Insights into the dynamics between viruses and their hosts in a hot spring microbial mat

Jessica K Jarett,Mária Džunková,Nikos Kyrpides,Frank A Corsetti,Simon Roux,Christopher B Trivedi,Frederik Schulz,Eric Becraft,Ramunas Stepanauskas,Hope A Johnson,David Paez-Espino,Stephanie A Carr,Emiley Eloe-Fadrosh,Sean P Jungbluth,Natalia Ivanova,John R Spear,Tanja Woyke

doi:10.1038/s41396-020-0705-4

Abstract

Our current knowledge of host–virus interactions in biofilms is limited to computational predictions based on laboratory experiments with a small number of cultured bacteria. However, natural biofilms are diverse and chiefly composed of uncultured bacteria and archaea with no viral infection patterns and lifestyle predictions described to date. Herein, we predict the first DNA sequence-based host–virus interactions in a natural biofilm. Using single-cell genomics and metagenomics applied to a hot spring mat of the Cone Pool in Mono County, California, we provide insights into virus–host range, lifestyle and distribution across different mat layers. Thirty-four out of 130 single cells contained at least one viral contig (26%), which, together with the metagenome-assembled genomes, resulted in detection of 59 viruses linked to 34 host species. Analysis of single-cell amplification kinetics revealed a lack of active viral replication on the single-cell level. These findings were further supported by mapping metagenomic reads from different mat layers to the obtained host–virus pairs, which indicated a low copy number of viral genomes compared to their hosts. Lastly, the metagenomic data revealed high layer specificity of viruses, suggesting limited diffusion to other mat layers. Taken together, these observations indicate that in low mobility environments with high microbial abundance, lysogeny is the predominant viral lifestyle, in line with the previously proposed “Piggyback-the-Winner” theory.

Highlights

To first assess the overall microbial community structure of the Cone Pool hot spring microbial mat, 16S rRNA gene amplicon analysis was performed on the mat layers B, C, E, F, G and H (Fig. 1), exclusive of the cone tip, which has previously been published [57]
By detecting viral contigs in both SAGs and metagenome-assembled genomes (MAGs) from the Cone Pool microbial mat, we linked 59 viruses with 34 hosts, many of them belonging to taxonomic groups with no cultured representatives
Single-cell genomics paired with metagenomic read recruitment provided insights into viral host range and distribution across the mat layers, as well as predicted viral lifestyle

Summary

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Single-cell genomics represents a unique opportunity to link viruses and hosts with experimental evidence, because a certain portion of cells collected directly from an environment contain viruses in the cell or attached to the cell [25, 26] This approach has shed light on important aspects of viral biology, such as horizontal gene transfer [27], the ability of viruses to reprogram their host’s energy metabolism [28] and micro-diversity within viral genomes [29]. We combined single-cell genomics with bulk shotgun metagenomics to predict different aspects of host–virus interactions, including viral host range, viral genome copy number compared to its host, and diffusion of viruses across the mat layers. The Cone Pool mat has many functional similarities to other microbial mats, such as limited diffusion of viruses into deeper layers and diurnal vertical migration of redox gradients [57], which suggests that the results of this study might be more broadly applicable to other structured biofilms in different environments

Methods

Results and discussion

Conclusions

Compliance with ethical standards