H. suis infection in the stomach and bacterial pathogenesis associated with MALT lymphoma in humans.

Data availability.The complete genome sequence of H. suis strain SNTW101c was deposited in NCBI GenBank under the accession numbers AP019774 (chromosome), AP019775 (pSNTW101c_1), and AP019776 (pSNTW101c_2). The raw sequence data are available in the Sequence Read Archive with the accession numbers DRX176097 (Illumina) and DRX176341 (MinION).

ACKNOWLEDGMENTS

We thank Tsutomu Tomida and Mitsuhiro Hashimoto (Timelapse Vision, Inc., Japan) for their support in microscopic observation of live bacteria.

This work was supported by grants from the Japan Agency for Medical Research and Development/Japan International Cooperation Agency to M.S. (grant JP19fk0108052) and K.S. (grant JP18fk0108061), a Grant-in-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science to H.M. (grant 19H03474), and a Grant-in-Aid for Scientific Research (C) to M.N. (grant 17K09361).

FOOTNOTES

    • Received 28 October 2019.
    • Accepted 24 November 2019.
    • Published 2 January 2020.
  • Copyright © 2020 Rimbara et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

REFERENCES

  1. 1.↵
    1. Haesebrouck F,
    2. Pasmans F,
    3. Flahou B,
    4. Chiers K,
    5. Baele M,
    6. Meyns T,
    7. Decostere A,
    8. Ducatelle R
    . 2009. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 22:202–223. doi:10.1128/CMR.00041-08.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    1. Matsui H,
    2. Takahashi T,
    3. Murayama SY,
    4. Uchiyama I,
    5. Yamaguchi K,
    6. Shigenobu S,
    7. Suzuki M,
    8. Rimbara E,
    9. Shibayama K,
    10. Øverby A,
    11. Nakamura M
    . 2016. Draft genome sequence of Helicobacter suis strain SNTW101, isolated from a Japanese patient with nodular gastritis. Genome Announc 4:e00934-16. doi:10.1128/genomeA.00934-16.
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    1. Baele M,
    2. Decostere A,
    3. Vandamme P,
    4. Ceelen L,
    5. Hellemans A,
    6. Mast J,
    7. Chiers K,
    8. Ducatelle R,
    9. Haesebrouck F
    . 2008. Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. Int J Syst Evol Microbiol 58:1350–1358. doi:10.1099/ijs.0.65133-0.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Blaecher C,
    2. Bauwens E,
    3. Tay A,
    4. Peters F,
    5. Dobbs S,
    6. Dobbs J,
    7. Charlett A,
    8. Ducatelle R,
    9. Haesebrouck F,
    10. Smet A
    . 2017. A novel isolation protocol and probe-based RT-PCR for diagnosis of gastric infections with the zoonotic pathogen Helicobacter suis. Helicobacter 22:e12369. doi:10.1111/hel.12369.
    OpenUrlCrossRef
  5. 5.↵
    1. Wick RR,
    2. Judd LM,
    3. Gorrie CL,
    4. Holt KE
    . 2017. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595. doi:10.1371/journal.pcbi.1005595.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Tanizawa Y,
    2. Fujisawa T,
    3. Kaminuma E,
    4. Nakamura Y,
    5. Arita M
    . 2016. DFAST and DAGA: Web-based integrated genome annotation tools and resources. Biosci Microbiota Food Health 35:173–184. doi:10.12938/bmfh.16-003.
    OpenUrlCrossRef
  7. 7.↵
    1. Vermoote M,
    2. Vandekerckhove TT,
    3. Flahou B,
    4. Pasmans F,
    5. Smet A,
    6. De Groote D,
    7. Van Criekinge W,
    8. Ducatelle R,
    9. Haesebrouck F
    . 2011. Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet Res 42:51. doi:10.1186/1297-9716-42-51.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. van Doorn LJ,
    2. Figueiredo C,
    3. Sanna R,
    4. Plaisier A,
    5. Schneeberger P,
    6. de Boer W,
    7. Quint W
    . 1998. Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 115:58–66. doi:10.1016/s0016-5085(98)70365-8.
    OpenUrlCrossRefPubMedWeb of Science
View Abstract
PreviousNext
Back to top
Download PDF
Citation Tools
Complete Genome Sequence of Helicobacter suis Strain SNTW101c, Originally Isolated from a Patient with Nodular Gastritis
Emiko Rimbara, Masato Suzuki, Hidenori Matsui, Masahiko Nakamura, Hirotaka Kobayashi, Shigetarou Mori, Keigo Shibayama
Microbiology Resource Announcements Jan 2020, 9 (1) e01340-19; DOI: 10.1128/MRA.01340-19

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print
Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Microbiology Resource Announcements article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Complete Genome Sequence of Helicobacter suis Strain SNTW101c, Originally Isolated from a Patient with Nodular Gastritis
(Your Name) has forwarded a page to you from Microbiology Resource Announcements
(Your Name) thought you would be interested in this article in Microbiology Resource Announcements.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Complete Genome Sequence of Helicobacter suis Strain SNTW101c, Originally Isolated from a Patient with Nodular Gastritis
Emiko Rimbara, Masato Suzuki, Hidenori Matsui, Masahiko Nakamura, Hirotaka Kobayashi, Shigetarou Mori, Keigo Shibayama
Microbiology Resource Announcements Jan 2020, 9 (1) e01340-19; DOI: 10.1128/MRA.01340-19
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • ANNOUNCEMENT
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

Cited By...

About

  • About MRA
  • Editor in Chief
  • Board of Editors
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • Getting Started
  • Submit a Manuscript
  • Author Warranty
  • Ethics
  • Contact Us
  • ASM Author Center

Follow #MRAJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Online ISSN: 2576-098X