IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36877-3.html
   My bibliography  Save this article

Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps

Author

Listed:
  • Xiyang Dong

    (Ministry of Natural Resources
    Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai))

  • Yongyi Peng

    (Ministry of Natural Resources
    Sun Yat-Sen University)

  • Muhua Wang

    (Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai)
    Sun Yat-Sen University)

  • Laura Woods

    (Monash University)

  • Wenxue Wu

    (Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai)
    Sun Yat-Sen University
    Hainan University)

  • Yong Wang

    (Tsinghua University)

  • Xi Xiao

    (China Geological Survey)

  • Jiwei Li

    (Chinese Academy of Sciences)

  • Kuntong Jia

    (Sun Yat-Sen University)

  • Chris Greening

    (Monash University)

  • Zongze Shao

    (Ministry of Natural Resources
    Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai))

  • Casey R. J. Hubert

    (University of Calgary)

Abstract

Deep sea cold seep sediments host abundant and diverse microbial populations that significantly influence biogeochemical cycles. While numerous studies have revealed their community structure and functional capabilities, little is known about genetic heterogeneity within species. Here, we examine intraspecies diversity patterns of 39 abundant species identified in sediment layers down to 430 cm below the sea floor across six cold seep sites. These populations are grouped as aerobic methane-oxidizing bacteria, anaerobic methanotrophic archaea and sulfate-reducing bacteria. Different evolutionary trajectories are observed at the genomic level among these physiologically and phylogenetically diverse populations, with generally low rates of homologous recombination and strong purifying selection. Functional genes related to methane (pmoA and mcrA) and sulfate (dsrA) metabolisms are under strong purifying selection in most species investigated. These genes differ in evolutionary trajectories across phylogenetic clades but are functionally conserved across sites. Intrapopulation diversification of genomes and their mcrA and dsrA genes is depth-dependent and subject to different selection pressure throughout the sediment column redox zones at different sites. These results highlight the interplay between ecological processes and the evolution of key bacteria and archaea in deep sea cold seep extreme environments, shedding light on microbial adaptation in the subseafloor biosphere.

