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Coevolution between marine Aeromonas and phages reveals temporal trade-off patterns of phage resistance and host population fitness

The ISME Journal volume 17, pages 2200–2209 (2023)Cite this article

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Abstract

Coevolution of bacteria and phages is an important host and parasite dynamic in marine ecosystems, contributing to the understanding of bacterial community diversity. On the time scale, questions remain concerning what is the difference between phage resistance patterns in marine bacteria and how advantageous mutations gradually accumulate during coevolution. In this study, marine Aeromonas was co-cultured with its phage for 180 days and their genetic and phenotypic dynamics were measured every 30 days. We identified 11 phage resistance genes and classified them into three categories: lipopolysaccharide (LPS), outer membrane protein (OMP), and two-component system (TCS). LPS shortening and OMP mutations are two distinct modes of complete phage resistance, while TCS mutants mediate incomplete resistance by repressing the transcription of phage genes. The co-mutation of LPS and OMP was a major mode for bacterial resistance at a low cost. The mutations led to significant reductions in the growth and virulence of bacterial populations during the first 60 days of coevolution, with subsequent leveling off. Our findings reveal the marine bacterial community dynamics and evolutionary trade-offs of phage resistance during coevolution, thus granting further understanding of the interaction of marine microbes.

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Fig. 1: Eleven phage resistance genes were identified and classified into three categories: polysaccharide (PS) synthesis, outer membrane protein (OMP), and two-component system (TCS).
Fig. 2: Three patterns of phage resistance involving LPS shortening, OMP mutation, and transcriptional repression by TCS.
Fig. 3: The mutation frequency changes of phage resistance genes during the coevolution of bacteria and phage within 180 days.
Fig. 4: Phage resistance leads to a gradual decline in bacterial growth, virulence, and fitness during coevolution.
Fig. 5: Schematic diagram of three phage resistance patterns and their cost during coevolution.

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Data availability

Whole genome re-sequencing data were submitted to GenBank under BioProject ID: PRJNA972433 and PRJNA972467. The RNA-seq data were submitted to GenBank under BioProject ID: PRJNA972427. The sequence data for the A. salmonicida JNG were deposited at GenBank under accession no. CP122987-CP122989.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 32025038), the Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism grant 2021 Sci & Tech 03-28 (Shanghai Municipal Education Commission), China Agriculture Research System of MOF and MARA (CARS-47), and ECUST-OPM Innovation Institute Open Fund (20230801).

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  1. These authors contributed equally: Zhenhe Xu, Zihan Ding.

Authors and Affiliations

  1. State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China

    Zhenhe Xu, Zihan Ding, Lijia Shi, Yuzhen Xie, Zhuang Wang & Qin Liu

  2. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), 519000, Zhuhai, China

    Yuanxing Zhang

  3. Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai, 200237, China

    Yuanxing Zhang, Zhuang Wang & Qin Liu

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Contributions

Conceptualization: XZ DZ; Data curation: XZ DZ. Funding acquisition: LQ ZY; Investigation: XZ DZ SL XY; Project administration: LQ ZY WZ; Supervision: LQ WZ; Validation: XZ DZ SL; Visualization: XZ; Writing – original draft: XZ DZ; Writing – review and editing: XZ LQ ZY.

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Correspondence to Zhuang Wang or Qin Liu.

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Xu, Z., Ding, Z., Shi, L. et al. Coevolution between marine Aeromonas and phages reveals temporal trade-off patterns of phage resistance and host population fitness. ISME J 17, 2200–2209 (2023). https://doi.org/10.1038/s41396-023-01529-3

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