Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system

Abstract

Bacterial viruses are widespread and abundant across natural and engineered habitats. They influence ecosystem functioning through interactions with their hosts. Laboratory studies of phage–host pairs have advanced our understanding of phenotypic and genetic diversification in bacteria and phages. However, the dynamics of phage–host interactions have been seldom recorded in complex natural environments. We conducted an observational metagenomic study of the dynamics of interaction between Gordonia and their phages using a three-year data series of samples collected from a full-scale wastewater treatment plant. The aim was to obtain a comprehensive picture of the coevolution dynamics in naturally evolving populations at relatively high time resolution. Coevolution was followed by monitoring changes over time in the CRISPR loci of Gordonia metagenome-assembled genome, and reciprocal changes in the viral genome. Genome-wide analysis indicated low strain variability of Gordonia, and almost clonal conservation of the trailer end of the CRISPR loci. Incorporation of newer spacers gave rise to multiple coexisting bacterial populations. The host population carrying a shorter CRISPR locus that contain only ancestral spacers, which has not acquired newer spacers against the coexisting phages, accounted for more than half of the total host abundance in the majority of samples. Phages genome co-evolved by introducing directional changes, with no preference for mutations within the protospacer and PAM regions. Metagenomic reconstruction of time-resolved variants of host and viral genomes revealed how the complexity at the population level has important consequences for bacteria-phage coexistence.

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Fig. 1: Reconstruction of the spacer arrangement of Gordonia’s CRISPR-1 across the complete set of metagenomes from Perez et al. [38].
Fig. 2: Abundance of the main CRISPR-1 variants over time.
Fig. 3: Phage DC-56 genome map highlighting the position of protospacers.
Fig. 4: Occurrence of phage DC-56 SNVs and abundance of matching spacers over time.
Fig. 5: Phylogenetic signal analysis of reconstructed phage DC-56.

Data availability

Sequencing data are available at NCBI BioProject under accession no. PRJNA484416. Genome sequences and CRISPR reconstruction scripts are available at https://github.com/GuerreroCRISPR/Gordonia-CRISPR.

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Acknowledgements

This work was supported by grants from AySA-CONICET (Res. 3816/11 and 1371/15) and FONCyT (PICT 0746/15). The funders had no role in study design, data analysis, decision to publish, or preparation of the manuscript.

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Guerrero, L.D., Pérez, M.V., Orellana, E. et al. Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system. ISME J (2020). https://doi.org/10.1038/s41396-020-00802-z

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