The devil in the details: Phage microhabitats as drivers of soil biogeochemistry

• Applicant: Kyle Mason-Jones, Ph.D.
• Subject Area: Soil Sciences ; Microbial Ecology and Applied Microbiology
• Term: since 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 521889691

Soil organic matter (SOM) is the Earth’s largest pool of organic carbon (C), and a crucial source of the essential plant nutrients nitrogen (N) and phosphorus (P). Soil microorganisms are the principal agents of SOM transformation and a nexus of global C and nutrient cycles. These microbes are strongly affected by viruses, notably viruses infecting bacteria (phages). In the ocean, phages kill 20% of bacteria every day, causing a ‘viral shunt’ that releases large amounts of organic matter and associated nutrients from bacterial biomass. This promotes ocean productivity as well as C storage in bacterial residues. Although phages are abundant in soil, to date they have been neglected in soil biogeochemistry. My research group will for the first time study how soil microhabitats govern phage infection and thus bacterial death; establish whether this gives rise to a comparable viral shunt in soil, and quantify the effects on plant nutrient and CO2 release as well as the stabilization of microbial residues. We will go beyond phenomenological descriptions to reveal the mechanisms of these processes, including direct dispersal limitations (e.g. phage sorption to mineral surfaces) and indirect effects (shaping traits of the phage community, with potential feedback to dispersal). Soil microhabitats will be characterized by state-of-the-art imaging to determine their microscale structure, including the 3D aqueous habitat (by synchrotron micro computed tomography), the distribution of organic matter (scanning electron microscopy) and the mineralogy of surfaces (Raman microspectroscopy). Specimen soil phages will be isolated to enable detailed characterization of their biophysical interactions and for testing the importance of the microhabitat in phage dispersal. Microhabitat impacts on phage infection and biogeochemical cycling will be experimentally determined in soil using coupled isotopic and molecular methods: 18O-DNA stable isotope probing to monitor phage production and bacterial death; functional gene abundance to identify affected bacterial processes; and isotope pool dilution and gas measurements for C, N and P mineralization rates. Isotopic labelling of specimen phages and hosts (13C, 15N, 33P) will demonstrate independently how phage infection redirects element flows. These experiments will provide the first mechanistic understanding of how soil phages, under the influence of their habitat, participate in biogeochemical cycles of global importance. We will go on to show how different patterns of microhabitat change affect phages. Microhabitats may also have a dynamic effect through evolutionary adaptation of phages. Understanding such processes is essential for predicting how phage communities will respond to human interventions or global change. Project findings will be integrated into a dynamic microscale model as a first step toward predictive phage ecology for improved agriculture and land management.

• DFG Programme: Independent Junior Research Groups