Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth’s crust

Abstract

The continental subsurface houses a major portion of life’s abundance and diversity, yet little is known about viruses infecting microbes that reside there. Here, we used a combination of metagenomics and genome-informed microscopy to show that highly abundant carbon-fixing organisms of the uncultivated genus Candidatus Altiarchaeum are frequent targets of previously unrecognized viruses in the deep subsurface. Analysis of CRISPR spacer matches displayed resistances of Ca. Altiarchaea against eight predicted viral clades, which showed genomic relatedness across continents but little similarity to previously identified viruses. Based on metagenomic information, we tagged and imaged a putatively viral genome rich in protospacers using fluorescence microscopy. Virus-targeted genomeFISH revealed a lytic lifestyle of the respective virus and challenges previous predictions that lysogeny prevails as the dominant viral lifestyle in the subsurface. CRISPR development over time and imaging of 18 samples from one subsurface ecosystem suggest a sophisticated interplay of viral diversification and adapting CRISPR-mediated resistances of Ca. Altiarchaeum. We conclude that infections of primary producers with lytic viruses followed by cell lysis potentially jump-start heterotrophic carbon cycling in these subsurface ecosystems.

Virus-associated organosulfur metabolism in human and environmental systems

“…All genes identified are categorized as Class I AMGs, or those for central metabolic functions but auxiliary to productive viral infection (Hurwitz and U’Ren, 2016). These AMGs were detected on 3,749 non-redundant viral genomes from all major bacterial dsDNA viral families ( Myoviridae, Podoviridae and Siphoviridae ) including viruses infecting an archaea (Rahlff et al, 2020) and eukaryote (amoeba) (Schulz et al, 2020). Therefore, AMGs for organosulfur metabolism were identified on viruses infecting all three domains of life, representing a shared metabolic constraint regardless of host domain.…”

Seasonal dynamics of natural Ostreococcus viral infection at the single cell level using VirusFISH

“…Promising alternatives to explore in situ viral‐host interactions are phageFISH (Allers et al ., 2013), and its variants direct‐geneFISH (Barrero‐Canosa et al ., 2017), VirusFISH (Castillo et al ., 2020), or single‐molecule FISH (Vincent et al ., 2021). Although their use in nature has been limited, phageFISH was recently used to pinpoint the host of an archaeal virus previously identified in an environmental metagenomic dataset (Hochstein et al ., 2016) and to demonstrate viral lysis of an autotrophic key player in the Earth's crust (Rahlff et al ., 2020). Likewise, single‐molecule FISH was recently used to quantify active viral infection in an induced Emiliania huxleyi bloom during a mesocosm experiment (Vincent et al ., 2021).…”