IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33782-z.html
   My bibliography  Save this article

Genome-centric analysis of short and long read metagenomes reveals uncharacterized microbiome diversity in Southeast Asians

Author

Listed:
  • Jean-Sebastien Gounot

    (Genome Institute of Singapore)

  • Minghao Chia

    (Genome Institute of Singapore)

  • Denis Bertrand

    (Genome Institute of Singapore)

  • Woei-Yuh Saw

    (National University of Singapore
    Baker Heart and Diabetes Institute)

  • Aarthi Ravikrishnan

    (Genome Institute of Singapore)

  • Adrian Low

    (Temasek Life Sciences Laboratory, 1 Research Link)

  • Yichen Ding

    (Temasek Life Sciences Laboratory, 1 Research Link)

  • Amanda Hui Qi Ng

    (Genome Institute of Singapore)

  • Linda Wei Lin Tan

    (National University of Singapore)

  • Yik-Ying Teo

    (National University of Singapore
    National University of Singapore
    National University of Singapore)

  • Henning Seedorf

    (Temasek Life Sciences Laboratory, 1 Research Link
    National University of Singapore)

  • Niranjan Nagarajan

    (Genome Institute of Singapore
    National University of Singapore)

Abstract

Despite extensive efforts to address it, the vastness of uncharacterized ‘dark matter’ microbial genetic diversity can impact short-read sequencing based metagenomic studies. Population-specific biases in genomic reference databases can further compound this problem. Leveraging advances in hybrid assembly (using short and long reads) and Hi-C technologies in a cross-sectional survey, we deeply characterized 109 gut microbiomes from three ethnicities in Singapore to comprehensively reconstruct 4497 medium and high-quality metagenome assembled genomes, 1708 of which were missing in short-read only analysis and with >28× N50 improvement. Species-level clustering identified 70 (>10% of total) novel gut species out of 685, improved reference genomes for 363 species (53% of total), and discovered 3413 strains unique to these populations. Among the top 10 most abundant gut bacteria in our study, one of the species and >80% of strains were unrepresented in existing databases. Annotation of biosynthetic gene clusters (BGCs) uncovered more than 27,000 BGCs with a large fraction (36–88%) unrepresented in current databases, and with several unique clusters predicted to produce bacteriocins that could significantly alter microbiome community structure. These results reveal significant uncharacterized gut microbial diversity in Southeast Asian populations and highlight the utility of hybrid metagenomic references for bioprospecting and disease-focused studies.

