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Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography

The ISME Journal volume 17, pages 2079–2089 (2023)Cite this article

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Abstract

Wetlands store 20–30% of the world’s soil carbon, and identifying the microbial controls on these carbon reserves is essential to predicting feedbacks to climate change. Although viral infections likely play important roles in wetland ecosystem dynamics, we lack a basic understanding of wetland viral ecology. Here 63 viral size-fraction metagenomes (viromes) and paired total metagenomes were generated from three time points in 2021 at seven fresh- and saltwater wetlands in the California Bodega Marine Reserve. We recovered 12,826 viral population genomic sequences (vOTUs), only 4.4% of which were detected at the same field site two years prior, indicating a small degree of population stability or recurrence. Viral communities differed most significantly among the seven wetland sites and were also structured by habitat (plant community composition and salinity). Read mapping to a new version of our reference database, PIGEONv2.0 (515,763 vOTUs), revealed 196 vOTUs present over large geographic distances, often reflecting shared habitat characteristics. Wetland vOTU microdiversity was significantly lower locally than globally and lower within than between time points, indicating greater divergence with increasing spatiotemporal distance. Viruses tended to have broad predicted host ranges via CRISPR spacer linkages to metagenome-assembled genomes, and increased SNP frequencies in CRISPR-targeted major tail protein genes suggest potential viral eco-evolutionary dynamics in response to both immune targeting and changes in host cell receptors involved in viral attachment. Together, these results highlight the importance of dispersal, environmental selection, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography.

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Fig. 1: Sampling design and overarching compositional patterns for Bodega Bay viral and prokaryotic communities.
Fig. 2: Global distribution and habitat context of Bodega Bay vOTUs, leveraging the PIGEONv2.0 database.
Fig. 3: Comparisons of viral variant (sub-population) diversity in local and global contexts.
Fig. 4: Bodega Bay virus-host linkages and putative interactions derived from CRISPR spacer-protospacer matches.

Data availability

Raw sequencing reads are available at NCBI under BioProject number PRJNA913601, and sequence processing and statistical analysis code can be found on GitHub (https://github.com/AnneliektH/BodegaBay2021). The PIGEONv2.0 database vOTU sequences, the vOTU sequences recovered in this dataset, and MAGs recovered in this dataset are available on Dryad (https://datadryad.org/), using the following https://doi.org/10.25338/B8C934 (datasets with the most recent date stamp are the most current).

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Acknowledgements

We thank Sara Geonczy and Devyn Durham for their help with sampling, Christian Santos-Medellín for helpful discussions, and the University of California, Davis Natural Reserves site directors and staff, particularly Suzanne Olyarnik at the Bodega Marine Reserve, for facilitating site access and providing logistical support. Funding for this work was provided by the U.S. Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research (BER), Genomic Science Program, award number DE-SC0021198 (grant to JBE).

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  1. Department of Plant Pathology, University of California, Davis, CA, USA

    Anneliek M. ter Horst, Jane D. Fudyma & Joanne B. Emerson

  2. Bodega Marine Reserve, University of California, Davis, Bodega Bay, CA, USA

    Jacqueline L. Sones

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  1. Anneliek M. ter Horst
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Contributions

JE and AH designed the experiments. JF, JS and AH collected samples for this study, with JS providing information about the plant community at field sites. AH performed laboratory work and analyzed the data. JE and AH wrote the manuscript.

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Correspondence to Joanne B. Emerson.

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ter Horst, A.M., Fudyma, J.D., Sones, J.L. et al. Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography. ISME J 17, 2079–2089 (2023). https://doi.org/10.1038/s41396-023-01516-8

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