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Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities

Author

Listed:
  • Nils Giordano

    (UMR 6004)

  • Marinna Gaudin

    (UMR 6004)

  • Camille Trottier

    (UMR 6004)

  • Erwan Delage

    (UMR 6004)

  • Charlotte Nef

    (PSL Université Paris)

  • Chris Bowler

    (PSL Université Paris
    FR2022/Tara Oceans GOSEE)

  • Samuel Chaffron

    (UMR 6004
    FR2022/Tara Oceans GOSEE)

Abstract

Marine microorganisms form complex communities of interacting organisms that influence central ecosystem functions in the ocean such as primary production and nutrient cycling. Identifying the mechanisms controlling their assembly and activities is a major challenge in microbial ecology. Here, we integrated Tara Oceans meta-omics data to predict genome-scale community interactions within prokaryotic assemblages in the euphotic ocean. A global genome-resolved co-activity network revealed a significant number of inter-lineage associations across diverse phylogenetic distances. Identified co-active communities include species displaying smaller genomes but encoding a higher potential for quorum sensing, biofilm formation, and secondary metabolism. Community metabolic modelling reveals a higher potential for interaction within co-active communities and points towards conserved metabolic cross-feedings, in particular of specific amino acids and group B vitamins. Our integrated ecological and metabolic modelling approach suggests that genome streamlining and metabolic auxotrophies may act as joint mechanisms shaping bacterioplankton community assembly in the global ocean surface.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46374-w
    DOI: 10.1038/s41467-024-46374-w
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    1. Malte Herold & Susana Martínez Arbas & Shaman Narayanasamy & Abdul R. Sheik & Luise A. K. Kleine-Borgmann & Laura A. Lebrun & Benoît J. Kunath & Hugo Roume & Irina Bessarab & Rohan B. H. Williams & Jo, 2020. "Integration of time-series meta-omics data reveals how microbial ecosystems respond to disturbance," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    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. Akshit Goyal & Tong Wang & Veronika Dubinkina & Sergei Maslov, 2021. "Ecology-guided prediction of cross-feeding interactions in the human gut microbiome," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. T. J. Browning & E. P. Achterberg & J. C. Yong & I. Rapp & C. Utermann & A. Engel & C. M. Moore, 2017. "Iron limitation of microbial phosphorus acquisition in the tropical North Atlantic," Nature Communications, Nature, vol. 8(1), pages 1-7, August.
    5. Chris S. Smillie & Mark B. Smith & Jonathan Friedman & Otto X. Cordero & Lawrence A. David & Eric J. Alm, 2011. "Ecology drives a global network of gene exchange connecting the human microbiome," Nature, Nature, vol. 480(7376), pages 241-244, December.
    6. Kevin R. Arrigo, 2005. "Erratum: Marine microorganisms and global nutrient cycles," Nature, Nature, vol. 438(7064), pages 122-122, November.
    7. Qiyun Zhu & Uyen Mai & Wayne Pfeiffer & Stefan Janssen & Francesco Asnicar & Jon G. Sanders & Pedro Belda-Ferre & Gabriel A. Al-Ghalith & Evguenia Kopylova & Daniel McDonald & Tomasz Kosciolek & John , 2019. "Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    8. David K. Ngugi & Silvia G. Acinas & Pablo Sánchez & Josep M. Gasol & Susana Agusti & David M. Karl & Carlos M. Duarte, 2023. "Abiotic selection of microbial genome size in the global ocean," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Lucas Paoli & Hans-Joachim Ruscheweyh & Clarissa C. Forneris & Florian Hubrich & Satria Kautsar & Agneya Bhushan & Alessandro Lotti & Quentin Clayssen & Guillem Salazar & Alessio Milanese & Charlotte , 2022. "Biosynthetic potential of the global ocean microbiome," Nature, Nature, vol. 607(7917), pages 111-118, July.
    10. Kevin R. Arrigo, 2005. "Marine microorganisms and global nutrient cycles," Nature, Nature, vol. 437(7057), pages 349-355, September.
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