Suggested Citation

  • Jean-Sebastien Gounot & Minghao Chia & Denis Bertrand & Woei-Yuh Saw & Aarthi Ravikrishnan & Adrian Low & Yichen Ding & Amanda Hui Qi Ng & Linda Wei Lin Tan & Yik-Ying Teo & Henning Seedorf & Niranjan, 2022. "Genome-centric analysis of short and long read metagenomes reveals uncharacterized microbiome diversity in Southeast Asians," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33782-z
    DOI: 10.1038/s41467-022-33782-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33782-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33782-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Himel Mallick & Ali Rahnavard & Lauren J McIver & Siyuan Ma & Yancong Zhang & Long H Nguyen & Timothy L Tickle & George Weingart & Boyu Ren & Emma H Schwager & Suvo Chatterjee & Kelsey N Thompson & Je, 2021. "Multivariable association discovery in population-scale meta-omics studies," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-27, November.
    2. Chirag Jain & Luis M. Rodriguez-R & Adam M. Phillippy & Konstantinos T. Konstantinidis & Srinivas Aluru, 2018. "High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    3. Feng Zhu & Yanmei Ju & Wei Wang & Qi Wang & Ruijin Guo & Qingyan Ma & Qiang Sun & Yajuan Fan & Yuying Xie & Zai Yang & Zhuye Jie & Binbin Zhao & Liang Xiao & Lin Yang & Tao Zhang & Junqin Feng & Liyan, 2020. "Metagenome-wide association of gut microbiome features for schizophrenia," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Woei-Yuh Saw & Erwin Tantoso & Husna Begum & Lihan Zhou & Ruiyang Zou & Cheng He & Sze Ling Chan & Linda Wei-Lin Tan & Lai-Ping Wong & Wenting Xu & Don Kyin Nwe Moong & Yenly Lim & Bowen Li & Nisha Es, 2017. "Establishing multiple omics baselines for three Southeast Asian populations in the Singapore Integrative Omics Study," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    5. Gene W. Tyson & Jarrod Chapman & Philip Hugenholtz & Eric E. Allen & Rachna J. Ram & Paul M. Richardson & Victor V. Solovyev & Edward M. Rubin & Daniel S. Rokhsar & Jillian F. Banfield, 2004. "Community structure and metabolism through reconstruction of microbial genomes from the environment," Nature, Nature, vol. 428(6978), pages 37-43, March.
    6. Stephanie L. Schnorr & Marco Candela & Simone Rampelli & Manuela Centanni & Clarissa Consolandi & Giulia Basaglia & Silvia Turroni & Elena Biagi & Clelia Peano & Marco Severgnini & Jessica Fiori & Rob, 2014. "Gut microbiome of the Hadza hunter-gatherers," Nature Communications, Nature, vol. 5(1), pages 1-12, May.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Yuxuan Du & Fengzhu Sun, 2023. "MetaCC allows scalable and integrative analyses of both long-read and short-read metagenomic Hi-C data," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Aarthi Ravikrishnan & Indrik Wijaya & Eileen Png & Kern Rei Chng & Eliza Xin Pei Ho & Amanda Hui Qi Ng & Ahmad Nazri Mohamed Naim & Jean-Sebastien Gounot & Shou Ping Guan & Jasinda Lee Hanqing & Lihua, 2024. "Gut metagenomes of Asian octogenarians reveal metabolic potential expansion and distinct microbial species associated with aging phenotypes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Georges P. Schmartz & Jacqueline Rehner & Madline P. Gund & Verena Keller & Leidy-Alejandra G. Molano & Stefan Rupf & Matthias Hannig & Tim Berger & Elias Flockerzi & Berthold Seitz & Sara Fleser & Sa, 2024. "Decoding the diagnostic and therapeutic potential of microbiota using pan-body pan-disease microbiomics," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Aarthi Ravikrishnan & Indrik Wijaya & Eileen Png & Kern Rei Chng & Eliza Xin Pei Ho & Amanda Hui Qi Ng & Ahmad Nazri Mohamed Naim & Jean-Sebastien Gounot & Shou Ping Guan & Jasinda Lee Hanqing & Lihua, 2024. "Gut metagenomes of Asian octogenarians reveal metabolic potential expansion and distinct microbial species associated with aging phenotypes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Ruairi C. Robertson & Thaddeus J. Edens & Lynnea Carr & Kuda Mutasa & Ethan K. Gough & Ceri Evans & Hyun Min Geum & Iman Baharmand & Sandeep K. Gill & Robert Ntozini & Laura E. Smith & Bernard Chasekw, 2023. "The gut microbiome and early-life growth in a population with high prevalence of stunting," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Max E. Schön & Vasily V. Zlatogursky & Rohan P. Singh & Camille Poirier & Susanne Wilken & Varsha Mathur & Jürgen F. H. Strassert & Jarone Pinhassi & Alexandra Z. Worden & Patrick J. Keeling & Thijs J, 2021. "Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Ruchi Shroff & Carla Ramos Cortés, 2020. "The Biodiversity Paradigm: Building Resilience for Human and Environmental Health," Development, Palgrave Macmillan;Society for International Deveopment, vol. 63(2), pages 172-180, December.
