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Freshwater genome-reduced bacteria exhibit pervasive episodes of adaptive stasis

Author

Listed:
  • Lucas Serra Moncadas

    (University of Zurich)

  • Cyrill Hofer

    (University of Zurich)

  • Paul-Adrian Bulzu

    (Biology Centre of the Czech Academy of Sciences)

  • Jakob Pernthaler

    (University of Zurich)

  • Adrian-Stefan Andrei

    (University of Zurich)

Abstract

The emergence of bacterial species is rooted in their inherent potential for continuous evolution and adaptation to an ever-changing ecological landscape. The adaptive capacity of most species frequently resides within the repertoire of genes encoding the secreted proteome (SP), as it serves as a primary interface used to regulate survival/reproduction strategies. Here, by applying evolutionary genomics approaches to metagenomics data, we show that abundant freshwater bacteria exhibit biphasic adaptation states linked to the eco-evolutionary processes governing their genome sizes. While species with average to large genomes adhere to the dominant paradigm of evolution through niche adaptation by reducing the evolutionary pressure on their SPs (via the augmentation of functionally redundant genes that buffer mutational fitness loss) and increasing the phylogenetic distance of recombination events, most of the genome-reduced species exhibit a nonconforming state. In contrast, their SPs reflect a combination of low functional redundancy and high selection pressure, resulting in significantly higher levels of conservation and invariance. Our findings indicate that although niche adaptation is the principal mechanism driving speciation, freshwater genome-reduced bacteria often experience extended periods of adaptive stasis. Understanding the adaptive state of microbial species will lead to a better comprehension of their spatiotemporal dynamics, biogeography, and resilience to global change.

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  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47767-7
    DOI: 10.1038/s41467-024-47767-7
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    1. Xukang Shen & Siliang Song & Chuan Li & Jianzhi Zhang, 2022. "Synonymous mutations in representative yeast genes are mostly strongly non-neutral," Nature, Nature, vol. 606(7915), pages 725-731, June.
    2. Akintunde Emiola & Julia Oh, 2018. "High throughput in situ metagenomic measurement of bacterial replication at ultra-low sequencing coverage," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    3. Edward Geisinger & Nadav J. Mortman & Yunfei Dai & Murat Cokol & Sapna Syal & Andrew Farinha & Delaney G. Fisher & Amy Y. Tang & David W. Lazinski & Stephen Wood & Jon Anthony & Tim Opijnen & Ralph R., 2020. "Antibiotic susceptibility signatures identify potential antimicrobial targets in the Acinetobacter baumannii cell envelope," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    4. 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.
    5. Edward Geisinger & Nadav J. Mortman & Yunfei Dai & Murat Cokol & Sapna Syal & Andrew Farinha & Delaney G. Fisher & Amy Y. Tang & David W. Lazinski & Stephen Wood & Jon Anthony & Tim Opijnen & Ralph R., 2020. "Author Correction: Antibiotic susceptibility signatures identify potential antimicrobial targets in the Acinetobacter baumannii cell envelope," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    6. Lynn J. Rothschild & Rocco L. Mancinelli, 2001. "Life in extreme environments," Nature, Nature, vol. 409(6823), pages 1092-1101, February.
    7. Sheila M Reynolds & Lukas Käll & Michael E Riffle & Jeff A Bilmes & William Stafford Noble, 2008. "Transmembrane Topology and Signal Peptide Prediction Using Dynamic Bayesian Networks," PLOS Computational Biology, Public Library of Science, vol. 4(11), pages 1-14, November.
    8. Brent C. Christner & John C. Priscu & Amanda M. Achberger & Carlo Barbante & Sasha P. Carter & Knut Christianson & Alexander B. Michaud & Jill A. Mikucki & Andrew C. Mitchell & Mark L. Skidmore & Tris, 2014. "A microbial ecosystem beneath the West Antarctic ice sheet," Nature, Nature, vol. 512(7514), pages 310-313, August.
    9. Brent C. Christner & John C. Priscu & Amanda M. Achberger & Carlo Barbante & Sasha P. Carter & Knut Christianson & Alexander B. Michaud & Jill A. Mikucki & Andrew C. Mitchell & Mark L. Skidmore & Tris, 2014. "Correction: Corrigendum: A microbial ecosystem beneath the West Antarctic ice sheet," Nature, Nature, vol. 514(7522), pages 394-394, October.
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