Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Friends and Foes: How Microbial Predators Influence Nutrient Cycling in Soil

Authors:

Dishant Utpalbhai Patel1,2* (dishant-utpalbhai.patel@nau.edu), Javier A. Ceja-Navarro1,2, Matthew Heidenblut1,2, Benjamin J. Koch1,2, Jeffrey Propster1, Rebecca L. Mau1,2, Michaela Hayer1, Egbert Schwartz1,2, Paul Dijkstra1,2, Ember M. Morrissey3, Michelle C. Mack1,2, Bram Stone4, Kirsten S. Hofmockel4, Steven Blazewicz5, Jennifer Pett-Ridge5,6, Bruce A. Hungate1,2

Institutions:

1Center for Ecosystem Science and Society, Northern Arizona University; 2Department of Biological Sciences, Northern Arizona University; 3Division of Plant and Soil Sciences, West Virginia University; 4Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory; 5Physical and Life Science Directorate, Lawrence Livermore National Laboratory; 6Life and Environmental Sciences Department, University of California–Merced

Goals

This project asks how ecological interactions (cooperative and antagonistic) within the soil microbiome influence soil carbon (C) cycling and persistence. The researchers’ primary goals are to (1) test how 23 years of climate change alter microbial interactions and affect the fate of soil carbon; (2) quantify microbiome interactions that change the biochemical community-scale efficiency of carbon use and its fate; and (3) infer ecological interactions using machine learning and ecological models.

Abstract

Soil ecosystems are critical in the global carbon budget, and climate change can disrupt their functioning. In a northern Arizona climate change experiment, long-term alterations in temperature and precipitation have changed plant composition and primary production, leading to increased ecosystem respiration and photosynthesis but reduced soil carbon levels. However, much remains unknown about how microbial trophic interactions influence soil nutrient dynamics and how climate change affects these interactions. The research team hypothesizes that warming initially triggers cooperative interactions for complex carbon source degradation and top-down control of microbial communities by protists. Over time, as available carbon is depleted, predatory bacteria and viruses become the dominant top-down forces, altering predation modes and the fate and persistence of soil carbon.

To test the team’s hypotheses, researchers are conducting parallel field and laboratory experiments. In the field, researchers added plant roots highly labeled with carbon-13 (13C) to mixed conifer forest soils under warmed and unwarmed conditions in field mesocosms to trace carbon flow through the microbial food web.

Preliminary findings suggest that while total ecosystem respiration remained relatively constant in both conditions, plant root respiration was approximately 1.5 times higher in warmed soil than in unwarmed soil. Ongoing metatranscriptomics, metagenomics, and quantitive stable-isotope probing (qSIP) amplicon sequencing will identify potential trophic interactions driving carbon utilization dynamics.

In the laboratory, researchers are conducting trophic manipulation experiments using mixed conifer forest soils to investigate how predatory protists and bacteria influence carbon fate. Initially, microbial enrichments derived from researchers’ field soils, including diverse populations across life domains, were established. Prevalent microbial communities in the enrichments, identified as high-quality metagenome-assembled genomes, include bacterial groups such as Bacteriovorax sp., Pseudobdellovibrio sp., Bdellovibrio sp., Rhodoferax sp., Pedobacter sp., and Burkholderia sp., protists like Spumella sp. and Acanthamoeba sp., and viruses such as Mimivirus sp. and Kisquinquevirus sp.

The reintroduction of enriched protists and their prevalence in soil microcosms, along with their impact on bacterial communities, were assessed by quantifying gene expression using reverse transcription-quantitative polymerase chain reaction (RT-qPCR) of 18S rRNA and 16S rRNA. Expression of 18S rRNA genes in protist-treated soils (soil and protists in water to 60% water holding capacity) was 90-fold higher than in controls (soil and water only), indicating a higher protist prevalence. Anticipated lower 16S rRNA expression in protist-treated soils suggests antagonistic associations. Ongoing oxygen-18 qSIP amplicon sequencing analysis will confirm findings and allow the calculation of the growth rates of targeted communities.

Predatory bacteria isolated from microbial enrichments will be used in trophic manipulation experiments alongside sorted protist populations to track 13C’s fate from labeled plant roots and study ecological dynamics and microbial community interactions.

Funding Information

This research is supported by the U.S. DOE Office of Science, BER program GSP under Award Number DE-SC0023126 to Northern Arizona University. Work at Lawrence Livermore National Laboratory was performed under the U.S. DOE Contract DE-AC52-07NA27344 and Award SCW1779. Work at Pacific Northwest National Laboratory was performed under the U.S. DOE Contract DE-AC05-76RLO 1830 and FWP 79962.