    5. Kelly J. Whaley-Martin & Lin-Xing Chen & Tara Colenbrander Nelson & Jennifer Gordon & Rose Kantor & Lauren E. Twible & Stephanie Marshall & Sam McGarry & Laura Rossi & Benoit Bessette & Christian Baro, 2023. "O2 partitioning of sulfur oxidizing bacteria drives acidity and thiosulfate distributions in mining waters," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Manish Boolchandani & Kevin S. Blake & Drake H. Tilley & Miguel M. Cabada & Drew J. Schwartz & Sanket Patel & Maria Luisa Morales & Rina Meza & Giselle Soto & Sandra D. Isidean & Chad K. Porter & Mark, 2022. "Impact of international travel and diarrhea on gut microbiome and resistome dynamics," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Nenad Macesic & Jane Hawkey & Ben Vezina & Jessica A. Wisniewski & Hugh Cottingham & Luke V. Blakeway & Taylor Harshegyi & Katherine Pragastis & Gnei Zweena Badoordeen & Amanda Dennison & Denis W. Spe, 2023. "Genomic dissection of endemic carbapenem resistance reveals metallo-beta-lactamase dissemination through clonal, plasmid and integron transfer," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Minghui Cheng & Yingjie Xu & Xiao Cui & Xin Wei & Yundi Chang & Jun Xu & Cheng Lei & Lei Xue & Yifan Zheng & Zhang Wang & Lingtong Huang & Min Zheng & Hong Luo & Yuxin Leng & Chao Jiang, 2024. "Deep longitudinal lower respiratory tract microbiome profiling reveals genome-resolved functional and evolutionary dynamics in critical illness," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Zhirui Cao & Dejun Fan & Yang Sun & Ziyu Huang & Yue Li & Runping Su & Feng Zhang & Qing Li & Hongju Yang & Fen Zhang & Yinglei Miao & Ping Lan & Xiaojian Wu & Tao Zuo, 2024. "The gut ileal mucosal virome is disturbed in patients with Crohn’s disease and exacerbates intestinal inflammation in mice," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    10. Jiandui Mi & Xiaoping Jing & Chouxian Ma & Fuyu Shi & Ze Cao & Xin Yang & Yiwen Yang & Apurva Kakade & Weiwei Wang & Ruijun Long, 2024. "A metagenomic catalogue of the ruminant gut archaeome," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    11. Xiaoquan Su & Weihua Pan & Baoxing Song & Jian Xu & Kang Ning, 2014. "Parallel-META 2.0: Enhanced Metagenomic Data Analysis with Functional Annotation, High Performance Computing and Advanced Visualization," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-13, March.
    12. Vincent Somerville & Nadine Thierer & Remo S. Schmidt & Alexandra Roetschi & Lauriane Braillard & Monika Haueter & Hélène Berthoud & Noam Shani & Ueli Ah & Florent Mazel & Philipp Engel, 2024. "Genomic and phenotypic imprints of microbial domestication on cheese starter cultures," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    13. Sandra M. Holmberg & Rachel H. Feeney & Vishnu Prasoodanan P.K. & Fabiola Puértolas-Balint & Dhirendra K. Singh & Supapit Wongkuna & Lotte Zandbergen & Hans Hauner & Beate Brandl & Anni I. Nieminen & , 2024. "The gut commensal Blautia maintains colonic mucus function under low-fiber consumption through secretion of short-chain fatty acids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    14. Natasha Spottiswoode & Alexandra Tsitsiklis & Victoria T. Chu & Hoang Van Phan & Catherine DeVoe & Christina Love & Rajani Ghale & Joshua Bloomstein & Beth Shoshana Zha & Cole P. Maguire & Abigail Gla, 2024. "Microbial dynamics and pulmonary immune responses in COVID-19 secondary bacterial pneumonia," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Shibu Yooseph & Granger Sutton & Douglas B Rusch & Aaron L Halpern & Shannon J Williamson & Karin Remington & Jonathan A Eisen & Karla B Heidelberg & Gerard Manning & Weizhong Li & Lukasz Jaroszewski , 2007. "The Sorcerer II Global Ocean Sampling Expedition: Expanding the Universe of Protein Families," PLOS Biology, Public Library of Science, vol. 5(3), pages 1-35, March.
    16. Jordy Evan Sulaiman & Jaron Thompson & Yili Qian & Eugenio I. Vivas & Christian Diener & Sean M. Gibbons & Nasia Safdar & Ophelia S. Venturelli, 2024. "Elucidating human gut microbiota interactions that robustly inhibit diverse Clostridioides difficile strains across different nutrient landscapes," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    17. M. C. Rühlemann & C. Bang & J. F. Gogarten & B. M. Hermes & M. Groussin & S. Waschina & M. Poyet & M. Ulrich & C. Akoua-Koffi & T. Deschner & J. J. Muyembe-Tamfum & M. M. Robbins & M. Surbeck & R. M. , 2024. "Functional host-specific adaptation of the intestinal microbiome in hominids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Youwen Qin & Xin Tong & Wei-Jian Mei & Yanshuang Cheng & Yuanqiang Zou & Kai Han & Jiehai Yu & Zhuye Jie & Tao Zhang & Shida Zhu & Xin Jin & Jian Wang & Huanming Yang & Xun Xu & Huanzi Zhong & Liang X, 2024. "Consistent signatures in the human gut microbiome of old- and young-onset colorectal cancer," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Ruobing Wang & Anru Zhang & Shijun Sun & Guankun Yin & Xingyu Wu & Qi Ding & Qi Wang & Fengning Chen & Shuyi Wang & Lucy Dorp & Yawei Zhang & Longyang Jin & Xiaojuan Wang & Francois Balloux & Hui Wang, 2024. "Increase in antioxidant capacity associated with the successful subclone of hypervirulent carbapenem-resistant Klebsiella pneumoniae ST11-KL64," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Lucas Serra Moncadas & Cyrill Hofer & Paul-Adrian Bulzu & Jakob Pernthaler & Adrian-Stefan Andrei, 2024. "Freshwater genome-reduced bacteria exhibit pervasive episodes of adaptive stasis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33782-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.