Suggested Citation

  • Xiyang Dong & Yongyi Peng & Muhua Wang & Laura Woods & Wenxue Wu & Yong Wang & Xi Xiao & Jiwei Li & Kuntong Jia & Chris Greening & Zongze Shao & Casey R. J. Hubert, 2023. "Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36877-3
    DOI: 10.1038/s41467-023-36877-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36877-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36877-3?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. 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.
    2. Siegfried Schloissnig & Manimozhiyan Arumugam & Shinichi Sunagawa & Makedonka Mitreva & Julien Tap & Ana Zhu & Alison Waller & Daniel R. Mende & Jens Roat Kultima & John Martin & Karthik Kota & Shamil, 2013. "Genomic variation landscape of the human gut microbiome," Nature, Nature, vol. 493(7430), pages 45-50, January.
    3. Rika E. Anderson & Julie Reveillaud & Emily Reddington & Tom O. Delmont & A. Murat Eren & Jill M. McDermott & Jeff S. Seewald & Julie A. Huber, 2017. "Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    4. Xiyang Dong & Jayne E. Rattray & D. Calvin Campbell & Jamie Webb & Anirban Chakraborty & Oyeboade Adebayo & Stuart Matthews & Carmen Li & Martin Fowler & Natasha M. Morrison & Adam MacDonald & Ryan A., 2020. "Thermogenic hydrocarbon biodegradation by diverse depth-stratified microbial populations at a Scotian Basin cold seep," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Luis Pedro Coelho & Renato Alves & Álvaro Rodríguez Río & Pernille Neve Myers & Carlos P. Cantalapiedra & Joaquín Giner-Lamia & Thomas Sebastian Schmidt & Daniel R. Mende & Askarbek Orakov & Ivica Let, 2022. "Towards the biogeography of prokaryotic genes," Nature, Nature, vol. 601(7892), pages 252-256, January.
    6. Antje Boetius & Katrin Ravenschlag & Carsten J. Schubert & Dirk Rickert & Friedrich Widdel & Armin Gieseke & Rudolf Amann & Bo Barker Jørgensen & Ursula Witte & Olaf Pfannkuche, 2000. "A marine microbial consortium apparently mediating anaerobic oxidation of methane," Nature, Nature, vol. 407(6804), pages 623-626, October.
    7. Xiyang Dong & Chris Greening & Jayne E. Rattray & Anirban Chakraborty & Maria Chuvochina & Daisuke Mayumi & Jan Dolfing & Carmen Li & James M. Brooks & Bernie B. Bernard & Ryan A. Groves & Ian A. Lewi, 2019. "Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    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. Xiyang Dong & Chuwen Zhang & Yongyi Peng & Hong-Xi Zhang & Ling-Dong Shi & Guangshan Wei & Casey R. J. Hubert & Yong Wang & Chris Greening, 2022. "Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Shaojun Pan & Chengkai Zhu & Xing-Ming Zhao & Luis Pedro Coelho, 2022. "A deep siamese neural network improves metagenome-assembled genomes in microbiome datasets across different environments," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Daidai Wu & Tiantian Sun & Rui Xie & Mengdi Pan & Xuegang Chen & Ying Ye & Lihua Liu & Nengyou Wu, 2019. "Characteristics of Authigenic Minerals around the Sulfate-Methane Transition Zone in the Methane-Rich Sediments of the Northern South China Sea: Inorganic Geochemical Evidence," IJERPH, MDPI, vol. 16(13), pages 1-18, June.
    4. Richard B. Coffin & Leila J. Hamdan & Joseph P. Smith & Paula S. Rose & Rebecca E. Plummer & Brandon Yoza & Ingo Pecher & Michael T. Montgomery, 2014. "Contribution of Vertical Methane Flux to Shallow Sediment Carbon Pools across Porangahau Ridge, New Zealand," Energies, MDPI, vol. 7(8), pages 1-25, August.
    5. Maria De La Fuente & Sandra Arndt & Héctor Marín-Moreno & Tim A. Minshull, 2022. "Assessing the Benthic Response to Climate-Driven Methane Hydrate Destabilisation: State of the Art and Future Modelling Perspectives," Energies, MDPI, vol. 15(9), pages 1-32, May.
    6. Zhi-Ping Zhong & Jingjie Du & Stephan Köstlbacher & Petra Pjevac & Sandi Orlić & Matthew B. Sullivan, 2024. "Viral potential to modulate microbial methane metabolism varies by habitat," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. 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.
    8. Yunru Chen & Liang Dong & Weikang Sui & Mingyang Niu & Xingqian Cui & Kai-Uwe Hinrichs & Fengping Wang, 2024. "Cycling and persistence of iron-bound organic carbon in subseafloor sediments," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. 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.
    10. 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.
    11. 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.
    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. Xianzhe Gong & Álvaro Rodríguez Río & Le Xu & Zhiyi Chen & Marguerite V. Langwig & Lei Su & Mingxue Sun & Jaime Huerta-Cepas & Valerie Anda & Brett J. Baker, 2022. "New globally distributed bacterial phyla within the FCB superphylum," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    14. 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.
    15. Klaus Wallmann & Elena Pinero & Ewa Burwicz & Matthias Haeckel & Christian Hensen & Andrew Dale & Lars Ruepke, 2012. "The Global Inventory of Methane Hydrate in Marine Sediments: A Theoretical Approach," Energies, MDPI, vol. 5(7), pages 1-50, July.
    16. 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.
    17. 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.
    18. 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.
    19. Nils Giordano & Marinna Gaudin & Camille Trottier & Erwan Delage & Charlotte Nef & Chris Bowler & Samuel Chaffron, 2024. "Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Ling Zhong & Menghan Zhang & Libing Sun & Yu Yang & Bo Wang & Haibing Yang & Qiang Shen & Yu Xia & Jiarui Cui & Hui Hang & Yi Ren & Bo Pang & Xiangyu Deng & Yahui Zhan & Heng Li & Zhemin Zhou, 2023. "Distributed genotyping and clustering of Neisseria strains reveal continual emergence of epidemic meningococcus over a century," Nature Communications, Nature, vol. 14(1), pages 1-13, 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:14:y:2023:i:1:d:10.1038_s41467-023-36877-3. 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.