Rewetting of a seasonally dry California grassland soil helps microbe-preying viruses thrive

Three microbes at different stages of lysing (Download Image)

A bacterial cell first having viruses attached (left), and then propagated (middle), and then lysed (right). (Image: Victor Leshyk/Northern Arizona University). (Graphics: Amanda Levasseur).

Beneath the Earth's surface, a relentless conflict unfolds as soil viruses prey on their tiny microbial hosts, fundamentally shaping our planet's ecosystems.

New research from Lawrence Livermore National Laboratory (LLNL) scientists and their collaborators at the University of California, Berkeley illuminates a fascinating phenomenon: the demise of soil bacteria and other unicellular microbes at the onset of the rainy season. As these microbes initially proliferate, so do viruses, which in turn kill the microbes, releasing a burst of carbon dioxide into the atmosphere.

In a new paper in Nature Communications, the team took a closer look at what happens to soil microbiomes at “wet-up” (the period immediately following rain). The team identified which types of microbes were present in the soil and roughly how common they were. They then simulated wet-up by adding water with a molecular label to the soil, an approach called “stable-isotope probing.” The DNA sequences that bore the added molecular label would come from bacteria, archaea and viruses that were multiplying rapidly, taking up the molecule to make new copies of DNA. This allowed the researchers to capture a close-up view of community changes during the wet-up period. 

Rewetting of seasonally dry soils induces dramatic shifts in viral biomass and diversity,” said LLNL scientist Steven Blazewicz, the senior author who designed and led the experimental work. “Our work which combines stable isotope probing, metagenomics and viromics, provides compelling evidence that viral infection contributes to microbial turnover and the associated release of CO2.” 

Mediterranean biomes, such as those found in various regions of California, soil microbes are influenced by yearly patterns of alternating wet and dry periods. They remain largely dormant during the dry summer and early fall. The first rainfall triggers the beginning of the growing season for many plants and enlivens the microbial community, or microbiome, in the soil. During the period immediately following this rain, bacteria and other unicellular soil microbes multiply rapidly. A massive die-off of microbes happens simultaneously, releasing a significant burst of carbon dioxide into the atmosphere.

The research team found that not only does wet-up induce rapid multiplication of bacteria and other unicellular organisms in the soil, but they also reveal a surge in the populations of viruses that prey on them. Significantly, it is estimated that almost half of the microbial die-off and related carbon release following wet-up could be attributed to soil viruses.

A single virus on top of bacterial cells in extracellular polymeric substance and other bacteria and fungal hyphae attached to a soil aggregate. Image by Victor Leshyk/Northern Arizona University.

To unravel the mystery of where these viruses reside during the dry season, the team explored the hypothesis that they might be concealed within bacterial cells in a non-infectious state, but the data from these studies don’t support that. Instead, it appears that viruses endure independently in the soil. Essentially, dry soil serves as a reservoir for numerous bacteria-hunting viruses that persist until wet conditions return.

Blazewicz said: "Dry soil harbors a diverse yet low biomass of virions, with only a subset thriving during wet-up. In contrast to recent theories suggesting the prevalence of temperate viruses in soil, our evidence indicates that wet-up is dominated by lytic viruses. We estimate that viruses drive a measurable and continuous rate of cell infections, contributing to up to 46% of microbial deaths one week after wet-up."

The research team emphasizes that a deeper understanding of soil microbiome dynamics will pave the way for innovative strategies to sequester carbon in the soil, potentially mitigating the impacts of climate change.

LLNL’s Jennifer Pett-Ridge also contributed to the conception, design and implementation of this study. The work was funded by the Department of Energy, Office of Science, Science Focus Area “Microbes Persist.”

--Hope Henderson of the DOE Joint Genome Institute contributed to this story.